Agriculturally Important Fungi for Sustainable Agriculture: Volume 2: Functional Annotation for Crop Protection [1st ed.] 9783030484736, 9783030484743

Table of contents :
Front Matter ....Pages i-xviii
Agriculturally Important Fungi for Crop Protection (Pavidharshini Selvasekaran, Ramalingam Chidambaram)....Pages 1-53
Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses (Fatma A. Abo Nouh, Ahmed M. Abdel-Azeem)....Pages 55-80
Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress in Plants (Deepika Goyal, Sushma Mishra, Prem Kumar Dantu)....Pages 81-100
Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi (Prem Chandra, Enespa, Ranjan Singh)....Pages 101-148
Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense (Shomaila Sikandar, Asfand Yar Saqib, Imran Afzal)....Pages 149-179
Fungal Endophytes: A Source for Biological Control Agents (Hiran Kanti Santra, Debdulal Banerjee)....Pages 181-216
Aspergillus Mycotoxins: Potential as Biocontrol Agents (Fatma A. Abo Nouh, Sara A. Gezaf, Ahmed M. Abdel-Azeem)....Pages 217-237
Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health (Hesham A. El Enshasy, Kugan Kumar Ambehabati, Ashraf F. El Baz, Santosh Ramchuran, R. Z. Sayyed, Divina Amalin et al.)....Pages 239-259
Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance and Disease Resistance (Fatma A. Abo Nouh, Hebatallah H. Abo Nahas, Ahmed M. Abdel-Azeem)....Pages 261-283
Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes (K. Kiran Kumar)....Pages 285-311
Global Scenario of Advance Fungal Research in Crop Protection (Vanita Yadav, Murthy M. V. S. N. Lekkala, Challa Surekha, Nageswara Rao Reddy Neelapu)....Pages 313-346
Functional Annotation of Agriculturally Important Fungi for Crop Protection: Current Research and Future Challenges (Ajar Nath Yadav, Divjot Kour, Tanvir Kaur, Rubee Devi, Neelam Yadav)....Pages 347-356
Back Matter ....Pages 357-370

Citation preview

Fungal Biology

Ajar Nath Yadav · Shashank Mishra  Divjot Kour · Neelam Yadav  Anil Kumar  Editors

Agriculturally Important Fungi for Sustainable Agriculture Volume 2: Functional Annotation for Crop Protection

Fungal Biology Series Editors Vijai Kumar Gupta AgroBioSciences (AgBS) and Chemical & Biochemical Sciences (CBS) Department Mohammed VI Polytechnic University (UM6P) Benguerir, Morocco Maria G. Tuohy School of Natural Sciences National University of Ireland Galway Galway, Ireland

About the Series Fungal biology has an integral role to play in the development of the biotechnology and biomedical sectors. It has become a subject of increasing importance as new fungi and their associated biomolecules are identified. The interaction between fungi and their environment is central to many natural processes that occur in the biosphere. The hosts and habitats of these eukaryotic microorganisms are very diverse; fungi are present in every ecosystem on Earth. The fungal kingdom is equally diverse, consisting of seven different known phyla. Yet detailed knowledge is limited to relatively few species. The relationship between fungi and humans has been characterized by the juxtaposed viewpoints of fungi as infectious agents of much dread and their exploitation as highly versatile systems for a range of economically important biotechnological applications. Understanding the biology of different fungi in diverse ecosystems as well as their interactions with living and non-living is essential to underpin effective and innovative technological developments. This series will provide a detailed compendium of methods and information used to investigate different aspects of mycology, including fungal biology and biochemistry, genetics, phylogenetics, genomics, proteomics, molecular enzymology, and biotechnological applications in a manner that reflects the many recent developments of relevance to researchers and scientists investigating the Kingdom Fungi. Rapid screening techniques based on screening specific regions in the DNA of fungi have been used in species comparison and identification, and are now being extended across fungal phyla. The majorities of fungi are multicellular eukaryotic systems and therefore may be excellent model systems by which to answer fundamental biological questions. A greater understanding of the cell biology of these versatile eukaryotes will underpin efforts to engineer certain fungal species to provide novel cell factories for production of proteins for pharmaceutical applications. Renewed interest in all aspects of the biology and biotechnology of fungi may also enable the development of “one pot” microbial cell factories to meet consumer energy needs in the 21st century. To realize this potential and to truly understand the diversity and biology of these eukaryotes, continued development of scientific tools and techniques is essential. As a professional reference, this series will be very helpful to all people who work with fungi and should be useful both to academic institutions and research teams, as well as to teachers, and graduate and postgraduate students with its information on the continuous developments in fungal biology with the publication of each volume. More information about this series at http://www.springer.com/series/11224

Ajar Nath Yadav  •  Shashank Mishra Divjot Kour • Neelam Yadav • Anil Kumar Editors

Agriculturally Important Fungi for Sustainable Agriculture Volume 2: Functional Annotation for Crop Protection

Editors Ajar Nath Yadav Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture Eternal University Sirmour, Himachal Pradesh, India Divjot Kour Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture Eternal University Baru Sahib, Sirmour, India

Shashank Mishra Biotechnology QCQA Laboratory, Biotech Park Lucknow, Uttar Pradesh, India Neelam Yadav Gopi Nath PG College Veer Bahadur Singh Purvanchal University Ghazipur, Uttar Pradesh, India

Anil Kumar Rani Lakshmi Bai Central Agricultural University Jhansi, Uttar Pradesh, India

ISSN 2198-7777     ISSN 2198-7785 (electronic) Fungal Biology ISBN 978-3-030-48473-6    ISBN 978-3-030-48474-3 (eBook) https://doi.org/10.1007/978-3-030-48474-3 © Springer Nature Switzerland AG 2020 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

Sustainable agriculture is the only solution in providing food security to feed the gigantic population, with resource limitation being a foremost challenge for the global community. Sustainable agriculture requires limited use of harmful chemical fertilizers and pesticides. Among diverse groups of microbes, soil and plant fungal communities play an important role in plant growth, development, and soil health. The beneficial fungal communities help to promote plant growth directly or indirectly via different plant growth-promoting mechanisms viz: releasing plant growth regulators; solubilization of phosphorus, potassium and zinc; biological nitrogen fixation or by producing siderophores, ammonia, HCN and other secondary metabolites. The plant growth promoting fungal communities with multifunctional PGP attributes could be used as biofertilizers and biocontrol agents replacing chemical fertilizers and pesticides in the environmental as eco-friendly agents for sustainable agriculture and environment. Fungal communities possess a huge sink of capability by which they act as bioprotectants and biostimulants as well as for mitigation of different abiotic stress in plants. The utilization of beneficial soil and plant fungal resources will surely support sustainable agriculture. The present book on “Agriculturally Important Fungi for Sustainable Agriculture, Volume 2: Functional Annotation for Crop Protection” covers soil- and plant-associated fungal communities and their role in plant growth promotion, and crop productivity for sustainable agriculture. This book will be immensely useful to the biological sciences, especially to microbiologists, microbial biotechnologists, biochemists, researchers, and scientists dealing with fungal biotechnology. We have the honour that the leading scientists who have extensive, in-depth experience and expertise in plant-microbe interaction and fungal biotechnology took the time and

v

vi

Preface

made efforts to contribute these outstanding chapters. Each chapter is written by internationally recognized researchers and scientists so that the readers are given an up-to-date and detailed account of our knowledge of fungal biotechnology and its innumerable agricultural applications. Sirmour, Himachal Pradesh, India  Ajar Nath Yadav Lucknow, Uttar Pradesh, India   Shashank Mishra Baru Sahib, Sirmour, India   Divjot Kour Ghazipur, Uttar Pradesh, India   Neelam Yadav Jhansi, Uttar Pradesh, India   Anil Kumar

Acknowledgements

All the authors are sincerely acknowledged for contributing up-to-date information on agriculturally important fungi, their biodiversity and biotechnological applications for sustainable agriculture and environments. The editors are thankful to all the authors for their valuable contributions. All editors would like to thank their families who were very patient and supportive during this journey. Our sincere thanks to the whole Springer team who was directly or indirectly involved in the compilation of this book. We are grateful to the many people who helped to bring this book to light. Editors wish to thank Mr. Eric Stannard, Senior Editor, Botany, Springer; Dr. Vijai Kumar Gupta, and Prof Maria G.  Tuohy, Series editor, Fungal Biology Springer; Ms. Saveetha Balasundaram, Project Coordinator, Springer for generous assistance, constant support, and patience in initializing the volume. The editor Dr. Ajar Nath Yadav is grateful to his Ph.D. research scholars Tanvir Kaur, Rubee Devi, Divjot Kour, Kusam Lata Rana and colleagues for their support, love, and motivation in all his efforts during this project. We are very sure that this book will be great interest to the scientists, graduates, undergraduates, and postdocs who are investigating fungal biology and biotechnology.

vii

Contents

1 Agriculturally Important Fungi for Crop Protection��������������������������    1 Pavidharshini Selvasekaran and Ramalingam Chidambaram 2 Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses������������������������������������������������������������������������������������   55 Fatma A. Abo Nouh and Ahmed M. Abdel-Azeem 3 Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress in Plants����������������������������������������������   81 Deepika Goyal, Sushma Mishra, and Prem Kumar Dantu 4 Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi ����������������������������������������������������������������������  101 Prem Chandra, Enespa, and Ranjan Singh 5 Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense����������������������������������������������������������������  149 Shomaila Sikandar, Asfand Yar Saqib, and Imran Afzal 6 Fungal Endophytes: A Source for Biological Control Agents��������������  181 Hiran Kanti Santra and Debdulal Banerjee 7 Aspergillus Mycotoxins: Potential as Biocontrol Agents����������������������  217 Fatma A. Abo Nouh, Sara A. Gezaf, and Ahmed M. Abdel-Azeem 8 Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health����������������������������������������������������������������  239 Hesham A. El Enshasy, Kugan Kumar Ambehabati, Ashraf F. El Baz, Santosh Ramchuran, R. Z. Sayyed, Divina Amalin, Daniel J. Dailin, and Siti Zulaiha Hanapi 9 Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance and Disease Resistance����������������������������������  261 Fatma A. Abo Nouh, Hebatallah H. Abo Nahas, and Ahmed M. Abdel-Azeem ix

x

Contents

10 Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes��������������������������������������������������������������������������������  285 K. Kiran Kumar 11 Global Scenario of Advance Fungal Research in Crop Protection������������������������������������������������������������������������������������  313 Vanita Yadav, Murthy M. V. S. N. Lekkala, Challa Surekha, and Nageswara Rao Reddy Neelapu 12 Functional Annotation of Agriculturally Important Fungi for Crop Protection: Current Research and Future Challenges������������������������������������������������������������  347 Ajar Nath Yadav, Divjot Kour, Tanvir Kaur, Rubee Devi, and Neelam Yadav Index������������������������������������������������������������������������������������������������������������������  357

Contributors

Ahmed M. Abdel-Azeem  Systematic Mycology Laboratory, Botany Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt Hebatallah H. Abo Nahas  Zoology Department, Faculty of Science, Suez Canal University, Ismailia, Egypt Fatma  A.  Abo  Nouh  Systematic Mycology Laboratory, Botany Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt Imran Afzal  Department of Biology, Lahore Garrison University, Lahore, Pakistan Divina Amalin  Biological Control Research Unit, Center for Natural Sciences and Environmental Research, De La Salle University, Manila, Philippines Kugan  Kumar  Ambehabati  Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Malaysia Debdulal  Banerjee  Microbiology and Microbial Biotechnology, Department of Botany and Forestry, Vidyasagar University, Midnapore, West Bengal, India Prem  Chandra  Department of Environmental Microbiology, School for Environmental Sciences, Babasaheb Bhimrao Ambedkar University (a central university), Lucknow, Uttar Pradesh, India Ramalingam Chidambaram  Food Science and Technology, School of Biosciences and Technology, Vellore Institute of Technology, Vellore, Tamil Nadu, India Daniel J. Dailin  Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Malaysia Prem  Kumar  Dantu  Department of Botany, Dayalbagh Educational Institute, Deemed University, Agra, Uttar Pradesh, India

xi

xii

Contributors

Rubee Devi  Department of Biotechnology, Eternal University, Sirmour, Himachal Pradesh, India Enespa  Department Plant Pathology, Sri Mahesh Prasad Degree College, University of Lucknow, Lucknow, Uttar Pradesh, India Ashraf  F.  El Baz  Genetic Engineering and Biotechnology Research Institute, Sadat University, Sadat City, Egypt Hesham  A.  El Enshasy  Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Malaysia Sara  A.  Gezaf  Botany Department, Faculty of Science, Al-Arish University, North Sinai, Egypt Deepika Goyal  Department of Botany, Dayalbagh Educational Institute, Deemed University, Agra, Uttar Pradesh, India Siti  Zulaiha  Hanapi  Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Malaysia Tanvir Kaur  Department of Biotechnology, Eternal University, Sirmour, Himachal Pradesh, India Divjot Kour  Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Sirmour, Himachal Pradesh, India K.  Kiran  Kumar  Department of Nematology, ICAR-Central Citrus Research Institute, Nagpur, Maharashtra, India Murthy  M.  V.  S.  N.  Lekkala  Department of Biochemistry and Bioinformatics, Institute of Science, Gandhi Institute of Technology and Management (GITAM), (Deemed-to-be University), Visakhapatnam, Andhra Pradesh, India Sushma Mishra  Department of Botany, Dayalbagh Educational Institute, Deemed University, Agra, Uttar Pradesh, India Nageswara Rao Reddy Neelapu  Department of Biochemistry and Bioinformatics, Institute of Science, Gandhi Institute of Technology and Management (GITAM), (Deemed-to-be University), Visakhapatnam, Andhra Pradesh, India Santosh  Ramchuran  Bioprocess Development Department, CSIR Biosciences, Pretoria, South Africa Hiran Kanti Santra  Microbiology and Microbial Biotechnology, Department of Botany and Forestry, Vidyasagar University, Midnapore, West Bengal, India Asfand Yar Saqib  Department of Biology, Lahore Garrison University, Lahore, Pakistan R. Z. Sayyed  Department of Microbiology, PSGVP Mandal’s, Arts, Science, and Commerce College, Shahada, Maharashtra, India

Contributors

xiii

Pavidharshini Selvasekaran  Food Science and Technology, School of Biosciences and Technology, Vellore Institute of Technology, Vellore, Tamil Nadu, India Shomaila Sikandar  Department of Biology, Lahore Garrison University, Lahore, Pakistan Ranjan Singh  Department of Environmental Science, School for Environmental Sciences, Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow, Uttar Pradesh, India Challa  Surekha  Department of Biochemistry and Bioinformatics, Institute of Science, Gandhi Institute of Technology and Management (GITAM), (Deemedto-be University), Visakhapatnam, Andhra Pradesh, India Ajar  Nath  Yadav  Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Sirmour, Himachal Pradesh, India Neelam Yadav  Gopi Nath PG College, Veer Bahadur Singh Purvanchal University, Ghazipur, Uttar Pradesh, India Vanita  Yadav  Department of Biochemistry and Bioinformatics, Institute of Science, Gandhi Institute of Technology and Management (GITAM), (Deemedto-be University), Visakhapatnam, Andhra Pradesh, India

About the Editors

loc Ajar Nath Yadav  is an Assistant Professor (Sr. Scale) in the Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Himachal Pradesh, India. He has 5 years of teaching and 11 years of research experiences in the field of Microbial Biotechnology, Microbial Diversity, and Plant-Microbe-Interactions. Dr. Yadav obtained doctorate in Microbial Biotechnology, jointly from IARI, New Delhi and BIT, Mesra, Ranchi, India; M.Sc. (Biotechnology) from Bundelkhand University and B.Sc. (CBZ) from the University of Allahabad, India. Dr. Yadav has 296 publications, with h-index of 39, i10-index of 92, and 4045 citations (Google Scholar). Dr. Yadav is editor of 11 Springer-Nature, 04 CRC Press Taylor and Francis and 02 Elsevier books. Dr. Yadav has got 12 Best Paper Presentation Awards, and 01 Young Scientist Award (NASI-Swarna Jayanti Purskar). Dr. Yadav received the “Outstanding Teacher Award” in 6th Annual Convocation 2018 by Eternal University, Baru Sahib, Himachal Pradesh. Dr. Yadav has a longstanding interest in teaching at the UG, PG, and PhD level and is involved in taking courses in microbiology and microbial biotechnology. Dr. Yadav has guided 01 Ph.D. and 01 M.Sc. Scholar and presently he is guiding 03 scholars for PhD degree. He has been serving as an editor/editorial board member and reviewer for more than 35 national and international peer-reviewed journals. He has lifetime membership of Association of Microbiologists in India and Indian Science Congress Council, India. Please visit https://sites.google.com/site/ajarbiotech/ for more details.

xv

xvi

About the Editors

Shashank  Mishra  is presently working as Scientist “C”, Biotech Park, Lucknow, Uttar Pradesh, India. He obtained his doctorate degree in Science “Industrial Biotechnology” in 2015, from Birla Institute of Technology, Mesra, Ranchi, India; M.Phil. (Biotechnology) in 2008 from Alagappa University, Tamil Nadu; M.Sc. (Botany) in 2005 from Dr. R.M.L. University, Ayodhya; M.Sc. (Biotechnology) in 2004 from Barkatullah University, Bhopal, and B.Sc. (Botany and Chemistry) in 2001 from Dr. R.M.L. University, Ayodhya, India. He has made pioneering contributions in the area of Microbial Biotechnology; Natural product synthesis and Environmental Microbiology for food, pharmaceutical, and Human Health. In his credit 21 publications [06 research papers, 02 review articles, 03 books, and 10 book chapters] in different reputed international and national journals and publishers with 82 citation, h-index-05, and i10-index 04 (Google Scholar). He has reported first time with high concentration of phenolic compounds by optimizing various parameters and published in peer-reviewed and refereed international journals. He has published 16 abstracts in different conferences/symposiums/workshops. He has presented 16 papers presentation [12 poster + 04 oral] in conferences/symposiums and got 01 best poster presentations Award, Dr. Mishra has contributed in organizing 07 conference/workshops. He has deposited 03 nucleotide sequences to NCBI GenBank databases: in public domain. Dr. Mishra and group have isolated and characterized 03 microbes (bacteria and microalgae) from Tulsi and paddy plantation site and transformed ferulic acid into value-added phenolic compounds, viz., vanillin, vanillic acid, and 4-vinylguaiacol. He has a long-standing interest in teaching at the UG, PG, and Ph.D. level and is involved in taking courses in industrial biotechnology, bioprocess engineering and technology, environmental biotechnology, environmental microbiology, industrial microbiology, microbial biotechnology and techniques in microbiology and biotechnology. He is reviewer in 06 international journals including BMC Microbiology, Indian Phytopathology, PLOS One, Scientific Reports and Archive of Phytopathology and Plant Protection, and 3 Biotech. He has lifetime membership of Association of Microbiologists of India (AMI) and Vigyan Bharti (VIBHA). Divjot Kour  is currently working as Project Assistant in DEST funded project “Development of Microbial Consortium as Bioinoculants for Drought and Low Temperature Growing Crops for Organic Farming in Himachal Pradesh”. Dr. Kour obtained doctorate degree in Microbial Biotechnology from Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Himachal Pradesh, India. She obtained M.Phil. in Microbiology in 2017 from Shoolini University of Biotechnology and

About the Editors

xvii

Management Sciences, Solan, Himachal Pradesh; M.Sc. in Microbiology from University of Jammu, Jammu and Kashmir in 2015, and B.Sc. from University of Jammu, Jammu and Kashmir in 2014. She has research experience of 04 years. In her credit 39 publications (11 research/reviews and 28 book chapters) in different reputed international, national journals and publishers. She is editor of 02 books in Springer. She has published 18 abstracts in different conferences/symposiums/ workshops. She has presented 09 papers in national and international conferences/ symposiums and got 05 best paper presentation awards. In her credit more than 700 microbes (bacteria and fungi) isolated from diverse sources. She has the membership of National Academy of Sciences and Agro Environmental Development Society, India. Neelam  Yadav  is currently working on microbial diversity from diverse sources and their biotechnological applications in agriculture and allied sectors. She obtained her post graduation degree from Veer Bahadur Singh Purvanchal University, Uttar Pradesh, India. She has research interest in the area of beneficial microbiomes and their biotechnological application in agriculture, medicine, environment, and allied sectors. In her credit 59 research/review/book chapters publication in different reputed international, national journals and publishers. She is editor of 02 books in Elsevier, 03 in CRC press, Taylor & Francis, and 05 in Springer. She is the Editor/associate editor/reviewer of different international and national journals including Plos One, Extremophiles, Annals of Microbiology, Journal of Basic Microbiology, Advance in Microbiology and Biotechnology. She has lifetime membership of Association of Microbiologists in India, Indian Science Congress Council, India, and National Academy of Sciences, India. Anil  Kumar  is Director, Education, Rani Lakshmi Bai Central Agricultural University, Near Pahuj dam Gwalior Road, Jhansi (UP). He has 30 years of research, teaching, and administrative experience in various capacities. He had worked as Professor & Head (2006– till date), Associate Professor (2003–2006), and Assistant Professor (1993–1999), Dept. of Molecular Biology & Genetic Engineering, G. B. Pant University of Agriculture & Technology, Pantnagar. He has to his credit more than 200 publications including research papers, reviews, and chapters contributed to books, popular articles, books/bulletins/manuals. His research interests focus on diverse but specific areas of agricultural importance at national and international level employing the tools and techniques of molecular biology and immunology. Dr. Kumar has strengthened the area of molecular plant pathology, for combating

xviii

About the Editors

the Karnal bunt which is an economically important disease of wheat, he followed three approaches, viz., Plant disease surveillance through molecular/immunological diagnostics; Pathogen Indexing Programme through Molecular Pathotyping, and Characterization of disease resistance and Pathogenesis through Molecular signaling investigating the role of MAP kinases and Cystatin gene families as candidate genes. It was postulated that stoichiometric balance of cystatin and cysteine protease might be contributing to disease resistance and susceptibility. Dr. Kumar has filed several patents on synthesis of nano delivery vesicles for facilitation of uptake of fat soluble vitamins, nano-curcuminoids for better bio-availability, and nano-iron pro-booster technology for agronomic bio-­fortification. His pioneer research work has been highlighted by several magazines like NATURE and published in several international journals of repute with citation index: >2398, h-index 27, and i10 index 82. He has been an outstanding teacher and researcher who is credited with many awards and recognitions, viz., Dr. Radhakrishnan Best Teacher Award, INSA Best Teacher Award, Dr. C. Subramaniam Outstanding Teacher Award, Outstanding Faculty Recognition, Dr. B.B. Singh Outstanding Researcher Award, and also conferred three times “Governor’s Award” for best research in the year 2015, 2017, and 2019 from different organizations including university ICAR, INSA, and DBT.

Chapter 1

Agriculturally Important Fungi for Crop Protection Pavidharshini Selvasekaran and Ramalingam Chidambaram

Contents 1.1  I ntroduction 1.2  T  he Role of Fungi as Biofertilizers 1.2.1  Advantages of Fungal Biofertilizers 1.3  The Role of Fungi as a Biocontrol Agent 1.4  Fungal Endophytes 1.4.1  Direct Mechanism 1.4.2  Indirect Mechanism 1.4.3  The Advantages of Fungal Endophytes Over Chemical Methods 1.5  Arbuscular Mycorrhizae and Its Role in Agriculture 1.6  Penicillium and Its Role as Plant Growth Promotion 1.6.1  The Role of Penicillium Under Abiotic Conditions 1.7  Trichoderma for Sustainable Agriculture 1.7.1  Mycoparasitism 1.7.2  Antibiosis 1.7.3  Competition and Competence of Rhizosphere 1.7.4  Enzyme Production 1.7.5  Enhancement of Host Defense Response 1.7.6  Growth Promotion of Host Plants 1.7.7  Phosphate Solubilization 1.7.8  Drought Tolerance 1.8  Piriformospora indica 1.8.1  Acquisition of Phosphorus 1.8.2  Acquisition of Other Nutrients 1.8.3  Plant Growth and Development 1.8.4  Role in the Tolerance of Biotic and Abiotic Stress 1.9  Notable Research on the Role of Fungi in Agriculture 1.10  Conclusion and Future Perspective References

 2  3  4  5  7  8  10  15  15  17  18  20  21  22  23  23  24  24  25  26  27  28  29  29  30  33  34  35

P. Selvasekaran · R. Chidambaram (*) Food Science and Technology, School of Biosciences and Technology, Vellore Institute of Technology, Vellore, Tamil Nadu, India e-mail: [email protected] © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_1

1

2

P. Selvasekaran and R. Chidambaram

1.1  Introduction Fungi are one of the most important pathogens of crop plants in agriculture and forestry but they are also used as potential biocontrol agents to prevent and control plant disease. In recent years, the development of fungi for biocontrol of diseases, pests, and weeds has received a significant amount of interest among the community of scientists and researchers (Rangel et al. 2018). Public concerns on the usage of pesticides in the agricultural field and their effect on the environment are increasing day by day. Many fungi are being developed and mass produced as a commercially available biocontrol agents and are used in agriculture to promote the growth of plant and increase plant defense mechanism (Vega et al. 2009) as well as to control plant disease (Costa et al. 2012), terrestrial weeds (Monteiro, AC, Machado 2012). These biocontrol agents can also control and reduce aquatic weeds, plant-parasitic nematodes (Siddiqui and Mahmood 1996), and insects (Alston et  al. 2005; Li et al. 2010). Recent study in agricultural system on the role of Arbuscular mycorrhiza suggests that they can improve salinity tolerance and drought tolerance of their host plant by increasing the nutrient uptake, accumulation of organic solutes, and reducing the oxidative stress as a result of enhanced activity of catalase, peroxidase, calmodulin, superoxide dismutase, and ascorbate peroxidase (Abdel Latef and Chaoxing 2014; Chandrasekaran et al. 2014; Huang et al. 2014). An important role in stress tolerance is enhanced by symbiotic mycorrhizal fungi in both forest and agricultural ecosystems by improving nutrient uptake and drought tolerance and restricting base cation leaching as well as by mitigating the toxic effects of aluminum and other heavy metals (Finlay 2008; Finlay et al. 2009; Yadav 2017, 2019b). The non-mycorrhizal fungi such as Trichoderma are well known for mediating stress reactions in plants and have the potential to parasitize or antagonize plant pathogenic fungi by stimulating the defense response and increasing the plant growth (Druzhinina et al. 2011; Sharma et al. 2019). The other fungi species such as Piriformospora indica induce disease resistance, tolerate salt stress, and promote the growth of crops through their capacity of glutathione ascorbate cycle mediated antioxidation activity (Waller et al. 2005). The enhancement of plant growth utilizing plant bio-stimulants and to access novel molecules by exploiting the fungal stress response to be used in agriculture is of current interest (Calvo et al. 2014; Yadav 2018). Endophytic microbes specifically endophytic fungi are those that have established an equilibrium with their host during the evolution and are recognized as a potential source of a wide variety of bioactive secondary metabolites (Rana et al. 2019a; Tan and Zou 2001; Sonaimuthu et  al. 2010; Gangadevi and Muthumary 2008). Their relationship with the host plant can vary from bordering on the pathogen to symbiotic. They adopt a different type of symbiosis such as facultative saprobic, exploitative, parasitic, and mutualistic (Clay and Schardl 2002). In most cases, the plant hosts are benefited by asymptomatic relationship. However in few cases they may exhibit beneficial or pathogenic effects (Photita et  al. 2001; Wei

1  Agriculturally Important Fungi for Crop Protection

3

et al. 2007; Neubert et al. 2006) Few endophytic fungi exhibit mutualistic relationship with single plant species and not with the other plant species whereas some species have the potential to associate with wide range of plant host as well as association of endophyte with specific host tissue has also been reported (Hardoim et al. 2015; Yadav et al. 2020d). Fungal endophytes are ubiquitous and have been found in the majority of plant species that have been studied to date (Rana et al. 2019b; Yadav et al. 2019b). However, the literature available on the association between few plant host and endophytic fungi is limited and has to be explored further (Brundrett 2007). Endophytic fungi by secreting selected secondary metabolites have found to be associated with the plants to promote growth (Dai et al. 2008), protect from insects and disease (Wilkinson et al. 2000; Tanaka et al. 2005), and improve stress resistance (Lewis 2004). These secondary metabolites produced by endophytic fungi also have been identified as the source of antidiabetic, insecticidal, anticancer, immunosuppressive, and biocontrol compounds. These novel compounds help as remedies with their valuable biological and chemical characteristics for the health problems of plants, animals, and humans. The fungal endophytes have been represented as “chemical synthesizer inside the plant” because of the production of a variety of these useful chemical compounds (Yadav et al. 2020b, c). Fungal diversity on earth is contributed significantly by endophytic fungi (Photita et al. 2001). Their biological distribution and diversity are massive in tropical rainforest and temperate zone. The detection of novel compounds from this group of fungi is extensively studied to investigate their potential to be used in pharmaceutical, medical, industrial, and agricultural sectors. A noteworthy discovery is the use of these compounds in agriculture as a biocontrol agent (Mane and Vedamurthy 2018). Fungal endophytes contribute to the fitness of plants by enabling the adaption of plant host to abiotic and biotic stresses. They establish a symbiotic relationship between their hosts and confer disease and pest resistance to host by enhancing their fitness, increasing the growth to resist stresses to the maximum extent, and promote the production of secondary metabolites (Gautam and Avasthi 2019; Rastegari et al. 2020a). Therefore, the use of fungi for the purpose of sustainable agriculture is of major interest.

1.2  The Role of Fungi as Biofertilizers Biofertilizers are an important source of essential nutrients for plants and crops. They are inexpensive and eco-friendly. They play a vital role in improving the nutrient status of soil, increase soil fertility, and, thus, crop productivity. Biofertilizers are the formulation of living microbes including bacteria, actinomycetes, and fungi (Kour et al. 2020d). They can be applied directly to plant roots, soil, seed, and seedlings. Due to their inherent biological activity of the microorganisms, they help in mobilization and accessibility of nutrients (Pal et al. 2015). Fungal biofertilizers can be applied alone or in combination to the natural fields and can be beneficial directly

4

P. Selvasekaran and R. Chidambaram

or indirectly to plant development, yield, and growth through various methods (Rai et al. 2013; Yadav et al. 2019c). The roots of herbs, trees, xerophytes, epiphytes, aquatics, shrubs, trees, aquatics, hydrophytes, and terrestrial plants are reported to develop mycorrhizal associations when grown with the insufficient availability of essential elements such as zinc, phosphorus, nitrogen, iron, sulfur, boron, and copper (Rastegari et al. 2020b; Singh and Yadav 2020). Fungal biofertilizers that solubilize phosphate are the biological agents that are commonly employed for improving the growth and development of plants by enhancing the phosphorus uptake. The phosphate solubilizing property of fungi contributes significantly to the soil phosphate availability to plants. Several fungi have phosphate solubilizing property, the most common are Saccharomycopsis schoenii, Cryptococcus luteolus, Trichosporon beigelii, Rhodotorula aurantiaca A, Kluyveromyces walti, Neosartorya fisheri var. fischeri, Candida montana, Penicillium purpurogenum var. rubrisclerotium, and Zygoascus hellenicus (Birhanu et al. 2017). The fungi that solubilize phosphate belonging to the genera Fusarium, Aspergillus, Penicillium sp. are also found in the rhizospheric region of various plants. The fungal genera of Penicillium, Chaetomium, and Aspergillus are of widespread occurrence (Yadav et al. 2018, 2019c). The commonly employed fungi for the production of biofertilizer are Trichoderma which is predominantly present in agricultural soils. The rhizosphere inhabited by Trichoderma species can also interact and parasitize with other fungi. These species have long been recognized as they enhance crop nutrition, nutrient acquisition, and augment plant productivity. The metabolites produced by these species serve as a fungicide against the fungal pathogens that cause disease (Harman et al. 2008; Chang 1986; Vinale et al. 2009). The utilization of Trichoderma as a culture filtrate and its inoculation in soil enhances biomass production and plant growth. The application of this fungus as a model organism is feasible as they are easy to cultivate under laboratory conditions for the evaluation of beneficial interaction between plants and microbes. They can be used as a novel tool to enhance the productivity of plants (Varma et al. 2012).

1.2.1  Advantages of Fungal Biofertilizers • They are renewable sources of nutrients and sustain soil health. • They increase the yield of grains by 20–40% and replace 40–50% of chemical fertilizers. • They enhance plant growth by secreting growth-promoting hormones and also secrete antibiotic and fungi static substances. They do not have an adverse effect on soil fertility and plant growth. • Phosphate solubilizing or phosphate mobilizing fungal biofertilizer converts insoluble soil phosphate into soluble soil phosphate due to the secretion of various organic acids. Under optimum condition, they can mobilize or solubilize about 40–50 kg phosphorus and results in a 20–30% increase in the crop yield.

1  Agriculturally Important Fungi for Crop Protection

5

• They enhance the uptake of P, Zn, S, and water leading to increased yield and uniform crop growth. They improve the hardiness of the stock transplant and enhance resistance to root disease. • They liberate the substance that promotes growth, vitamins, and maintain soil fertility. • They stabilize C:N ratio of soil and decompose the residues of the plant. • Fungal biofertilizers act as an antagonist and help in the biocontrol of disease by suppressing the incidence of soil-borne pathogens. • Fungal biofertilizer plays a significant role in the recycling of plant nutrients. • Fungal biofertilizers are eco-friendly, non-pollutants as well as cost-­effective (Table 1.1) (Pal et al. 2015)

1.3  The Role of Fungi as a Biocontrol Agent Currently, the rapidly growing research area with a significant role in increased food production and plant yield is “biocontrol.” The phenomenon of biocontrol agent helps to sustain the food crop quality and to reduce the risks that result from the increased utilization of hazardous chemicals and synthetic pesticides. The major factor responsible for 10–30% of annual crop productivity loss is plant disease. In spite of the development of water management practice, an agricultural practice that has posed to be the effective management of plant disease, new techniques in agronomy, the development of disease-resistant varieties, there are still pathogens for which the synthetic chemicals are broadly used for the management of the disease (Kour et al. 2019b; Yadav et al. 2020a). The attractive choice of using the biocontrol agent against different pathogens has emerged as the most common and significant factor responsible for the death of insects in a large populations (Villa et al. 2017). Several postharvest diseases are biologically balanced using fungal species that have antagonist properties. The worldwide scientist is attracted by this area of research. The components of the biocontrol system are influenced by various factors such as UV light, temperature, pH, as well as abiotic and biotic stresses (Kumar et  al. 2019a, b; Yadav 2019a). The biocontrol agent preparation is significantly affected by various abiotic stress factors which lead to modification of functionality. Therefore, knowledge on the survivability of biocontrol agents under certain environmental conditions and the development of the procedure to make the biocontrol agent resist stress tolerance is required to maintain their commercial exploitation and effectiveness. The experimental studies on various biocontrol agents on different plant species have been studied to understand their reaction under varied environmental conditions (Sui et al. 2015) (Table 1.2).

List of agriculturally important fungal biofertilizer Zinc solubilizing biofertilizer • Ericoid mycorrhiza (oidiodendron maius) • Penicillium simplicissimum • Saccharomyces spp. • Aspergillus niger Potash solubilizing biofertilizer • Aspergillus spp. (A. terreus, A. fumigatus, A. niger) • Ectomycorrhizal fungi Phosphate mobilizing biofertilizer • Arbuscular mycorrhiza, Glomus spp. (G. viscosum, (G. mosseae/G. cerebriforme/G. manihotis/G. aggregatum, G. intraradices, G. versiforme, G. deserticola, G. radiatum, G. globiferum, G. monosporum, G. microcarpum, G. halonatum) • Paraglomus, Geosiphon, Acaulospora spp. (A. delicata, A. foveate, Sclerocystis clavispora, A. scrobiculata) • Archaeospora, Scutellospora spp. (S. scutata, S. erythropa, S. calospora) • Ectomycorrhiza (Pisolithus tinctorius, Amanita sp., Tuber sp., Lactarius sp., Elaphomyces sp., Pisolithus sp., Piriformospora indica, Cenococcum sp., Rhizopogon sp.) • Entrophospora, Gerdemannia, Gigaspora (Gigaspora rosea) Phosphorus solubilizing biofertilizer • Aspergillus spp. (A. tubingensis/A. niger/A. terreus/A. awamori/A. fumigatus/A. tubingensis/A. melleus) • Penicillium spp. (P. rubrum/P. expansum/P. citrinum, P. simplicissimum/P. frequentans/P. oxalicum/P. bilaji/P. albidum/P. italicum) • Trichoderma spp. (T. virens/T. asperellum, T. viride/T. harzianum) • Fusarium spp. (F. moniliforme/F. udam) • Mucor spp. (M. ramosissimus/M. mucedo/M. hiemalis) • Candida spp. (C. scotti, C. krissii) • Tritirachium spp. (T. album/T. egenum) Biofertilizer enriching compost • Trichoderma spp. (T. virens/T. asperellum, T. viride/T. harzianum) • Aspergillus spp. (A. terreus/A. awamori/A. fumigatus, A. tubingensis/A. niger) • Pleurotus spp. (P. ostreatus/P. flabellatus) • Fusarium spp. (F. solani/F. oxysporum) • Chaetomium spp. (C. bostrychodes, C. olivaceum)

Table 1.1  Fungal biofertilizers for crop protection and sustainable agriculture

Manoharachary et al. (2005) Singh and Singh (2008) Whitelaw (1999) Harman et al. (2004) Of (2009), Pal et al. (2015)

Manoharachary et al. (2005) Menon and Mohan (2007) Burton and Knight (2005) Harman et al. (2004) Manoharachary et al. (2005) Of (2009) Pal et al. (2015)

Adholeya et al. (2005) da Silva (2006) Rai et al. (2013) Anderson and Cairney (2007), Pal et al. (2015)

Lian et al. (2008) Alves et al. (2010)

Reference Martino et al. (2003) Franz et al. (1991) Martino et al. (2003) Wold and Suzuki (1976)

6 P. Selvasekaran and R. Chidambaram

1  Agriculturally Important Fungi for Crop Protection

7

Table 1.2  Fungal communities as biocontrol agents against plant species S. No. Fungi 1. Pichia guilliermondii 2. Pichia membranifaciens 3. 4. 5. 6. 7. 8.

9. 10. 11.

12. 13.

14. 15.

Plant species Glycine max Vitis vinifera

Reference

Santos and Marquina (2004) Candida oleophila Vitis vinifera Porat et al. (2003) Lentinus conatus Arachis hypogaea Lakshmanan et al. (2008) Penicillium roqueforti; Penicillium viridicatum Allium cepa Khokhar et al. (2013) Streptomyces lydicus WYEC108 P. sativum Yuan and Crawford (1995) Trichoderma asperellum Tv5SC, T. harzianum Helianthus annuus, Prasad (2015) Th4d SC Ricinus communis Capsicum annuum Rahman et al. Trichoderma virens IMI-392430, T. (2012) pseudokoningii IMI-392431, T. harzianum IMI-392432, T. harzianum IMI-392433, T. harzianum IMI-392434 Trichoderma koningii, Trichoderma Pisum sativum Nelson et al. harzianum (1988) Pichia angusta Malus domestica Fiori et al. (2008) Alam et al. (2011) Penicillium sp. EU0013 Solanum lycopersicum; Brassica oleracea Leucosporidium scottii At 17 Malus domestica Vero et al. (2013) Penicillium citrinum VFI-51 Sorghum bicolor Meesala and Subramaniam (2016) Saccharomycopsis schoenii Citrus X sinensis Hashem et al. (2012) Penicillium adametzioides Vitis vinifera Ahmed et al. (2015)

1.4  Fungal Endophytes The efficient and new biological control agents used for the control of pathogens and insects and the bioremediation of the environment are fungal endophytes (Guo et al. 2008). The evidence shows that the fungal endophytes play a significant role in protecting the host from the disease, supporting plant health and plant physiology. Fungal endophytes obtain nutrition, propagation opportunities, protection and shelter from their host by internal plant tissue colonization. This symbiotic relationship helps the host by promoting the overall health and reducing environmental sensitivity. The best offer to the control of chemical disease is the use of endophytes (Yao et al. 2017). To control the plant diseases these biocontrol agents utilize direct and indirect strategies by promoting the accumulation of bioactive compounds, increasing tolerance against stress, and enhancing fitness. An in-depth

8

P. Selvasekaran and R. Chidambaram

understanding of the mechanism involved in the association of plants and fungal endophytes is of major interest to optimize the efficacy as well as for the registration of products that are used for plant protection (Rana et al. 2019a; Suman et al. 2016; Yadav et al. 2018). The possible mechanism that is considered to be adopted by the fungal endophytes against the pathogens may be mycoparasitism, induction, antibiosis, direct and indirect inhibition, competition, and improvement of host plant resistance (Yu et al. 2010; Nisa et al. 2015; Gautam and Avasthi 2019). The aspects that are involved in the control of disease by these biocontrol agents are discussed below.

1.4.1  Direct Mechanism Recent studies have proved the ability of the fungal endophytes to protect the host plant from various diseases and damages due to the activity of plant pathogenic microorganisms. The fungal endophytes produce bioactive compounds which have the potential to inhibit the growth of pathogenic microorganism directly. Some researchers have proposed a few possible mechanisms by the use of fungal endophytes and their secondary metabolites to suppress the pathogens (Yadav et  al. 2017b, c). However, the knowledge on the mechanism between plant, endophyte, and pathogen is to be explored further. In direct mechanism fungal endophytes secrete lytic enzymes and produce antibiotics or the pathogens are directly suppressed through antibiosis, mycoparasitism, and competition (Bamisile et al. 2018; Mejía et al. 2008; Ganley et al. 2008; Gautam and Avasthi 2019). 1.4.1.1  Mycoparasitism Few endophytes exhibit hyper parasitism distinct from antibiosis and competition. The plant pathogenic fungi are often attacked by these fungi that act as mycoparasites either to inhibit or suppress their growth. One of the most popular examples of mycoparasitism is Trichoderma. Prior to making any contact, Trichoderma detects the fungal pathogen and the extracellular exochitinase is produced in lower levels and discharges the oligomers of cell wall from the target fungus (Harman et  al. 2004). This mechanism initiates the Trichoderma to release toxic endochitinase that can degrade the target plant-fungal pathogen. The hyphae of the plant pathogens including Rhizoctonia solani is parasitized by the Trichoderma species (Grosch et al. 2006). A novel endophytic fungus Acremonium strictum isolated from Dactylis glomerate has been reported (Rivera-Varas et al. 2007) for the activity of mycoparasitism against Helminthosporium solani. In the process of mycoparasitism the binding of chemical compounds between the host fungus and mycoparasite occurs initially. One such example is binding of lecithin in the cell wall of the host fungi to the carbohydrate present in the cell wall of Trichoderma. Later the establishment of contact with the host fungus is inhabited by the hyphae of the mycoparasite. Several

1  Agriculturally Important Fungi for Crop Protection

9

lytic enzymes are involved along with the mechanisms in the cell wall degradation of the host fungi (Cao et al. 2009). These findings have proven that the pest damage in the agricultural crops can be limited by the mycoparasitic activity of the endophytic fungi and can prove to be a potential alternative to the use of chemical pesticides (Gautam and Avasthi 2019). 1.4.1.2  Competition One of the important methods used by the fungal endophytes against the proliferation and infection of the plant pathogen is competition. This process involves competition between the endophytic fungi and pathogens for space and few common resources (Mejía et al. 2008). Few endophytic organisms can control plant pathogens involving such mechanisms and they could be used as an effective biocontrol agent against the plant disease. The effect on traditional rice varieties by the most frequently isolated endophytic fungi on the growth of plant and incidence of blast disease was evaluated by Atugala and Deshappriya (2015). The study concluded that a range of mechanisms of antagonistic activity was utilized by the endophytic fungi including the competition for antibiosis, substrate, and mycoparasitism. Studies across the world (Atugala and Deshappriya 2015; Mejía et  al. 2008; Richmond 2004) demonstrated the use of endophytic fungi as a management strategy against numerous harmful pathogens (Gautam and Avasthi 2019). 1.4.1.3  Antibiosis A wide spectrum of secondary metabolites is produced by fungal endophytes with the ability to reduce the attacks from various pests and insects. These fungi possess antibacterial, antifungal as well as insecticidal properties that strongly inhibit the growth of plant pathogens and infectious microorganisms (Gautam et al. 2013). The single or multiple kinds of antibiotics which has been proven to be effective has been reported to be produced by single fungus including aromatic compounds, polypeptides, terpenoids, and alkaloids. Researchers (Mejía et al. 2008; Wei et al. 2007) have been carrying out the examination of antibiotic compounds produced by endophytic fungi and have proven that the plants inoculated with endophytic fungi induce the defense mechanism in the host plant. It has been determined that the cultures of endophytic fungi possess the antibiotic properties against several plant pathogens after a series of tests involving liquid broths of endophytic fungi. It was also reported by Atugala and Deshappriya (2015); Kim et al. (2007); Wessels (1999) that the proteins secreted by the species of endophytic fungi act as a protein related with pathogenicity to suppress the activity of plant pathogens by degrading the cell wall. Several studies reported that various chemical compounds are produced with the antibiotic property against pathogens by the fungal endophytes. The examination of the interaction between the endophytic fungi and Puccinia recondite f. sp. tritici was done by Dingle and McGee (2003) and found that the leaf rust disease

10

P. Selvasekaran and R. Chidambaram

caused by this fungus was suppressed by the fungal endophytes. An endophytic fungus Phomopsis cassiae isolated from Cassia spectabilis (Lu et al. 2000a) secretes a chemical compound 3,11,12-trihydroxycadalene which was found to be effective against Cladosporium Cladosporioides and Cladosporium sphaerospermum. The antifungal activities of 183 endophytic fungi isolated from 15 plant species from 15 locations in Korea against pathogens causing rice sheath blight disease, tomato gray mold disease, rice blast disease, wheat leaf rust disease, tomato late blight disease and barley powdery mildew diseases such as Corticium sasakii, Botrytis cinerea, Magnaporthe grisea, P. recondita, and Blumeria graminis f. sp. hordei, respectively, were evaluated by Park et al. (2003). In another study examination of woody angiosperm Theobroma cacao associated with fungal endophytes against foliar pathogen sp was done (Arnold et al. 2003) and the study revealed that inoculation of leaf tissues by the assemblage of endophytic fungi that are isolated from asymptomatic and infected host limited the damage caused by a significant foliar pathogen (Gautam and Avasthi 2019).

1.4.2  Indirect Mechanism The association of plants with fungal endophytes has a direct impact on the growth and development of the host plant. The host performance is affected in terms of morphology, growth, physiology, and biochemistry. The important reason for the improvement of host health is due to the production of secondary metabolites by these fungi along with the establishment of a symbiotic relationship (Kaur et  al. 2020; Singh et al. 2020; Yadav et al. 2019a). The association of endophytic mycobiota with the host plant is believed to be responsible for the fate of pathogen attack (Wei et al. 2007; Vyas and Bansal 2018). These beneficial microbes can decrease the disease incidence, plant stress, increase the efficiency of nitrogen fixation, improve the nutrient uptake, growth rate of the shoot and root, and improve resistance (Liu et al. 2001; Kuldau and Bacon 2008). These properties of fungal endophytes can be used to play an essential role in the field of food safety, agriculture, and maintenance of environmental equilibrium (Rana et  al. 2020). The indirect mechanism adapted by fungal endophytes in the control of pest and disease is given below. 1.4.2.1  Production of Metabolites In the adaption of plants to biotic and abiotic stresses, the plant-fungal symbiotic association plays an important role by the production of secondary metabolites (Yadav 2019a). The significant factor in the production of various metabolites is the association between plants and endophytic fungi. The environmental and eco-­ friendly approach to control various plant diseases is the use of endophytic fungi (Rana et al. 2019a, b). The host plant is benefited by the endophytic fungi as they

1  Agriculturally Important Fungi for Crop Protection

11

Table 1.3  Bioactive compounds produced by fungal endophytes Fungal endophyte Cladosporium delicatulum

Balansia obtecta

Bioactive compounds Plumbagin (5-hydroxyl-2-methylnaptalene-1,4-­ dione) Ergobalancine

Melanconium betulinum

3-hydroxypropionic acid

Phomopsis phaseoli

3-hydroxypropionic acid

Neotyphodium coenophialum

Ergovaline

Acremonium coenophialum

Chitinases

Neotyphodium sp. Fusarium redolens

Ergonovine Peimisine and imperialine-3β-D-glucoside fumiclavine, A, fumiclavine B, fumiclavine C and Chanoclavine aldehyde Piperine

Aspergillus fumigatus

Colletotrichum gloeosporioides Rhinocladiella sp., Helminthosporium sp., Chalara sp., Phoma sp., Hypoxylon sp., Phomopsis sp., Xylaria sp. Xylaria sp. YX-28 Penicillium sp. Ampelomyces sp. Morinia pestalozzioides

Bioactive cytochalasines

7-amino-4-methylcoumarin Berkeleydione O-methyl alaternin and altersolanol A Moriniafungin

Pestalotiopsis adusta Periconia sp. Chaetomium chiversii C5-36-62

Aurasperone A, fonsecinone A, asperpyrone B, rubrofusarin B Pestalachlorides Periconicin A Radicicol

Pestalotiopsis jester

Hydroxyjesterone, jesterone

Muscodor albus

1-Butano, 3-methylacetate

Pestalotiopsis microspora

Ambuic acid

Colletotrichum gloeosporioides Epichloe festucae

Colletotric acid Cyclonerodiol, IAA, diacetamide, IEtOH, indole-3-carboxaldehyde, methylindole-3-carboxylate

Aspergillus niger

Reference Venkateswarulu et al. (2018) Tintjer and Rudgers (2006) Chomcheon et al. (2005) Chomcheon et al. (2005) Tintjer and Rudgers (2006) Gautam and Avasthi (2019) Miles et al. (1996) Pan et al. (2015) Panaccione (2005)

Chithra et al. (2014) Isaka et al. (2001)

Xu et al. (2008) Davis et al. (2005) Miller et al. (1998) Gautam and Avasthi (2019) Song et al. (2004) Li et al. (2008) Kim et al. (2004) Turbyville et al. (2006) Li and Strobel (2001) Strobel and Daisy (2003) Li and Strobel (2001) Zou et al. (2000) Yue et al. (2000)

12

P. Selvasekaran and R. Chidambaram

prevent the colonization of pathogenic organisms (Arnold et al. 2003). It has been reported that fungal endophytes secrete a few chemical compounds that inhibit the plant pathogenic fungi based on the experimental studies. The endophytes isolated from the medicinal plants have cytotoxic metabolites, a fungicidal and bactericidal activity which can produce secondary metabolites in the tissue of the host and kill the pathogens (Zhang et al. 2006). It has been reported that the endophytic fungi produce secondary metabolites to protect the host plant from disease and pest (Sudha et  al. 2016). These bioactive compounds serve as mediators for specific communication and interaction with the host plant. The competition, fitness, and growth of the host plant are triggered by the endopytic fungi upon production of the secondary metabolites that inhibit the pathogens. These metabolites are categorized into flavonoids, quinones, chinones, saponins, xanthones, phenolic acid, alkaloids, tetralones, benzopyranones, tannins, and several others. The research on the secondary metabolites and their antipathogenic effects produced by the endophytic fungi to explore their application as a biocontrol agent in various fields has been conducted worldwide. It was reported that Fusarium spp. E4 and E5 promoted the content of terpenoids and the growth of Euphorbia pekinensis (Gautam and Avasthi 2019). Another study reported (Strobel and Daisy 2003) the production of 25–28 volatile compounds by an endophytic fungi Muscodor albus, isolated from the branches of Cinnamomum zeylanicum. These volatile compounds are capable of inhibiting the selected bacteria and fungi. Another endophytic fungus Muscodor crispans of Ananas ananassoides produces a mixture of volatile compounds containing an antibacterial and antifungal property with inhibitory effect against pathogenic fungi such as Botrytis cinerea, P. palmivora, Pythium ultimum, Fusarium culmorum, Alternaria helianthi, Rhizoctonia solani, Verticillium dahliae, and bacteria including Xanthomonas axonopodis (Yuan et  al. 2017). Currently, researchers are investigating the endophytic fungi production of secondary metabolites which can inhibit the insects (Gautam and Avasthi 2019) (Table 1.3). 1.4.2.2  Growth of Root and Shoot In the process of plant growth, the plant host and mutualistic organisms producing compounds that regulate the growth of the plant and antimicrobial substances are asymptomatically colonized by the endophytic fungi to enhance the competitiveness, growth, and fitness of the host in nature (Sudha et al. 2016). These fungi help the host plant in phosphate solubilization whereas the plant provides food and shelter. These fungi also help to enhance the uptake of phosphorus, nitrogen fixation, production of siderophores including several other plant hormones such as gibberellins, auxin, ethylene, abscisins, and IAA which are important for the regulation of plant growth (Boddey et  al. 2003; Firáková et  al. 2007). Hamayun et  al. (2009) examined the endophyte Cladosporium sphaerospermum isolated from Glycine max for the production of bioactive molecules that promote plant growth. The study revealed that Cladosporium sphaerospermum produces GA3, GA4, and GA7 growth hormones that are associated with inducing the plant growth in soybean and rice. It was reported (Khan et  al. 2013) that the endophytic fungi Fusarium

1  Agriculturally Important Fungi for Crop Protection

13

tricinctum and Alternaria alternata produce the derivatives of indole acetic acid that promote the plant growth. In another study by Li and Zhang (2015) an apestalotin analogue was characterized by Pestalotiopsis microspora. The research revealed that the germination rate of Distylium chinense was significantly increased by Pestalotin a study conducted on the root colonizing endophytic fungus Piriformospora indica,  by Johnson et  al. (2014) revealed that the association of fungi with the root modulates the growth-promoting phytohormones, develops the host plant, and enhances the uptake of essential nutrients and translocation. The height and weight of plants along with other growth-promoting parameters such as weight of roots and shoots are also influenced through the colonization with the endophytic fungi (Lopez and Sword 2015). It is known that the plant growth can be actively or passively developed by the endophytic fungi through various mechanisms such as biochemical and molecular mechanisms. However, the mechanisms underlying the habitat adapted symbiotic relationship and high stress tolerance of plant remains unknown (Gautam and Avasthi 2019). 1.4.2.3  Improvement of Physiological Function The mechanism of plant defense against the phytopathogenic organisms is promoted by the fungal endophytes through the enhancement of plant growth. The host plant can survive various biotic and abiotic stresses by colonization with endophytes. In many studies, the enhancement of physiological processes of the host plans was noted (Yong et al. 2009). The phytohormones that may influence physiological functions of plants produced by fungal endophytes are also demonstrated in many studies. The defense response of the host plant is found to be enhanced by the fungal endophytes. However, more energy is required to increase defense responses. The endophytic colonization of the host plant improves the uptake of nitrogen, phosphorus, and other essential nutrients and enhances the metabolic activity such as physiological functions and increases the growth of plant (Bolton 2009). The compounds that interfere in the cell division of plant are also produced by the endophytic fungi. The substances like IAA that are known to regulate plant processes are produced by an endophytic fungus, Colletotrichum sp. in Artemisia annua (Lu et al. 2000b). Dai et al. (2008) studied the influence of the Fusarium sp. an endophytic fungus on the growth of Euphorbia pekinensis and the extract obtained from this fungus functions as an auxin. The growth of the host plant is influenced due to this phytohormone effect. Nitrogen fixation is one of the important functions performed by the endophytic fungi to their host. The impact of Phomopsis liquidambaris on N dynamics in rice was investigated by Yang et al. (2015) and it was found that the available nitrate and ammonium present in the rhizosphere soil of the endophytic fungi under low N conditions significantly infect rice. The ability to suppress the soil nitrification by the endophytic fungi was also reported. The potential of Brachiaria species to increase the nitrification of soil was observed by Cardoso et  al. (2017) due to the release of an inhibitory compound called brachialactone from the roots of the plant growing with the endophytic association.

14

P. Selvasekaran and R. Chidambaram

1.4.2.4  Plant Stress Reduction The endophytic fungi were found to enhance the tolerance of plants to abiotic stresses in addition to increasing the fitness, competitiveness, and growth of the host plants (Aly et al. 2011). The endophytic colonization of fungi supports and protects plants to tolerate the environment under high stress such as high temperature, salt, and drought (Rodriguez et al. 2008). The fitness of the plants such as Dichanthelium lanuginosum is increased by the presence of endophytic fungi in the areas with high soil temperature. The endophytic fungi promote tolerance against water stress, salt stress, and high soil temperature (Bartels et al. 2002). Therefore, such symbiosis is considered of great significance in helping the plants to tolerate and adapt globe climatic change (Selim 2012). Such beneficial potential of endophytic fungi on plants has increased interest to improve the production of crop plants by the use of endophytic microbes (Kour et al. 2020c). However, the mechanism of the symbiotic interaction resulting in the ability of the plant to tolerate high stress is not studied in depth. The colonization of fungal endophytes with the tissues of the plant enhances the ability to adapt stresses based on habitat (Murphy et al. 2015). The grasses obtained from coastal beaches in the United States such as Dicanthium lanuginosum and Leymus mollis were reported to grow in geothermal soils due to their symbiotic relationship with fungal endophytes Curvularia protuberata and Fusarium culmorum, respectively, which confers tolerance towards heat and salt (Rodriguez et al. 2008; Gautam and Avasthi 2019). 1.4.2.5  An Improvement of Plant Resistance The endophytic fungi also possess the capability to induce disease resistance. Several mechanisms behind these resistances were proposed such as improved nutrient uptake, root growth, and nitrogen fixation. The decrease in the plant stress has a direct impact on the growth as well as the development of the host plants and enables them to resist the phytopathogens (Sudha et al. 2016; Bae et al. 2009). The toxic compounds produced by certain plants with endophytic colonization are reported to be effective as a pest repellent (Akello et al. 2007). The process of competition and production of biocidal compounds or phytoalexins can improve the resistance of the host plants colonized with the fungal endophytes and their molecular studies showed significant changes in the metabolism of the plant such as biochemical production which induces the mechanism of defense and resistance against the pathogen. During the endophytism certain protein that acts as pathogenicity related proteins is produced that are reported to suppress the activity of plant pathogen (Li et al. 2004). The promotion of plant growth enhanced by the fungal endophytes is another benefit that enhances the capacity of the plant to develop resistance against various pathogens. The study on the ability of fungal endophytes to induce resistance among host plants was done by many researchers. The barley plants are reported to be resistant against Blumeria graminis, Fusarium culmorum, leaf and vascular pathogens that are inoculated with Piriformospora indica. They also

1  Agriculturally Important Fungi for Crop Protection

15

exhibited an increase in tolerance towards salt stress. The endophytic fungi such as Colletotrichum sp. and Cryptosporiopsis cf. quercina are reported to be effective against various phytopathogens such as Gaeumannomyces graminis, Rhizoctonia cerealis, Pyricularia oryzae, and Phytophthora capsici (Lu et  al. 2000b). The Festuca rubra L., when inoculated with the endophyte Epichloe festucae the induced resistance was observed against Sclerotinia homoeocarpa which causes dollar spot disease (Clarke et al. 2006).

1.4.3  T  he Advantages of Fungal Endophytes Over Chemical Methods • The genetic resistance against numerous plant pathogens is developed by colonization with fungal endophytes. Hence, the requirement for the use of chemical pesticides to prevent and control numerous foliar phytopathogens that have a high rate of sporulation is reduced. They are well suited for widespread dissemination as airborne propagules. • The beneficial microbes are affected by the use of synthetic chemicals although they inhibit pathogens. During the treatment with pesticide, the effective root nodule formation with the nitrogen-fixing bacteria is decreased and inhibited. This proves endophytic fungi as a potential alternative over synthetic chemicals. • The systemic fungicide increases the chance of fungicide resistance by pathogens though they help in the control of plant pathogens. The fungal endophytes manage these pathogens in a better way and reduce the development of resistance by pathogens. • The requirement of farmers on the synthetic chemical is reduced by the use of fungal endophytes thereby reducing the exposure of user and environment to the synthetic chemicals that are harmful. • The use of endophytic fungi as a biocontrol agent, an eco-friendly and cost-­ effective method when compared to all the other methods. The cultivation of eco-friendly fungi, their handling is easy and environmentally friendly (Gautam and Avasthi 2019).

1.5  Arbuscular Mycorrhizae and Its Role in Agriculture The term mycorrhizae was derived from the Greek words mycos and rhiza which means fungus and root, respectively (Wang and Qiu 2006). Mycorrhiza is categorized into arbuscular, ectendo, ecto, ericoid, abutoid, monotropoid, and orchid mycorrhiza. One of the most effective microorganisms involved in the stabilization of soil structure is Arbuscular mycorrhiza (SWABY 1949; Miller and Jastrow 2000). They are economically important types of microorganisms and are exploited

16

P. Selvasekaran and R. Chidambaram

commercially in forestry and agriculture. Arbuscular mycorrhiza is a monophyletic lineage of obligate mycobionts (Schwarzott et al. 2001). They form symbiotic associations with plant roots belonging to phylum Glomeromycota (Owen et al. 2015). About 80–90% of extant plant species are mycorrhizal as phylum is an ancient form of symbiosis in plants. Mycorrhiza penetrates the root cell walls of plants and develops arbuscules, hypae, and vesicles (intra-radical structures) in the cortical cells of the host and hyphae and spores (extra radical structures) in soil. Bidirectional flux characterizes the mutualistic association whereas the acquisition of soil nutrients in phytobiont is enhanced by mycobiont while the phytobiont provides carbon sources (photo assimilates) to the mycobiont (Buscot et al. 2000; Brundrett 2009). The ability of Arbuscular fungi to form hyphae for nutrient uptake with highly favorable surface area to volume ratio and to secrete enzymes and organic acids is due to the mutualistic association (Owen et al. 2015). The interaction between plants and microbes has a major impact on the functioning of the plant and ecology of the plant community (Boon et al. 2014; Vimal et al. 2017). Mycorrhiza along with plant root hairs increases soil-root contact area as they are the vital components at the soil–root interface through their extra radical hyphae. Hence, they improve plant nutrient uptake mainly phosphate (Jakobsen et al. 2005; Bucher 2007), iron (Treeby and Bag 1992), calcium (Azcón and Barea 1992), manganese, nitrogen, and zinc. Arbuscular mycorrhiza is also beneficial to improve the nutrient acquisition of plants in soils with a low fertility rate. They serve as a substitute for reduced fertilizer input and lead to sustainable agriculture (Galvez et al. 2001). The beneficial attributes to host by Arbuscular mycorrhiza include: • Increased plant tolerance to salinity, drought, and metal pollution (abiotic stress) and pathogenic infection, herbivory (biotic stress) (Augé 2004) • Increases plant growth and development by improving the rooting of micro-­ propagated plantlets. • They contribute to plant nutrition acquisition by influencing the chemical and microbial ecology of the mycorrhizosphere (Azcón and Barea 1992) • In a disturbed ecosystem, they help to improve energy flow, nutrient cycling, and plant establishment. • The symbiosis by Arbuscular mycorrhiza fungi helps to stimulate the synthesis of secondary plant metabolites which are essential for the plants to tolerate environmental induced stresses and beneficial to human beings through their antioxidant activity and protective nutrient compounds. • They enhance plant diversity as they interconnect several individual and unrelated plant species • Arbuscular mycorrhiza enhances the soil bioremediation as they are involved in phytoremediation-use of plants for the uptake of pollutants. They are beneficial in revegetation and restoration of contaminated and disturbed areas as they help in alleviating toxicity of metals to plants by reducing the translocation of metal from the root to shoot.

1  Agriculturally Important Fungi for Crop Protection

17

• Arbuscular mycorrhizal fungal hyphae improve the soil stability, water retention, and binding property through the extra radical mycelial network and secretion of glomalin which is a hydrophobic proteinaceous substance.

1.6  Penicillium and Its Role as Plant Growth Promotion Penicillium as an ascomycetous fungus is a genus which is significant for the production of food and drug in the environment. In the human body, the antibiotic penicillin produced by Penicillium restricts the spreading of certain bacteria. Penicillium belongs phylogenetically to Trichocomaceae and is an anamorph genus (Berbee et al. 1995; Samson 2016). The name Penicillium is derived from the word penicillus which means little brush. It has been reported that Penicillium spp. intermingles with the roots of plants and crops to enhance their growth (Shivanna et al. 1994; Khan et  al. 2008). Several plant hormones such as gibberellins (GA), indole-3-­ acetic acid (IAA) are secreted by this fungus and are involved in phosphate solubilization (Khan et al. 2008, 2011; Radhakrishnan et al. 2013). Penicillium species are widely spread in nature across various soil environments such as dessert soil, cultivated soil, beach soil, forest soil, and marine habitats (Chandanie et al. 2006). Penicillium species are of great interest to researchers as they secrete herbicides, insecticides, antibiotics, mycotoxins, antioxidants, anticancer compounds, and extracellular enzymes (Munns and Tester 2008). The production of phytohormones such as gibberellins, auxin, cytokinin, solubilization of minerals and antagonism against phytopathogens are the key mechanism involved in promoting plant growth by Penicillium species (Volpin et al. 1995). The phosphorus uptake, growth, and yield of several crops such as pomegranate, sesame, and wheat are promoted by the inoculation of Penicillium species with PGP in soil. The upregulation of IAA which is a plant growth-promoting phytohormone during stress conditions promotes plant growth (Faeth and Fagan 2002). It has been reported that under oxidative stress Sesamum indicum L. treated with Penicillium showed a significant increase in IAA. The species of Penicillium and Phoma glomerata produce gibberellins and IAA to promote the growth of the host plant under the condition of abiotic stress. The phytohormone gibberellins regulate various physiological processes such as fruit set, floral development, flowering, seed germination, and shoot growth (Khan et al. 2011). The level of GA is increased in host plants with the help of the endophytic Penicillium population under abiotic stresses such as heat, heavy metals, and salinity. The production of GA by various species of Penicillium has been reported such as P. funiculosum under drought and salinity (Waqas et al. 2012), P. janthinellum LK5 under the stress of cadmium toxicity (Khan et al. 2013), and P. resedanum under drought, heat, and salinity (Khan et al. 2013).

18

P. Selvasekaran and R. Chidambaram

1.6.1  The Role of Penicillium Under Abiotic Conditions The tolerance of host plants against various pathogens and metal toxicity is provided by Penicillium. The tolerance in host plants against metal toxicity can be enhanced by different strains of Penicillium. The strains of Penicillium simplicissimum and Penicillium janthinellum synthesize citric acid and are known to reduce zinc and aluminum toxicity (Zhang et al. 2002). Similarly, the cadmium content is reduced by the strains of Penicillium species obtained from the polluted industrial sediments (Massaccesi et al. 2002). Studies on the potential of Solanum lycopersicum against cadmium toxicity proved that the metal toxicity can be mitigated by Penicillium species by the synthesis of enzymes and various other bioactive metabolites. Plants under cadmium stress are addressed through the complexation and compartmentation (Mazid et al. 2011). Sulfur is one of the most significant nutrients for plants along with a component of glutathione which is considered to be active in the detoxification of heavy metals (Howden et  al. 1995). Under the exposure to cadmium and Pencillium, the glutathione and the sulfur content of the root increased. The sulfur content is enhanced by treatment with Penicillium that increases the synthesis of glutathione required for the synthesis of phytochelatin (Rüegsegger et al. 1990). The calcium content under cadmium stress increases by the treatment of Penicillium. In the plant growth, calcium plays an essential role and is a key molecule in the signal transduction under biotic and abiotic stress conditions (White and Broadley 2003). The plants need to reduce the peroxidation of lipids in the cell membrane and enhance their capacity to intake nutrients and antioxidant activities to reduce the effects of metal toxicity and to increase the plant yield (Siddiqui et al. 2011). The potential of antioxidant activity of plants against cadmium is stimulated by the Penicillium janthinellum and lowers the content of cadmium in roots as well as protects the plant from electrolytic leakage induced by cadmium. The plant generates ROS due to the membrane damage caused by the cadmium injury and releases the product MDA resulting in from the breakdown of aldehydic lipid in the membrane. The plants treated with Penicillium during cadmium stress have significantly less MDA indicating less injury to the functional membrane. Studies have shown that osmotic stress is induced by drought and salinity stress which is transmitted through the abscisic acid-dependent and the abscisic acid-independent pathways (Mauch-Mani and Mauch 2005; Cao et al. 2014). It has been observed that the synthesis of abscisic acid is low under stress and fungal treatment (Hause et al. 2007; Jahromi et al. 2008). The minimum effort is required by plants for the synthesis of abscisic acid and to control the movement of the guard cell under stress conditions as the water balance in the plant can be improved by Penicillium treatment. The exposure of the plant to stresses like cold and drought significantly increases the expression of the RAB18 gene while the heat shock suppresses the gene. However, in Penicillium-treated and salinity-stressed plant the mRNA of RAB18 accumulation is noted.

1  Agriculturally Important Fungi for Crop Protection

19

Table 1.4  The role of Penicillium species against abiotic stress Penicillium species P. funiculosum

Abiotic stress Copper Salinity

Penicillium sp. LWL3

Drought and salinity

P. resedanum Osmotic LK6 stress

P. minioluteum LHL09 Penicillium spp.

Salinity

Salinity

P. Cadmium janthinellum

Steps in stress mitigation Potassium plays a significant role in the oxidative stress response and helps the synthesis of glutathione associated with the stress tolerance. Increased level of calcium, potassium, and phosphorus Lower content of abscisic acid and higher content of GA and IAA. The vegetative growth through GA is promoted by fungal association whereas IAA promotes the plant growth regulation The higher level of gibberellin and indole acetic acid is exhibited by the culture filtrates of Penicillium. The host plant had increased plant height, shoot length, increased biomass and chlorophyll content Lower level of superoxide anion formation and lipid peroxidation and higher levels of catalase, peroxidase, glutathione, and polyphenol indicated lower injury of membrane in plants associated with Penicillium as the plants had minimum lipid peroxidation and electrolytic leakage Increase in the secretion of GA4 and GA7 and decrease in the production of abscisic acid Sesame seeds treated with Penicillium had increased root growth of seedling due to the amino acid present in the culture medium Plants inoculated with Penicillium had higher stomatal conductance. Higher content of catalase, glutathione, and ABA. Elimination of ROS during the response of plant to Cd stress involves the enzyme catalase

Plant source Soybean Soybean

Reference Khan et al. (2011) Khan and Lee (2013)

Cucumber Waqas et al. (2012)

Capsicum annuum

Khan et al. (2013)

Soyabean

Mazid et al. (2011)

Arachis hypogaea

Radhakrishnan et al. (2013)

Tomato

Khan and Lee (2013)

The interaction of fungi and the production of phytohormone GA might have activated the expression of RAB18 (Ghelis et al. 2000). Similarly, the same results had been noted by the exogenous abscisic acid-induced RAB18 in the abscisic acid mutant of Arabidopsis thaliana (Ghelis et al. 2000). In plants treated with Penicillium the upregulation of RAB18 under salinity stress is due to the anionic channel activation during stomatal closure as confirmed by the increased ionic flux (Bray et al. 2000). The accumulation of abscisic acid is correlated with the increased

20

P. Selvasekaran and R. Chidambaram

Table 1.5  The mechanism involved in the suppression of plant pathogens by Trichoderma species Trichoderma sp. T. virens “Q” strain

Biocontrol factors Induction of plant phytoalexin by antibiotic compound, gliovirin

Target organism Pythium/Rhizopus oryzae

BAFC 742, T. harzianum

Chitinase and β-1,3-Glucanase

BAFC2232, Sclerotinia sclerotianum Pythium ultimum, Rhizoctonia solani, Meloidogyne incognita Serpula lacrymans

T. harzianum T-203, Antibiotics gliotoxin and gliovirin T. virens isolate GL3 and other inhibitory metabolites and GL21 T. harzianum 25, T. viride T. pseudokoningii, T. harzianum, T. virens, T. lignorum, T. hamatum T. viridae, T. harzianum

T. harzianum 1051, T. harzianum 39.1

Antibiotics and anthraquinones Unknown inhibitory substance, metabolites, antibiotics, extracellular or action of lytic enzyme Cellulolytic, proteolytic, lipolytic and pectinolytic enzyme. Unknown antibiotic compounds such as peptides and cyclic polypeptides N-acetylglucosaminidase, chitinase, total cellulase, endoglucanase,aryl-­ β-­glucosidase, protease, and amylase

Rhizoctonia solani

Disease Cotton seedling disease Fungal-­ soybean plant Damping-­ off of cucumber Fungal wood decay Damping-­ off of bean

Aspergillus flavus and Fungal seed associated Fusarium moniliforme Crinipellis perniciosa Witches’ broom disease of cocoa

electrolytic flux which causes a reduction in the elongation of shoot, rate of photosynthesis, chlorophyll content, leaf area, development of flower and fruit. The treatment of plants with endophytic fungi P. janthinellum mitigates the negative effect as the plants synthesize abscisic acid in smaller amounts to deal with the stressful condition. This mechanism of growth promotion is related to the effects of exogenous GA3 treatment under stress (Hamayun et  al. 2010; Iqbal and Ashraf 2013) (Table 1.4).

1.7  Trichoderma for Sustainable Agriculture The species of Trichoderma suppresses the severity of disease by antagonizing the pathogens and improves the growth of the plant through different modes of actions through the combination of mechanisms such as the production of cell wall degrading enzymes, antibiotics, competition for growth production and key nutrients, stimulation of mechanism of plant defense, parasitism of host fungus, and induced systematic systemic resistance (Jayalakshmi et al. 2009).

1  Agriculturally Important Fungi for Crop Protection

21

1.7.1  Mycoparasitism Mycoparasitism is an effective mechanism and has long been involved in the suppression of pathogenic fungi by Trichoderma species (Vinale et al. 2013). The process of mycoparasitism is complex involving chemotrophic growth on the host by the antagonist, host recognition by the mycoparasite, attachment, and coiling of pathogen hyphae, excretion of extracellular enzymes followed by lysis and exploitation of host (Chet et al. 1990). The suppression of R. solani by T. lignorum was reported. The hyphal cell walls of the pathogen are lysed by enzymes such as Table 1.6  Volatile compounds and antibiotics produced by Trichoderma species Volatile compounds Β-1,3-glucanase Alamethicin, paracelsin, trichotoxin Succinic acid, heptelidic acid 6-n-Pentyl-2H-pyran-2one,6-n-pentyl-2H-pyran-2-one Trichorzianines, propionic acid, trichoviridin, 3-(3-isocyano-6-­ oxabicyclo(3,10)hex-2-eh-5yl) Chitin-1-4-b-chitobiosidase n-acetyl, b-d-glucosaminase, endochitinase Harzianolide(3-(2-hydroxyl-propyl))-4(hexa-2′-dienyl-2(5H00 furanone Harzianum A Harzianone Limonene Pachybasin Koninginin F Trichodermin Trichoviridin Trichodermol Trichosetin Viridin, gliotoxin Chitobiase Chitinase Protease Viridol, 9-epi-viridol Isomenthone, isopentyl acetate, menthone Octadecyl ester, arachidic acid, butyl ester, phenol, isopropyl myristate, acetic acid, acetone, bicyclohepatan-2-ol, butanoic acid, phenol, lindane, isopropyl ester, carbolic acid, 1-methylethyl ester

Reference Khan and Mohiddin (2018) Lumsden (1989) Howell et al. (1993) Claydon et al. (1991) Baldwin et al. (1981) Khan and Mohiddin (2018) Malmierca et al. (2012) Miao et al. (2012) Nemčovič et al. (2008) Liu et al. (2009) Song et al. (2010) Watts et al. (1988) Marquez et al. (1983) Reino et al. (2008) Marfori et al. (2002) Haggag and Mohamed (2002) Khan and Mohiddin (2018) Köhl et al. (2019) Köhl et al. (2019) Phuwapraisirisan et al. (2006) Polizzi et al. (2011) Siddiquee et al. (2012)

22

P. Selvasekaran and R. Chidambaram

proteases, chitinases, β-1,3-glucanases during the activity of mycoparasitism (De La Cruz et  al. 1992). The degradation of the cell wall, inhibition of mycelium growth, and spore germination of pathogenic plant fungi are associated with the properties of the enzyme, β-1,3-glucanases (Lin et al. 2007). The degradation of the pathogen cell wall and hyphal membranes and cell walls are reported (Grandgirard et al. 2002) to be associated with proteases produced by T. harzianum T-39. The hydrolytic enzymes, exogalacturonase, and endopolygalacturonase produced by Botrytis cinerea that reduces the severity of gray mold can be deactivated by the proteases. The mycoparasitic activity of Trichoderma species against plant pathogenic fungi was reported by Kotze et al. (2011) (Table 1.5).

1.7.2  Antibiosis The term antibiosis is defined as the process of inhibition and destruction of the microorganisms by the action of specific or non-specific substances and by the production of growth inhibiting antibiotics (Haggag and Mohamed 2007). Several species of Trichoderma and various other biological agents produce enormous antibiotics (Handelsman and Stabb 1996). The species of Trichoderma are also known to produce extracellular enzymes that are involved in biocontrol of plant pathogenic fungi (Monte 2001). It has been reported that T. lignorum produces a toxic substance called gliotoxin lethal to R. solani and Sclerotinia americana. But later it was found that gliotoxin was produced by Gliocladium virens and not T. lignorum (Webster and Lomas 1964). It has also been reported that the culture filtrate of T. harzianum inhibits the growth of F. longipes and F. solani by 74% and 60%, respectively. The produced toxins suppressed the disease development by affecting the spore germination (fungistasis) and causing mortality to the cells (antibiosis). Trichoderma species produces antibiotics such as harzianic acid (Vinale et  al. 2013), viridian (Zafari et  al. 2008), gliotoxin (Anitha and Murugesan 2005), viridiol (Phuwapraisirisan et  al. 2006), alamethicins (Aidemark et  al. 2010), and several others (Goulard et al. 1995). The process of action of these antibiotics is synergized by combining with the enzymes that degrade the cell wall and by producing a strong inhibitory effect on the pathogens (Vinale et  al. 2008). T. harzianum produces Trichotoxin A50 that is reported (Suwan et al. 2000) to inhibit the growth of mycelium and sporangium produced by P. palmivora. (Table 1.6) enlists the volatile compounds and antibiotics produced by Trichoderma species.

1  Agriculturally Important Fungi for Crop Protection

23

1.7.3  Competition and Competence of Rhizosphere An excellent competitor for nutritional resources and space is the species of Trichoderma. The displacement of the pathogen can be achieved by the competition between pathogens and the biocontrol agents. These species compete for food, essential elements in soil with other fungi. They modify the rhizosphere through acidification of soil and inhibit the growth of pathogens (Benítez et  al. 2004). Trichoderma species are either added to the soil directly or as seed treatments and grow spontaneously along with the developing root system thereby protecting the plant against pathogens (Howell et al. 2000). The colonization of Chondrostereum purpureum, the pathogen of plum trees was suppressed by T. viride (Corke and Hunter 1979). The determination of the antagonism expressed by various strains of Trichoderma spp against F. oxysporum and several other plant pathogens involves competition for carbon (Sivan 1989). The Fusarium species on several different crops were controlled by T. harzianum T-35 through nutrient competition and colonization of the rhizosphere (Viterbo et al. 2007). In the rhizosphere of cotton, the competition for carbon is involved in the suppression of F. oxysporum f. sp. melonis (Sivan 1989).

1.7.4  Enzyme Production Trichoderma species produces several different enzymes that play an important role in the disease suppression and growth promotion of plant (Mohiddin et al. 2010). The polysaccharides, glucans, and chitin that provide rigidity to fungal cell walls are broken by the enzymes produced by Trichoderma species and destroy the integrity of the cell wall. Metcalf and Wilson (2001) reported that endo and exochitinases produced by T. Koningii (Tr%) help in the penetration and destruction of the plant pathogen cells without harming the tissue of the plant. Trichoderma species also produce various hydrolytic enzymes such as β-1,3-glucanase, chitinase, and proteases as well as volatile and non-volatile antibiotics (Elad 1983). Elad and Kapat (1999) reported that the biocontrol of B. cinerea by the T. harzianum (T39) is due to the proteases that are produced by the T. harzianum. These proteases inactivate the production of hydrolytic enzymes by B. cinerea. The solution of protease produced by the biocontrol fungus partially deactivates the hydrolytic enzymes when applied to the bean leaves and reduces the severity of disease by 70–100%.

24

P. Selvasekaran and R. Chidambaram

1.7.5  Enhancement of Host Defense Response The important mechanism of disease suppression by Trichoderma spp. is the stimulation of host defense response (Harman 2006). The induction of resistance mechanisms such as hypersensitive response induced systematic resistance and systematic acquired resistance protects the plants from pathogens when the strains of Trichoderma are added to the rhizosphere (Haggag 2008). Induced resistance has been observed by De Meyer et al. (1998); Koike et al. (2001) with an unidentified Trichoderma sp. on cucumber, T. harzainum on bean, and T. virens on cotton. The seedlings of cotton treated with the strains of T. virens (Howell et al. 2000) had a higher level of compounds such as terpenoids that are related to the mechanism of defense and higher peroxidase activity in the roots of the host plant. The peroxidase activity induced by T. virens has also been reported (Howell et al. 2000) in the seedlings of cotton more than in the control experiment. The production of phytoalexin in the cells of grapevine (Calderón et al. 1993) is elicited by ethylene-inducing xylanase produced by the T. viride. The stimulation of significantly higher terpenoid levels in cotton was noted in the culture filtrates of few effective strains of T. virens and the elicitors are mostly glycoproteins or proteins (Hanson and Howell 2004). The root inoculation of the cucumber seedling which is 7-day old in an aseptic hydroponic system with T. harzianum has been reported (Yedidia et  al. 1999) to induce the response of defense in the leaves and roots of the treated plants. The activation of systematic acquired resistance in plants correlates with the expression of pathogenesis-related genes such as acidic and basic β-1,3-glucanase and chitinase which acts against the cell wall of plant pathogen (Ferreira et  al. 2007). The systematic resistance induced by Trichoderma species in plants is phenotypically similar to that of systematic acquired resistance (Yedidia et al. 2000). The cellulase and xylanase derived from Trichoderma are well known in inducing the biosynthesis of ethylene (Martinez et al. 2001). The high activity of phenylalanine ammonia lyase, polyphenoloxidase, peroxidase, and total phenolics has been recorded in the plants that are pretreated with Trichoderma, Bacillus, and Pseudomonas (Khan and Mohiddin 2018).

1.7.6  Growth Promotion of Host Plants The growth of plants can be stimulated, enhanced, and improved by the Trichoderma species. It has been reported (Chang 1986) that seed germination of pepper was induced two days earlier in soil treated with T. harzianum than in the untreated soil. The flowering and the blooms increased in the plant Chrysanthemums and the weight as well as height was greater in either raw or steamed soil treated with T. harzianum (Baker 1984). These responses were noted consistently with population densities of T. harzianum greater than 108 cfu/g soil irrespective of the application form. Dry matter of bean plants was increased by Trichoderma koningii at

1  Agriculturally Important Fungi for Crop Protection

25

106–108 conidia/g of soil (Baker 1984). Sivan (1989) speculated that the growth promotion of plant may be due to the activity of the biocontrol fungus that reduces the concentration of plant growth inhibitory substances or increase the concentration of compounds that are related to the defense mechanism of plant. Thus, the growth promotion of plants may be due to the production of growth-promoting hormones or increased nutrient uptake by the plants (Sivan 1989). The application of Trichoderma species can strengthen the defense mechanism of plants. It has been reported (Rabeendran et al. 2000) that by dipping transplants in spore suspensions (107 conidia/mL) of T. tomentosum and T. longipile can increase the surface area (58–71%), dry weight of root (100–158%), dry weight of shoot (91–102%) of cabbage. In a field trial, yield of lettuce treated with T. longipile 6Sr4 increased significantly. The lateral root production and biomass production were stimulated by Trichoderma virens (Contreras-Cornejo et al. 2009). The infectivity on bean plants by R. solani (Bakarat et al. 2007) was reduced by the conidial suspension of Trichoderma isolates at 3 × 107 cfu and increased the growth. The increase in fresh weight, dry weight, and plant height by 133%, 217%, and 160% was noted respectively. Moreover, after 14 and 28 days the reduction of 60%–40% of disease was recorded (Yobo et al. 2009). Okoth et al. (2011) reported the rise in maize seed germination as a result of coating with Trichoderma.

1.7.7  Phosphate Solubilization The major nutrient required for the growth and development of the plant is phosphorus. It is present in an unutilized form in the soil. They are converted by phosphate solubilizing microorganisms to be utilized by plants (Kour et al. 2020a, b, 2019a). In recent years species of Trichoderma have also been reported to solubilize phosphorus. A clear zone of phosphate solubilization was recorded by Saraf et al. (2013) after 3 days of inoculation with Trichoderma isolate MJ3 on the Pikovskaya agar Table 1.7  Total percentage increase in the yield of various crops after the treatment with Trichoderma species Crop Potato Cotton Chickpea Mustard Maize Mung bean Strawberry Black pepper Tomato Rice

Percentage of yield 65 320 124 110 82 40 90 180 150 87

Reference Drahansky et al. (2016) Harman et al. (2004) Khan and Mohiddin (2018) Haque et al. (2012) Sankar and Sharma (2001) Dubey (2003) Porras et al. (2007) Ayub et al. (2010) Dutta and Das (2002) Barari (2016)

26

P. Selvasekaran and R. Chidambaram

media. The 14 strains of Trichoderma species isolated from the rhizosphere of the forest tree such as deodar, bamboo, guava, pinus, and oak for their potential of in vitro solubilized phosphate in the culture broth containing tricalcium phosphate as the sole source of phosphate (Khan et al. 2008). The maximum amount of phosphate solubilization was shown by Trichoderma isolate DRT followed by T. harzianum after 96 h incubation period at 30 °C (Kapri and Tewari 2010). The phosphate solubilization under the environment of low temperature was induced by fungal root endophytes with maximum solubilization by T. pseudokongingii. Similarly, the solubilization of phosphorus from ten isolates of Trichoderma species derived from the rhizosphere has been reported (Saravanakumar et al. 2013). In the evaluation of plant growth promotion among the 12 fungal endophytes, Chaetomium globosum, Fusarium fusarioides, mucor species, and Aspergillus versicolour showed the production of HCN.  Rawatand studied  T. virens (SE6 and KT28), Aspergillus flavus (BRT11), T. viride (KT6) for their potential of plant growth promotion  and indicated that only three isolates, SE6, KT6, and BRT11 showed the production of HCN (Rawat and Tewari 2011). During the isolation of six Trichoderma isolates for the potential of in vitro plant growth promotion only Trichoderma produced HCN.  Colonization of root by the strains of Trichoderma frequently enhances the growth and development of root, abiotic stress resistance, productivity of the crop, uptake, and use of nutrients. After the addition of T. hamatum or T. koningii the productivity of crops in fields increased up to 300%. The experiments that were carried out by treating the seeds with Trichoderma spores in greenhouses significantly showed greater yield. When the plant seeds were separated from Trichoderma by a cellophane membrane, they showed an equal degree of yield enhancement. This indicates the production of growth factors from Trichoderma that enhances seed germination, growth of the plant, and the yield. Besides having the inhibitory effect on the germ tube elongation and conidial germination of Botrytis cinerea, the T. harzianum T39 also reduces the production and activity of the pectolytic enzymes. The reduction in the activity of pectolytic enzymes can increase the accumulation of pectic enzymes that is oligogalacturonides. The host plant defense can be elicited by these sugars, thus checking the development of the disease. Chet et al. concluded that the promotion of plant growth may be due to the increased uptake of nutrients and the production of plant hormones (Khan and Mohiddin 2018) (Table 1.7).

1.7.8  Drought Tolerance One of the major environmental stresses that affect the growth of plant and crop production is drought (Kour et al. 2020c). In traditional agricultural practice, the effectiveness of the use of chemical or synthetic fertilizers is also significantly affected by drought (Saba 2012). Improvement in the stimulation of plant growth and soil fertility in the dry and drought areas is one of the major issues that farmers have been facing for decades. Few species such as T. harzianum, T.

1  Agriculturally Important Fungi for Crop Protection

27

longibrachiatum, T. viride, T. hamatum, and T. koningii are efficient biocontrol agents that can inhibit the growth of pathogens in the soil, thereby improving the overall health of the plant. Trichoderma species also help in sustaining the plants under drought conditions which are considered as biological methods. The interaction of the plant with Trichoderma species increases the yield, development, and stress tolerance in various conditions. These species occur almost in all the ecosystems and constitute one of the parts on the microflora of the rhizosphere. The alleviation of damage is induced by Trichoderma through reactive oxygen species, improvement in the efficiency of water use, and phytohormone secretion that enhances the growth of plants under drought stress (Khan and Mohiddin 2018). Trichoderma is considered a virulent organism that stimulates the growth of plant under the suboptimal conditions. The plant symbionts help in either inducing plants to scavenge ROS or by preventing the production of ROS under abiotic stress. Symbiotic plants spend significantly less water when compared to the non-­symbiotic plants. Tomato and rice with the Trichoderma species used less fluid than the non-­ symbiotic plants. Trichoderma protects the plants against ROS by increasing the ROS scavenging capacity. The antioxidative enzymes such as peroxidase, superoxide dismutase, glutathione-reductase, and glutathione-S-transferase as well as other detoxifying enzymes present in leaves increase due to the inoculation of roots with Trichoderma species. The superoxide dismutase converts the toxic superoxide to hydrogen peroxide and oxygen through the dismutation reaction. The application of T. atroviride ID20G increases the fresh and dry weight of the roots of maize under the drought stress. Besides inducing the antioxidant enzyme activity, the fungal strains also increased the carotenoid and chlorophyll content of the seedlings. The colonization of root by T. atroviride ID20G prevented the increase in lipid peroxidation and also reversed the changes in the contents of pigment and efficiency of photosystem caused by drought. The seeds that are subjected to oxidative stress restored vigor after treatment with the Trichoderma T22. Furthermore, in cucumber plants, the peroxidase gene was primed after inoculation with Trichoderma species. In tomato seeds, the percentage of germination increased after the application of T. harzianum T22 under osmotic conditions. An increase in the content of lipid peroxide in young seedlings was reported in a study with an increase in the water potential of the media whereas the seedlings that are treated with T22 have significantly less lipid peroxide than the untreated seedlings (Khan and Mohiddin 2018).

1.8  Piriformospora indica The endophytic Agaricomycetes fungus Piriformospora indica owing to its exceptional ability to efficiently promote the growth of plant, protection, and tolerance to stress has received significant attention over the past few decades and mimics the capabilities of Arbuscular Mycorrhizae. This is an axenically cultivable fungus exhibiting the versatility for hosting and colonizing plant species through direct

28

P. Selvasekaran and R. Chidambaram

manipulation of plant hormones-signaling pathway during mutualism. The root colonization by Piriformospora indica promotes plant performance and enhances the proliferation of root by the production of indole-3-acetic acid. The production of indole-3-acetic acid also improves the nutrient acquisition and improves the growth and productivity of the crop. Through the signal transduction pathway, this fungus can induce local and systemic resistance to viral and fungal plant disease. The plant stress tolerance is conferred through the stimulation of components involved in the defense mechanisms and expressing the genes related to stress by the P. indica. Therefore, micro-propagated plantlets can be biotized by this fungus as well as the transplantation shock can be overcome. P. indica can also be involved in various symbiotic relationships such as symbiosis of tripartite and promotes the rhizobacteria thereby enhancing the population dynamics of plant growth. Hence, Piriformospora indica has the potential to be utilized as a bio protector, bioregulator, biofertilizer, biotization agent, and plant growth promoter.

1.8.1  Acquisition of Phosphorus Phosphorus is one of the important essential nutrients. The phosphorus present in the soil cannot be directly accessed by the plants as the phosphorus is in the form of scarcely soluble complexes. Hence, the deficiency of phosphorus impedes the production of crops throughout the world. It was reported that the uptake of radiolabeled phosphorous from the culture media was mediated by the Piriformospora indica. The acid phosphatases are also produced by this fungus in significant amounts which helps the host plants to access insoluble, condensed, and complex forms of phosphate in the soil (Yadav et al. 2010). Isolation of high-affinity phosphate transporter, identification and characterization of their functional property from the root endophytic fungus P. indica revealed that the phosphate transporter is essential for the transport of phosphate to the host plants (Johri et al. 2015). The mechanism behind the transport of phosphate from fungus to plant is still not clear but the hypothesis states that it might occur at the plant-fungus interface. This process requires two transporters. The first transporter to enable the phosphate efflux from the fungus and the second transporter to mediate the uptake of phosphate by the plants (Rausch and Bucher 2002). The reports concerning the involvement of P. indica in the transfer of phosphate are contradictory. It has been reported that the phosphate uptake in Arabidopsis seedling is enhanced by Piriformospora indica 2–3 times higher (Shahollari et al. 2005). It has been reported by Yadav et al. (2010) on the influence of phosphate on the biomass of Z. mays plant that was colonized with P. indica. Increased biomass and total phenolic content were observed in the plants colonized with P. indica of wild type as compared with non-colonized (Yadav et al. 2010). The growth-promoting activity of P. indica was observed to be higher under the condition of low phosphate as compared with the condition under high phosphate. Hence it has been concluded that P. indica can be a potential agent for

1  Agriculturally Important Fungi for Crop Protection

29

utilization in sustainable agriculture to improve the production of the crop in lands deficient with phosphate (Gill et al. 2016).

1.8.2  Acquisition of Other Nutrients The growth and development of the plant are restricted due to the deficiency of other nutrients such as nitrogen and zinc (Rana et al. 2019c). The plants uptake nitrogen either in the form of nitrate or ammonium (Esseling and Emons 2004; Kour et al. 2020d; Yadav et  al. 2017a). It was reported by Sherameti et  al. (2005) that Arabidopsis seedling and Nicotiana tabaccum when co-cultivated with P. indica is accompanied by the transfer of N from the Petri plates containing agar to the seedlings. This effect is activated by the enzyme that plays a significant role in the acquisition of nitrate, NADH-dependent nitrate reductase. It has been proposed that the growth-promoting effect of P. indica is accompanied by the enzymes that are involved in the metabolism of nitrate and starch (Gill et al. 2016).

1.8.3  Plant Growth and Development The growth, development, and yield of many crops, horticulture, and other medicinal plants were increased by the P. indica (Varma et al. 2012). In several crops seed germination and development induced by this fungus have been reported (Pham et al. 2008; Kumar et al. 2009; Vadassery et al. 2008). The enhanced seed development and production have been reported in A. thaliana as a result of microdomains present in the plasma membrane such as pii-2 and AT5g16590. The H. vulgare seeds inoculated with P. indica showed higher viability (Harrach et al. 2013). The germinated seeds under adverse conditions showed a higher survival rate when immersed in the homogenate containing P. indica. In vascular plants, the early seed germination is facilitated by the filtrate of P. indica. The seed oil yield from the Helianthus annuus was evidenced to be influenced by the culture filtrate of P. indica (Bagde et  al. 2011). As a result of root colonization by P. indica the members of angiosperms, gymnosperms, bryophytes, and pteridophytes were reported to have higher seed yield. In medicinal plants the inoculation and colonization role of P. indica has been seen as utmost significance (Hock 2012). In medicinal plants, the colonization by P. indica has been reported including Lantana camara, Coleus forskohlii, Linum album, Bacopa monnieri, Ocimum sanctum, Stevia rebaudiana, Chlorophytum borivilianum, Artemisia annua, Withania somnifera,, Linum album, Spilanthes calva, Trigonella foenumgraecum (Kumar et al. 2009; Das et al. 2014; Sharma and Agrawal 2013). In C. forskohlii increased content of secondary metabolites and chemical compounds have been reported due to the colonization of roots by P. indica (Das et al. 2014). The hypertrophy B. monnieri nuclei and the growth, the level of bacoside endogenous, and antioxidant

30

P. Selvasekaran and R. Chidambaram

activity are enhanced by P. indica (Prasad et al. 2013). The properties of medicinal plants such as H. annuus, A. elegans, A. indica were increased by their colonization with P. indica (Bagde et al. 2011). In the cell culture of L. album the inoculation of P.  indica improved the anticancer drug podophyllotoxin. In the herbaceous plant such as A. annua and S. rebaudiana their leaf area and biomass were enhanced when cultivated with P. indica. The medicinal plants namely W. somnifera and S. calva were reported to have a positive impact on their growth in a field trial when inoculated with P. indica (Rai et al. 2001). In W. somnifera and A. annua the productivity of biomass was enhanced by in  vitro co-cultivation with the filtrate of P. indica (Baishya et al. 2015). In view of the colonization role of P. indica in crop plants, it has been reported that the enhanced growth and production of biomass have been observed in Ridax procumbans, Oryza sativa, Phaseolus vulgaris, Saccharum officinarum, Zea mays, Abrus precatorius (Varma et al. 2012). The plant root growth is promoted by P. indica due to their role in the production of auxin as well as their interaction with ethylene signaling. They stimulate the synthesis of the secondary metabolites such as betulinic acid, ursolic acid, oleanolic acid in the suspension culture of L. camara. Further, this fungus can be used as a biopriming agent due to its symbiotic effect on the overall growth of plant biomass (Gill et al. 2016).

1.8.4  Role in the Tolerance of Biotic and Abiotic Stress There has been an extensive report on the ability of Piriformospora indica to increase the tolerance capacity of plants against various abiotic stress including heavy metal toxicity, salinity, and low temperature. In Triticum aestivum and Arabidopsis seedlings, the colonization with P. indica mediated tolerance against high salinity and drought stress, respectively (Zarea et  al. 2012; Sherameti et  al. 2008). The activation of genes that are related to defense mechanisms such as LOX2, PR, and ERFI are reported (Zarea et al. 2012) to be activated by colonization with P. indica. The interaction of P. indica with the roots of A. thaliana can be used as a unique model system to study the symbiotic relationship. The ability to deliver molecules such as effectors has been evolved by the mutualistic fungi P. indica to enhance and manipulate the microbial infection and host metabolism, respectively. These molecules play an important role in the establishment as well as the maintenance of symbiosis in endo and ectomycorrhiza and allow the manipulation of plant defense response (Vahabi et al. 2015a). The antioxidant defense enzymes such as monodehydroascorbate reductase and dehydroascorbate reductase including other components related to the ROS scavenging system have been reported to be modulated by the P. indica (Vadassery et al. 2008). The upregulation of various enzymes involved in the ROS metabolism of the plants exposed to salinity is mediated by P. indica colonization. The tolerance of plants against various abiotic stresses such as heat, salinity, drought, and heavy metal was conferred by the inoculation of P. indica. In addition to protection against abiotic stresses, P. indica also provides protection against various biotic stresses

1  Agriculturally Important Fungi for Crop Protection

31

Table 1.8  The role Piriformospora indica in major crops under biotic stress Host plant H. vulgare A. thaliana

Beneficial roles Provides protection against Rhizoctonia solani which causes root rot. Significant reduction in the development of disease caused by Verticillium dahlia Protection against Alternaria brassicae which causes leaf blight Protection against V. dahlia which causes Verticillium wilt Provides protection against Rhizoctonia solani and Verticillium longisporum which causes root rot and Verticillium wilt

L. esculentum Provides protection against Thielaviopsis basicola and Fusarium oxysporum that causes black root rot and Fusarium wilt Provides protection against V. dahlia and Pepino mosaic virus which causes Verticillium wilt and yellow leaf mosaic Triticum Protection against head blight disease caused by Fusarium aestivum

Reference Qiang et al. (2012) Sun et al. (2014) Vahabi et al. (2015b) Sun et al. (2014) Knecht et al. (2010) Qiang et al. (2012) Fakhro et al. (2010) Rabiey et al. (2015)

Table 1.9  The role of Piriformospora indica in major crops under abiotic stress Host plant T. aestivum

Beneficial roles Mitigation of stress caused by Zinc deficiency Increase in stress tolerance again st cadmium

Oryza sativa

Increase in salinity stress

Hordeum vulgare Increase the tolerance against salinity stress by increasing the ratio of foliar potassium/sodium Solanum Tolerance against osmotic stress and toxicity of lycopersicum chloride Sesamum indicum Increases the growth as well as tolerance against drought stress Nicotiana Increased cadmium tolerance tabacum H. vulgare Tolerance against low temperature stress and increase in the yield of crop Enhanced tolerance against drought stress Enhanced salinity tolerance and increase in the biomass of aerial plants

Reference Abadi and Sepehri (2016) Shahabivand et al. (2012) Jogawat et al. (2013) Alikhani et al. (2013) Gill et al. (2016) Gill et al. (2016) Hui et al. (2015) Gill et al. (2016) Ghabooli et al. (2013) (Gill et al. (2016)

such as pathogenic fungi, bacteria, and virus. The genes encoding the enzymes responsible for the synthesis of ascorbate in Arabidopsis are due to the greater colonization by P. indica. Research Van Wees et al. (2008) concerning the greenhouse study of Solanum lycopersicum Mill inoculated with the culture filtrates of P. indica showed a significant increase in their growth under osmotic stress and chloride toxicity. The

32

P. Selvasekaran and R. Chidambaram

Table 1.10  The role of Piriformospora indica in major crops under normal conditions Host plants Centella asiatica

Beneficial roles of P. indica Increase in the fresh weight of plant, root, and leaf number Hordeum vulgare Increase in the viability and survival of seeds as well as vegetative and yield of grain Populus and Early germination of seeds as well as increase in Jatropha formation of seed and the yield Brassica campestris Increase in the fresh weight of root and shoot Oryza sativa Tridax procumbens Nicotiana attenuata Cyclamen persicum Lycopersicon esculentum Foeniculum vulgare Vegetable crops Helianthus annuus

Reference Gill et al. (2016) Harrach et al. (2013) Prasad et al. (2013) Sun et al. (2010) Improvement and increase in the length of root and Jogawat et al. shoot along with their dry weight (2013) Increase in the fresh and dry weight and the length of Gill et al. root and shoot (2016) Gill et al. Increase in the length of stalk, number of flowers, weight of seed and fresh weight of fruit (2016) Increase in the number of leaves and flowers Ghanem et al. (2014) Increase in the growth of seedling Anith et al. (2015) Increase in the height of the plant, dry weight of the root Gill et al. and shoot (2016) Induced germination and formation of the seed. Prasad et al. Increased seed value and yield of crops (2013) Increase in the yield of seed with high content of oil and Bagde et al. lipid biosynthesis (2011)

mechanism underlying the development of resistance by P. indica has already been studied for abiotic and biotic stresses in plants colonized with rhizobacteria but very less research has been done on the mechanism underlying the resistance induced by P. indica against various abiotic and biotic stresses. The observation on the interaction that is beneficial between the host plant and fungus has been reported to upregulate various genes that are related to the mechanism of defense including PR genes involved in pathogenesis and ethylene signaling genes (ERF1) in pathogen attack (Molitor et al. 2011). The plant H. vulgare is protected from Fusarium culmorum and Blumeria graminis which cause root damage and shoot infection, respectively (Molitor et al. 2011). The activity of antagonism by the endophytic fungus, P. indica directly inhibits various root pathogens except for F. culmorum (Waller et al. 2005), F. oxysporum (Saba 2012), and P. herpotrichoides (Serfling et al. 2007). The resistance of host plants against various root pathogens was also reported to be associated with the root colonization of P. indica. The crop plants result in better vegetative and generative development as they are defended against various viral and fungal pathogens. To the economically important agricultural and horticultural crops, the Piriformospora indica has been found to possess the potential as a bio protective agent. The resistance against fungal disease is increased in plants by the utilization

1  Agriculturally Important Fungi for Crop Protection

33

of P. indica. It has been reported (Molitor et al. 2011) that the H. vulgare plants, when colonized with the P. indica, became free from the fungal pathogen such as F. culmorum. The plants treated with the P. indica were protected against root pathogens such as Cochliobolus sativus fungus (Oelmüller et  al. 2009). The systemic resistance against the biotrophic leaf pathogen such as B. graminis f. sp. hordei in H. vulgare roots was developed by colonization with P. indica (Waller et al. 2005). This fungus has also been involved in the biocontrol of take-all diseases of T. aestivum and Fusarium wilt disease of lentil. Therefore from the reports, P. indica is a multifunctional agent providing service such as nutrient uptake, stress tolerance, disease resistance, and promotion of growth (Gill et  al. 2016) (Tables 1.8, 1.9, and 1.10).

1.9  Notable Research on the Role of Fungi in Agriculture • Mittal et al. (2008) evaluated the growth and seed production of Cicer arietinum in the pot experiments under greenhouse conditions by the impact of six phosphate solubilizing fungi including four strains of Penicillium citrinum and two strains of Aspergillus awamori. Result of the study showed an increase in seed number, seed weight, and shoot height in the inoculated plants and higher in the plants inoculated with the strains of Aspergillus awamori. • Kapri and Tewari (2010) evaluated Cicer arietinum after the application of inoculation containing P-solubilizing Trichoderma sp. and found that it increased all the growth parameters such as fresh and dry weight of shoot and root, length of shoot and root in phosphate deficient soil. • Promwee et al. (2014) observed when Hevea brasiliensis was inoculated with phosphorus solubilizing fungus Trichoderma harzianum and rock phosphate it resulted in increased fresh and dry weight of shoot and root, circumstances of the stem, leaf number, and height of the plant compared with the control containing only the rock phosphate. • Saxena et al. (2015) evaluated the combined effect of the phosphorus solubilizing Aspergillus niger and Bacillus sp. on the growth, development, and yield of Cicer arietinum. The result of the study indicated an increased growth of the plants with dual inoculations than with single inoculation or uninoculated plants. • Priyadharsini and Muthukumar (2017) evaluated Curvularia geniculata by inoculation with Cajanus cajan and reported that the inoculated plants showed better growth because of the role of fungus in solubilization of phosphorus and production of IAA • Zhou et al. (2018) observed in the studies involving Alternaria sp. increased the biomass of dry root and accumulation of secondary metabolites of Salvia miltiorrhiza and the seedlings of the plant showed increase in fresh as well as dry weight as well as enhancement in the total phenolic content, lithospermic acids A and B. The study concluded that this fungus stimulates the growth of root as well as production of secondary metabolites.

34

P. Selvasekaran and R. Chidambaram

• The influence of Arbuscular mycorrhizal fungus including Glomus intraradices and Glomus mosseae with or without the presence of nitrogen fixer, solubilizers of phosphate and potassium on the soil properties, and growth of maize was evaluated by Wu et al. (2005). The result was concluded as the application of Glomus mosseae increased the biomass yield and height of the seedling as the inoculum increased the total P, N, K, and organic matter in the soil. • Saravanan et al. (2011) reported fungal genera such as Penicillium simplicissimum, Absidia cylindrospora, Aspergillus niger, Absidia glauca, and Absidia spinosa with the potential to solubilize the insoluble zinc. • Saravanan et  al. (2011) reported various Ericoid mycorrhizae such as Suillus bovinus, Beauveria caledonica, Suillus luteus, Hymenoscyphus ericae, Paxillus involutus, and Oidiodendron maius with the potential to solubilize insoluble zinc. • Martino et al. (2003) demonstrated the potential of Oidiodendron maius to solubilize insoluble inorganic zinc compounds • Altomare et  al. (1999) evaluated the capability of Trichoderma harzianum a plant growth-promoting and biocontrol agent to solubilize in vitro some insoluble and sparingly soluble minerals. The observed result was solubilization of metallic zinc, MnO2, and rock phosphate. • Anastasiou et  al. (2014) isolated Penicillium dalea, Aspergillus terreus, Aspergillus oryzae possessing the capacity to solubilize manganese from the low-­grade manganese mine tailing.

1.10  Conclusion and Future Perspective The growth development and use of synthetic pesticides and fertilizers have significantly enhanced the protection of crops but their use also has disadvantages such as environmental related problems such as drought, salinity, and pathogen resistance. Further, these chemicals are not successful in different crop fields to sustain the production of crops. Green technology such as the use of beneficial fungi may pose to be a significant alternative to these chemicals. Among various beneficial fungi Arbuscular mycorrhiza, Trichoderma, Penicillium, fungal endophytes, and Piriformospora indica have the potential to deal with the various stresses such as drought, nutrient deficiency, soil salinity, and disease tolerance. The beneficial role of these fungi is being studied by researchers. On the contrary, the majority of the crop growers have remained unaware of the utility of these fungi. Hence, requires the spread of awareness among the farmers’ community. Further continuous research is required to identify and isolate an efficient fungus with the multifarious characteristics of disease suppression and growth promotion. Acknowledgment  The authors are thankful to Vellore Institute of Technology, Vellore, India for providing constant encouragement and infrastructural facilities.

1  Agriculturally Important Fungi for Crop Protection

35

References Abadi VAJM, Sepehri M (2016) Effect of Piriformospora indica and Azotobacter chroococcum on mitigation of zinc deficiency stress in wheat (Triticum aestivum L.). Symbiosis 69:9–19. https://doi.org/10.1007/s13199-015-0361-z Abdel Latef AAH, Chaoxing H (2014) Does inoculation with Glomus mosseae improve salt tolerance in pepper plants? J Plant Growth Regul 33:644–653. https://doi.org/10.1007/ s00344-014-9414-4 Adholeya A, Tiwari P, Singh R (2005) Large-scale inoculum production of arbuscular mycorrhizal fungi on root organs and inoculation strategies. Vitr Cult Mycorrhizas 4:315–338. https://doi. org/10.1007/3-540-27331-x_17 Ahmed H, Strub C, Hilaire F, Schorr-Galindo S (2015) First report: Penicillium adametzioides, a potential biocontrol agent for ochratoxin-producing fungus in grapes, resulting from natural product pre-harvest treatment. Food Control 51:23–30. https://doi.org/10.1016/j. foodcont.2014.10.034 Aidemark M, Tjellström H, Sandelius AS, Stålbrand H, Andreasson E, Rasmusson AG et al (2010) Trichoderma viride cellulase induces resistance to the antibiotic pore-forming peptide alamethicin associated with changes in the plasma membrane lipid composition of tobacco BY-2 cells. BMC Plant Biol 10:274. https://doi.org/10.1186/1471-2229-10-274 Akello J, Dubois T, Gold CS, Coyne D, Nakavuma J, Paparu P (2007) Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J Invertebr Pathol 96:34–42. https://doi.org/10.1016/j.jip.2007.02.004 Alam SS, Sakamoto K, Inubushi K (2011) Biocontrol efficiency of Fusarium wilt diseases by a root-colonizing fungus Penicillium sp. Soil Sci Plant Nutr 57:204–212. https://doi.org/10.108 0/00380768.2011.564996 Alikhani M, Khatabi B, Sepehri M, Nekouei MK, Mardi M, Salekdeh GH (2013) A proteomics approach to study the molecular basis of enhanced salt tolerance in barley (Hordeum vulgare L.) conferred by the root mutualistic fungus Piriformospora indica. Mol BioSyst 9:1498–1510. https://doi.org/10.1039/c3mb70069k Alston DG, Rangel DEN, Lacey LA, Golez HG, Jeong JK, Roberts DW (2005) Evaluation of novel fungal and nematode isolates for control of Conotrachelus nenuphar (Coleoptera: Curculionidae) larvae. Biol Control 35:163–171. https://doi.org/10.1016/j.biocontrol.2005.06.011 Altomare C, Norvell W, Björkman T, Harman G (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65:2926–2933 Alves L, Oliveira VL, Filho GNS (2010) Utilization of rocks and ectomycorrhizal fungi to promote growth of eucalypt. Braz J Microbiol 41:676–684. https://doi.org/10.1590/ S1517-83822010000300018 Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845. https://doi.org/10.1007/s00253-011-3270-y Anastasiou E, Lorentz KO, Stein GJ, Mitchell PD (2014) Prehistoric schistosomiasis parasite found in the Middle East. Lancet Infect Dis 14:553–554. https://doi.org/10.1016/ S1473-3099(14)70794-7 Anderson IC, Cairney JWG (2007) Ectomycorrhizal fungi: exploring the mycelial frontier. FEMS Microbiol Rev 31:388–406. https://doi.org/10.1111/j.1574-6976.2007.00073.x Anith KN, Sreekumar A, Sreekumar J (2015) The growth of tomato seedlings inoculated with co-cultivated Piriformospora indica and Bacillus pumilus. Symbiosis 65:9–16. https://doi. org/10.1007/s13199-015-0313-7 Anitha R, Murugesan K (2005) Production of gliotoxin on natural substrates by Trichoderma virens. J Basic Microbiol 45:12–19. https://doi.org/10.1002/jobm.200410451 Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654. https:// doi.org/10.1073/pnas.2533483100

36

P. Selvasekaran and R. Chidambaram

Atugala DM, Deshappriya N (2015) Effect of endophytic fungi on plant growth and blast disease incidence of two traditional rice varieties. J Natl Sci Found Sri Lanka 43:173–187. https://doi. org/10.4038/jnsfsr.v43i2.7945 Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381. https://doi.org/10.4141/S04-002 Ayub A, Sultana N, Faruk M, Rahman M, Mamun A (2010) Control of rhizome rot disease of ginger (Zingiber officinale rose) by chemicals, soil amendments and soil antagonist. Agriculturist 7:57–61. https://doi.org/10.3329/agric.v7i1.5254 Azcón R, Barea JM (1992) The effect of vesicular-arbuscular mycorrhizae in decreasing Ca acquisition by alfalfa plants in calcareous soils. Biol Fertil Soils 13:155–159. https://doi. org/10.1007/BF00336272 Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL et al (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295. https://doi.org/10.1093/ jxb/erp165 Bagde US, Prasad R, Varma A (2011) Influence of culture filtrate of Piriformospora indica on growth and yield of seed oil in Helianthus annus. Symbiosis 53:83–88. https://doi.org/10.1007/ s13199-011-0114-6 Baishya D, Deka P, Kalita MC (2015) In vitro co-cultivation of Piriformospora indica filtrate for improve biomass productivity in Artemisia annua (L.). Symbiosis 66:37–46. https://doi. org/10.1007/s13199-015-0331-5 Bakarat R, Al-mahareeq F, Ali M, Al-Masri M (2007) Biological control of Rhizoctonia solani by indigenous Trichoderma spp. isolates from Palestine. Hebron Univ Res J 3:1–15 Baker R (1984) The controlled experiment in the scientific method with special emphasis on biological control. Phytopathology 74:1019. https://doi.org/10.1094/phyto-74-1019 Baldwin JE, Derome AE, Field LD, Gallagher PT, Taha AA, Thaller V et al (1981) Biosynthesis of a cyclopentyl dienyl isonitrile acid in cultures of the fungus Trichoderma hamatum (Bon.) Bain. aggr. J Chem Soc Chem Commun 1981:1227–1229. https://doi.org/10.1039/C39810001227 Bamisile BS, Dash CK, Akutse KS, Keppanan R, Wang L (2018) Fungal endophytes: beyond herbivore management. Front Microbiol 9:1–11. https://doi.org/10.3389/fmicb.2018.00544 Barari H (2016) Biocontrol of tomato Fusarium wilt by Trichoderma species under in vitro and in vivo conditions. Cercet Agron Mold 49:91–98. https://doi.org/10.1515/cerce-2016-0008 Bartels RA, Paul A, Green H, Kapteyn HC, Murnane MM, Backus S et al (2002) Generation of spatially coherent light at extreme ultraviolet wavelengths. Science 297:376–378. https://doi. org/10.1126/science.1072191 Benítez T, Rincón AM, Limón MC, Codón AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260 Berbee ML, Yoshimura A, Sugiyama J, Taylor JW (1995) Is Penicillium monophyletic? An evaluation of phylogeny in the family Trichocomaceae from 18S, 5.8S and ITS ribosomal DNA sequence data. Mycologia 87:210–222. https://doi.org/10.2307/3760907 Birhanu G, Zerihun T, Genene T, Endegena A, Misganaw W, Endeshaw A (2017) Phosphate solubilizing fungi isolated and characterized from Teff rhizosphere soil collected from North Showa zone, Ethiopia. Afr J Microbiol Res 11:687–696. https://doi.org/10.5897/ ajmr2017.8525 Boddey RM, Urquiaga S, Alves BJR, Reis V (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252:139–149. https://doi.org/10.102 3/A:1024152126541 Bolton M (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant-Microbe Interact 22:487–497 Boon E, Meehan CJ, Whidden C, Wong DHJ, Langille MGI, Beiko RG (2014) Interactions in the microbiome: communities of organisms and communities of genes. FEMS Microbiol Rev 38:90–118. https://doi.org/10.1111/1574-6976.12035

1  Agriculturally Important Fungi for Crop Protection

37

Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses in biochemistry and molecular biology of plants. Am Soc Plant Physiol 139:1158–1203. https://doi.org/10.1104/ pp.105.065698.various Brundrett MC (2007) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. Microb Root Endophytes 9:281–298. https://doi.org/10.1007/3-540-33526-9_16 Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. https://doi.org/10.1007/ s11104-008-9877-9 Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26. https://doi.org/10.1111/j.1469-8137.2006.01935.x Burton EM, Knight JD (2005) Survival of Penicillium bilaiae inoculated on canola seed treated with Vitavax RS and Extender. Biol Fertil Soils 42:54–59. https://doi.org/10.1007/ s00374-005-0862-7 Buscot F, Munch JC, Charcosset JY, Gardes M, Nehls U, Hampp R (2000) Recent advances in exploring physiology and biodiversity of ectomycorrhizas highlight the functioning of these symbioses in ecosystems. FEMS Microbiol Rev 24:601–614. https://doi.org/10.1016/ S0168-6445(00)00048-6 Calderón AA, Zapata JM, Muñoz R, Pedreño MA, Barceló AR (1993) Resveratrol production as a part of the hypersensitive-like response of grapevine cells to an elicitor from Trichoderma viride. New Phytol 124:455–463. https://doi.org/10.1111/j.1469-8137.1993.tb03836.x Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. https://doi.org/10.1007/s11104-014-2131-8 Cao R, Liu X, Gao K, Mendgen K, Kang Z, Gao J et al (2009) Mycoparasitism of endophytic fungi isolated from reed on soilborne phytopathogenic fungi and production of cell wall-degrading enzymes in vitro. Curr Microbiol 59:584–592. https://doi.org/10.1007/s00284-009-9477-9 Cao MJ, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M et al (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615. https://doi.org/10.1111/tpj.12407 Cardoso JA, Odokonyero K, Madhusudana Rao I, de la Cruz Jimenez J, Botwright Acuna T (2017) Potential role of fungal endophytes in biological nitrification inhibition in Brachiaria grass species. J Plant Biochem Physiol 5:1–9. https://doi.org/10.4172/2329-9029.1000191 Chandanie WA, Kubota M, Hyakumachi M (2006) Interactions between plant growth promoting fungi and arbuscular mycorrhizal fungus Glomus mosseae and induction of systemic resistance to anthracnose disease in cucumber. Plant Soil 286:209–217. https://doi.org/10.1007/ s11104-006-9038-y Chandrasekaran M, Boughattas S, Hu S, Oh SH, Sa T (2014) A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza 24:611–625. https://doi. org/10.1007/s00572-014-0582-7 Chang Y-C (1986) Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. Plant Dis 70:145. https://doi.org/10.1094/pd-70-145 Chet I, Ordentlich A, Shapira R, Oppenheim A (1990) Mechanisms of biocontrol of soil-borne plant pathogens by Rhizobacteria. Plant Soil 129:85–92. https://doi.org/10.1007/BF00011694 Chithra S, Jasim B, Sachidanandan P, Jyothis M, Radhakrishnan EK (2014) Piperine production by endophytic fungus Colletotrichum gloeosporioides isolated from Piper nigrum. Phytomedicine 21:534–540. https://doi.org/10.1016/j.phymed.2013.10.020 Chomcheon P, Wiyakrutta S, Sriubolmas N, Ngamrojanavanich N, Isarangkul D, Kittakoop P (2005) 3-Nitropropionic acid (3-NPA), a potent antimycobacterial agent from endophytic fungi: Is 3-NPA in some plants produced by endophytes? J Nat Prod 68:1103–1105. https:// doi.org/10.1021/np050036a Clarke BB, White JF, Hurley RH, Torres MS, Sun S, Huff DR (2006) Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Dis 90:994–998. https://doi.org/10.1094/ PD-90-0994

38

P. Selvasekaran and R. Chidambaram

Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:99–127. https://doi.org/10.1086/342161 Claydon N, Hanson JR, Truneh A, Avent AG (1991) Harzianolide, a butenolide metabolite from cultures of Trichoderma harzianum. Phytochemistry 30:3802–3803. https://doi. org/10.1016/0031-9422(91)80115-H Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592. https://doi.org/10.1104/pp.108.130369 Corke ATK, Hunter T (1979) Biocontrol of Nectria galligena infection of pruning wounds on apple shoots. J Hortic Sci 54:47–55. https://doi.org/10.1080/00221589.1979.11514847 Costa LB, Rangel DEN, Morandi MAB, Bettiol W (2012) Impact of UV-B radiation on Clonostachys rosea germination and growth. World J Microbiol Biotechnol 28:2497–2504. https://doi.org/10.1007/s11274-012-1057-7 da Silva E (2006) Handbook of microbial biofertilizers. CRC Press, Boca Raton Dai CC, Yu BY, Li X (2008) Screening of endophytic fungi that promote the growth of Euphorbia pekinensis. Afr J Biotechnol 7:3505–3510 Das A, Tripathi S, Varma A (2014) In vitro plant development and root colonization of Coleus forskohlii by Piriformospora indica. World J Microbiol Biotechnol 30:1075–1084. https://doi. org/10.1007/s11274-013-1526-7 Davis RA, Andjic V, Kotiw M, Shivas RG (2005) Phomoxins B and C: polyketides from an endophytic fungus of the genus Eupenicillium. Phytochemistry 66:2771–2775. https://doi. org/10.1016/j.phytochem.2005.09.004 De La Cruz J, Hidalgo-Gallego A, Lora JM, Benitez T, Pintor-Toro J, Llobell A (1992) Isolation and characterization of three chitinases from Trichoderma harzianum. Eur J Biochem 206:859–867. https://doi.org/10.1111/j.1432-1033.1992.tb16994.x De Meyer G, Bigirimana J, Elad Y, Höfte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279–286. https://doi. org/10.1023/A:1008628806616 Dingle J, McGee PA (2003) Some endophytic fungi reduce the density of pustules of Puccinia recondita f. sp. tritici in wheat. Mycol Res 107:310–316. https://doi.org/10.1017/ S0953756203007512 Drahansky M, Paridah M, Moradbak A, Mohamed A, Owolabi F, Taiwo A, Asniza M, Abdul Khalid SH (2016) We are IntechOpen, the world’s leading publisher of open access books built by scientists, for scientists TOP 1%. Intech, London, p 13. https://doi.org/10.5772/57353 Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E et  al (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759. https://doi.org/10.1038/nrmicro2637 Dubey SC (2003) Integrated management of web blight of urd and mung bean. Indian Phytopathol 56:413–417 Dutta P, Das BC (2002) Management of collar rot of tomato by Trichoderma spp. and chemicals. Indian Phytopath 55:235–237 Elad Y (1983) Parasitism of Trichoderma spp. on Rhizoctonia solani and Sclerotium rolfsii-- scanning electron microscopy and fluorescence microscopy. Phytopathology 73:85. https://doi. org/10.1094/phyto-73-85 Elad Y, Kapat A (1999) The role of Trichoderma harzianum protease in the biocontrol of Botrytis cinerea. Eur J Plant Pathol 105:177–189. https://doi.org/10.1023/A:1008753629207 Esseling JJ, Emons AMC (2004) Dissection of nod factor signalling in legumes: cell biology, mutants and pharmacological approaches. J Microsc 214:104–113. https://doi. org/10.1111/j.0022-2720.2004.01322.x Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42:360–368

1  Agriculturally Important Fungi for Crop Protection

39

Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Büttner C, Grosch R et al (2010) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200. https://doi.org/10.1007/s00572-009-0279-5 Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM et  al (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–700. https://doi. org/10.1111/j.1364-3703.2007.00419.x Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126. https://doi.org/10.1093/jxb/ern059 Finlay R, Wallander H, Smits M, Holmstrom S, van Hees P, Lian B et  al (2009) The role of fungi in biogenic weathering in boreal forest soils. Fungal Biol Rev 23:101–106. https://doi. org/10.1016/j.fbr.2010.03.002 Fiori S, Fadda A, Giobbe S, Berardi E, Migheli Q (2008) Pichia angusta is an effective biocontrol yeast against postharvest decay of apple fruit caused by Botrytis cinerea and Monilia fructicola. FEMS Yeast Res 8:961–963. https://doi.org/10.1111/j.1567-1364.2008.00424.x Firáková S, Šturdíková M, Múčková M (2007) Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia 62:251–257. https://doi.org/10.2478/ s11756-007-0044-1 Franz A, Burgstaller W, Schinner F (1991) Leaching with Penicillium simplicissimum: influence of metals and buffers on proton extrusion and citric acid production. Appl Environ Microbiol 57:769–774 Galvez L, Douds DD, Drinkwater LE, Wagoner P (2001) Effect of tillage and farming system upon VAM fungus populations and mycorrhizas and nutrient uptake of maize. Plant Soil 228:299–308. https://doi.org/10.1023/A:1004810116854 Gangadevi V, Muthumary J (2008) Taxol, an anticancer drug produced by an endophytic fungus Bartalinia robillardoides Tassi, isolated from a medicinal plant, Aegle marmelos Correa ex Roxb. World J Microbiol Biotechnol 24:717–724. https://doi.org/10.1007/s11274-007-9530-4 Ganley RJ, Sniezko RA, Newcombe G (2008) Endophyte-mediated resistance against white pine blister rust in Pinus monticola. For Ecol Manag 255:2751–2760. https://doi.org/10.1016/j. foreco.2008.01.052 Gautam AK, Avasthi S (2019) Fungal endophytes: potential biocontrol agents in agriculture. In: Kumar A, Singh AK, Choudhary KK (eds) Role of plant growth promoting microorganisms in sustainable agriculture and nanotechnology. Woodhead Publishing, Cambridge, pp 241–283. https://doi.org/10.1016/B978-0-12-817004-5.00014-2 Gautam AK, Kant M, Thakur Y (2013) Isolation of endophytic fungi from Cannabis sativa and study their antifungal potential. Arch Phytopathol Plant Protect 46:627–635. https://doi.org/1 0.1080/03235408.2012.749696 Ghabooli M, Khatabi B, Ahmadi FS, Sepehri M, Mirzaei M, Amirkhani A et  al (2013) Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J Proteome 94:289–301. https://doi.org/10.1016/j. jprot.2013.09.017 Ghanem G, Ewald A, Zerche S, Hennig F (2014) Effect of root colonization with Piriformospora indica and phosphate availability on the growth and reproductive biology of a Cyclamen persicum cultivar. Sci Hortic 172:233–241. https://doi.org/10.1016/j.scienta.2014.04.022 Ghelis T, Dellis O, Jeannette E, Bardat F, Cornel D, Miginiac E et al (2000) Abscissic acid specific expression of RAB18 involves activation of anion channels in Arabidopsis thaliana suspension cells. FEBS Lett 474:43–47. https://doi.org/10.1016/S0014-5793(00)01574-X Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW et al (2016) Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol 7:1–20. https://doi. org/10.3389/fmicb.2016.00332 Goulard C, Hlimi S, Rebuffat S, Bodo B (1995) Trichorzins HA and MA, antibiotic peptides from Trichoderma harzianum: I. fermentation, isolation and biological properties. J Antibiot 48:1248–1253. https://doi.org/10.7164/antibiotics.48.1248

40

P. Selvasekaran and R. Chidambaram

Grandgirard J, Poinsot D, Krespi L, Nénon JP, Cortesero AM (2002) Costs of secondary parasitism in the facultative hyperparasitoid Pachycrepoideus dubius: does host size matter? Entomol Exp Appl 103:239–248 Grosch R, Scherwinski K, Lottmann J, Berg G (2006) Fungal antagonists of the plant pathogen Rhizoctonia solani: selection, control efficacy and influence on the indigenous microbial community. Mycol Res 110:1464–1474. https://doi.org/10.1016/j.mycres.2006.09.014 Guo B, Wang Y, Sun X, Tang K (2008) Bioactive natural products from endophytes: a review. Appl Biochem Microbiol 44:153–158 Haggag W (2008) Biotechnological aspects of plant resistant for fungal diseases management. Am J Sustain Agric 2:1–18 Haggag WM, Mohamed HAA (2002) Enhancement of antifungal metabolite production from gamma-ray induced mutants of some Trichoderma species for control onion white rot disease. Plant Pathol Bull 11:45–56 Haggag W, Mohamed H (2007) Biotechnological aspects of microorganisms used in plant biological control. Am J Sustain Agric 1:7–12 Hamayun M, Khan SA, Iqbal I, Na CI, Khan AL, Hwang YH et al (2009) Chrysosporium pseudomerdarium produces gibberellins and promotes plant growth. J Microbiol 47:425–430. https:// doi.org/10.1007/s12275-009-0268-6 Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I et al (2010) Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia 102:989–995. https://doi.org/10.3852/09-261 Handelsman J, Stabb EV (1996) Biocontrol of soil borne plant pathogens. Plant Cell 8:1855–1869. https://doi.org/10.1105/tpc.8.10.1855 Hanson LE, Howell CR (2004) Elicitors of plant defense responses from biocontrol strains of Trichoderma virens. Phytopathology 94:171–176 Haque MM, Ilias G, Molla A (2012) Impact of Trichoderma-enriched biofertilizer on the growth and yield of mustard (Brassica rapa L.) and tomato (Solanum lycopersicon Mill.). Agriculture 10:109–119. https://doi.org/10.3329/agric.v10i2.13148 Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/ mmbr.00050-14 Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194. https://doi.org/10.1094/PHYTO-96-0190 Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species- opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. https://doi.org/10.1038/nrmicro797 Harman GE, Björkman T, Ondik K, Shoresh M (2008) Changing paradigms on the mode of action and uses of Trichoderma spp. for biocontrol. Outlooks Pest Manag 19:24–29. https://doi. org/10.1564/19feb08 Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel KH (2013) The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol Plant-Microbe Interact 26:599–605. https:// doi.org/10.1094/MPMI-09-12-0216-R Hashem M, Agami R, Alamri SA (2012) Effect of soil amendment with yeasts as bio-­fertilizers on the growth and productivity of sugar beet. Afr J Agric Res 7:6613–6623. https://doi. org/10.5897/AJAR12.1989 Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110 Hock B (2012) Fungal associations, 2nd edn. Springer, Berlin, pp  1–406. https://doi. org/10.1007/978-3-642-30826-0 Howden R, Andersen CR, Coldsbrough B, Cobbett CS (1995) A cadmium-sensitive, glutathione-­ deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073

1  Agriculturally Important Fungi for Crop Protection

41

Howell CR, Stipanovic RD, Lumsden RD (1993) Antibiotic production by strains of Gliocladium virens and its relation to the biocontrol of cotton seedling diseases. Biocontrol Sci Tech 3:435–441. https://doi.org/10.1080/09583159309355298 Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS, Wheeler MH (2000) Erratum: induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 90:248–252 Huang YM, Srivastava AK, Zou YN, Ni QD, Han Y, Wu QS (2014) Mycorrhizal-induced calmodulin mediated changes in antioxidant enzymes and growth response of drought-stressed trifoliate orange. Front Microbiol 5:1–8. https://doi.org/10.3389/fmicb.2014.00682 Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191 Iqbal M, Ashraf M (2013) Gibberellic acid mediated induction of salt tolerance in wheat plants: growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environ Exp Bot 86:76–85. https://doi.org/10.1016/j.envexpbot.2010.06.002 Isaka M, Jaturapat A, Rukseree K, Danwisetkanjana K, Tanticharoen M, Thebtaranonth Y (2001) Phomoxanthones A and B, novel xanthone dimers from the endophytic fungus Phomopsis species. J Nat Prod 64:1015–1018. https://doi.org/10.1021/np010006h Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53. https://doi.org/10.1007/s00248-007-9249-7 Jakobsen I, Chen B, Munkvold L, Lundsgaard T, Zhu YG (2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant Cell Environ 28:928–938. https://doi.org/10.1111/j.1365-3040.2005.01345.x Jayalakshmi SK, Raju S, Usha Rani S, Benagi VI, Sreeramulu K (2009) Trichoderma harzianum L 1 as a potential source for lytic enzymes and elicitor of defense responses in chickpea (Cicer arietinum L.) against wilt disease caused by Fusarium oxysporum f. sp. ciceri. Aust J Crop Sci 3:44–52 Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M, Varma A et al (2013) Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behav 8:37–41. https://doi.org/10.4161/psb.26891 Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agric 52:103–122 Johri AK, Oelmüller R, Dua M, Yadav V, Kumar M, Tuteja N et al (2015) Fungal association and utilization of phosphate by plants: success, limitations, and future prospects. Front Microbiol 6:1–13. https://doi.org/10.3389/fmicb.2015.00984 Kapri A, Tewari L (2010) Phosphate solubilization potential and phosphatase activity of rhizospheric Trichoderma spp. Braz J Microbiol 41. https://doi.org/10.1590/ S1517-83822010005000001 Kaur T, Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Dhaliwal HS, Saxena AK (2020) Microbe-mediated biofortification for micronutrients: present status and future challenges. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 1–17. https://doi.org/10.1016/B978-0-12-820528-0.00002-8 Khan AL, Lee IJ (2013) Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol 13:86. https://doi. org/10.1186/1471-2229-13-86 Khan MR, Mohiddin FA (2018) Trichoderma: its multifarious utility in crop improvement. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, Amsterdam, pp 263–291. https://doi.org/10.1016/B978-0-444-63987-5.00013-X Khan SA, Hamayun M, Yoon H, Kim HY, Suh SJ, Hwang SK et al (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:1–10. https://doi.org/10.1186/1471-2180-8-231

42

P. Selvasekaran and R. Chidambaram

Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–861 Khan AL, Waqas M, Hamayun M, Al-Harrasi A, Al-Rawahi A, Lee IJ (2013) Co-synergism of endophyte Penicillium resedanum LK6 with salicylic acid helped Capsicum annuum in biomass recovery and osmotic stress mitigation. BMC Microbiol 13:51. https://doi. org/10.1186/1471-2180-13-51 Khokhar I, Haider MS, Mukhtar I, Mushtaq S (2013) Biological control of Aspergillus niger, the cause of Black-rot disease of Allium cepa L. (onion), by Penicillium species. J Agrobiol 29:23–28. https://doi.org/10.2478/v10146-012-0003-5 Kim S, Shin DS, Lee T, Oh KB (2004) Periconicins, two new fusicoccane diterpenes produced by an endophytic fungus Periconia sp. with antibacterial activity. J Nat Prod 67:448–450. https:// doi.org/10.1021/np030384h Kim HY, Choi GJ, Lee HB, Lee SW, Lim HK, Jang KS et  al (2007) Some fungal endophytes from vegetable crops and their anti-oomycete activities against tomato late blight. Lett Appl Microbiol 44:332–337. https://doi.org/10.1111/j.1472-765X.2006.02093.x Knecht K, Seyffarth M, Desel C, Thurau T, Sherameti I, Lou B et  al (2010) Expression of BvGLP-1 encoding a germin-like protein from sugar beet in Arabidopsis thaliana leads to resistance against phytopathogenic fungi. Mol Plant-Microbe Interact 23:446–457. https://doi. org/10.1094/MPMI-23-4-0446 Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:1–19. https://doi. org/10.3389/fpls.2019.00845 Koike N, Hyakumachi M, Kageyama K, Tsuyumu S, Doke N (2001) Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. Eur J Plant Pathol 107:523–533. https://doi.org/10.102 3/A:1011203826805 Kotze C, Van Niekerk J, Mostert L, Halleen F, Fourie P (2011) Evaluation of biocontrol agents for grapevine pruning wound protection against trunk pathogen infection. Phytopathol Mediterr 50:247–263 Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A, Sayyed RZ, Hesham AE-L, Dhaliwal HS, Saxena AK (2019a) Drought-tolerant phosphorus-solubilizing microbes: biodiversity and biotechnological applications for alleviation of drought stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting rhizobacteria for sustainable stress management, Rhizobacteria in abiotic stress management, vol 1. Springer, Singapore, pp 255–308. https:// doi.org/10.1007/978-981-13-6536-2_13 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019b) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Perspective for value-added products and environments, vol 2. Springer, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V, Dhaliwal HS, Saxena AK (2020a) Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolour L.) by drought-adaptive and phosphorus-solubilizing microbes. Biocatal Agric Biotechnol 23:101501. https://doi.org/10.1016/j.bcab.2020.101501 Kour D, Rana KL, Sheikh I, Kumar V, Yadav AN, Dhaliwal HS, Saxena AK (2020b) Alleviation of drought stress and plant growth promotion by Pseudomonas libanensis EU-LWNA-33, a drought-adaptive phosphorus-solubilizing bacterium. Proc Natl Acad Sci India Sec B Biol Sci. https://doi.org/10.1007/s40011-019-01151-4 Kour D, Rana KL, Yadav AN, Sheikh I, Kumar V, Dhaliwal HS, Saxena AK (2020c) Amelioration of drought stress in Foxtail millet (Setaria italica L.) by P-solubilizing drought-tolerant microbes with multifarious plant growth promoting attributes. Environ Sustain. https://doi. org/10.1007/s42398-020-00094-1

1  Agriculturally Important Fungi for Crop Protection

43

Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal HS, Saxena AK (2020d) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi. org/10.1016/j.bcab.2019.101487 Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71. https://doi.org/10.1016/j.biocontrol.2008.01.023 Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790. https://doi.org/10.1099/ mic.0.019869-0 Kumar M, Kour D, Yadav AN, Saxena R, Rai PK, Jyoti A, Tomar RS (2019a) Biodiversity of methylotrophic microbial communities and their potential role in mitigation of abiotic stresses in plants. Biologia 74:287–308. https://doi.org/10.2478/s11756-019-00190-6 Kumar V, Joshi S, Pant NC, Sangwan P, Yadav AN, Saxena A, Singh D (2019b) Molecular approaches for combating multiple abiotic stresses in crops of arid and semi-arid region. In: Singh SP, Upadhyay SK, Pandey A, Kumar S (eds) Molecular approaches in plant biology and environmental challenges. Springer, Singapore, pp  149–170. https://doi. org/10.1007/978-981-15-0690-1_8 Lakshmanan P, Jagadeesan R, Sudha A, Rajesh M, Prabhakara S, Prasad MA (2008) Potentiality of a new mushroom fungus Lentinus connatus Berk. for the production of biomanure from sugarcane trash (Saccharum officinarum L.) and its impact on the management of groundnut root rot diseases. Arch Phytopathol Plant Protect 41:273–289. https://doi. org/10.1080/03235400600680907 Lewis GC (2004) Effects of biotic and abiotic stress on the growth of three genotypes of Lolium perenne with and without infection by the fungal endophyte Neotyphodium lolii. Ann Appl Biol 144:53–63. https://doi.org/10.1111/j.1744-7348.2004.tb00316.x Li JY, Strobel GA (2001) Jesterone and hydroxy-jesterone antioomycete cyclohexenone epoxides from the endophytic fungus Pestalotiopsis jesteri. Phytochemistry 57:261–265. https://doi. org/10.1016/S0031-9422(01)00021-8 Li X, Zhang L (2015) Endophytic infection alleviates Pb2+ stress effects on photosystem II functioning of Oryza sativa leaves. J Hazard Mater 295:79–85. https://doi.org/10.1016/j. jhazmat.2015.04.015 Li HM, Sullivan R, Moy M, Kobayashi DY, Belanger FC (2004) Expression of a novel chitinase by the fungal endophyte in Poa ampla. Mycologia 96:526–536. https://doi.org/10.1080/1557253 6.2005.11832951 Li E, Jiang L, Guo L, Zhang H, Che Y (2008) Pestalachlorides A-C, antifungal metabolites from the plant endophytic fungus Pestalotiopsis adusta. Bioorg Med Chem 16:7894–7899. https:// doi.org/10.1016/j.bmc.2008.07.075 Li Z, Alves SB, Roberts DW, Fan M, Delalibera I, Tang J et al (2010) Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Sci Tech 20:117–136. https://doi.org/10.1080/09583150903431665 Lian B, Wang B, Pan M, Liu C, Teng HH (2008) Microbial release of potassium from K-bearing minerals by thermophilic fungus Aspergillus fumigatus. Geochim Cosmochim Acta 72:87–98. https://doi.org/10.1016/j.gca.2007.10.005 Lin C, Yang J, Sun H, Huang X, Wang R, Zhang KQ (2007) Purification and characterization of a β-1,3-glucanase from the novel mycoparasite Periconia byssoides. Biotechnol Lett 29:617–622. https://doi.org/10.1007/s10529-006-9287-0 Liu CH, Zou WX, Lu H, Tan RX (2001) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88:277–282. https://doi.org/10.1016/ S0168-1656(01)00285-1 Liu SY, Lo CT, Shibu MA, Leu YL, Jen BOY, Peng KC (2009) Study on the anthraquinones separated from the cultivation of Trichoderma harzianum strain Th-R16 and their biological activity. J Agric Food Chem 57:7288–7292. https://doi.org/10.1021/jf901405c

44

P. Selvasekaran and R. Chidambaram

Lopez DC, Sword GA (2015) The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control 89:53–60. https://doi.org/10.1016/j.biocontrol.2015.03.010 Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000a) New bioactive metabolites produced by. Plant Sci 151:67–73. https://doi.org/10.1016/S0168-9452(99)00199-5 Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000b) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151:67–73. https://doi. org/10.1016/S0168-9452(99)00199-5 Lumsden RD (1989) Biological control of damping-off caused by Pythium ultimum and Rhizoctonia solani with Gliocladium virens in soil less mix. Phytopathology 79:361. https:// doi.org/10.1094/phyto-79-361 Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R, Monte E et al (2012) Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl Environ Microbiol 78:4856–4868. https://doi.org/10.1128/ AEM.00385-12 Mane RS, Vedamurthy AB (2018) The fungal endophytes: sources and future prospects. J Med Plants Stud 6:121–126 Manoharachary C, Sridhar K, Singh R, Adholeya A, Suryanarayanan TS, Rawat S et al (2005) Fungal biodiversity: distribution, conservation and prospecting of fungi from India. Curr Sci 89:58–71 Marfori EC, Kajiyama S, Fukusaki EI, Kobayashi A (2002) Trichosetin, a novel tetramic acid antibiotic produced in dual culture of Trichoderma harzianum and Catharanthus roseus callus. Z Naturforsch 57:465–470. https://doi.org/10.1515/znc-2002-5-611 Marquez JA, Horan AC, Kalyanpur M, Lee BK, Loebenberg D, Miller GH et  al (1983) The Hazimicins, a new class of antibiotics. J Antibiot 36:1101–1108 Martinez C, Blanc F, Le Claire E, Besnard O, Nicole M, Baccou JC (2001) Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat-­denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 127:334–344. https://doi.org/10.1104/ pp.127.1.334 Martino E, Perotto S, Parsons R, Gadd GM (2003) Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biochem 35:133–141. https://doi.org/10.1016/S0038-0717(02)00247-X Massaccesi G, Romero MC, Cazau MC, Bucsinszky AM (2002) Cadmium removal capacities of filamentous soil fungi isolated from industrially polluted sediments, in La Plata (Argentina). World J Microbiol Biotechnol 18:817–820. https://doi.org/10.1023/A:1021282718440 Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414. https://doi.org/10.1016/j.pbi.2005.05.015 Mazid M, Khan Zeba H, Quddusi S, Khan TA, Mohammad F, Mohd M et al (2011) Significance of Sulphur nutrition against metal induced oxidative stress in plants. J Stress Physiol Biochem 7:165–184 Meesala S, Subramaniam G (2016) Penicillium citrinum VFI-51 as biocontrol agent to control charcoal rot of sorghum (Sorghum bicolor (L.) Moench). Afr J Microbiol Res 10:669–674. https://doi.org/10.5897/ajmr2015.7831 Mejía LC, Rojas EI, Maynard Z, Van Bael S, Arnold AE, Hebbar P et  al (2008) Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol Control 46:4–14. https://doi. org/10.1016/j.biocontrol.2008.01.012 Menon S, Mohan V (2007) Isolation of potential phosphate solubilizing bacteria from the rhizosphere of fast growing native tree species. pp 98–105 Metcalf DA, Wilson CR (2001) The process of antagonism of Sclerotium cepivorum in white rot affected onion roots by Trichoderma koningii. Plant Pathol 50:249–257. https://doi. org/10.1046/j.1365-3059.2001.00549.x

1  Agriculturally Important Fungi for Crop Protection

45

Miao FP, Liang XR, Yin XL, Wang G, Ji NY (2012) Absolute configurations of unique harziane diterpenes from Trichoderma species. Org Lett 14:3815–3817. https://doi.org/10.1021/ ol3014717 Miles CO, Lane GA, Di Menna ME, Garthwaite I, Piper EL, Ball OJP et al (1996) High levels of ergonovine and lysergic acid amide in toxic Achnatherum inebrians accompany infection by an Acremonium-like endophytic fungus. J Agric Food Chem 44:1285–1290. https://doi. org/10.1021/jf950410k Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Arbuscular mycorrhizas: physiology and function. Springer, Berlin, pp  3–18. https://doi. org/10.1007/978-94-017-0776-3_1 Miller CM, Miller RV, Garton-Kenny D, Redgrave B, Sears J, Condron MM et al (1998) Ecomycins, unique antimycotics from Pseudomonas viridiflava. J Appl Microbiol 84:937–944. https://doi. org/10.1046/j.1365-2672.1998.00415.x Mittal V, Singh O, Nayyar H, Kaur J, Tewari R (2008) Stimulatory effect of phosphate-­solubilizing fungal strains (Aspergillus awamori and Penicillium citrinum) on the yield of chickpea (Cicer arietinum L. cv. GPF2). Soil Biol Biochem 40:718–727. https://doi.org/10.1016/j. soilbio.2007.10.008 Mohiddin FA, Khan MR, Khan SM, Bhat BH (2010) Why Trichoderma is considered super hero (super fungus) against the evil parasites? Plant Pathol J 9:92–102. https://doi.org/10.3923/ ppj.2010.92.102 Molitor A, Zajic D, Voll LM, Pons-Kühnemann J, Samans B, Kogel KH et al (2011) Barley leaf transcriptome and metabolite analysis reveals new aspects of compatibility and Piriformospora indica-mediated systemic induced resistance to powdery mildew. Mol Plant-Microbe Interact 24:1427–1439. https://doi.org/10.1094/MPMI-06-11-0177 Monte E (2001) Understanding Trichoderma: between biotechnology and microbial ecology. Int Microbiol 4:1–4. https://doi.org/10.1007/s101230100001 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911 Murphy BR, Doohan FM, Hodkinson TR (2015) Fungal root endophytes of a wild barley species increase yield in a nutrient-stressed barley cultivar. Symbiosis 65:1–7. https://doi.org/10.1007/ s13199-015-0314-6 Nelson EB, Harman GE, Nash GT (1988) Enhancement of Trichoderma -induced biological control of Pythium seed rot and pre-emergence damping-off of peas. Soil Biol Biochem 20:145–150. https://doi.org/10.1016/0038-0717(88)90030-2 Nemčovič M, Jakubíková L, Víden I, Farkaš V (2008) Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol Lett 284:231–236. https://doi. org/10.1111/j.1574-6968.2008.01202.x Neubert K, Mendgen K, Brinkmann H, Wirsel SGR (2006) Only a few fungal species dominate highly diverse mycofloras associated with the common reed. Appl Environ Microbiol 72:1118–1128. https://doi.org/10.1128/AEM.72.2.1118-1128.2006 Nisa H, Kamili AN, Nawchoo IA, Shafi S, Shameem N, Bandh SA (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: A review. Microb Pathog 82:50–59. https://doi.org/10.1016/j.micpath.2015.04.001 Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17. https://doi. org/10.1007/s13199-009-0009-y Of O (2009) The world of organic agriculture, vol 2. IFOAM, Bonn, pp 42–54 Okoth SA, Otadoh JA, Ochanda JO (2011) Improved seedling emergence and growth of maize and beans by Trichoderma harzianum. Trop Subtrop Agroecosyst 13:65–71 Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorus acquisition. Appl Soil Ecol 86:41–54. https://doi.org/10.1016/j.apsoil.2014.09.012

46

P. Selvasekaran and R. Chidambaram

Pal S, Singh HB, Farooqui A, Rakshit A (2015) Fungal biofertilizers in Indian agriculture: perception, demand and promotion. J Eco-friendly Agric 10:101–113 Pan BF, Su X, Hu B, Yang N, Chen Q, Wu W (2015) Fusarium redolens 6WBY3, an endophytic fungus isolated from Fritillaria unibracteata var. wabuensis, produces peimisine and imperialine-3β-d-glucoside. Fitoterapia 103:213–221. https://doi.org/10.1016/j. fitote.2015.04.006 Panaccione DG (2005) Origins and significance of ergot alkaloid diversity in fungi. FEMS Microbiol Lett 251:9–17. https://doi.org/10.1016/j.femsle.2005.07.039 Park JH, Park JH, Choi GJ, Lee SW, Jang KS, Choi YH et al (2003) Screening for antifungal endophytic fungi against six plant pathogenic fungi. Mycobiology 31:179. https://doi.org/10.4489/ myco.2003.31.3.179 Pham GH, Kumari R, Singh A, Malla R, Prasad R, Sachdev M et  al (2008) Axenic culture of symbiotic fungus Piriformospora indica. Plant Surf Microbiol 30:593–613. https://doi. org/10.1007/978-3-540-74051-3_30 Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophytic fungi of wild banana (Musa acuminata) at Doi Suthep Pui National Park, Thailand. Mycol Res 105:1508–1513. https://doi. org/10.1017/S0953756201004968 Phuwapraisirisan P, Rangsan J, Siripong P, Tip-Pyang S (2006) 9-epi-viridiol, a novel cytotoxic furanosteroid from soil fungus Trichoderma virens. Nat Prod Res 20:1321–1325. https://doi. org/10.1080/14786410601101969 Polizzi V, Adams A, Picco AM, Adriaens E, Lenoir J, Van Peteghem C et  al (2011) Influence of environmental conditions on production of volatiles by Trichoderma atroviride in relation with the sick building syndrome. Build Environ 46:945–954. https://doi.org/10.1016/j. buildenv.2010.10.024 Porat R, Vinokur V, Weiss B, Cohen L, Daus A, Goldschmidt EE et al (2003) Induction of resistance to Penicillium digitatum in grapefruit by β-aminobutyric acid. Eur J Plant Pathol 109:901–907. https://doi.org/10.1023/B:EJPP.0000003624.28975.45 Porras M, Barrau C, Romero F (2007) Effects of soil solarization and Trichoderma on strawberry production. Crop Prot 26:782–787 Prasad RDNT (2015) Liquid formulation of Trichoderma species for management of gray mold in castor (Ricinus communis L.) and Alternaria leaf blight in sunflower (Helianthus annuus L.). J Biofertiliz Biopest 06:1–11 Prasad R, Kamal S, Sharma PK, Oelmüller R, Varma A (2013) Root endophyte Piriformospora indica DSM 11827 alters plant morphology, enhances biomass and antioxidant activity of medicinal plant Bacopa monniera. J Basic Microbiol 53:1016–1024. https://doi.org/10.1002/ jobm.201200367 Priyadharsini P, Muthukumar T (2017) The root endophytic fungus Curvularia geniculata from Parthenium hysterophorus roots improves plant growth through phosphate solubilization and phytohormone production. Fungal Ecol 27:69–77. https://doi.org/10.1016/j. funeco.2017.02.007 Promwee A, Issarakraisila M, Intana W, Chamswarng C, Yenjit P (2014) Phosphate solubilization and growth promotion of rubber tree (Hevea brasiliensis Muell. Arg.) by Trichoderma strains. J Agric Sci 6:8. https://doi.org/10.5539/jas.v6n9p8 Qiang X, Zechmann B, Reitz MU, Kogel KH, Schäfer P (2012) The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24:794–809. https://doi.org/10.1105/ tpc.111.093260 Rabeendran N, Moot DJ, Jones EE, Stewart A (2000) Inconsistent growth promotion of cabbage and lettuce from Trichoderma isolates. Pathol Fruit Veg N Z Plant Prot 53:143–146 Rabiey M, Ullah I, Shaw MW (2015) The endophytic fungus Piriformospora indica protects wheat from Fusarium crown rot disease in simulated UK autumn conditions. Plant Pathol 64:1029–1040. https://doi.org/10.1111/ppa.12335

1  Agriculturally Important Fungi for Crop Protection

47

Radhakrishnan R, Shim KB, Lee BW, Hwang CD, Pae SB, Park CH et al (2013) IAA-producing Penicillium sp. NICS01 triggers plant growth and suppresses Fusarium sp.-induced oxidative stress in sesame (Sesamum indicum L.). J Microbiol Biotechnol 23:856–863. https://doi. org/10.4014/jmb.1209.09045 Rahman MA, Rahman MM, Ferdousi M, Alam MF (2012) Use of culture filtrates of Trichoderma strains as a biological control agent against Colletotrichum capsici causing Anthracnose fruit rot disease of chili. J Biol Environ Sci 2:9–18 Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128. https://doi.org/10.1007/s005720100115 Rai A, Rai S, Rakshit A (2013) Mycorrhiza-mediated phosphorus use efficiency in plants. Environ Exp Biol 11:107–117 Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Diversity and enzymes perspectives, vol 1. Springer, Cham, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rana KL, Kour D, Yadav AN (2019c) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162 Rana KL, Kour D, Yadav N, Yadav AN (2020) Endophytic microbes in nanotechnology: current development, and potential biotechnology applications. In: Kumar A, Singh VK (eds) Microbial endophytes. Woodhead Publishing, Cambridge, pp 231–262. https://doi.org/10.1016/ B978-0-12-818734-0.00010-3 Rangel DEN, Finlay RD, Hallsworth JE, Dadachova E, Gadd GM (2018) Fungal strategies for dealing with environment- and agriculture-induced stresses. Fungal Biol 122:602–612. https:// doi.org/10.1016/j.funbio.2018.02.002 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37. https://doi.org/10.1007/s00425-002-0921-3 Rawat R, Tewari L (2011) Effect of abiotic stress on phosphate solubilization by biocontrol fungus Trichoderma sp. Curr Microbiol 62:1521–1526. https://doi.org/10.1007/s00284-011-9888-2 Reino JL, Guerrero RF, Hernández-Galán R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123. https://doi.org/10.1007/ s11101-006-9032-2 Richmond DS (2004) Competition between Turfgrasses and Dandelion. https://doi.org/10.2135/ cropsci2004.6000 Rivera-Varas VV, Freeman TA, Gudmestad NC, Secor GA (2007) Mycoparasitism of Helminthosporium solani by Acremonium strictum. Phytopathology 97:1331–1337. https:// doi.org/10.1094/PHYTO-97-10-1331 Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416. https://doi. org/10.1038/ismej.2007.106 Rüegsegger A, Schmutz D, Brunold C (1990) Regulation of glutathione synthesis by cadmium in Pisum sativum L. Plant Physiol 93:1579–1584. https://doi.org/10.1104/pp.93.4.1579

48

P. Selvasekaran and R. Chidambaram

Saba H (2012) Trichoderma  – a promising plant growth stimulator and biocontrol agent. Mycosphere 3:524–531. https://doi.org/10.5943/mycosphere/3/4/14 Samson RA (2016) Phylogenetic analysis of Penicillium subgenus Penicillium using partial β -tubulin sequences. Stud Mycol 49:175–200 Sankar P, Sharma RC (2001) Management of charcoal rot of maize with Trichoderma viride. Indian Phytopathol 54:390–391 Santos A, Marquina D (2004) Killer toxin of Pichia membranifaciens and its possible use as a biocontrol agent against grey mould disease of grapevine. Microbiology 150:2527–2534. https:// doi.org/10.1099/mic.0.27071-0 Saraf M, Thakkar A, Pandya U, Joshi M, Parikh J (2013) Potential of plant growth promoting microorganisms as biofertilizers and biopesticides and it’s exploitation in sustainable agriculture. J Microbiol Biotechnol Res 3:54–62 Saravanakumar K, Shanmuga Arasu V, Kathiresan K (2013) Effect of Trichoderma on soil phosphate solubilization and growth improvement of Avicennia marina. Aquat Bot 104:101–105. https://doi.org/10.1016/j.aquabot.2012.09.001 Saravanan VS, Kumar MR, Sa TM (2011) Bacteria in agrobiology: plant nutrient management. Bact Agrobiol Plant Nutr Manag. https://doi.org/10.1007/978-3-642-21061-7 Saxena J, Saini A, Ravi I, Chandra S, Garg V (2015) Consortium of phosphate-solubilizing bacteria and fungi for promotion of growth and yield of chickpea (Cicer arietinum). J Crop Improv 29:353–369. https://doi.org/10.1080/15427528.2015.1027979 Schwarzott D, Walker C, Schubler A (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421 Selim K (2012) Biology of endophytic fungi. Curr Res Environ Appl Mycol 2:31–82. https://doi. org/10.5943/cream/2/1/3 Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531. https://doi.org/10.1094/PHYTO-97-4-0523 Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58. https://doi.org/10.1016/j. plaphy.2012.07.018 Shahollari B, Varma A, Oelmüller R (2005) Expression of a receptor kinase in Arabidopsis roots is stimulated by the basidiomycete Piriformospora indica and the protein accumulates in Triton X-100 insoluble plasma membrane microdomains. J Plant Physiol 162:945–958. https://doi. org/10.1016/j.jplph.2004.08.012 Sharma G, Agrawal V (2013) Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica. World J Microbiol Biotechnol 29:1133–1138. https://doi.org/10.1007/s11274-013-1263-y Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P, Thakur S, Thakur N, Sudheer S, Yadav N, Yadav AN, Rastegari AA, Singh K (2019) Trichoderma: biodiversity, ecological significances, and industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Diversity and enzymes perspectives, vol 1. Springer, Cham, pp 85–120. https://doi.org/10.1007/978-3-030-10480-1_3 Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-­ degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in. J Biol Chem 280:26241–26247. https://doi.org/10.1074/jbc.M500447200 Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant-Microbe Interact 21:799–807. https://doi. org/10.1094/MPMI-21-6-0799

1  Agriculturally Important Fungi for Crop Protection

49

Shivanna MB, Meera MS, Hyakumachi M (1994) Sterile fungi from zoysiagrass rhizosphere as plant growth promoters in spring wheat. Can J Microbiol 40:637–644. https://doi. org/10.1139/m94-101 Siddiquee S, Cheong BE, Taslima K, Kausar H, Hasan MM (2012) Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. J Chromatogr Sci 50:358–367. https://doi.org/10.1093/ chromsci/bms012 Siddiqui ZA, Mahmood I (1996) Biological control of plant parasitic nematodes by fungi: a review. Bioresour Technol 58:229–239. https://doi.org/10.1016/S0960-8524(96)00122-8 Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L.  Protoplasma 248:503–511. https://doi.org/10.1007/s00709-010-0197-6 Singh DP, Singh HB (2008) Microbial wealth regulates crop quality and soil health. pp 25–26 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Singh A, Kumari R, Yadav AN, Mishra S, Sachan A, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–16. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Sivan A (1989) The possible role of competition between Trichoderma harzianum and Fusarium oxysporum on rhizosphere colonization. Phytopathology 79:198. https://doi.org/10.1094/ phyto-79-198 Sonaimuthu V, Krishnamoorthy S, Johnpaul M (2010) Taxol producing endophytic fungus Fusarium culmorum SVJM072 from medicinal plant of Tinospora cordifolia-a first report. J Biotechnol 150:425–425. https://doi.org/10.1016/j.jbiotec.2010.09.588 Song YC, Li H, Ye YH, Shan CY, Yang YM, Tan RX (2004) Endophytic naphthopyrone metabolites are co-inhibitors of xanthine oxidase, SW1116 cell and some microbial growths. FEMS Microbiol Lett 241:67–72 Song F, Dai H, Tong Y, Ren B, Chen C, Sun N et  al (2010) Trichodermaketones A-D and 7-O-methylkoninginin D from the marine fungus Trichoderma koningii. J Nat Prod 73:806–810. https://doi.org/10.1021/np900642p Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502. https://doi.org/10.1128/mmbr.67.4.491-502.2003 Sudha V, Govindaraj R, Baskar K, Al-Dhabi NA, Duraipandiyan V (2016) Biological properties of endophytic fungi. Braz Arch Biol Technol 59:1–7. https://doi. org/10.1590/1678-4324-2016150436 Sui Y, Wisniewski M, Droby S, Liu J (2015) Responses of yeast biocontrol agents to environmental stress. Appl Environ Microbiol 81:2968–2975. https://doi.org/10.1128/ AEM.04203-14 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh D, Abhilash P, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, research perspectives. Springer, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7 Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017. https://doi.org/10.1016/j.jplph.2010.02.013 Sun C, Shao Y, Vahabi K, Lu J, Bhattacharya S, Dong S et  al (2014) The beneficial fungus Piriformospora indica protects Arabidopsis from Verticillium dahliae infection by down regulation plant defense responses. BMC Plant Biol 14:1–16. https://doi.org/10.1186/ s12870-014-0268-5 Suwan S, Isobe M, Kanokmedhakul S, Lourit N, Kanokmedhakul K, Soytong K et  al (2000) Elucidation of high micro-heterogeneity of an acidic-neutral trichot-

50

P. Selvasekaran and R. Chidambaram

oxin mixture from Trichoderma harzianum by electrospray ionization q­uadrupole time-of-flight mass spectrometry. J Mass Spectrom 35:1438–1451. https://doi. org/10.1002/1096-9888(200012)35:123.0.CO;2-Q Swaby RJ (1949) The relationship between micro-organisms and soil aggregation. J Gen Microbiol 3:236–254. https://doi.org/10.1099/00221287-3-2-236 Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459. https://doi.org/10.1039/b100918o Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050. https://doi. org/10.1111/j.1365-2958.2005.04747.x Tintjer T, Rudgers JA (2006) Grass-herbivore interactions altered by strains of a native endophyte. New Phytol 170:513–521. https://doi.org/10.1111/j.1469-8137.2006.01720.x Treeby T, Bag PM (1992) The role of mycorrhizal fungi and non-mycorrhizal micro-organisms in iron nutrition of citrus. Soil Biol Biochem 24:857–864 Turbyville TJ, Wijeratne EMK, Liu MX, Burns AM, Seliga CJ, Luevano LA et al (2006) Search for Hsp90 inhibitors with potential anticancer activity: isolation and SAR studies of radicicol and monocillin I from two plant-associated fungi of the Sonoran desert. J Nat Prod 69:178–184. https://doi.org/10.1021/np058095b Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B et al (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant-Microbe Interact 21:1371–1383. https://doi.org/10.1094/MPMI-21-10-1371 Vahabi K, Sherameti I, Bakshi M, Mrozinska A, Ludwig A, Oelmüller R (2015a) Microarray analyses during early and later stages of the Arabidopsis/Piriformospora indica interaction. Genomics Data 6:16–18. https://doi.org/10.1016/j.gdata.2015.07.019 Vahabi K, Sherameti I, Bakshi M, Mrozinska A, Ludwig A, Reichelt M et al (2015b) The interaction of Arabidopsis with Piriformospora indica shifts from initial transient stress induced by fungus-released chemical mediators to a mutualistic interaction after physical contact of the two symbionts. BMC Plant Biol 15:1–15. https://doi.org/10.1186/s12870-015-0419-3 Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448. https://doi.org/10.1016/j.pbi.2008.05.005 Varma A, Bakshi M, Lou B, Hartmann A, Oelmueller R (2012) Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus. Agric Res 1:117–131. https://doi.org/10.1007/ s40003-012-0019-5 Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S et al (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159. https://doi.org/10.1016/j. funeco.2009.05.001 Venkateswarulu N, Shameer S, Bramhachari PV, Basha SKT, Nagaraju C, Vijaya T (2018) Isolation and characterization of plumbagin (5- hydroxyl- 2- methylnaptalene-1,4-dione) producing endophytic fungi Cladosporium delicatulum from endemic medicinal plants: Isolation and characterization of plumbagin producing endophytic fungi from endemic. Biotechnol Rep 20:e00282. https://doi.org/10.1016/j.btre.2018.e00282 Vero S, Garmendia G, González MB, Bentancur O, Wisniewski M (2013) Evaluation of yeasts obtained from Antarctic soil samples as biocontrol agents for the management of postharvest diseases of apple (Malus × domestica). FEMS Yeast Res 13:189–199. https://doi. org/10.1111/1567-1364.12021 Villa F, Cappitelli F, Cortesi P, Kunova A (2017) Fungal biofilms: targets for the development of novel strategies in plant disease management. Front Microbiol 8:1–10. https://doi.org/10.3389/ fmicb.2017.00654 Vimal SR, Singh JS, Arora NK, Singh S (2017) Soil-plant-microbe interactions in stressed agriculture management: a review. Pedosphere 27:177–192. https://doi.org/10.1016/ S1002-0160(17)60309-6

1  Agriculturally Important Fungi for Crop Protection

51

Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-­ plant-­ pathogen interactions. Soil Biol Biochem 40:1–10. https://doi.org/10.1016/j. soilbio.2007.07.002 Vinale F, Ghisalberti EL, Sivasithamparam K, Marra R, Ritieni A, Ferracane R et  al (2009) Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 48:705–711. https://doi. org/10.1111/j.1472-765X.2009.02599.x Vinale F, Nigro M, Sivasithamparam K, Flematti G, Ghisalberti EL, Ruocco M et  al (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347:123–129. https://doi.org/10.1111/1574-6968.12231 Viterbo A, Inbar J, Hadar Y, Chet I (2007) Plant disease biocontrol and induced resistance via fungal mycoparasites. In: Environmental and microbial relationships. Springer, Berlin, pp 127–146. https://doi.org/10.1007/978-3-540-71840-6_8 Volpin H, Phillips DA, Okon Y, Kapulnik Y (1995) Suppression of an isoflavonoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol 108:1449–1454. https://doi. org/10.1104/pp.108.4.1449 Vyas P, Bansal A (2018) Fungal endophytes: role in sustainable agriculture. Fungi their role. Sustain Dev Curr Perspect 7:107–120. https://doi.org/10.1007/978-981-13-0393-7_7 Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391. https://doi.org/10.1073/pnas.0504423102 Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. https://doi.org/10.1007/s00572-005-0033-6 Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH et al (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773. https://doi.org/10.3390/molecules170910754 Watts R, Dahiya J, Chaudhary K, Tauro P (1988) Isolation and characterization of a new antifungal metabolite of Trichoderma reesei. Plant Soil 107:81–84. https://doi.org/10.1007/BF02371547 Webster J, Lomas N (1964) Does Trichoderma viride produce gliotoxin and viridin? Trans Br Mycol Soc 47:535–540. https://doi.org/10.1016/s0007-1536(64)80031-0 Wei Y, Gao Y, Zhang X, Su D, Wang Y, Xu H (2007) Fungal diversity distribution and diversity of Epichloë. Fungal Divers 24:329–345 Wessels JGH (1999) Fungi in their own right. Fungal Genet Biol 27:134–145. https://doi. org/10.1006/fgbi.1999.1125 White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511. https://doi.org/10.1093/ aob/mcg164 Whitelaw MA (1999) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151. https://doi.org/10.1016/S0065-2113(08)60948-7 Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL (2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol Plant-­ Microbe Interact 13:1027–1033. https://doi.org/10.1094/MPMI.2000.13.10.1027 Wold WSM, Suzuki I (1976) The citric acid fermentation by Aspergillus niger: regulation by zinc of growth and acidogenesis. Can J Microbiol 22:1083–1092. https://doi.org/10.1139/m76-159 Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166. https://doi.org/10.1016/j.geoderma.2004.07.003 Xu F, Zhang Y, Wang J, Pang J, Huang C, Wu X et  al (2008) Benzofuran derivatives from the mangrove endophytic fungus Xylaria sp. (#2508). J Nat Prod 71:1251–1253. https://doi. org/10.1021/np070602x Yadav AN (2017) Agriculturally important microbiomes: biodiversity and multifarious PGP attributes for amelioration of diverse abiotic stresses in crops for sustainable agriculture. Biomed J Sci Tech Res 1:1–4

52

P. Selvasekaran and R. Chidambaram

Yadav AN (2018) Biodiversity and biotechnological applications of host-specific endophytic fungi for sustainable agriculture and allied sectors. Acta Sci Microbiol 1:01–05 Yadav AN (2019a) Endophytic fungi for plant growth promotion and adaptation under abiotic stress conditions. Acta Sci Agric 3:91–93 Yadav AN (2019b) Fungal white biotechnology: conclusion and future prospects. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Perspective for sustainable environments, vol 3. Springer, Cham, pp  491–498. https://doi. org/10.1007/978-3-030-25506-0_20 Yadav V, Kumar M, Deep AK, Kumar H, Sharma R, Tripathi T et al (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544. https://doi.org/10.1074/jbc.M110.111021 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan V, Dhaliwal HS, Saxena AK (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Verma P, Kour D, Rana KL, Kumar V, Singh B, Chauahan VS, Sugitha T, Saxena AK, Dhaliwal HS (2017b) Plant microbiomes and its beneficial multifunctional plant growth promoting attributes. Int J Environ Sci Nat Resour 3:1–8. https://doi.org/10.19080/ IJESNR.2017.03.555601 Yadav AN, Verma P, Singh B, Chauhan VS, Suman A, Saxena AK (2017c) Plant growth promoting bacteria: biodiversity and multifunctional attributes for sustainable agriculture. Adv Biotechnol Microbiol 5:1–16 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018) Biodiversity of the genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering, Penicillium system properties and applications. Elsevier, Amsterdam, pp  3–18. https://doi.org/10.1016/ B978-0-444-63501-3.00001-6 Yadav AN, Kour D, Rana KL, Yadav N, Singh B, Chauhan VS, Rastegari AA, Hesham AE-L, Gupta VK (2019a) Metabolic engineering to synthetic biology of secondary metabolites production. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  279–320. https://doi.org/10.1016/ B978-0-444-63504-4.00020-7 Yadav AN, Mishra S, Singh S, Gupta A (2019b) Recent advancement in white biotechnology through fungi, Diversity and enzymes perspectives, vol 1. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi, Perspective for sustainable environments, vol 3. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, Perspective for diversity and crop productivity, vol 1. Springer, Cham Yadav AN, Rastegari AA, Yadav N, Kour D (2020b) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020d) Plant microbiomes for sustainable agriculture. Springer, Cham Yang B, Wang XM, Ma HY, Yang T, Jia Y, Zhou J et al (2015) Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Front Microbiol 6:1–15. https://doi.org/10.3389/fmicb.2015.00982 Yao YQ, Lan F, Qiao YM, Wei JG, Huang RS, Li LB (2017) Endophytic fungi harbored in the root of Sophora tonkinensis Gapnep: diversity and biocontrol potential against phytopathogens. Microbiology 6:1–17. https://doi.org/10.1002/mbo3.437 Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070

1  Agriculturally Important Fungi for Crop Protection

53

Yedidia I, Benhamou N, Kapulnik Y, Chet I (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol Biochem 38:863–873. https://doi.org/10.1016/S0981-9428(00)01198-0 Yobo KS, Laing MD, Hunter CH (2009) Effects of single and dual applications of selected Trichoderma and Bacillus isolates on performance of dry bean seedlings grown in composted pine bark growth medium under shadehouse conditions. J Plant Nutr 32:1271–1289. https:// doi.org/10.1080/01904160903005996 Yong YH, Dai CC, Gao FK, Yang QY, Zhao M (2009) Effects of endophytic fungi on growth and two kinds of terpenoids for Euphorbia pekinensis. Chin Tradit Herb Drug 40:1136–1139 Yu H, Zhang L, Li L, Zheng C, Guo L, Li W, Sun P et al (2010) Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiol Res 165:437–449. https://doi.org/10.1016/j.micres.2009.11.009 Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61:3119–3128 Yuan Y, Feng H, Wang L, Li Z, Shi Y, Zhao LH et al (2017) Potential of endophytic fungi isolated from cotton roots for biological control against Verticillium wilt disease. PLoS One 12:1–12. https://doi.org/10.1371/journal.pone.0170557 Yue Q, Miller CJ, White JF, Richardson MD (2000) Isolation and characterization of fungal inhibitors from Epichloe 1 festucae. J Agric Food Chem 48:4687–4692 Zafari D, Koushki MM, Bazgir E (2008) Biocontrol evaluation of wheat take-all disease by Trichoderma screened isolates. Afr J Biotechnol 7:3650–3656 Zarea MJ, Hajinia S, Karimi N, Mohammadi Goltapeh E, Rejali F, Varma A (2012) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol Biochem 45:139–146. https://doi.org/10.1016/j. soilbio.2011.11.006 Zhang D, Duine JA, Kawai F (2002) The extremely high Al resistance of Penicillium janthinellum F-13 is not caused by internal or external sequestration of Al. BioMetals 15:167–174. https:// doi.org/10.1023/A:1015289808484 Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771. https://doi.org/10.1039/b609472b Zhou LS, Tang K, Guo SX (2018) The plant growth-promoting fungus (PGPF) Alternaria sp. A13 markedly enhances salvia miltiorrhiza root growth and active ingredient accumulation under greenhouse and field conditions. Int J Mol Sci 19:1–14. https://doi.org/10.3390/ijms19010270 Zou WX, Meng JC, Lu H, Chen GX, Shi GX, Zhang TY et al (2000) Metabolites of Colletotrichum gloeosporioides, an endophytic fungus in Artemisia mongolica. J Nat Prod 63:1529–1530. https://doi.org/10.1021/np000204t

Chapter 2

Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses Fatma A. Abo Nouh and Ahmed M. Abdel-Azeem

Contents 2.1  I ntroduction 2.2  A  biotic Stress Effect on Agriculture Crops 2.2.1  Salt 2.2.2  Drought 2.2.3  Temperature 2.2.4  Flood 2.2.5  Heavy Metals 2.3  Fungal Symbiont 2.4  Fungal Symbiosis 2.4.1  Habitat-Adapted Symbioses 2.5  Stress Tolerance Mechanisms 2.5.1  Osmotic Adjustment 2.5.2  Water-Use Efficiency 2.5.3  Osmotic Protection 2.5.4  Reactive Oxygen Species (ROS) 2.5.5  Antioxidant Enzymes 2.6  Fungi Conferring Adaptation of Agriculture Crops to Abiotic Stress 2.6.1  Salt Tolerance 2.6.2  Drought Tolerance 2.6.3  Heat Tolerance 2.6.4  Flood Tolerance 2.6.5  Heavy Metals Tolerance References

 55  57  58  59  59  60  60  61  62  64  65  65  65  66  66  67  67  68  69  70  71  71  72

2.1  Introduction Agriculture is considered to be one of the most vulnerable sectors to climate change. Crop production, particularly in tropical regions is facing increasing stresses caused due to natural and anthropogenic factors. Stress in plants refers to external

F. A. Abo Nouh · A. M. Abdel-Azeem (*) Systematic Mycology Laboratory, Botany Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_2

55

56

F. A. Abo Nouh and A. M. Abdel-Azeem

conditions that adversely affect growth, development, or productivity of plants (Verma et al. 2013). Stresses trigger a wide range of plant responses like altered gene expression, cellular metabolism, changes in growth rates, crop yields, etc. (Kour et al. 2019b). A plant stress usually reflects some sudden changes in environmental condition. Plant stress can be divided into two primary categories namely abiotic stress and biotic stress (Yadav et al. 2017a). Abiotic stress imposed on plants by environment may be either physical or chemical, while biotic stress exposed to the crop plants is a biological unit like diseases, insects, etc. (Verma et al. 2013). Plants in natural systems and crop lands are simultaneously exposed to both biotic and abiotic stresses. Abiotic stresses such as drought (water stress), excessive watering (water logging), extreme temperatures (cold, frost, and heat), salinity, and mineral toxicity negatively impact growth, development, yield, and seed quality of crops and other plants (Yadav et al. 2020c). Abiotic stress tolerance plays a vital role in determining crop productivity and distribution of plant species across the environment (Boyer 1982; Chaves et al. 2003). These factors are likely to cause serious negative impacts on crop growth and yields and impose severe pressure on our land and water resources (Grover et al. 2011). Environmental stresses such as drought, extreme temperatures, salinity, or chemical toxicity bring serious consequences to crop production, causing collectively more than 50% yield losses worldwide (Wang and Frei 2011). Due to global climate change, abiotic stresses are expected to become more widespread in the coming decades and will pose serious threats to global food security (Ashmore et al. 2006; Battisti and Naylor 2009). Among the environmental stresses, water stress commonly, known as “drought,” is considered as one of the major challenges to crop production worldwide (Yue et al. 2006; Kour et al. 2020a, 2020b, c). If the crop is subjected to stress, particularly drought during its early stage of growth, germination and seedling establishment are severely arrested mainly owing to low water uptake, low energy supply, and hindered enzyme functions (Okcu et al. 2005; Kour et al. 2019a). Oxidative stress, which frequently accompanies high temperature, salinity, or drought stress may cause denaturation of functional and structural proteins (Smirnoff 1998). Plant responses to abiotic stresses are complex, involving signal reception and transduction followed by genetic and physiological responses. It is perceived that all plants are capable of perceiving and responding to stress (Bartels and Sunkar 2005). Some biochemical processes which are common to all plant stress responses are: the production of osmolytes, altering water movement, and scavenging reactive oxygen species (ROS) (Singh et al. 2011). The interaction of microbes with the plant can be traced back to the origin of plants. Fossil records indicate that fungi have been associated with plants since at least 400 MYA and might have played an important role in the movement of plants from an aquatic arena to comparatively dry terrestrial habitats (Rodriguez et  al. 2008). The most well-known plant–microbe interaction is the mutualism between mycorrhizal fungi and plants where both partners generally benefit from each other (Verma et al. 2017a, b). However, under natural settings, plants form relationships with endophytic fungi which can be beneficial or harmful for the partners depending on host types and natural and environmental situations (Dastogeer and Wylie

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

57

2017). Nasim (2010) showed that the growth and health of colonized plants are improved and they obtain increased protection against biotic and abiotic stresses detrimental to their survival. Among the sustainable efforts, the role of root-associated microbes especially arbuscular mycorrhizal (AM) fungi in imparting stress tolerance has been exploited by many researchers in the recent years (Evelin et al. 2009; Garg and Singla 2012; Garg and Pandey 2015). Mycorrhizal symbioses are ubiquitous system of green technology. In these symbioses, the fungal mycelia scavenge through soil for resources (often phosphorus or nitrogen) and provide these resources to plants in exchange of organic carbon. The associations are mutualistic most often but sometimes exist as parasitism depending upon fungal nature (Prasad 2017). They are ubiquitous soilborne fungi, whose origin and divergence date back to over 450 million years (Gutjahr and Parniske 2013). Besides mycorrhizal endophytes, non-mycorrhizal endophytes (hereafter referred to as endophytes) have been recovered from most plants. Fungal endophytes are microfungi that internally infect living plant tissues without causing disease or any harm to plants, and live in mutualistic association with plants for at least a part of their life cycle (Rana et al. 2019a; Rodriguez et al. 2009; Lugtenberg et al. 2016; Jain and Pundir 2017; Lata et al. 2018; Chhipa and Deshmukh 2019). The existence of fungal endophytes from fossil records suggests that endophyte–host associations may have evolved from the time of development of first higher plants on earth (Dastogeer and Wylie 2017). The plant provides nutrition to the endophytes, while in return endophytes help in adaption to abiotic conditions like nutrients limitation, salination and extreme pH, drought, temperature variation, and protection from pathogens, insects, and nematodes (Chhipa and Deshmukh 2019; Abo Nouh 2019; Yadav et al. 2015a, b; Verma et al. 2016)

2.2  Abiotic Stress Effect on Agriculture Crops Fundamentally, plants require energy (light), water, carbon, and mineral nutrients for growth. Abiotic stress is defined as environmental conditions that reduce growth and yield below optimum levels. Plant responses to abiotic stresses are dynamic and complex (Skirycz and Inze 2010); they are both elastic (reversible) and plastic (irreversible). The plant responses to stress are dependent on the tissue or organ affected by the stress (Cramer et al. 2011). Abiotic stresses, such as drought, salinity, extreme temperatures (heat and cold), heavy metal toxicity, and oxidative stress are serious threats to agriculture and result in the deterioration of the environment (Singh et al. 2011; Saxena et al. 2016; Yadav 2017, 2019; Yadav and Yadav 2018). A global water shortage due to significant climatic changes is the leading cause of these abiotic stresses including drought, extreme temperatures, and salinity (Redman et al. 2011; Hussain et al. 2018). Abiotic stress is the primary cause of crop loss worldwide, reducing average yields for most major crop plants by more than 50% (Boyer 1982). Abiotic stress leads to a series of morphological, physiological, biochemical, and molecular changes that adversely affect plant growth and productivity (Yadav 2017;

58

F. A. Abo Nouh and A. M. Abdel-Azeem

Wang et  al. 2001). Drought, salinity, and extreme temperatures, which are often interconnected, result in oxidative burst and cellular damage (Kaur et al. 2020; Rana et al. 2020; Yadav et al. 2019b). For example, water stress and salinization, which are apparent osmotic stress, disrupt the ion distribution and metabolism in the cell (Raghuwanshi 2018). A plant’s first line of defense against abiotic stress is in its roots. One of the primary responses to abiotic stress such as high salinity is the disruption of the Na+/K+ ratio in the cytoplasm of the plant cell. The phytohormone abscisic acid (ABA) plays an important role during plant adaptation to environmental stress such as high salinity, drought, low temperature, or mechanical wounding (Gull et al. 2019). Among abiotic stresses, drought stress, soil salinity, and accumulation of heavy metals (HM) in the soil are one of the major grounds of diminished plant performance and restrained crop yield worldwide (López-Ráez 2016). In response, plants modify their root morphology, ultrastructure (Fusconi and Berta 2012), which may modulate their physiology and biochemistry to limit stress-­ induced damages and/or facilitate the repair of damaged systems (Latef et al. 2016).

2.2.1  Salt Salinity is defined as the presence of excessive amounts of soluble salts that hinder or affect the normal functions of plant growth (Yadav et  al. 2020b). Worldwide, more than 45 million hectares of irrigated land have been damaged by salt, and 1.5 million hectares are taken out of production each year as a result of high salinity levels in the soil (Munns and Tester 2008). It was found that salinity stress resulted in decrease of water content, accumulation of hydrogen peroxide, and electrolyte release in plants (Mandhania et al. 2006). Throughout the world about 45 million hectares of irrigated land is affected by salt (Munns and Tester 2008). Salt stress affects plants in numerous ways such as ion toxicity, nutritional disorders, physiological drought, oxidative stress, modification of metabolic processes, membrane incompetence, and reduction of cell division (Zhu 2007). At low salt concentrations, yields are mildly affected or not affected at all (Maggio et al. 2001). When a plant is exposed to high salt at germination it causes physiological drought and reduction in leaf expansion. The osmotic effects of salinity stress can be observed immediately after salt application and are believed to continue for the duration of exposure, resulting in inhibited cell expansion and cell division, as well as stomatal closure (Munns 2002). If plants are exposed for long time to salinity, plants face ionic stress, which can direct to premature senescence of adult leaves, and thus a reduction in the photosynthetic area available to support continued growth (Cramer and Nowak 1992). High salt concentration in soil affects plants in two ways such as high concentrations of salts in the soil upset the ability of roots to extract water, and high concentrations of salts within the plant itself can be toxic, resulting in an inhibition of many physiological and biochemical processes such as nutrient uptake and assimilation (Batool et al. 2014). During the onset and development of salt stress within a plant, all the major processes such as

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

59

photosynthesis, protein synthesis, and energy and lipid metabolism are affected (Carillo et al. 2011; Singh et al. 2020; Yadav et al. 2020a).

2.2.2  Drought Agricultural drought indicates an extended dry period that results in crop stress and crop yield. It causes the dehydration of cells and osmotic imbalance (Mahajan and Tuteja 2005). Water stress may occur either due to excess of water (i.e., flooding) or water-deficit (i.e., drought stress) conditions (Kour et al. 2020a, 2019b; Rana et al. 2019b). In the latter condition, the absence of adequate water table which is required for normal plant growth, development, and reproducibility results in drought/water stress (Latef et al. 2016). Severe droughts occur periodically in several major food-­ producing countries, having far-reaching impacts on global food production and supply. Drought is the most significant abiotic stress, adversely affecting the productivity and distribution of crop plants worldwide. For example, drought alone affects up to 45% of the global agricultural land (Hussain et al. 2018). Plants reduce their growth of shoots under drought conditions and reduce their metabolic demands. After that protective compounds are synthesized by plants under drought by mobilizing metabolites required for their osmotic adjustment (Gull et  al. 2019; Yadav et al. 2018a, b).

2.2.3  Temperature Greaves (1996) defines suboptimal temperature stress as any reduction in growth or induced metabolic, cellular, or tissue injury that results in limitations to the genetically determined yield potential, caused as a direct result of exposure to temperatures above or below the thermal thresholds for optimal biochemical and physiological activity or morphological development. High temperature stress causes extensive denaturation and aggregation of cellular proteins, which lead to cell death (Singh et al. 2011; Verma et al. 2019; Yadav et al. 2019a). Heat stress significantly affects plant growth and development by imparting loss of plant vigor and inhibition of seed germination, retarded growth rate, decreased biomass production, wilting and burning of leaves and reproductive organs, abscission and senescence of leaves, damage as well as discoloration of fruit, reduction in yield and cell death, and enhanced oxidative stress (Begum et al. 2019). The Intergovernmental Panel on Climate Change (IPCC 2007) reported that global temperatures are predicted to increase by 1.8–3.6 °C by the end of this century due to climate changes (Hussain et al. 2018). Increase in temperature throughout the globe has become a great concern, which not only affects the growth of plants but their productivity as well especially in agricultural crops plants. When plants encounter heat stress the percentage of seed germination, photosynthetic efficiency, and yield declines (Gull

60

F. A. Abo Nouh and A. M. Abdel-Azeem

et al. 2019). Low temperature stress causes impairment of metabolic processes, by alterations in membrane properties, changes in structure of proteins, and interactions between macromolecules as well as inhibition of enzymatic reactions (Verma et al. 2019; Yadav et al. 2018c; Singh et al. 2011).

2.2.4  Flood Flooding may be defined as any situation of excess water. Sudden inundation following high rainfall events also poses a severe physiological stress on crops. The effect of water logging of roots and lower stems are apparent as a range of symptoms on the shoots, including rapid wilting and severe physiological disruption (Latef et al. 2016). There are two typical kinds of flood. One is short duration over a few weeks and not very deep, termed a “flash flood” and the other is deep flooding that lasts for a long time, called as “deep-water flood.” Flash floods are unexpected and uncontrollable, and its flooding water level can reach 50 cm in the rain fed lowlands of the humid and semi-humid tropics of South and Southeast Asia. In these areas, flash floods at the seedling stage of rice cause severely reduced yields of rice grain (Hattori et al. 2011).

2.2.5  Heavy Metals Accumulation of toxic metals such as cadmium (Cd), lead (Pb), arsenic (As), and mercury (Hg) in the soil or within plants is considered as another abiotic stress that negatively affects environmental health and threatens ecosystem sustainable food production/sustainability. Such HMs are produced by various natural activities as well as by different anthropogenic activities such as metal smelting, use and drainage of chemical agro-products (e.g., fertilizers and pesticides), mining tail dumping, and burning of fossil fuels (Wang and Chen 2006). Heavy metal like Cu is taken up by plant cell by specific transport systems. “Free” Cu is extremely dangerous because it will reduce molecular oxygen leading to increased formation of superoxide, hydrogen peroxide, and hydroxyl radicals switching normal metabolism to programmed cell death (Singh et  al. 2011). At elevated levels, HMs have been documented to cause several morphological, physiological, biochemical, and structural changes in plants including inhibition of seed germination, decrease in root elongation, growth inhibition, disturbance in cellular homeostasis, suppression of photosynthesis rate, leaf chlorosis, and premature leaf senescence (Benavides et al. 2005; Kour et al. 2020d; Yadav et al. 2020d). In addition, toxic metals have been reported to get translocated to different plant parts where they interfere with active sites of many enzymes including phosphatase, ATPase, and enzymatic antioxidants (Latef et al. 2016), thereby destroying protein structures and replacing crucial elements resulting in deficiency symptoms (Bhandari and Garg 2017).

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

61

2.3  Fungal Symbiont There are two major classes of fungal symbionts associated with plants: (1) Endophytic fungi, which reside entirely within plant tissues and may be associated with roots, stems, and/or leaves; and (2) Mycorrhizal fungi that reside only in roots but extend out into the rhizosphere (Singh et al. 2011; Rana et al. 2019b). Based on the survey conducted in the last 20 years on endophytes, it is thought that the majority, if not all plants, have one or more types of these endophytes and numerous endophytic species; in some cases, above a hundred can be found in a certain plant species (Arnold 2007). Rodriguez et al. (2009) classified the endophytes under two major groups, viz. clavicipitaceous and non-clavicipitaceous on the basis of phylogeny and life history traits. Clavicipitaceous fungal endophytes are limited to certain grasses, while non-clavicipitaceous ones have a broad host range including both nonvascular and vascular plant species. In addition, recent reviews propose that members of the non-clavicipitaceous group can be segregated into three subgroups on the basis of host range, type of tissue infected, pattern spread, in planta infection and the establishment, diversity, and benefits given to hosts (Rodriguez et al. 2009; Dastogeer and Wylie 2017). Endophytic fungi which are predominantly ascomycetous are ubiquitous and have been isolated from all groups of plants starting from the lower forms like mosses and ferns to the higher ones including the conifers and the angiosperm plants (Arnold 2007), as they have been recovered from plants adapted to a wide range of ecosystems that include hot deserts, Arctic tundra, mangroves, temperate and tropical forests, grasslands and savannahs, croplands (Lugtenberg et al. 2016), and extreme arctic, alpine, and xeric environments (Ali et al. 2018). Colonization by endophytic fungi promotes plant growth by protecting against several fungal and bacterial borne diseases, assisting in the uptake of available phosphorus or improving the ecological adaptation abilities of the host by providing tolerance to counteract against biotic and abiotic stresses (Schulz et al. 1999; Schulz and Boyle 2005; Yadav et al. 2017a, b). Endophytic fungi have been classified into Clavicipitales, with few hosts within the monocots, and non-clavicipitaceous species inhabiting both monocots and eudicots (Carroll 1988), which probably represent the majority of microbial symbionts which interact with plants, with a great diversity occurring both at taxonomical and at functional levels (Jain and Pundir 2017). Class 2 endophytes have a broad host range of both monocot and eudicot plants, are the largest group of fungal symbionts, are readily culturable on artificial media, and are thought to colonize all plants in natural ecosystems (Rodriguez et al. 2008). Class 2 endophytes confer stress tolerance to host species and play a significant role in the survival of at least some plants in high-stress environments (Rodriguez et al. 2004). For example, class 2 endophytes confer heat tolerance to plants growing in geothermal soils (Redman et al. 2002), the extent of tree leaf colonization by endophytes correlates with the ability to resist pathogens (Arnold et al. 2003), and endophytes confer drought tolerance to multiple host species (Waller et al. 2005).

62

F. A. Abo Nouh and A. M. Abdel-Azeem

Mycorrhizae are highly evolved soil fungi involved in tripartite interaction mutualistic associations amid soil and plant. The associations formed by Glomeromycota fungi in plants usually colonize in arbuscules and often vesicles thus, known as vesicular mycorrhiza (AM) and vesicular-arbuscular mycorrhizas (VAM). These are members of Zygomycetes, Ascomycetes, and Basidiomycetes classes of fungi kingdom (Prasad 2017). The term symbiosis in mycorrhiza association is used to describe their highly interdependent or obligatory mutualistic relationships with the plants where the host plant receives mineral nutrients and in turn fungus harness photosynthetically derived carbon compounds (Prasad 2015). AMF, belonging to the phylum Glomeromycota (Schüβler et al. 2001) are the obligate biotrophs that have been documented to form symbioses with the roots of more than 80% of terrestrial plant species (except in the plants belonging to families Amaranthaceae, Brassicaceae, Proteaceae, Commelinaceae, Polygonaceae, Cyperaceae, Juncaceae, and Chenopodiaceae) (Gutjahr and Parniske 2013). Mycorrhizal symbionts have long been investigated and considered as the primary mutualistic fungal symbionts associated with plant roots (Diouf et al. 2003). AMF found in rhizosphere and associated with several vascular plants have tremendous contribution in sustainable agriculture as well as agricultural ecosystems management (Prasad 2017). The beneficial effects of indigenous AM fungi on the nutrition replenishment for plants depend on both the abundance and type of fungi present in the soil (Prasad and Gautam 2000). AMF also benefit plants by increasing nutrient water uptake, resistance against phytopathogens, adaptation to a variety of environmental stresses such as drought, heat, salinity and heavy metal contamination, production of growth hormones and certain enzymes, and even in the uptake of radioactive elements (Prasad 2017). AMF are ecologically significant to the majority of vascular plants. It is quite easier to separate the list of mycorrhizae from others (Harley and Smith 1983).

2.4  Fungal Symbiosis Symbiosis, defined as the permanent association between two or more specifically distinct organisms, at least during a part of the life cycle, is known to be a ubiquitous and important aspect of life on Earth (Kour et  al. 2019b). Evolutionarily, plants require some specialized microbial partners in order to adapt to certain ecological niches and maintain their normal growth and development (Yuan et al. 2010; Rana et al. 2019c). There are several outcomes of symbiotic interactions defined by the fitness benefits realized by each partner (Lewis and Clements 1986). Benefits to fungal symbionts can be positive (mutualism, commensalism, and parasitism), neutral (amensalism and neutralism), or negative (competition). Benefits to host plants can also be positive (mutualism), neutral (commensalism and neutralism), or negative (parasitism, competition, and amensalism) (Rodriguez et al. 2008). While it is fairly straightforward to determine the impact of symbiosis on host fitness, it is more challenging to determine the benefits for fungal endophytes. Mutualistic benefits for endophytes may involve acquiring nutrients from hosts, abiotic and biotic

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

63

stress avoidance and dissemination by seed transmission (Schardl et  al. 2004; Schulz 2006). Commensal symbioses have no beneficial or detrimental effects on hosts whereas parasitic symbioses negatively affect host fitness by decreasing growth rates and/or fecundity, or inducing disease symptoms that may result in lethality (Redman et al. 2001). Successful plant–fungal symbioses involve at least three events: penetration by the fungus into plant tissues; colonization of plant tissues by the invading fungus; expression of a fungal symbiotic lifestyle (Pieterse and Dicke 2007; Yadav et  al. 2019d). It is assumed that some form of biochemical and/or genetic communication occurs between the symbionts and hosts that allow mutualists to confer physiological benefits to hosts (Singh et al. 2011). Rodriguez et al. (2008) however, current studies suggest that fungi may express different symbiotic lifestyles in response to host genotypes or environmental factors (Yadav et al. 2019c). For example, depending on the physiological status of plants, some mycorrhizal fungi may be mutualistic or parasitic (Johnson et al. 1997). One of the most interesting aspects of lifestyle expression is that the initial phases of infection and colonization by pathogens, mutualists, and commensals are identical for many fungi (Rodriguez et al. 2004). Thus, the mode of recognition and early signaling processes are crucial in understanding how a plant can differentiate between a beneficial and a detrimental microbe and express a lifestyle accordingly (Vadassery and Oelmüller 2009). A very early event in the interaction of pathogenic, mycorrhizal, or endophytic microbes with a plant cell is an increase in the intracellular calcium (Ca2+) levels within seconds or minutes after the recognition of the two partners. Ca2+ ion is a second messenger in numerous plants signaling pathways, coupling extracellular stimuli to intracellular and whole-plant responses. The cellular Ca2+ level is tightly regulated and even a small change in its concentration provides information for protein activation and signaling (Vadassery and Oelmüller 2009; Singh et al. 2011). A diverse kind of relationships exists between the fungal endophytes and plant ranging from mutualistic (Redman et al. 2002), symbiotic, and commensal (Deckert et al. 2001) to pathogens (Schulz et al. 1998). However, the state of the interaction between endophyte and host may be transitory, and many factors could make changes in their mode of interaction (Schardl et  al. 2004). For example, Colletotrichum spp. are classified as virulent pathogens, yet several species can express mutualistic lifestyles in non-disease hosts. Mutualistic benefits conferred by Colletotrichum spp. include disease resistance, growth enhancement, and/or drought tolerance (Redman et al. 2001; Singh et al. 2011). When C. magna is introduced into different tomato cultivars, the fungus may express mutualistic, commensal, or parasitic lifestyles. Whereas parasitic and mutualistic lifestyles are easily observed, commensal lifestyles are often designated when no host fitness benefit is observed. However, depending on the traits being assessed, the commensal designation may be misleading (Rodriguez and Redman 2008). For example, C. gloeosporioides was designated a pathogen of strawberry and a commensal of tomato because it conferred no disease protection (Redman et al. 2001); Nevertheless, C. gloeosporioides increased plant biomass and conferred drought tolerance to tomato plants and was therefore designated a mutualist (Rodriguez and Redman 2008).

64

F. A. Abo Nouh and A. M. Abdel-Azeem

2.4.1  Habitat-Adapted Symbioses In fact, symbiotic fungi are responsible for the adaptation of plants to environmental stresses (Khan et al. 2012), and these tolerances can be transferred to agricultural plants (Rodriguez et  al. 2008; Redman et  al. 2011); these endophytes have been commercialized to improve agriculture in relation to climate changes, which involve increasing tolerance to drought and water stress and tolerance to high temperature and high salinity (Lugtenberg et al. 2016). The ability of endophytes recovered from grasses were applied to confer drought & water stress, high temperature and high salinity to genetically distant plants such as tomato (Chaw et al. 2004). The concept that fungal endophytes adapt to stress in a habitat-specific manner has been confirmed with different fungal and plant species, and different environmental stresses (Redman et al. 2002). This habitat-specific adaptation is defined as HA-symbiosis, and it is hypothesized that this allows plants to establish and survive in high-stress habitats (Rodriguez and Redman 2008). During performing laboratory and field studies of Class II endophytes from plants from geothermal soils, coastal beaches, and agricultural fields, Rodriguez and co-researchers observed a new ecological phenomenon and defined as habitat-adapted symbiosis. They have determined that endophytes from these habitats confer habitat-specific stress tolerance to plants. This habitat-specific phenomenon provides an intergenomic epigenetic mechanism for plant adaptation and survival in high-stress habitats (Rodriguez et  al. 2008; Singh et al. 2011). For example, within the geothermal soils of Yellowstone National Park, WY, a plant species (Dichanthelium lanuginosum) has been studied and found to be colonized by one dominant endophyte (Curvularia protuberata). C. protuberate confers heat tolerance to the host plant, and neither the fungus nor the plant can survive separately from one another when exposed to heat stress >38 °C (Redman et al. 2002). A comparative study of C. protuberata isolates from geothermal and nongeothermal plants revealed that the ability to confer heat tolerance was specific to isolates from geothermal plants, hence the ability to confer heat tolerance is a habitat-adapted phenomenon (Rodriguez et  al. 2008). Another example, a native dunegrass (Leymus mollis) on coastal beaches of Puget Sound, WA, L. mollis which is colonized by one dominant fungal endophyte (Fusarium culmorum), F. culmorum confers salt tolerance to the host plant which cannot survive in coastal habitats without the habitat-adapted endophyte. A comparative evaluation of F. culmorum isolates from L. mollis and a noncoastal plant revealed that the ability to confer salt tolerance was specific to isolates from the coastal plants, indicating that the ability to confer salt tolerance is a habitat-adapted phenomenon (Rodriguez et  al. 2008; Singh et al. 2011). Evaluation of C. protuberata, F. culmorum, and C. magna isolates further supports habitat-specific adaptation of endophytes: C. protuberata confers heat but not disease or salt tolerance; F. culmorum confers salt but not heat or disease tolerance; and C. magna confers disease but not heat or salt tolerance (Rodriguez et al. 2008).

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

65

2.5  Stress Tolerance Mechanisms Symbiotically conferred stress tolerance involves at least two mechanisms: (1) activation of host stress response systems soon after exposure to stress, allowing the plants to avoid or mitigate the impacts of the stress (Redman et al. 1999) and (2) biosynthesis of antistress biochemicals by endophytes (Miller et al. 2002)

2.5.1  Osmotic Adjustment Drought, heat, and salt stress affect plant–water relations triggering complex plant responses, which include increased production of osmolytes (Bray 1997). Osmotic potential is determined primarily by two components: solute potential and matrix potential, and it is likely that symbiotic fungi contribute to the matrix potential, which is particularly important in helping plants retain water and thereby enhance plant drought tolerance (Singh et al. 2011). Upon exposure to heat stress, nonsymbiotic panic grass and tomato plants significantly increased osmolyte concentrations as predicted. Increased osmolyte concentrations correlated with the development of subsequent wilting and desiccation symptoms prior to plant death (Rodriguez et al. 2008). In contrast, symbiotic plants either maintained the same (panic grass and Rutgers tomato), (Márquez et al. 2007) or lower (Tiger-Like tomato) (Rodriguez et al. 2008), osmolyte concentrations when compared to non-stressed controls. The differences in osmolyte patterns in tomato may be reflective of differences in the varieties (Rutgers versus Tiger-Like). Most investigations of Epichloe effects on stress tolerance focus on osmotic adjustment, water relations and drought recovery (Cheplick et al. 2000), accumulation of drought protective osmolytes in the grass tissues (Richardson et al. 1992), and photosynthetic rates under water or heat stress (Amalric et al. 1999). Under water stress, the tall fescue endophyte is also associated with a significant increase in cell wall elasticity as measured by bulk modulus tissue elasticity, and by turgid weight to dry weight ratio (TW/DW) (White et al. 1992); likewise, Neotyphodium uncinatum increases TW/DW in water-stressed meadow fescue (Rodriguez et al. 2008).

2.5.2  Water-Use Efficiency Symbiotic plants consumed significantly less water than nonsymbiotic plants regardless of the colonizing endophyte. Panic grass, rice, tomato, and dunegrass plants all used significantly less fluid than nonsymbiotic plants (Singh et al. 2011). Since these symbiotic plants achieve increased biomass levels, decreased water consumption suggests more efficient water usage. Decreased water consumption and increased water-use efficiency may provide a unique mechanism for symbiotically

66

F. A. Abo Nouh and A. M. Abdel-Azeem

conferred drought tolerance. Substantial (>50%) stand losses in tall fescue were reported after removing the endophyte from this grass (Read and camp 1986). These losses are typically associated with drought periods, and endophyte-infected tall fescue exhibits improved recovery after drought compared to endophyte-free tall fescue (Arachevaleta et al. 1989). It was suggested that grass endophytes, particularly N. coenophialum in tall fescue, affect plant–water relations, nutrient acquisition, as well as allocation and photosynthetic assimilation (Bacon 1993).

2.5.3  Osmotic Protection Osmotic protection is more likely than stomatal conductance to be involved in drought protection in tall fescue, (Richardson et al. 1993) but reduced stomatal conductance might be important to conserving water in Festuca arizonica–Neotyphodium sp. interactions (Morse et al. 2002). Some speculation regarding osmoprotectants centers around the fungal loline alkaloids, which are abundant in those symbiota for which the endophyte has a documented and consistent positive effect on drought tolerance (Malinowski and Belesky 2000). Other potential osmoregulators and protectants are soluble sugars and sugar alcohols, produced by the endophyte, plant, or both (Richardson et al. 1992).

2.5.4  Reactive Oxygen Species (ROS) A plant biochemical process common to all abiotic and biotic stresses is the accumulation of ROS.  ROS are extremely toxic to biological cells causing oxidative damage to DNA, lipids, and proteins. On the other hand, ROS can act as signaling molecules for stress responses and generation of ROS is an early event in plant response to stress (Apel and Hirt 2004). Tanaka et al. (2006) Therefore, in a pathogenic or symbiotic association, both the plant and the microbe must be able to deal with a complex mixture of ROS coming from both sides. ROS are not necessarily harmful for the partners and, depending on the model considered, they can also help to signal and limit/control the interaction (Rouhier et al. 2008). Certainly, low ROS concentrations are known to be required for signaling, growth, and development, while high concentrations are detrimental to the cell and can damage various macromolecules. It is of primary importance for the development of plant–microbe interactions that ROS produced at the interface between the partners, that is, in the extracellular matrices, cell walls, and more generally the apoplast compartment (Rouhier et al. 2008). Symbiotic and nonsymbiotic plants when exposed to ±stress (panic grass and tomato to heat stress and dunegrass and tomato to salt stress) revealed that in the absence of stress, both nonsymbiotic and symbiotic plant leaf tissues for all plants (panic grass, tomato, dunegrass) remained green indicating the absence of ROS

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

67

generation and hence lack of stress response. In contrast, when exposed to stress, nonsymbiotic tissues bleached white indicating the generation of ROS while symbiotic tissues remained green. This suggests that endophytes either scavenge ROS or induce plants to more efficiently scavenge ROS, or prevent ROS production when exposed to abiotic stress (Singh et al. 2011).

2.5.5  Antioxidant Enzymes It is a common belief that antioxidant enzymes play an important role in fungal symbiosis conferring abiotic stress tolerance. These enzymes include the low molecular-weight compounds are involved in the removal of ROS either directly (superoxide dismutases, catalases and ascorbate- or thioldependent peroxidases) or indirectly through the regeneration of the two major redox molecules in the cell, ascorbate and glutathione (glutathione reductases, dehydroascorbate reductases, and monodehydroascorbate reductases) (Rouhier et al. 2008). An interesting feature of the interplay between oxidants and antioxidants is that it occurs in all subcellular compartments including plastids and mitochondria, two sites of extensive ROS production (Navrot et  al. 2007). Under salt stress conditions P. indica increases the tolerance of a salt-sensitive barley (Hordeum vulgare) cultivar to severe salt stress. P. indica-colonized plants contained higher ascorbate concentrations in roots compared with noncolonized plants, while the ratio of ascorbate vs. dehydroascorbate was not significantly altered and catalase, ascorbate peroxidase, glutathione reductase, dehydroascorbate reductase, and monodehydroascorbate reductase activities were increased (Waller et al. 2005; Singh et al. 2011).

2.6  F  ungi Conferring Adaptation of Agriculture Crops to Abiotic Stress Several studies have shown that endophytes may be profitable to plants harnessing in stressed conditions, like the presence of pollutants, heavy metals, organic compounds with chlorinated aromatic molecules, high salinity, elevated temperature, and drought, by basically controlling the oxidative stress (Raghuwanshi 2018). Class II endophytes confer heat tolerance to plants growing in geothermal soils (Redman et al. 2002), the extent of tree leaf colonization by endophytes correlates with the ability to resist pathogens (Arnold et  al. 2003) and endophytes confer drought tolerance to multiple host species (Waller et al. 2005). Class I endophytes frequently increase plant biomass, confer drought tolerance, and produce chemicals that are toxic to animals and decrease herbivory (Singh et al. 2011). For example, Neotyphodium and Epichloë endophytes as grass symbionts which improved the plant’s growth and its ability to resist biotic and abiotic stresses and found that

68

F. A. Abo Nouh and A. M. Abdel-Azeem

volatile organic compounds have shown to be important in plant’s response to stress factors (Jain and Pundir 2017). The plant’s root colonized with P. indica showed tolerance in different abiotic stresses like extreme temperature, salinity, drought, and heavy metals (Chhipa and Deshmukh 2019). Mycorrhizal symbiosis is a key component in helping plants survive under adverse environmental conditions (Augé et  al. 1992). AMF benefit plants by increasing nutrient water uptake, resistance against phytopathogens, and adaptation to a variety of environmental stresses such as drought, heat, salinity, and heavy metal contamination (Prasad 2017).

2.6.1  Salt Tolerance Less availability of water to the agricultural fields and consequent increase in soil salinization have become a growing challenge in the agricultural sector in many parts of the world and are expected to raise due to climate change effects. Grass species growing on coastal areas harbor symbiotic fungal endophytes which strengthen them against salinity and heat (Rodriguez et al. 2008). These endophytes have been reported to induce salt tolerance in several noncoastal plants. Leymus mollis (dunegrass), plants harboring endophyte Fusarium culmorum, flourished on the coastal beaches of the USA, which are areas of high salinization. Salt-sensitive plants not growing in coastal areas were able to develop salt tolerance when inoculated with the endophyte Fusarium culmorum (Rodriguez et  al. 2008). Redman et al. (2011) showed that some class 2 fungal endophytes can confer salt and drought tolerance to two commercial rice varieties which were not adapted to these stresses. Moreover, these endophytes reduced water consumption by 20–30% while increasing growth rate, reproductive yield, and biomass of greenhouse grown plants. Colonization of plants by P. indica shows salt tolerance, and this attribute is well demonstrated in tobacco (Nicotiana) and members of Poaceae family like barley (Hordeum vulgare L.), wheat (Triticum), and rice (Oryza sativa) which involve the detoxification of ROS by initiating production of antioxidants and enhancing the photosynthetic efficiency (Johnson et al. 2014). Tolerance of the host Festuca arundinacea against a hydrocarbon mixture was enhanced by endophytic fungi Lewia (Cruz-Hernández et al. 2013). The endophytic fungi Lewia sp. has been isolated from Limonium tetragonum and Phragmites australis, which grow in high salt conditions (Khalmuratova et al. 2015). Colletotrichum magna and C. protuberata are well reported for water stress tolerance in wheat (Triticum sp.), tomato (Solanum lycopersicum), and watermelon (Citrullus lanatus) plants (Raghuwanshi 2018). Penicillium sp. and Phoma glomerata significantly increased plant biomass, related growth parameters, assimilation of essential nutrients such as potassium, calcium, magnesium, and reduced the sodium toxicity in cucumber plants under salinity and drought stress, when compared with control plants (Abo Nouh 2019). Trichoderma sp. and P. indica showed drought and salt tolerance in cacao, barley, and Chinese cabbage plant (Chhipa and Deshmukh 2019).

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

69

AMF fungi widely occur in salt stressed environment (Wang and Liu 2001). Recent literature suggest that AM fungi play a vital role in alleviating the effects of salinity (Al-Karaki et al. 2001a, b) and enhance the ability of the plants to cope with salt stress (Jahromi et al. 2008) by compensating nutritional imbalances imposed by salinization through improved nutrient acquisition, improving plant nutrient uptake (Asghari et al. 2005) and ion balance (Giri et al. 2007) protecting enzyme activity (Rabie and Almadini 2005) and facilitating water uptake (Ruiz-Lazano and Azcon 1995). Salt resistance was improved by AM colonization in maize (Feng et  al. 2000), mung bean (Jindal et al. 1993), and clover (Ben Khaled et al. 2003) with the AM effect correlated with improved osmoregulation or proline accumulation. Also enhance relative water content in Zucchini leaves (Colla et al. 2008), water potential of maize plants (Feng et al. 2000), and chlorophyll concentration in the leaves of several plant species like Sesbania aegyptiaca, S. grandiflora, and Lotus glaber (Sannazzaro et al. 2006). Mycorrhizal maize plants had greater biomass than non-­ mycorrhizal plants under salt stress, thus implying that mycorrhizal plants grow better than non-mycorrhizal plants under saline conditions (Sheng et  al. 2008). Similar trend were also reported in various other crops, e.g., tomato (Al-Karaki et al. 2001a, b), cotton (Feng and Zhang 2003), and barley (Mohammed et al. 2003). AMF-inoculated Allium sativum plants showed improved growth traits including leaf area index, and fresh and dry biomass under saline conditions (Borde et al. 2010).

2.6.2  Drought Tolerance Fungal endophytes have been shown to provide fitness benefit to plants when exposed to water-limiting conditions. Perhaps the most widely documented example of endophyte-mediated drought stress tolerance in plants is the enhanced drought tolerance of tall fescue and perennial ryegrass due to infection of the endophyte Neotyphodium coenophialum (Dastogeer and Wylie 2017). Interestingly, all fungal endophytes conferred drought tolerance to plants regardless of the habitat of origin (Rodriguez et  al. 2008). Kane (2011) studied the leaf-inhabiting endophyte Neotyphodium lolii to assess its potential benefits or harm in drought stress tolerance of native perennial ryegrass collections formerly obtained from the Mediterranean regions. The findings showed that endophyte colonization can help improve biotic stress tolerance such as drought in N. lolii (Cheplick 2006; Suman et al. 2016). Curvularia protuberata (Cp4666D) and Fusarium culmorum (FcRed1) isolates from geothermal soil and Costal Beach both conferred similar levels of drought tolerance in tomato (Rodriguez et al. 2008) and rice (Redman et al. 2011). Endophytes Chaetomium globosum and Penicillium resedanum isolated from Capsicum annuum plants promoted shoot length and biomass of the host plants subjected to drought stress (Khan et al. 2012). Drought-challenged tomato plants showed higher root and shoot biomass when inoculated with class 2 fungal endophytes, including Alternaria sp. and Trichoderma harzianum (Azad and Kaminskyj 2016). Epichloë species may enhance the eco-physiology of host plants and enable

70

F. A. Abo Nouh and A. M. Abdel-Azeem

plants to counter abiotic stresses such as drought and metal contamination (Rodriguez et al. 2009). Penicillium brevicompactum isolated from wild barley species was helpful in drought tolerance improvement of barley plant in drought condition (Chhipa and Deshmukh 2019). Extensive amount of research literature indicates that mycorrhizae often have a substantive impact on water movement into, through, and out of host plants, with consequent effects on plant tissue hydration and leaf physiology (Nasim 2010). They usually increase host growth rates during drought, by affecting nutrient acquisition and possibly hydration and typically water-use efficiency, which are influenced by the kind of fungi involved (Augé 2001). Growing evidence indicates that association with AM fungi can improve overall plant growth and reproducibility by improving root length, leaf area, plant biomass, plant tissue hydration, and nutrient uptake under water-deficit condition (Bhandari and Garg 2017). Mycorrhizal plants may avoid drought to some extent through enhanced water uptake at low soil moisture levels. In onion, the effects seem to be conferred through improved phosphorus nutrition (Nelson and Safir 1982). An influence on host osmotic potential has been observed in wheat (Allen and Bosalis 1983). However, there is a strong evidence of drought stress alleviation by AMF in different crops such as wheat, barley, maize, soybean, strawberry, and onion (Ruiz-Lozano et al. 2015). Lavender plants inoculated with Glomus intraradices and Glomus sp. strain accumulated these compounds and exhibited high drought tolerance by improving water contents, root biomass, and N and P contents (Hussain et al. 2018). While working on sunflower plant exposed to drought stress, Gholamhoseini et al. (2013) stated that inoculation with G. mosseae improved availability of P, thus minimizing the impact of stress on seed oil percentage and oil yield. Zou et al. (2013) reported that when inoculated with Funneliformis mosseae, Poncirus trifoliata plants recorded lower tissue accumulation of this amino acid that related with improved plant growth and productivity under drought-stressed conditions.

2.6.3  Heat Tolerance Several possible mechanisms could confer thermotolerance. In plants, the fungal endophytes produce cell wall melanin that may dissipate heat along the hyphae and/ or complex with oxygen radicals generated during heat stress (Davidson et  al. 1996). Rhizosphere fungus Paraphaeosphaeria quadriseptata enhanced plant heat stress tolerance of Arabidopsis thaliana (Grover et al. 2011). An endophytic fungi Curvularia sp. were reecovered from the Dichanthelium lanuginosum grown under geothermal soils. C. protuberata isolated from a monocot have ability to confer heat tolerance to tomato (a dicot) (Grover et al. 2011), also increased heat tolerance in wheat in terms of height, weight of grain, and germination of second-generation seeds (Lata et al. 2018). Under low temperature and higher nutrient input, P. indica triggers flowering earlier and increases grain yield indicating its potential as an effective endophyte promoting growth (Shrivastava and Verma 2014). Endophytic

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

71

symbiont dark septate fungi (DSF) found in plants growing under stressed environments such as alpine habitats and arid grasslands have been reported to increase their resistance to drought and heat and facilitate the acquisition of nutrients (Grover et al. 2011). Rhizosphere fungus Paraphaeosphaeria quadriseptata enhanced plant heat stress tolerance of Arabidopsis thaliana (McLellan et al. 2007). Generally, AMF-­ inoculated plants show better growth under heat stress than do the non-AMF inoculated ones (Begum et al. 2019). AMF can increase plant tolerance to cold stress. Moreover, a majority of reports state that various plants inoculated with AMF at low temperature grow better than non-AMF inoculated plants (Liu et al. 2013). AMF support plants in combating cold stress and eventually improve plant development (Begum et al. 2019). Maya and Matsubara (2013) have reported the association of AMF Glomus fasciculatum with plant growth and development leading to positive changes in growth under the conditions of high temperature. For example, during cold stress, AMF-inoculated plants showed an enhanced water conservation capacity as well as its use efficiency (Zhu et al. 2010). The role of AMF during cold stress has also been reported to alter protein content in tomato and other vegetables (Abdel Latef and Chaoxing 2011).

2.6.4  Flood Tolerance AMF colonization by Glomus intraradices contributed substantially to the flood tolerance of Pterocarpus officinalis seedlings by improving plant growth and P acquisition in leaves. Flooding induced nodules both on adventitious roots and submerged parts of the stem (Grover et al. 2011). Mycorrhizal Casuarina equisetifolia seedlings could better adapt to flooding than noninoculated seedlings. This could be due to increased O2 diffusion and removal of ethanol through greater development of adventitious roots, aerenchymatous tissue, and hypertrophies lenticels on the root zone and submerged part of the stem (Rutto et al. 2002). The better tolerance of AM inoculated A. trifolium plants to flooding was mediated through an improvement of osmotic adjustment and proline in plant tissue (Neto et al. 2006).

2.6.5  Heavy Metals Tolerance Studies have documented that the presence of HM in excess concentrations not only reduces spore germination, mycelia growth, degree of colonization, and sporulation of these fungi but also causes a significant impact on their ecology and diversity (Bhandari and Garg 2017). Piriformospora indica has been extensively reported to improve crop tolerance to a number of abiotic stresses including salinity, low temperature, and heavy metal toxicity (Gill et al. 2016). In a study made by the root-­ associated dark septate endophyte Exophiala pisciphila of Zea mays analyzed under

72

F. A. Abo Nouh and A. M. Abdel-Azeem

increased soil Cd stress (0, 10, 50, 100  mg kg−1) showed enhanced antioxidant enzyme activity (Lata et al. 2018). Several studies have validated that AM fungi play a vital role in improving growth and productivity of host plants in metal-contaminated soils (Garg and Pandey 2015). In addition, more than 30 species of AM fungi have been identified in contaminated soils worldwide and some at high frequencies, such as Paraglomus occultum, G. clarum, G. intraradices, and Scutellospora pellucida (Bhandari and Garg 2017). Studies have further depicted that spores isolated from polluted soils are more tolerant to and germinated better in HM-polluted soil in comparison to spores isolated from non-polluted soils (Gaur and Adholeya 2004). Consequently, AM fungi have been validated to lower the translocation of metals from roots to aerial organs (Garg and Kaur 2012). In one of the studies, Garg and Kaur (2012) demonstrated that in comparison with non-AM pigeon pea plants, colonization with F. mosseae led to significant immobilization of metals—Cd and Zn in roots—thus leading to lower translocation of toxic ions in above-ground plant organs in mycorrhizal-­stressed plants. Similarly, colonization with R. intraradices restricted large amount of Pb in roots of woody legume Robinia pseudoacacia, thus preventing future damage to above-ground parts (Bhandari and Garg 2017). AMF association with wheat positively increased nutrient uptake under aluminum stress. Also in rice, AMF were very effective in lowering the levels of Cd in both the vacuoles and cell wall (Begum et al. 2019).

References Abdel Latef AA, Chaoxing H (2011) Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol Plant 33:1217–1225 Abo Nouh FA (2019) Endophytic fungi for sustainable agriculture. Microb Biosyst 4:31–44 Ali AH, Radwan U, El-Zayat S, El-Sayed MA (2018) Desert plant-fungal endophytic association: the beneficial aspects to their hosts. Biol Forum 10:138–145 Al-Karaki GN, Ammad R, Rusan M (2001a) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47 Al-Karaki GN, Hammad R, Rusan M (2001b) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47 Allen MF, Bosalis MG (1983) Effects of two species of VA mycorrhizal fungi on drought tolerance of winter wheat. New Phytol 93:67–76 Amalric C, Sallanon H, Monnet F, Hitmi A, Coudret A (1999) Gas exchange and chlorophyll fluorescence in symbiotic and non-symbiotic ryegrass under water stress. Photosynthetica 37:107–112 Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399 Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE (1989) Effect of the tall fescue endophyte on plant response to environmental stress. Agron J 81:83–90 Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

73

Arnold EA, Mejia LC, Kyllo D, Rojas E, Maynard Z, Robbins N et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654 Asghari H, Marchner P, Smith S, Smith F (2005) Growth reponses of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant Soil 273:245–256 Ashmore M, Toet S, Emberson L et al (2006) Ozone-a significant threat to future world food production? New Phytol 170:201–204 Augé RM (2001) Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42 Augé RM, Foster JG, Loescher WH, Stodola AJW (1992) Symplastic sugar and free amino acid molality of Rosa roots with regard to mycorrhizal colonization and drought. Symbiosis 12:1–17 Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68:73–78 Bacon CW (1993) Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte infected tall fescue. Agric Ecosyst Environ 44:123–141 Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58 Batool N, Shahzad A, Ilyas N (2014) Plants and Salt stress. Int J Agric Crop Sci 7:1439–14461 Battisti DS, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323:240–244 Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of Arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068 Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34 Ben Khaled L, Gomez AM, Ouarraqi EM, Oihabi A (2003) Physiological and biochemical responses to salt stress of mycorrhizal and/or nodulated clover seedlings (Trifolium alexandrium L.). Agronomie 23:571–580 Bhandari P, Garg N (2017) Arbuscular mycorrhizal symbiosis: a promising approach for imparting abiotic stress tolerance in crop plants. In: Singh DP et al (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 377–402 Borde M, Dudhane M, Jite PK (2010) AM fungi influences the photosynthetic activity, growth and antioxidant enzymes in Allium sativum L. under salinity condition. Not Sci Biol 2:64–71 Boyer JS (1982) Plant productivity and environment. Science 218:443–448 Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54 Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In: Shanker A (ed) Abiotic stress in plants mechanisms and adaptations. InTech, London, pp 21–38 Carroll G (1988) Fungal endophytes in stems and leaves from latent pathogen to mutualistic symbiont. Ecology 69:2–9 Chaves MM, Maroco JP, Pereira JS et al (2003) Understanding plant responses to drought- from genes to the whole plant. Funct Plant Biol 30:239–264 Chaw S, Chang C, Chen H, Li W (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441 Cheplick GP (2006) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exp Bot 60:202–210 Cheplick GP, Perera A, Koulouris K (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14:657–667 Chhipa H, Deshmukh SK (2019) Fungal endophytes: rising tools in sustainable agriculture production. In: Jha S (ed) Endophytes and secondary metabolites. Springer, Cham, pp 1–24 Colla G, Rouphae Y, Cardarelli M, Tulio M, Rivera CM, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhiza in zucchini plants grown at low and high phosphorus concentration. Biol Fertil Soils 44:501–509 Cramer GR, Nowak RS (1992) Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt stressed barley. Physiol Plant 84(600):605

74

F. A. Abo Nouh and A. M. Abdel-Azeem

Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163 Cruz-Hernández A, Tomasini-Campocosio A, Pérez-Flores LJ, Fernández-Perrino FJ, Gutiérrez-­ Rojas M (2013) Inoculation of seed-borne fungus in the rhizosphere of Festuca arundinacea promotes hydrocarbon removal and pyrene accumulation in roots. Plant Soil 362:261–270 Dastogeer KMG, Wylie SJ (2017) Plant–fungi association: role of fungal endophytes in improving plant tolerance to water stress. In: Singh DP et  al (eds) Plant-microbe interactions in agro-­ ecological perspectives. Springer, Singapore, pp 143–160 Davidson JF, Whyte B, Bissinger PH, Schiestl RH (1996) Oxidative stress is involved in heat-­ induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci 93:5116–5121 Deckert RJ, Melville LH, Peterson L et al (2001) Structural features of a Lophodermium endophyte during the cryptic life-cycle phase in the foliage of Pinus strobus. Mycol Res 105:991–997 Diouf D, Diop TA, Ndoye I (2003) Actinorhizal, mycorrhizal and rhizobial symbioses: how much do we know? Afr J Biotechnol 2:1–7 Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280 Feng G, Zhang FS (2003) Effect of arbuscualar mycorrhizal fungi on salinity tolerance of cotton. Chin J Ecol Agric 11:21–24 Feng G, Li XL, Zhang FS, Li SX (2000) Effect of AM fungi on water and nutrition status of corn plants under salt stress. Chin J Appl Ecol 11:595–598 Fusconi A, Berta G (2012) Environmental stress and role of arbuscular mycorrhizal symbiosis. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Springer, New York, pp 197–214 Garg N, Kaur H (2012) Influence of zinc on cadmium-induced toxicity in nodules of pigeon pea (Cajanus cajan L. Mill sp.) inoculated with arbuscular mycorrhizal (AM) fungi. Acta Physiol Plant 34:1363–1380 Garg N, Pandey R (2015) Effectiveness of native and exotic arbuscular mycorrhizal fungi on nutrient uptake and ion homeostasis in salt-stressed Cajanus cajan L. (Mill sp.) genotypes. Mycorrhiza 25:165–180 Garg N, Singla P (2012) The role of Glomus mosseae on key physiological and biochemical parameters of pea plants grown in arsenic contaminated soil. Sci Hortic 143:92–101 Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534 Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114 Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW, Ansari AA, Johri AK, Prasad R, Pereira E, Varma A, Tuteja N (2016) Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol 7:332 Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760 Greaves JA (1996) Improving sub optimal temperature tolerance in maize the search for variation. J Exp Bot 47:307–323 Grover M, Ali SKZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240 Gull A, Lone AA, Wani NUI (2019) “Biotic and Abiotic Stresses in Plants,” in Abiotic and Biotic Stress in Plants. IntechOpen) Gutjahr C, Parniske M (2013) Cell and developmental biology of the arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617 Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic, London Hattori YK, Nagai M, Ashikari (2011) Rice growth adapting to deepwater. Curr Opin Plant Biol 14:100–105

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

75

Hussain SS, Mehnaz S, KHM S (2018) Harnessing the plant microbiome for improved abiotic stress tolerance. In: Egamberdieva D, Ahmad P (eds) Plant microbiome: stress response, Microorganisms for sustainability, vol 5. Springer, Singapore, pp 21–43 IPCC (2007) Climate Change 2007: Synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri, R.K and Reisinger, A. (eds.)]. IPCC, Geneva, Switzerland, 104 pp Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53 Jain P, Pundir RK (2017) Potential role of endophytes in sustainable agriculture-recent developments and future prospects. In: Maheshwari DK (ed) Endophytes: biology and biotechnology, sustainable development and biodiversity, vol 15. Springer, Cham, pp 145–160 Jindal V, Atwal A, Sekhon BS, Rattan S, Singh R (1993) Effect of vesicular arbuscular mycorrhizae on metabolism of moong plants under NaCl salinity. Plant Physiol Biochem 31:475–481 Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586 Johnson JM, Alex T, Oelmuller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agric 52:103–122 Kane KH (2011) Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region. Environ Exp Bot 71:337–344 Kaur T, Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Dhaliwal HS, Saxena AK (2020) Microbe-mediated biofortification for micronutrients: present status and future challenges. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 1–17. https://doi.org/10.1016/B978-0-12-820528-0.00002-8 Khalmuratova I, Kim H, Nam Y, Oh Y, Jeong M, Choi H, You Y, Lee I, Shin J, Yoon H, You YH (2015) Diversity and plant growth promoting capacity of endophytic fungi associated with halophytic plants from the coast of Korea. Microbiology 43:373–383 Khan SA, Hamayun M, Khan AL, Shinwari ZK (2012) Isolation of plant growth promoting endophytic fungi from dicots inhabiting coastal sand dunes of Korea. Pak J Bot 44:1453–1460 Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A, Sayyed RZ, Hesham AE-L, Dhaliwal HS, Saxena AK (2019a) Drought-tolerant phosphorus-solubilizing microbes: biodiversity and biotechnological applications for alleviation of drought stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting rhizobacteria for sustainable stress management: volume 1: rhizobacteria in abiotic stress management. Springer, Singapore, pp 255–308. https://doi.org/10.1007/978-981-13-6536-2_13 Kour D, Rana KL, Yadav N, Yadav AN, Kumar A, Meena VS, Singh B, Chauhan VS, Dhaliwal HS, Saxena AK (2019b) Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: Kumar A, Meena VS (eds) Plant growth promoting rhizobacteria for agricultural sustainability: from theory to practices. Springer, Singapore, pp 19–65. https://doi.org/10.1007/978-981-13-7553-8_2 Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V, Dhaliwal HS, Saxena AK (2020a) Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolour L.) by drought-adaptive and phosphorus-solubilizing microbes. Biocatal Agric Biotechnol 23:101501. https://doi.org/10.1016/j.bcab.2020.101501 Kour D, Rana KL, Sheikh I, Kumar V, Yadav AN, Dhaliwal HS, Saxena AK (2020b) Alleviation of drought stress and plant growth promotion by Pseudomonas libanensis EU-LWNA-33, a drought-adaptive phosphorus-solubilizing bacterium. Proc Natl Acad Sci India Sec B Biol Sci. https://doi.org/10.1007/s40011-019-01151-4 Kour D, Rana KL, Yadav AN, Sheikh I, Kumar V, Dhaliwal HS, Saxena AK (2020c) Amelioration of drought stress in Foxtail millet (Setaria italica L.) by P-solubilizing drought-tolerant

76

F. A. Abo Nouh and A. M. Abdel-Azeem

microbes with multifarious plant growth promoting attributes. Environ Sustain. https://doi. org/10.1007/s42398-020-00094-1 Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal HS, Saxena AK (2020d) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi. org/10.1016/j.bcab.2019.101487 Lata R, Chowdhury S, Gond S, White JF (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Appl Microbiol 66:268–276 Latef AAHA, Hashem A, Rasool S, Abd-Allah EF, Alqarawi AA, Egamberdieva D, Jan S, Anjum NA, Ahmad P (2016) Arbuscular mycorrhizal Symbiosis and abiotic stress in plants: a review. J Plant Biol 59:407 Lewis GC, Clements RO (1986) A survey of ryegrass endophyte (Acremonium lolii) in the U.K. and its apparent ineffectuality on a seedling pest. J Agric Sci 107:633–638 Liu X, Song Q, Tang Y, Li W, Xu J, Wu J et al (2013) Human health risk assessment of heavy metals in soil–vegetable system: a multi-medium analysis. Sci Total Environ 463-464:530 López-Ráez JA (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243:1375–1385 Lugtenberg BJJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microb Ecol 92:1–17 Maggio A, Hasegawa PM, Bressan RA, Consiglio MF, Joly RJ (2001) Unravelling the functional relationship between root anatomy and stress tolerance. Funct Plant Biol 28:999–1004 Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158 Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940 Mandhania S, Madan S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biol Plant 50:227–231 Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515 Maya MA, Matsubara Y (2013) Influence of arbuscular mycorrhiza on the growth and antioxidative activity in Cyclamen under heat stress. Mycorrhiza 23:381–390 McLellan CA, Turbyville TJ, Wijeratne K, Kerschen A, Vierling E, Queitsch C, Whiteshell L, Gunatilaka AAL (2007) A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol 145:174–182 Miller JD, Mackenzie S, Foto M, Adams GW, Findlay JA (2002) Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycol Res 106:471–479 Mohammed MJ, Malkawi HI, Shibli R (2003) Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J Plant Nutr 26:125–137 Morse LJ, Day TA, Faeth SH (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environ Exp Bot 48:257–268 Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681 Nasim G (2010) The role of arbuscualar mycorrhizae in inducing resistance to drought and salinity stress in crops. In: Ashraf M et al (eds) Plant adaptation and phytoremediation. Springer, New York, pp 119–141 Navrot N, Rouhier N, Gelhaye E, Jacquot JP (2007) ROS generation and antioxidant systems in plant mitochondria. Physiol Plant 129:185–195 Nelson TN, Safir GR (1982) Increased drought tolerance of mycorrhizal onion plants cased by improved phosphorus nutrition. Planta 154:407–413

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

77

Neto D, Carvalho LM, Cruz C, Martin-Loucao MA (2006) How do mycorrhizas affect C and N relationships in flooded Aster trifolium plants? Plant Soil 279:51–63 Okcu G, Kaya DM, Atak M et al (2005) Effects of salt and drought stresses on germination and seedling growth of pea (Pisum sativum L). Turk J Agric For 29:237–242 Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569 Prasad K (2015) Biofertilizers: a new dimension for agriculture and environmental development to improve production in sustainable manner. J Basic Appl Mycol 11:5–13 Prasad K (2017) Biology, diversity and promising role of mycorrhizal endophytes for green technology. In: Maheshwari DK (ed) Endophytes: biology and biotechnology, sustainable development and biodiversity, vol 15. Springer, Cham, pp 267–302 Prasad K, Gautam SP (2000) Arbuscular mycorrhizal spore types present in the root zone of Dalbergia sissoo L. Vislesana. Res J Sci 7:013–018 Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222 Raghuwanshi R (2018) Fungal community in mitigating impacts of drought in plants. In: Gehlot P, Singh J (eds) Fungi and their role in sustainable development: current perspectives. Springer, Singapore, pp 267–382 Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Springer, Cham, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rana KL, Kour D, Yadav AN (2019c) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162 Rana KL, Kour D, Kaur T, Sheikh I, Yadav AN, Kumar V, Suman A, Dhaliwal HS (2020) Endophytic microbes from diverse wheat genotypes and their potential biotechnological applications in plant growth promotion and nutrient uptake. Proc Natl Acad Sci. https://doi. org/10.1007/s40011-020-01168-0 Read JC, Camp BJ (1986) The effect of the fungal endophyte Acremonium coenophialum in tall fescue on animal performance, toxicity and stand maintenance. Agron J 78:848–850 Redman RS, Ranson J, Rodriguez RJ (1999) Conversion of the pathogenic fungus Colletotrichum magna to a nonpathogenic endophytic mutualist by gene disruption. Mol Plant-Microbe Interact 12:969–975 Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716 Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298:1581 Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE 6:1–10 Richardson MD, Chapman GW Jr, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-­ infected tall fescue under drought. Crop Sci 32:1060–1061 Richardson MD, Hoveland CS, Bacon CW (1993) Photosynthesis and stomatal conductance of symbiotic and nonsymbiotic tall fescue. Crop Sci 33:145–149 Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114 Rodriguez RJ, Redman RS, Henson JM et al (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9:261–272

78

F. A. Abo Nouh and A. M. Abdel-Azeem

Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M (2008) Stress tolerance in plants via habitat-­ adapted symbiosis. Int Soc Microb Ecol J 2:404–416 Rodriguez RJ, White JF, Arnold AE, Redman RS et al (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330 Rouhier N, Koh CS, Gelhaye E, Corbier C, Favier F, Didierjean C et  al (2008) Redox based anti-oxidant systems in plants: biochemical and structural analyses. Biochim Biophys Acta 1780:1249–1260 Ruiz-Lazano JM, Azcon R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478 Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R et al (2015) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39:441–452 Rutto KL, Mizutani F, Kadoya K (2002) Effect of root-zone flooding on mycorrhizal and non-­ mycorrhizal peach (Prunus persica Batsch) seedlings. Sci Hortic 94:285–295 Sannazzaro AI, Oscar R, Edgardo A, Ana M (2006) Alleviation of salt stress in Lotus glaber by Glomus intraradices. Plant Soil 285:279–287 Saxena AK, Yadav AN, Rajawat M, Kaushik R, Kumar R, Kumar M, Prasanna R, Shukla L (2016) Microbial diversity of extreme regions: an unseen heritage and wealth. Indian J Plant Genet Resour 29:246–248 Schardl CL, Leuchtmann A, Spiering MJ et al (2004) Annu Rev Plant Biol 55:315–340 Schulz BJE (2006) Mutualistic interactions with fungal root endophytes. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 261–280 Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686 Schulz B, Guske S, Dammann U, Boyle C et al (1998) Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227 Schulz B, Römmert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103:1275–1283 Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421 Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscualar mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296 Shrivastava S, Verma A (2014) From Piriformospora indica to rootonic: a review. Afr J Microbial Res 8:2984–2992 Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191 Singh A, Kumari R, Yadav AN, Mishra S, Sachan A, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–16. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Skirycz A, Inze D (2010) More from less: plant growth under limited water. Curr Opin Biotechnol 21:197–203 Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotechnol 9:214–219 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh D, Abhilash P, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, research perspectives. Springer, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7 Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus—perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066 Vadassery J, Oelmüller R (2009) Calcium signaling in pathogenic and beneficial plant microbe interactions. Plant Signal Behav 4:1024–1027 Verma S, Nizam S, Verma PK (2013) Biotic and abiotic stress signalling in plants. Stress Signal Plants 1:25–49

2  Role of Fungi in Adaptation of Agricultural Crops to Abiotic Stresses

79

Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016) Molecular diversity and multifarious plant growth promoting attributes of Bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58 Verma P, Yadav AN, Khannam KS, Saxena AK, Suman A (2017a) Potassium-solubilizing microbes: diversity, distribution, and role in plant growth promotion. In: Panpatte DG, Jhala YK, Vyas RV, Shelat HN (eds) Microorganisms for green revolution: volume 1: microbes for sustainable crop production. Springer, Singapore, pp 125–149. https://doi.org/10.1007/978-981-10-6241-4_7 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017b) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-­ ecological perspectives: volume 2: microbial interactions and agro-ecological impacts. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22 Verma P, Yadav AN, Khannam KS, Mishra S, Kumar S, Saxena AK, Suman A (2019) Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of India. Saudi J Biol Sci 26:1882–1895. https://doi.org/10.1016/j.sjbs.2016.01.042 Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M et  al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance and higher yield. Proc Natl Acad Sci U S A 102:13386–13391 Wang J, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24:427–451 Wang Y, Frei M (2011) Stressed food—the impact of abiotic environmental stresses on crop quality. Agric Ecosyst Environ 141:271–286 Wang FY, Liu RJ (2001) A preliminary survey of arbuscular mycorrhizal fungi in saline alkaline soils of the Yellow river delta. Biodivers Sci 9:389–392 Wang WX, Vinocur B, Shoseyov O, Altman A (2001) Biotechnology of plant osmotic stress tolerance: physiological and molecular considerations. Acta Hortic 560:285–292 White RH, Engelke MC, Morton SJ, Johnson-Cicalese JM, Ruemmele BA (1992) Acremonium endophyte effects on tall fescue drought tolerance. Crop Sci 32:1392–1396 Yadav AN (2017) Agriculturally important microbiomes: biodiversity and multifarious PGP attributes for amelioration of diverse abiotic stresses in crops for sustainable agriculture. Biomed J Sci Tech Res 1:1–4 Yadav AN (2019) Endophytic fungi for plant growth promotion and adaptation under abiotic stress conditions. Acta Sci Agric 3:91–93 Yadav AN, Yadav N (2018) Stress-adaptive microbes for plant growth promotion and alleviation of drought stress in plants. Acta Sci Agric 2:85–88 Yadav AN, Sachan SG, Verma P, Saxena AK (2015a) Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. J Biosci Bioeng 119:683–693 Yadav AN, Sachan SG, Verma P, Tyagi SP, Kaushik R, Saxena AK (2015b) Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of Leh Ladakh (India). World J Microbiol Biotechnol 31:95–108 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan V, Dhaliwal HS, Saxena AK (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Verma P, Sachan SG, Saxena AK (2017b) Biodiversity and biotechnological applications of psychrotrophic microbes isolated from Indian Himalayan regions. Ecol Microbiol 1:48–54 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018a) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, Cambridge, pp 305–332 Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP, Saxena AK, Dhaliwal HS (2018b) Actinobacteria from rhizosphere: molecular diversity, distributions and potential biotechnolog-

80

F. A. Abo Nouh and A. M. Abdel-Azeem

ical applications. In: Singh B, Gupta V, Passari A (eds) New and future developments in microbial biotechnology and bioengineering. Springer, New York, pp 13–41. https://doi.org/10.1016/ B978-0-444-63994-3.00002-3 Yadav AN, Verma P, Sachan SG, Kaushik R, Saxena AK (2018c) Psychrotrophic microbiomes: molecular diversity and beneficial role in plant growth promotion and soil health. In: Panpatte DG, Jhala YK, Shelat HN, Vyas RV (eds) Microorganisms for green revolution-volume 2: microbes for sustainable agro-ecosystem. Springer, Singapore, pp  197–240. https://doi. org/10.1007/978-981-10-7146-1_11 Yadav AN, Gulati S, Sharma D, Singh RN, Rajawat MVS, Kumar R, Dey R, Pal KK, Kaushik R, Saxena AK (2019a) Seasonal variations in culturable archaea and their plant growth promoting attributes to predict their role in establishment of vegetation in Rann of Kutch. Biologia 74:1031–1043. https://doi.org/10.2478/s11756-019-00259-2 Yadav AN, Kour D, Sharma S, Sachan SG, Singh B, Chauhan VS, Sayyed RZ, Kaushik R, Saxena AK (2019b) Psychrotrophic microbes: biodiversity, mechanisms of adaptation, and ­biotechnological implications in alleviation of cold stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting rhizobacteria for sustainable stress management: volume 1: rhizobacteria in abiotic stress management. Springer, Singapore, pp 219–253. https:// doi.org/10.1007/978-981-13-6536-2_12 Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi, volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Yadav N, Sachan SG, Saxena AK (2019d) Biodiversity of psychrotrophic microbes and their biotechnological applications. J Appl Biol Biotechnol 7:99–108 Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N, Kour D (2020b) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020d) Plant microbiomes for sustainable agriculture. Springer, Cham Yuan Z, Zhang C, Lin FL (2010) Role of diverse non-systemic fungal endophytes in plant performance and response to stress: progress and approaches. J Plant Growth Regul 29:116–126 Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, Jin D et al (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228 Zhu JK (2007) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349 Zhu XC, Song FB, Xu HW (2010) Effects of arbuscular mycorrhizal fungi on photosynthetic characteristics of maize under low temperature stress. Acta Ecol Sin 21:470–475 Zou YN, Wu QS, Huang YM, Ni QD, He XH (2013) Mycorrhizal-mediated lower proline accumulation in Poncirus trifoliata under water deficit derives from the integration of inhibition of proline synthesis with increase of proline degradation. PLoS One 8:1–8

Chapter 3

Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress in Plants Deepika Goyal, Sushma Mishra, and Prem Kumar Dantu

Contents 3.1  3.2  3.3  3.4 

Introduction Background of Arbuscular Mycorrhizal Fungi Arbuscular Mycorrhizal Fungi as a Biofertilizer Mechanisms Used by AMF to Provide Drought Tolerance to Plants 3.4.1  Modification of Hormonal Balances 3.4.2  Improvement of Plant Water Status 3.4.3  Osmotic Adjustment 3.4.4  Antioxidant Activity 3.4.5  Higher Nutrients Absorption 3.4.6  Photosynthesis, Partitioning, and Production of Photoassimilates 3.5  Conclusion and Future Perspective References

 81  83  83  84  85  89  91  91  92  93  93  94

3.1  Introduction Now a days, we are suffering with a problem climate change which is causing drought in large areas of the earth (Sheffield et al. 2012). Drought is one of the most destructive abiotic stresses being faced by plants and it has widely attracted the attention of agricultural scientists and biotechnologists. Drought is a major concerned agriculture problem and reduces or limits plant growth and productivity (Kour et al. 2020b). A large piece of agricultural land is affected by drought and it adversely affects human society, economical rate, etc. (Disante et al. 2011; Mishra and Singh 2010). Drought stress limits water content available in soil, reduces cell size, membrane integrity, produces reactive oxygen species, and promotes leaf senescence causing reduction in crop productivity (Kour et al. 2020a; Tiwari et al. 2015). Apart from morphological changes there are some molecular changes in drought stressed plants such as increase in ethylene production (stress-responsive D. Goyal (*) · S. Mishra · P. K. Dantu Department of Botany, Dayalbagh Educational Institute, Deemed University, Agra, Uttar Pradesh, India © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_3

81

82

D. Goyal et al.

phytohormone), reduction in chlorophyll content, and inhibition in photosynthetic rate (Lata and Prasad 2011). Drought elevates accumulation of free radicals that induce change in membrane function, protein conformation, and lipid peroxidation leading to cell death (Tiwari et al. 2016; Yadav et al. 2020c, d, e). It is being believed by some scientists there will be increase in drought as time passes out due to climate change. Drought stress is among the most destructive abiotic stress that increased in intensity over the past decades affecting world’s food security (Kour et al. 2019; Singh and Yadav 2020). Drought stress may range from moderate and short to extremely severe and prolonged duration, restricting the crop yields (Austin 1989; Pereira and Chaves 1995). Drought is expected to cause serious plant growth problems for more than 50% of the arable lands by 2050 (Ashraf 1994; Vinocur and Altman 2005; Kasim et  al. 2013). Under drought stress plants adapt themselves through physiological, biochemical, and molecular responses (Ito et al. 2006) and control water status by adjustment of root hydraulic conduction, reduced transpiration, and stomatal closure (Parent et al. 2009). A change in plant stress-­responsive genes is found by transcriptomic and proteomic approaches (Hirayama and Shinozaki 2010; Deshmukh et  al. 2014; Liu et  al. 2015). Some genes are found upregulated whereas others are found downregulated. In molecular responses of drought, plants synthesize some specific proteins to impart drought tolerance such as LEA (late embryogenesis abundant), DSP (Desiccation stress protein), and dehydrins (Fig. 3.1). In addition, mycorrhizal association is a symbiotic non-pathogenic relationship between plant roots and fungal hyphae (Osonubi et al. 1991; Sieverding et al. 1991). In this mutualistic association, the fungi gain carbon compounds and other nutritional supplements from the roots of plants, and in return, provide the plant with macro and micronutrients such as nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), copper (Cu), and zinc (Zn) from the soil. The importance of mycorrhizae association in both agricultural and ecological systems had earlier been widely recognized (Mosse 1978; Osonubi et al. 1991). The increased plant growth by vesicular arbuscular mycorrhizae (VAM)

Drought Physiological responses Root signal recognition at the shoot Loss of turgor and osmotic adjustment Reduced transpiration rate and low stomatal conductance Decrease in plant carbon di-oxide concentration Reduced photosynthetic rate Reduced growth

Biochemical responses

Decreased activity of RuBisco enzyme Accumulation of metabolites like MDHA, glutathione, proline, glycine betane, polyamines and αtocopherol Increase in antioxidative enzymes like SOD,CAT,APX,POD,GR and MDHAR Reduced ROS accumulation

Molecular responses

Expression of stress response genes Increased expression of ABA biosynthetic genes Synthesis of specific proteins such as LEA, DSP, RAB, dehydrins Drought stress tolerance

Fig. 3.1  Plant’s physiological, biochemical, and molecular responses towards drought stress

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

83

association is usually due to increased mineral elements uptake by the hyphae from the soil, improved water relations and pest resistance of host plants (Farahani et al. 2008; Olawuyi et al. 2011a, b, 2012). VAM provided tolerance to a variety of abiotic stresses (Wilcox et al. 1990) and increased resistance to soil pathogens (Odebode et al. 1998; Pozo et al. 2002; Olawuyi et al. 2014a, b). Mycorrhizae can also resist drought in many plants under stress conditions; therefore, the plants infected with VAM are less likely to wilt under drought affected conditions as compared to non-­ inoculated plants (Lindermann and Hendrix 1982; Olawuyi et al. 2011a, b, 2014a, b).

3.2  Background of Arbuscular Mycorrhizal Fungi Arbuscular mycorrhizal fungi are soil-borne fungi that alleviate abiotic stress and improve plant growth and yield (Sun et al. 2018). Most of the AMF belong to the sub-phylum Glomeromycotina, of the phylum Mucoromycota (Spatafora et  al. 2016). AM fungi are classified in four orders namely, Glomerales, Archaeosporales, Paraglomerales, and Diversisporales and these orders include 25 genera (Redecker et  al. 2013). Mycorrhizae are obligate biotrophs and ingest carbon compounds (Bago et  al. 2000) and lipids to sustain their life cycle (Jiang et  al. 2017). AMF provide drought tolerance to plants and act as safety-valve against fungal pathogens (Smith and Read 2008; Jung et al. 2012). In this way, Mycorrhizae are playing a vital role to maintain energy system and global harmony (Yadav et al. 2019a, b, c). They act as biofertilizers and improve crop productivity under adverse conditions also (Gianinazzi et al. 2010).

3.3  Arbuscular Mycorrhizal Fungi as a Biofertilizer Biofertilizers are a mixture of naturally occurring substances which increase crop productivity without harming environment. Biofertilizers improve soil health and plant growth and development (Kour et  al. 2020c; Sadhana 2014; Yadav et  al. 2020a). From a long ago many researches are being conducted on AMF and myriad benefits are observed on soil health and crop productivity. Therefore, it is considered that AMF could be used as bio-fertilizer as a substitute of inorganic fertilizers due to their application can lower the quantitative use of chemical fertilizer input especially of phosphorus (Ortas 2012). Continuous exposure of herbicides, inorganic fertilizers, and fungicides has caused ecological imbalance and many threats to soil, plants, and human health, through their harmful effect on the quality of food products, soil composition, and aquatic bodies. It is believed that AMF can lower down the application of chemical fertilizers up to 50% for best agricultural production, but this estimate depends on the type of plant species and the prevalent stressful regimes (Rana et al. 2019; Yadav et al. 2020b). AMF are being used in various

84

D. Goyal et al.

applications such as to provide resistance to plants against various abiotic stress and biotic stress along with used as biofertilizers (Fig. 3.2).

3.4  M  echanisms Used by AMF to Provide Drought Tolerance to Plants There are certain mechanisms which explain how AMF provide resistance to plants against drought stress such as (1) adjustment of hormonal balance (Estrada-Luna and Davies Jr 2003), (2) enhancement of plant water status by improving hydraulic conductivity through an increase of water absorption by the external hyphae of VAM (Augé et al. 2007), (3) osmotic adjustment (Porcel and Ruiz-Lozano, 2004), (4) increase in antioxidant activity (Goicoechea et al. 2005), and (5) higher nutrients absorption (Al-Karaki 2006). This chapter describes these potential mechanisms adopted by mycorrhizae to alleviate drought stress being challenged by plants, and to improve yield and productivity of crops (Fig. 3.3).

AMF Plant stress tolerance

Nutrients uptake

Oxidative stress mitigation by upregulating anti-oxidant system Downregulation of lipoxygenase, by osmotic adjustment Regulation of Aquaporin genes ABA responsive genes Phytohormone biosynthesis pathways Such as ABA, Ethylene and Strigolactones Transciption factors

Specific transporters

Soil health Improves Soil moisture Fertility level Soil quality

Translocation from external environment to internal by modifying root morphology

Improved stress tolerance and enhanced yield Fig. 3.2  Diagrammatic representation of application of mycorrhizae in improving plant growth and imparting tolerance against abiotic stress

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

85

AMF

Drought stress

Alters

Cellular metabolism Gas exchange ROS and anti-oxidant balance Photosynthetic efficiency

Osmotic potential

Reduced growth and yield

Improved Photosynthetic efficiency Improved nutrient uptake and energy metabolism Enhanced secondary metabolite accumulation Enhanced water status and water use efficiency Osmotic adjustment and regulation of oxidative defense system

Growth maintainance and yield improvement

Fig. 3.3  Various mechanisms adopted by VAM fungi to provide drought tolerance to plants

3.4.1  Modification of Hormonal Balances Under drought stress, AMF build changes in content of isoprenoids in leaves of tomato plants (Solanum lycopersicum L.), increasing the level of essential isoprenoids instead of nonessential isoprenoids (Asensio et al. 2012). This increase in production of essential isoprenoids is due to increasing requirement and biosynthesis of compounds derived from carotenoids such as ABA and strigolactones in mycorrhizal plants (Asensio et  al. 2012). ABA, strigolactones, and jasmonic acid are the plant hormones where change in level is recorded in mycorrhizal plants under water-deficit conditions (Ludwig-Müller 2010). 3.4.1.1  Abscisic Acid and Strigolactones Till today, it is quite complex to understand mycorrhizal interaction in plants due to their contrasting effects on ABA concentrations in plants under drought stress. Beneficial effects of symbiosis include increase of transpiration and water absorption by roots (Augé 2001) and lowering concentrations of ABA (Aroca et al. 2013). On the other hand, in tomato concentration of ABA increases under drought stress (Asensio et al. 2012). This change in hormonal levels is due to AMF genotype and the host plant (Ludwig-Müller 2010); it is found through various studies that, under drought stress, the mutualistic association with AMF regulates the ABA content (Table  3.1) (Estrada-Luna and Davies Jr 2003). ABA is primary requirement of AMF for sustainability and colonization, in host plant especially in water-deficit stress (Ludwig-Müller 2010). In fact, in tomato, ABA increases the susceptibility of plants to AMF colonization and appears to play an indispensable role in the development and functionality of arbuscules (Herrera-Medina et al. 2007). A significant correlation has been found between ABA production and strigolactones (Aroca et al. 2013). Strigolactones are reported as a new class of phytohormones regulating

86

D. Goyal et al.

Table 3.1  Recent studies showing the effect of AMF on plants subjected to a drought stress Stress Host species Drought Glycine max

Drought

Drought

Drought

Drought

Drought

Drought

Drought Drought

Drought

Fungus species AMF

Observed responses Enhanced leaf proline, photosynthesis, leaf area index, relative growth rate, fresh weight, and dry weight of seeds Increased hyphal length, Poncirus Funneliformis trifoliata mosseae, Paraglomus hyphal water absorption rate, and leaf water occultum potential Olea europaea AMF Alleviated drought impact and increased turgor potential (Ψp) and mineral uptake Increased plant growth Triticum Glomus mosseae, parameters, and total aestivum Glomus chlorophyll pigments fasciculatum, Gigaspora decipiens Digitaria Rhizophagus Increased shoot dry matter, eriantha irregularis stomatal conductance, lipid peroxidation, H2O2 in shoot and root Triticum Glomus mosseae Increased osmotic aestivum potential, chlorophyll content and fluorescence, activities of antioxidant enzymes, ascorbic acid, enzymes of N and P metabolism, and contents of N, P, and K Triticum Rhizophagus Higher grain biomass, and durum intraradices higher contents of copper, iron, manganese, zinc, and gliadins in grains Ipomoea Glomus spp. Proline and soluble sugars batatas adjust osmotic potential Saccharum Glomus spp. Increased leaf water arundinaceum uptake, and levels of metabolites, phenolics, ascorbic acid, glutathione, antioxidant enzymes, chlorophyll fluorescence, and plant biomass Zea mays Rhizophagus Increased plant dry weight, intraradices uptake of P, N, K, and Mg in shoot, and water use efficiency

References Pavithra and Yapa (2018)

Zhang et al. (2018)

Sara et al. (2018)

Pal and Pandey (2017)

Pedranzani et al. (2016)

Rani (2016)

Goicoechea et al. (2016)

Yooyongwech et al. (2016) Mirshad and Puthur (2016)

Zhao et al. (2015)

(continued)

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

87

Table 3.1 (continued) Stress Host species Drought Solanum lycopersicum

Fungus species Rhizophagus irregularis, Glomus intraradices

Drought Pelargonium graveolens

Rhizophagus intraradices, Funneliformis mosseae

Drought Fragaria ananassa

F. mosseae BEG25, F. geosporus BEG11

Drought Robinia pseudoacacia L. Drought

Drought

Drought

Drought

Drought Drought

Drought

Drought

Observed responses Increased biomass production, efficiency of photosystem II, ABA accumulation and synthesis, and strigolactone production Improved nutrient concentration, plant biomass, and essential oil content, and glomalin related soil proteins (GRSP) Increased shoot and root fresh weights, WUE, and plant survival Increased dry biomass, WUE, and net photosynthetic rate

Funneliformis mosseae and Rhizophagus intraradices Improved water content Glycine max Septoglomus constrictum, Glomus and P and N levels spp. including Glomus aggregatum Antirrhinum Glomus deserticola Increased shoot and root majus diameter, shoot length, leaf area, leaf number per plant, water content, Chl content, and proline Vigna Glomus intraradices, Increased mineral content, subterranea Gigaspora gregaria, soluble sugars, and acid phosphatase, but reduced Scutellospora proline content gregaria Hordeum Glomus intraradices Increased root volume, P vulgare content, and activity of phosphatase enzyme Cucumis melo Glomus mosseae K/Na ratio has increased in several plant tissues Citrullus Glomus mosseae Water use efficiency, leaf lanatus water content, and leaf osmotic potential has increased Lactuca sativa Glomus mosseae Endogenous auxin and cytokinin levels are increased in the presence of G. mosseae Brassica Glomus occultum Yield and quality increased oleracea with mycorrhizae

References Ruiz-Lozano et al. (2016)

Amiri et al. (2015)

Boyer et al. (2015) Yang et al. (2015)

Grümberg et al. (2015)

Asrar et al. (2012)

Tsoata et al. (2015)

Bayani et al. (2015) Turrini et al. (2005) Ortas et al. (2011)

Huang et al. (2011); Varga et al. (1994) Augé (2001) (continued)

88

D. Goyal et al.

Table 3.1 (continued) Stress Host species Fungus species Observed responses Drought Lactuca sativa Glomus fasciculatum L-arabinose (L Ara), ribose (Rib); D-xylose (D Xyl), L-xylose (L Xyl), adonitol (Ado), betamethyl-D-­ xyloside (Mdx) levels increased Drought Solanum Glomus mosseae Water use efficiency, leaf melongena water content, and leaf osmotic potential has increased Drought Piper nigrum Glomus caledonium Activity of superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and ascorbate peroxidase (APX) in leaves of plants treated with Glomus increased Drought Cucumis melo Glomus mosseae Water use efficiency, leaf water content, and leaf osmotic potential has increased Drought Eriobotrya Funneliformis Increased growth, leaf japonica mosseae water, proline, osmotic adjustment in root Increase in growth, water Funneliformis Drought Phoenix potential, and relative dactylifera monosporum, Rhizophagus clarus, water content and Glomus deserticola Increase in phosphorus and Drought Citrullus Mixed inoculum of nitrogen content of roots, lanatus Rhizophagus increase in water use irregularis and efficiency of plants Funneliformis mosseae Drought Helianthus Funneliformis Increase in phosphorus and annuus mosseae nitrogen content of seeds, improvement in seed quality Drought Knautia Glomus sp. Increase in phosphorus arvensis content Drought Trifolium Glomus sp. Increase in relative water repens content Drought Tagetes erecta Septoglomus Increase in photosynthetic constrictum pigments, phosphorus content and improved flower quality

References Cho et al. (2006)

Berreck and Haselwandter 2001 Sannazzaro et al. 2006

Seymen et al. 2015

Zhang et al. (2015) Meddich et al. (2015)

Omirou et al. (2013)

Gholamhoseini et al. (2013)

Doubková et al. (2013) Benabdellah et al. (2011) Asrar and Elhindi (2011)

(continued)

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

89

Table 3.1 (continued) Stress Host species Drought Pistacia vera

Fungus species Claroideoglomus etunicatum

Observed responses Growth in secondary metabolite content and peroxidase activity

References Abbaspour et al. (2012)

the architecture and reproductive development of plants (Foo and Reid 2013), but the function for which they were initially recognized for is the intermediation capacity in the mycorrhizal symbiosis process, where they act as a molecular signal in unfavorable conditions for plants (López-Ráez et al. 2010). ABA and strigolactones are apocarotenoids (Auldridge et al. 2006) and their biosynthesis is similar to each other (Walter et al. 2010). It is found that ABA regulates synthesis and concentration of strigolactone. For example, tomato plants that were deficient in the synthesis of ABA or treated with ABA specific inhibitors demonstrated a reduced capacity for strigolactone biosynthesis (López-Ráez et al. 2010). 3.4.1.2  Jasmonic Acid and Abscisic Acid Colonization of AMF in host plants also affects the activation of the JA signal pathway (Tejeda-Sartorius et al. 2008). Under drought stress, JA acts as stress signal and increases ABA concentration by mutualistic interaction between host plant and mycorrhizae (Asensio et al. 2012). JA also plays important roles in the development and functionality of arbuscules together with ABA (Isayenkov et  al. 2005). The increase of JA could be related to the variation of the root osmotic potential, caused by an increase of carbohydrates from shoots (Ludwig-Müller 2010). It has been suggested that sugar could induce the expression of genes related to JA biosynthesis, which could elevate the JA level and produce an increase in the sink strength through the extracellular invertase, whose expression is induced in mycorrhizal roots (Schaarschmidt et al. 2006). The narrow relationship found between ABA and AMF colonization in water-deficit conditions, as well as the functionality of the arbuscules suggests that the association between AMF and some plants could be one strategy to deal with a water deficit, probably regulated by the interaction of ABA with other hormones (Table 3.1).

3.4.2  Improvement of Plant Water Status It is clear through previous studies that AMF make facilitate uptake and transport of water in host plants (Augé 2004). Gholamhoseini et  al. (2013) reported positive effect of independently colonizing AMF species (Funneliformis mosseae or Glomus hoi) in sunflowers (Helianthus annuus L.) and found improved water use efficiency as compared to non-inoculated host plant. This indicates AMF improves stomatal

90

D. Goyal et al.

conductance, transpiration rate, hydraulic conductivity, and water potential of leaves under drought stress (Table 3.1) (Augé 2004). Mycorrhizal fungi improve photosynthesis of host plant by improving the plant water status and increasing stomatal conductance which allow greater diffusion of CO2 within the mesophyll cells of leaves (Boldt et al. 2011). 3.4.2.1  Hydraulic Conductivity in Extraradical Hyphae and Roots Mycorrhizal fungi improve abiotic stress tolerance to plants by increase in hydraulic conductivity of roots (Augé et  al. 2008). This increased hydraulic conductivity results in larger root system and roots reach more deep into soil which has a positive effect on the relative water content (RWC) (Meddich et al. 2015) water potential, transpiration rate, and crop yield (Augé 2001). Mycorrhizal hyphae that are involved in water transport (Allen 2009) are characterized by a diameter between 2 μm and 5  μm and can penetrate smaller soil pores that are inaccessible to root hairs (10–20  μm diameter) and thereby absorb water that is not available to non-­ mycorrhizal plants (Marulanda et al. 2003). AMF produce a glycoprotein known as glomalin, which generates stable aggregates and beneficial effects on soil structures (Wu et al. 2008). Soil colonization by AMF is as important as root colonization by AMF and it affects water relationship in host plants (Augé et al. 2007). Difference in water improving capability by AMF is due to difference in their mycelium, hyphae length, and functional system (Table 3.1) (Cseresnyés et al. 2013). 3.4.2.2  Stomatal Conductance In water-deficit conditions AM provide strength to plants by change in stomatal conductance such as rosemary, tangerine, and rice (Augé et al. 2015; Wu and Xia 2006; Ruíz-Sánchez et al. 2011). On the contrary white clover (Trifolium repens L.) represents a decrease in stomatal conductance and an increase in the relative water content and water use efficiency (Benabdellah et al. 2011). (Table 3.1). However, this drought tolerance also depends on symbiosis between plant and mycorrhizae, for an instance inoculation of Rhizophagus irregularis in rose plants is not found successful to mitigate the stress (Klingeman et al. 2005). 3.4.2.3  Membrane Conductivity Symbiosis of AMF with host plant upregulates the expression of genes coding for aquaporins (Ruiz-Lozano 2003). Porcel et al. (2005) reported effect of inoculation of AMF in tobacco plants (Nicotiana tabacum) and found increased expression of genes coding for aquaporins, and increase in absorption of water by the plants (Porcel et al. 2005). On the other hand, Porcel et al. (2006) reported the effect of inoculation of F. mosseae and R. irregularis in lettuce (Lactuca sativa) and soy

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

91

plants (Glycine max) and found downregulation in genes coding for aquaporins and high relative water content as compared with non-inoculated plants. It indicates differential mechanisms adopted by VAM to alleviate drought stress. Apart from difference in VAM host plant also affects the mechanisms to cope up with stress.

3.4.3  Osmotic Adjustment Plants with mycorrhizae have a better osmotic adjustment than plants without mycorrhizae (Porcel and Ruiz-Lozano 2004). Abbaspour et  al. (2012) reported AMF increased level of compounds for osmotic adjustment in pistachio (Pistacia vera) and protected it from drought stress. Yooyongwech et al. (2016) found inoculation of Glomus sp. and Acaulospora sp. in sweet potato (Ipomoea batatas) provided tolerance against drought stress by increasing accumulation of osmotic compounds (Table 3.1). Proline is one of the chief osmolytes for osmotic adjustment and its accumulation has been found in plants inoculated with AMF such as white clover (Medina et al. 2010), sweet potato (Yooyongwech et al. 2016), Loquat (Eriobotrya japonica Lindl.) (Zhang et al. 2015), rice (Ruíz-Sánchez et al. 2011), and pistachio (Abbaspour et  al. 2012) in water deficit. On the other hand, some plants do not accumulate proline as a tolerance mechanism to water deficits. For example, mycorrhizal plants of the Indian coral tree (Erythrina variegata L.) displayed high tolerance to a water-deficit stress, associated with an accumulation of chlorophylls and carotenoids, but not proline (Manoharan et al. 2010). Inoculation of Glomus versiforme in citrus plant enhanced osmotic adjustment of plant by increasing level of macronutrients and micronutrients in plant (Jasper et al. 1991).

3.4.4  Antioxidant Activity Plants inoculated with AMF face low oxidative damage under water deficits and this is explained with the help of two mechanisms. According to first one hyphae help in water absorption and transfer it to the host plant, increasing the water level and decreasing the generation of reactive oxygen species (ROS). Caravaca et al. (2005) reported that non-inoculated plants of Myrtus communis and Phillyrea angustifolia under drought stress increased their superoxide dismutase (SOD), catalase (CAT), and total peroxidase (POX) activity as compared to inoculated plants. According to second mechanism there is an increase in the production of enzymatic and non-­ enzymatic antioxidants in plants symbiosed with AMF especially in water-deficit conditions (Zou et al. 2015; Amiri et al. 2015; Abbaspour et al. 2012). AM fungi are found to reduce the content of malondialdehyde and soluble protein in host plant and improved the activity of SOD and CAT (Gaspar et al. 1991). Recently, maize plants under water-deficit conditions have been found to be benefited by the AMF

92

D. Goyal et al.

symbiosis not only by a lower oxidative stress, but also by local restriction and non-­ systemic oxidative stress (Bárzana et  al. 2015). However, the exact mechanism involved is not yet clear and requires further experiments to better understand the actual function of AMF in the changes of reactive oxygen metabolism and antioxidants production (Table 3.1).

3.4.5  Higher Nutrients Absorption Under drought stress AM facilitate better nutrients supply to plants and increase pigments levels, stomatal conductance, transpiration rate, and CO2 assimilation rate providing strength to cope up with stress (Table 3.1). It is found in corn plant inoculation of different species of mycorrhizal fungi improves contents of mineral nutrients such as nitrogen (N), phosphorus (P), and magnesium (Mg) in roots and shoots of plants as compared to non-inoculated plants (Zhao et al. 2015; Zhang et al. 2014; Boldt et al. 2011). 3.4.5.1  Phosphorus Phosphorous (P) is a vital macronutrient for plants and is mandatory for all major metabolic processes such as photosynthesis, signal transduction, energy transfer, macromolecular biosynthesis, respiration, and nitrogen fixation in legumes (Rastegari et al. 2020a; Yadav et al. 2020e; Saber et al. 2005; Khan et al. 2010). Although phosphorous is abundant in soil, only 0.1% of the total phosphorous is available to plants (in the form of orthophosphates H2PO4− and HPO42−), thus making it a major limiting factor for plant growth (Zhou et al. 1992; Illmer and Schinner 1995). Since it is less mobile in soil through ion transporters and aquaporins AM improve its transport in host plants (Augé 2004). Inoculation of AM increase P content in plants such as marigold, wheat, sorghum, and squash (Asrar and Elhindi 2011; Al-Karaki et al. 2004; Wu and Xia 2006; Augé et al. 2007). AM mediated P accumulation increases root growth in plants which uptake water from depth (Rastegari et al. 2020b; Yadav et al. 2018) (Table 3.1). 3.4.5.2  Nitrogen AMF enhance the level of N in plants under drought stress, increasing the activity of the enzymes nitrate reductase (NR) and nitrite reductase (Table 3.1). Apart from increasing enzyme activity mycorrhizal fungi increase N transport through hyphae (Caravaca et al. 2005). Mycorrhizal fungi improve aquaporins activity which transports ammonium (Uehlein et al. 2007).

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

93

3.4.6  P  hotosynthesis, Partitioning, and Production of Photoassimilates Drought stress leads to accumulation of reactive oxygen species in plants and damages photosynthetic apparatus (Abbaspour et al. 2012) due to this NADPH and ATP become limiting factor for Calvin cycle. AMF inoculation improves photosynthetic rate of plants by increasing stomatal conductance and, therefore, CO2 fixing (Boldt et al. 2011). Increased stomatal conductance enhances the rate of photosynthesis in corn, guava, and rosemary (Estrada et al. 2013; Estrada-Luna et al. 2000; Sánchez-­ Blanco et al. 2004). Some of the non-stomatal factors also enhance photosynthesis rate by increasing accumulation of photosynthetic pigments, and protecting photosynthetic apparatus from reactive oxygen species, avoiding photo inhibition (Asrar and Elhindi 2011). Inoculation of AM increases content of photosynthetic pigments in marigold (Asrar and Elhindi 2011), Indian coral tree (Manoharan et al. 2010), sweet potato (Yooyongwech et al. 2016), and tangerine (Wu and Xia 2006). AMF improves the efficiency of photosystem II (PSII) (Fv/Fm) in corn, tomato, olive and black hawthorn plants (Ruíz-Sánchez et al. 2010; Yooyongwech et al. 2016; Estrada et al. 2013; Boldt et al. 2011). As a consequence of increase in (Fv/Fm) plants use the excitation energy more efficiently for CO2 assimilation (Table  3.1). This increased CO2 assimilation results in higher quantity of carbohydrates and plant biomass under drought stress (Boldt et al. 2011). F. mosseae (mycorrhizal fungi) establishes a symbiotic association with indian coral tree plants and increased contents of chlorophylls, carotenoids, and proteins and decreased the content of sugars, starches and proline (Manoharan et al. 2010). Wu and Xia (2006) reported symbiosis effect of Glomus versiforme with trifoliate orange (Poncirus trifoliata) and found increase in chlorophyll and carotenoids and decrease in sugars, starches, and proline. AMF are being used as an inoculum in sustainable production systems (Jeffries et al. 2003) because of the fact that their application can produce economic benefits, especially in crops of high commercial value (Borde et al. 2011).

3.5  Conclusion and Future Perspective As already discussed drought is one of the most threatening problems and reduces or limits plant growth and productivity and AM are the symbiotic organisms which can cope with it. There are many reports in literature where AM fungi are reported as alleviator of drought stress. However, there are no more reports on synergistic effect of AMF with rhizobacteria and endophytes. Plant growth promoting rhizobacteria and endophytes also mitigate stress. Thus it will be an advancement of research to find out combining effect. AM provide drought tolerance by maintaining osmoregulation. Studies have been done on the concentration of osmolytes, research should be focused on the genes coding for osmolytes. This molecular investigation will deal with interaction studies of AM and roots of higher plants. AM symbiosis

94

D. Goyal et al.

with plant also varies according to plant genotype and AM species. Thus research should be focused to find out which species can provide more drought tolerance. AM facillitate adjustment of hormonal balance in plants to provide tolerance but studies are done only for ABA and strigolactones wheresas Salicylic acid, brassinosteroids also involve during water deficit. Research should be planned to find out the synthesis and signaling mechanism of salicylic acid and brassinosteroids in AM under drought stress. Acknowledgments  Authors are thankful to Director, Dayalbagh Educational Institute (Deemed University), Agra for providing facilities and DG also acknowledge Department of Science and Technology (DST) for INSPIRE research fellowship.

References Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab M (2012) Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709 Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic 109(1):1–7 Al-Karaki G, McMichael BZ, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14(4):263–269 Allen MF (2009) Bidirectional water flows through the soil-fungal plant mycorrhizal continuum. New Phytol 182:290–293 Amiri R, Nikbakht A, Etemadi N (2015) Alleviation of drought stress on rose geranium [Pelargonium graveolens (L.) Herit.] in terms of antioxidant activity and secondary metabolites by mycorrhizal inoculation. Sci Hortic 197:373–380 Aroca R, Ruiz-Lozano JM, Zamarreño ÁM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170(1):47–55 Asensio D, Rapparini F, Peñuelas J (2012) AM fungi root colonization increases the production of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application. Phytochemistry 77:149–161 Ashraf M (1994) Organic substances responsible for salt tolerance in Eruca sativa. Biol Plant 36(2):255–259 Asrar AW, Elhindi KM (2011) Alleviation of drought stress of marigold (Tagetes erecta) plants by using arbuscular mycorrhizal fungi. Saudi J Biol Sci 18:93–98 Asrar AA, Abdel-Fattah GM, Elhindi KM (2012) Improving growth, flower yield, and water relations of snapdragon (Antirrhinum majus L.) plants grown under well watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica 50(2):305–316 Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42 Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381 Augé RM, Toler HD, Moore JL, Cho K, Saxton AM (2007) Comparing contributions of soil versus root colonization to variations in stomatal behavior and soil drying in mycorrhizal Sorghum bicolor and Cucurbita pepo. J Plant Physiol 164(10):1289–1299 Augé RM, Toler HD, Sams CE, Nasim G (2008) Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. Mycorrhiza 18(3):115–121 Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-­ analysis. Mycorrhiza 25(1):13–24

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

95

Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9(3):315–321 Austin RB (1989) Maximising crop production in water-limited environments Bago B (2000) Putative sites for nutrient uptake in arbuscular mycorrhizal fungi. Plant Soil 226:263–274 Bárzana G, Aroca R, Ruiz-Lozano JM (2015) Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 38:1613–1627 Bayani R, Saateyi A, Faghani E (2015) Influence of arbuscular mycorrhiza in phosphorus acquisition efficiency and drought-tolerance mechanisms in barley. Int J Biosci 7(1):86–94 Benabdellah K, Abbas Y, Abourouh M, Aroca R, Azcón R (2011) Influence of two bacterial isolates from degraded and non-degraded soils and arbuscular mycorrhizae fungi isolated from semi-­ arid zone on the growth of Trifolium repens under drought conditions: mechanisms related to bacterial effectiveness. Eur J Soil Biol 47:303–309 Berreck M, Haselwandter K (2001) Effect of the arbuscular mycorrhizal symbiosis upon uptake of cesium and other cations by plants. Mycorrhiza 10(6):275–280 Boldt K, Pörs Y, Haupt B, Bitterlich M, Kühn C, Grimm B, Franken P (2011) Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. J Plant Physiol 168(11):1256–1263 Borde M, Dudhane M, Jite P (2011) Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Prot 30(3):265–271 Boyer LR, Brain P, Xu XM, Jeffries P (2015) Inoculation of drought-stressed strawberry with a mixed inoculum of two arbuscular mycorrhizal fungi: effects on population dynamics of fungal species in roots and consequential plant tolerance to water deficiency. Mycorrhiza 25(3):215–227 Caravaca F, Alguacil MM, Hernández JA, Roldán A (2005) Involvement of antioxidant enzyme and nitrate reductase activities during water stress and recovery of mycorrhizal Myrtus communis and Phillyrea angustifolia plants. Plant Sci 169(1):191–197 Cho K, Toler H, Lee J, Ownley B, Stutz JC, Moore JL, Augé RM (2006) Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. J Plant Physiol 163(5):517–528 Cseresnyés I, Takács T, Végh KR, Anton A, Rajkai K (2013) Electrical impedance and capacitance method: a new approach for detection of functional aspects of arbuscular mycorrhizal colonization in maize. Eur J Soil Biol 54:25–31 Deshmukh R, Sonah H, Patil G, Chen W, Prince S, Mutava R, Nguyen HT (2014) Integrating omic approaches for abiotic stress tolerance in soybean. Front Plant Sci 5(244):1–12 Disante KB, Fuentes D, Cortina J (2011) Response to drought of Zn-stressed Quercus suber L. seedlings. Environ Exp Bot 70(2–3):96–103 Doubková P, Vlasáková E, Sudová R (2013) Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil 370:149–161 Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM (2013) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201:42–51 Estrada-Luna AA, Davies FT Jr (2003) Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated Chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J Plant Physiol 160(9):1073–1083 Estrada-Luna AA, Davies FT Jr, Egilla JN (2000) Mycorrhizal fungi enhancement of growth and gas exchange of micropropagated guava plantlets (Psidium guajava L.) during ex vitro acclimatization and plant establishment. Mycorrhiza 10(1):1–8 Farahani A, Lebaschi H, Hussein M, Hussein SA, Reza VA, Jahanfar D (2008) Effects of arbuscular mycorrhizal fungi, different levels of phosphorus and drought stress on water use efficiency: relative water content and praline accumulation rate of coriander (Coriandrum sativum L.). J Med Plant Res 2:125–131 Foo E, Reid JB (2013) Strigolactones: new physiological roles for an ancient signal. J Plant Growth Regul 32(2):429–442

96

D. Goyal et al.

Gaspar T, Penel C, Hadege D, Greppin H (1991) Biochemical, molecular and physiological aspects of plant peroxidases. In: Lobarzewski J, Greppin H, Penel C, Gaspar T (eds) Plant peroxidases. Geneva: Imprimerie Nationale, University of Geneva pp 249–280 Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20(8):519–530 Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114 Goicoechea N, Merino S, Sánchez-Díaz M (2005) Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules of Anthyllis cytisoides L. subjected to drought. J Plant Physiol 162(1):27–35 Goicoechea N, Bettoni MM, Fuertes-Mendizabal T, González-Murua C and Aranjuelo I (2016) Durum wheat quality traits affected by mycorrhizal inoculation, water availability and atmospheric CO2 concentration. Crop and Pasture Sci 67(2):147–155 Grümberg BC, Urcelay C, Shroeder MA, Vargas-Gil S, Luna CM (2015) The role of inoculum identity in drought stress mitigation by arbuscular mycorrhizal fungi in soybean. Biol Fertil Soils 51(1):1–10 Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175(3):554–564 Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61(6):1041–1052 Huang Z, Zou Z, He C, He Z, Zhang Z, Li J (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339(1–2):391–399 Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates—solubilization mechanisms. Soil Bio Bioche 27(3):257–263 Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139(3):1401–1410 Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M and Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant and Cell Physiol 47(1):141–153 Jasper DA, Abbott LK, Robson AD (1991) The effect of soil disturbance on vesicular—arbuscular mycorrhizal fungi in soils from different vegetation types. New Phytol 118(3):471–476 Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soil 37(1):1–16 Jiang Y, Wang W, Xie Q, Liu N, Liu L, Wang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Sci 356(6343):1172–1175 Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. Journal of chemical ecology 38(6):651–664 Kasim WA, Osman ME, Omar MN, El-Daim IAA, Bejai S, Meijer J (2013) Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul 32(1):122–130 Khan MSI, Roy SS, Pall KK (2010) Nitrogen and phosphorus efficiency on the growth and yield attributes of capsicum. Aca J Plant Sci 3(2):71–78 Klingeman WE, Van Iersel MW, Kang JG, Augé RM, Moore JL, Flanagan PC (2005) Whole-plant gas exchange measurements of mycorrhizal ‘Iceberg’ roses exposed to cyclic drought. Crop Prot 24(4):309–317 Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A, Sayyed RZ, Hesham AE-L, Dhaliwal HS, Saxena AK (2019) Drought-tolerant phosphorus-solubilizing microbes: biodiversity and biotechnological applications for alleviation of drought stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting rhizobacteria for sustainable stress management: volume 1: rhizobacteria in abiotic stress management. Springer, Singapore, pp 255–308. https://doi.org/10.1007/978-981-13-6536-2_13

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

97

Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V, Dhaliwal HS, Saxena AK (2020a) Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolour L.) by drought-adaptive and phosphorus-solubilizing microbes. Biocatal Agric Biotechnol 23:101501. https://doi.org/10.1016/j.bcab.2020.101501 Kour D, Rana KL, Sheikh I, Kumar V, Yadav AN, Dhaliwal HS, Saxena AK (2020b) Alleviation of drought stress and plant growth promotion by Pseudomonas libanensis EU-LWNA-33, a drought-adaptive phosphorus-solubilizing bacterium. Proc Natl Acad Sci India Sect B Biol Sci. https://doi.org/10.1007/s40011-019-01151-4 Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal HS, Saxena AK (2020c) Microbial biofertilizers: bioresources and eco-friendly technologies for ­agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi.org/10.1016/j. bcab.2019.101487 Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62(14):4731–4748 Lindermann RG, Hendrix JW (1982) Evaluation of plant response to colonization by vesicular arbuscular mycorrhizal fungi (A) host variables. In: Schenck NC (ed) Methods and principles of mycorrhizal research. American Phytopathological Society, St Paul, MN, pp 69–76 Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y and Sun Q (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15(1):152. López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187(2):343–354 Ludwig-Müller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 169–190 Manoharan PT, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. grown under different water stress conditions. Eur J Soil Biol 46(2):151–156 Marulanda A, Azcon R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119(4):526–533 Meddich A, Jaiti F, Bourzik W, El Asli A, Hafidi M (2015) Use of mycorrhizal fungi as a strategy for improving the drought tolerance in date palm (Phoenix dactylifera). Sci Hortic 192:468–474 Medina A, Roldán A, Azcón R (2010) The effectiveness of arbuscular-mycorrhizal fungi and Aspergillus niger or Phanerochaete chrysosporium treated organic amendments from olive residues upon plant growth in a semi-arid degraded soil. J Environ Manag 91(12):2547–2553 Mirshad PP and Puthur JT (2016) Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceum retz.). Environ Monit Assess 188(7):425 Mishra AK, Singh VP (2010) A review of drought concepts. J Hydrol 391(1–2):202–216 Mosse B (1978) Mycorrhiza and plant growth. In: Structure and Functioning of Plant Populations, Verhandelingen der Koninklike Nederlandse, Akademic van Wetenschappen, Afdeling Natuurkunde, Tweede Reeks, deel 70. North-Holland Publ, Amsterdam, pp 269–298 Odebode AC, Ladoye AO and Osonubi O (1997) Effect of Pythium Aphnidermatum and the Arbuscular Mycorrhizal fungus Glomus deserticola on Disease Severity and growth of Pepper. Int J Trop Plant Dis 15:85–92. Olawuyi OJ, Babatunde FE, Njoku CG (2011a) Yield, drought tolerance, early fruiting and flowering of okra (Abelmoschus esculentus) as affected by arbuscular mycorrhiza (Glomus deserticola) and inorganic fertilizer (NPK). In: Proc 2nd technical workshop of the Nigerian organic agric network (NOAN) 12–16 Sept 13–18 Olawuyi OJ, Odebode AC, Olakojo SA, Adesoye AI (2011b) Host parasite relationships of maize (Zea mays L.) and Striga lutea (lour) as influenced by Arbuscular mycorrhiza fungi. J Sci Res 10:186–198 Olawuyi OJ, Odebode AC, Olakojo SA and Adesoye AI (2012) Variation in maize tolerance to Striga lutea (Lour) and influence of arbuscular mycorrhizal fungi. International Journal of Basic. Appl Inno Res 1(1):1–5

98

D. Goyal et al.

Olawuyi OJ, Odebode AC, Babalola BJ, Afolayan ET, Onu CP (2014a) Potentials of arbuscular mycorrhiza fungus in tolerating drought of maize (Zea mays L.). Am J Plant Sci 5:779–786 Olawuyi OJ, Odebode AC, Olakojo SA, Popoola OO, Akanmu AO, Izenigu JO (2014b) Host pathogen interaction of maize (Zea mays L.) and Aspergillus Niger as influenced by mycorrhizal fungi (Glomus deserticola). Arch Agron Soil Sci 60:1577–1591 Omirou M, Ioannides IM, Ehaliotis C (2013) Mycorrhizal inoculation affects arbuscular mycorrhizal diversity in watermelon roots, but leads to improved colonization and plant response under water stress only. Appl Soil Ecol 63:112–119 Ortas I, Sari N, Akpinar Ç, Yetisir H (2011) Screening mycorrhiza species for plant growth, P and Zn uptake in pepper seedling grown under greenhouse conditions. Sci Hortic 128(2):92–98 Ortas I (2012) Do maize and pepper plants depend on mycorrhizae in terms of phosphorus and zinc uptake?. J Plant Nutr 35(11):1639–1656 Osonubi O, Mulongoy K, Awotoye OO, Atayese MO, Okali DUU (1991) Effects of ectomycorrhizal and vesicular-arbuscular mycorrhizal fungi on drought tolerance of four leguminous woody seedlings. Plant Soil 136(1):131–143 Pal A, Pandey S (2017) Symbiosis of arbuscular mycorrhizal fungi and Pennisetum glaucum l. improves plant growth and glomalin-related soil protein in barren soil. Int J Sci Invent Today 6(6):783–792 Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 149(4):2000–2012 Pavithra D, Yapa N (2018) Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundw Sustain Dev 7:490–494 Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM (2016) Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 26(2):141–152 Pereira JS, Chaves MM (1995) Plant responses to drought under climate change in Mediterranean-­ type ecosystems. In: Global change and Mediterranean-type ecosystems. Springer, New York, pp 140–160 Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55(403):1743–1750 Porcel R, Gómez M, Kaldenhoff R, Ruiz-Lozano JM (2005) Impairment of NtAQP1 gene expression in tobacco plants does not affect root colonisation pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought. Mycorrhiza 15(6):417–423 Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60(3):389–404 Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rastegari AA, Yadav AN, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge, MA Rastegari AA, Yadav AN, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge, MA Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidencebased consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23(7): 515–531

3  Arbuscular Mycorrhizae Associations and Role in Mitigation of Drought Stress…

99

Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13(6):309–317 Ruíz-Sánchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869 Ruíz-Sánchez M, Armada E, Muñoz Y, de Salamone IEG, Aroca R, Ruíz-Lozano JM, Azcón R (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168(10):1031–1037 Ruiz‐Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo‐Jiménez B, Porcel R and López‐ Ráez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant, Cell & Environment 39(2):441–452 Sadhana B (2014) Arbuscular Mycorrhizal Fungi (AMF) as a biofertilizer-a review. Int J Curr Microbiol App Sci 3(4):384–400 Sannazzaro AI, Ruiz OA, Alberto EO, Menéndez AB (2006) Alleviation of salt stress in Lotus glaber by Glomus intraradices. Plant Soil 285(1–2):279–287 Schaarschmidt S, Roitsch T, Hause B (2006) Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J Exp Bot 57(15):4015–4023 Seymen M, Türkmen O, Paksoy M (2015) Bacteria inoculation effects on yield, yield components and mineral contents of (Capsicum annum L.) bell pepper. Int J Agric economic. Development 3(1):29 Sieverding E, Friedrichsen J, Suden W (1991) Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Technical Cooperation, Federal Repuplic of Germany, Eschborn Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Sheffield J, Wood EF and Roderick ML (2012) Little change in global drought over the past 60 years. Nature 491(7424):435–438 Smith S, Read D (2008) Colonization of roots and anatomy of arbuscular mycorrhiza. Mycorrhizal Symbiosis. Academic Press: London: 42–90 Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, James TY (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046 Sun Z, Song J, Xin XA, Xie X and Zhao B (2018) Arbuscular mycorrhizal fungal 14-3-3 proteins are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis. Frontiers in microbiology 9:91. Tejeda-Sartorius M, Martínez de la Vega O, Délano-Frier JP (2008) Jasmonic acid influences mycorrhizal colonization in tomato plants by modifying the expression of genes involved in carbohydrate partitioning. Physiol Plant 133(2):339–353 Tiwari V, Chaturvedi AK, Mishra A, Jha B (2015) Introgression of the SbASR-1 gene cloned from a halophyte Salicornia brachiata enhances salinity and drought endurance in transgenic groundnut (Arachis hypogaea) and acts as a transcription factor. PLoS One 10(7):e0131567 Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117 Tsoata E, Njock SR, Youmbi E, Nwaga D (2015) Early effects of water stress on some biochemical and mineral parameters of mycorrhizal Vigna subterranea (L.) Verdc. (Fabaceae) cultivated in Cameroon. Int J Agron Agric Res 7:21–35 Turrini A, Sbrana C, Nuti MP, Pietrangeli BM, Giovannetti M (2005) Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 266(1–2):69–75 Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68(1):122–129 Varga SS, Korányi P, Preininger É, Gyurján I (1994) Artificial associations between Daucus and nitrogen-fixing Azotobacter cells in vitro. Physiol Plant 90(4):786–790

100

D. Goyal et al.

Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16(2):123–132 Walter MH, Floss DS, Strack D (2010) Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232(1):1–17 Wilcox HE, Mycorrhizal Associations (1990) In: Nakas JP, Hagedorn C (eds) Biotechnology of plant-microbe interactions. McGraw Hill, New York, pp 227–255 Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163(4):417–425 Wu QS, Xia RX, Zou YN (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44(1):122–128 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, New York, pp 305–332 Yadav AN, Mishra S, Singh S, Gupta A (2019a) Recent advancement in white biotechnology through fungi. Volume 1: diversity and enzymes perspectives. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. Volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi. Volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important Fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N (2020b) Microbiomes of extreme environments: biodiversity and biotechnological applications. CRC Press, Taylor & Francis, Boca Raton Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020d) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020e) Plant microbiomes for sustainable agriculture. Springer, Cham Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H and Tang M (2015) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158 Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-Um S (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 198:107–117 Zhang Y, Yao Q, Li J, Hu Y, Chen J (2014) Growth response and nutrient uptake of Eriobotrya japonica plants inoculated with three isolates of arbuscular mycorrhizal fungi under water stress condition. J Plant Nutr 37:690–703 Zhang Y, Yao Q, Li J, Wang Y, Liu X, Hu Y, Chen J (2015) Contributions of an arbuscular mycorrhizal fungus to growth and physiology of loquat (Eriobotrya japonica) plants subjected to drought stress. Mycol Prog 14(10):84 Zhang Y, Hu J, Bai J, Wang J, Yin R, Wang J, Lin X (2018) Arbuscular mycorrhizal fungi alleviate the heavy metal toxicity on sunflower (Helianthus annuus L.) plants cultivated on a heavily contaminated field soil at a WEEE-recycling site. Sci Total Environ 628:282–290 Zhou JR, Fordyce EJ, Raboy V, Dickinson DB, Wong MS, Burns RA, Erdman Jr JW (1992) Reduction of phytic acid in soybean products improves zinc bioavailability in rats. The J Nutri 122(12):2466–2473 Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J (2015) Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Appl Soil Ecol 88:41–49 Zou YN, Huang YM, Wu QS, He XH (2015) Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 25(2):143–152

Chapter 4

Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi Prem Chandra, Enespa, and Ranjan Singh

Contents 4.1  4.2  4.3  4.4  4.5 

Introduction Causes of Soil Salinization and Associated Problems Nature and Diversity of Plant Growth–Promoting Fungi Effects of Salinity on Crops Arbuscular Mycorrhizal Fungi 4.5.1  Arbuscular Mycorrhizal Fungi in Saline Soils 4.5.2  Arbuscular Mycorrhizal Fungi and Salinity Stress Alleviation 4.5.3  Ameliorative Mechanisms Involved in Abatement of Salt Stress in Crops 4.5.4  Improved Nutrient Uptake 4.5.5  Morphological and Physiological Alterations 4.5.6  Biochemical Alterations 4.5.7  Molecular and Ultrastructural Changes 4.6  Conclusion and Future Prospects References

 101  105  106  107  108  108  112  113  114  118  120  125  126  126

4.1  Introduction Salinity stress inhibits the growth of crops, production of biomass, seed germination, and crop productivity. It is known as an abiotic environmental factor and is common globally (Wani et al. 2016). Salt stress also inhibits the growth of shoots and roots, and perturbs plant metabolism and physiological status as a result of ionic disparity in plant cells (Munns and Tester 2008). Salinity stress is caused by accumulation of compatible solutes and upregulation of antioxidants in cell signaling

P. Chandra (*) Department of Environmental Microbiology, School for Environmental Sciences, Babasaheb Bhimrao Ambedkar University (a central university), Lucknow, Uttar Pradesh, India Enespa Department Plant Pathology, Sri Mahesh Prasad Degree College, University of Lucknow, Lucknow, Uttar Pradesh, India R. Singh Lucknow, India © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_4

101

102

P. Chandra et al.

pathways and cellular responses (Wang et al. 2003). Additionally, observations have shown that ∼6% of the total land area around the world and 50% of the irrigated land are acutely affected by salt stress (Shabala and Cuin 2008). In all plants, calcium is an essential element, which maintains the integrity and structures of membranes and cell walls through formation of intermolecular linkages (Baluška et al. 2003). Toxic accumulation of Na+ ions in the cytosol leads to increased ambient salt concentrations. Procurement and homeostasis of essential nutrients such as K+ and Ca2+ are affected by inconsistent presence of Na+ in both cellular and extracellular partitions (Banjara et  al. 2012). A low K+:Na+ ratio is another specific symptom of salt toxicity. For activation of many enzymes, the presence of K+ in the cytosol is essential (Maathuis and Amtmann 1999). Excess Na+ tends to substitute K+ with Na+ at binding sites and hence impairs cellular biochemistry because of physicochemical similarities between Na+ and K+ (Benito et al. 2014). Plants adapt by de novo synthesis of organic compatible solutes acting as osmolytes to cope with salt stress–induced osmotic problems (Paul 2013; Suman et al. 2016; Yadav et al. 2019a). The highly ordered states of membranes and quaternary protein structures are stabilized by glycine betaine, which acts as an osmoprotectant (Sakamoto and Murata 2001). Under salt stress, proline serves as a storage sink for carbon and nitrogen and also as a free-radical scavenger, stabilizes subcellular structures (membranes and proteins), and buffers cellular redox potential (Sotiropoulos 2007). Accumulation of reactive oxygen species (ROS) such as superoxide radicals (O) hydrogen peroxide (HO) and hydroxyl radicals (OH) is induced by salt stress, with detrimental effects on plant growth and metabolism (Cakmak 2005). Therefore, soil amendment through exploitation of soil fungi is of considerable importance (Besharati et al. 2018). In saline conditions, various biological approaches such as use of arbuscular mycorrhizal fungi (AMF) to enhance plant growth and tolerance of abiotic environmental stress are receiving increasing recognition from scientists (Evelin et al. 2009). AMF also improve nutrient access and physiological processes such as the water absorption capacity of plants by increasing root hydraulic conductivity and favorably adjusting the osmotic balance and composition of carbohydrates in saline soil (Abdelhamid et al. 2019; Yadav et al. 2019b). Therefore, excess salt accumulation in the root is also ameliorated, and various observations have demonstrated effects on osmotic adjustment (Arora and Sahni 2019). Pigeonpea (Cajanus cajan (L.)) is a major grain legume (pulse) annual crop in the tropics and subtropics. It can be used as a source of seed and forage for livestock and as a soil ameliorator in agroforestry and shifting cultivation systems (Dagar 2016). A number of cereals such as sorghum (Sorghum bicolor L.), pearl millet (Pennisetum glaucum L.), and maize (Zea mays  L.) have traditionally been grown in intercropping or mixed cropping systems (Gemenet et al. 2016). AMF can play an important role in improvement of salt tolerance in various crops. The main objective of this chapter is to characterize salt resistance approaches by describing membrane peroxidation, electrolyte leakage, osmolyte accumulation, and enzymatic antioxidant defense systems under

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

103

abiotic salinity stress (Laouane et al. 2019). To date, there is little information available on the effects of salinity on plant biomass and nitrogen fixation, antioxidant defense systems, and use of mycorrhizal inoculation for osmoprotection in legumes (Wang et al. 2016). Observations have revealed a possible interrelationship between AMF inoculation and tolerance of ionic, osmotic, and oxidative stress in pigeonpea exposed to long-term salinity. Trichoderma longibrachiatum T6 (T6) has been shown to promote wheat growth and induce plant resistance to parasitic nematodes (Zhang et al. 2016a, b). Aspergillus aculeatus has an important effect on mitigation of salt stress by producing indole-­3-­acetic acid and siderophores, thereby conferring stress tolerance on plants, as shown in perennial ryegrass (Li et al. 2019). The possible effects of 24-epibrassinolide and the AMF Glomus mosseae, singularly and collectively, on salt stress in wheat (Triticum aestivum L.) plants have been studied (Tofighi et al. 2017). Important indicators of salt stress, such as the growth rate and nutritive values of perennial ryegrass, have been observed in order to explain mechanisms of protection against salt stress in ryegrass (Hu et al. 2012). Antioxidant activities such as lipid peroxidation, photosynthetic routines, ionic homeostasis, and metabolic homeostasis have been scrutinized (Jackson et  al. 2007). It has been estimated that associations between roots and AMF are present in over 80% of terrestrial plant species such as halophytes, hydrophytes, and xerophytes (Uhlmann et al. 2006). Mycorrhizal application represents a good option to alleviate salt stress through biological processes. Additionally, AMF can expand host physiological processes such as the water absorption capacity of plants by increasing root hydraulic conductivity and favorably adjusting the osmotic balance and composition of carbohydrates (Syvertsen and Garcia-Sanchez 2014). This may lead to increased plant growth and consequent dilution of toxic ion effects (Al-Karaki 2000; Yadav and Saxena 2018). These benefits of AMF have encouraged their use for mycoremediation of saline soils (Kumar et  al. 2019a). Various plant growth– promoting fungi (PGPF) that reduce salinity stresses in various crops are listed in Table 4.1. These fungi—such as Aspergillus, Fusarium, Trichoderma, Penicillium, Piriformospora, Phoma, Claroideoglomus, Glomus, and Rhizoctonia—have a natural capability to stimulate various growth-related traits of plants and thereby benefit the plants (Contreras-Cornejo et al. 2009; Enespa and Chandra 2019). Various observations in dicots and monocots have shown that PGPF mimic well-­ studied plant growth–promoting rhizobacteria (PGPR) in their interactions with host plants (Chandra and Singh 2016; Kour et al. 2019b; Kumar et al. 2019b; Singh et  al. 2020; Yadav et  al. 2018a). As an example, treatment of seeds with PGPF inoculum can improve germination and seedling vigor, and induces growth of longer and larger shoots in different plants. Some PGPF may exert effects on root development and performance (Enespa and Chandra 2017). The photosynthetic capability of plants can also be enhanced by PGPF inoculation, stimulating early and vigorous flowering of the plants. Various PGPF have the capability to stimulate the production of the host’s secondary metabolites and increase crop productivity (Singh and Yadav 2020; Yadav et  al. 2019c). PGPF show beneficial effects on growth and changes in biochemical, physiological, and molecular mechanisms used

104

P. Chandra et al.

Table 4.1  Effects of fungi in plants subjected to salinity stresses Crops Triticum aestivum L.

Fungi Glomus mosseae

Effects Stimulated leaf enzymatic antioxidant activities including those of catalase (2.24-fold) and ascorbate peroxidase (2.18-fold); increased malondialdehyde concentrations (36.17%) and H2O2 concentrations (49.74%) Solanum Piriformospora indica Increased content of phenolic lycopersicum L. compounds and nonenzymatic antioxidants; increased activity of antioxidant enzymes Enhanced growth, biomass, root Cucumis Claroideoglomus sativus L. etunicatum, Rhizophagus activity, nutrient content, and gas exchange parameters in plants intraradices inoculated with arbuscular mycorrhizal fungi Ricinus communis Funneliformis mosseae, Increased chlorophyll content in leaves, increased P and Mg Rhizophagus uptake, and increased proline intraradices content, protecting plant growth Lolium perenne Aspergillus aculeatus Lowered Na:K ratio; lowered concentrations of metabolites, amino acids (alanine, proline, gamma aminobutyric acid, and asparagine), and soluble sugars (glucose and fructose); improved plant photosynthetic efficiency; reduced activity of antioxidant enzymes (peroxidase and catalase); attenuated lipid peroxidation (decreased H2O2 and malondialdehyde accumulation) Glomus fasciculatum Increased chlorophyll content Tomato cultivars coupled with an increased (Sultana-7 and chlorophyll a:b ratio Super Strain-B) Rice Trichoderma harzianum Better photosynthetic performance; higher pigment concentrations and high proline content Triticum durum Rhizophagus irregularis, Increased root biomass, N uptake, Desf. Funneliformis mosseae and aboveground N concentrations; greater stability of plasma membranes Triticum aestivum Trichoderma Promoted growth; induced plant longibrachiatum T6 resistance to parasitic nematodes

References Tofighi et al. (2017)

Ghorbani et al. (2018)

Hashem et al. (2018)

Zhang et al. (2018a, b)

Li et al. (2017)

Ebrahim and Saleem (2017)

Fileccia et al. (2017)

Zhang et al. (2016a, b) (continued)

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

105

Table 4.1 (continued) Crops Fungi Panicum turgidum Funneliformis mosseae, Rhizophagus intraradices, Claroideoglomus etunicatum

Effects Increased chlorophyll a, chlorophyll b, and carotenoid content; increased superoxide dismutase, peroxidase, catalase, and glutathione reductase activities

References Hashem et al. (2015)

by host plants to alleviate salt stress (Zhang et al. 2016a, b; Rastegari et al. 2020a). This chapter discusses the effects of salinity on PGPF—such as colonization, hyphal length, and sporulation both in  vivo and in  vitro—and the presence of fungi in saline soils.

4.2  Causes of Soil Salinization and Associated Problems The physicochemical processes resulting from the presence of various salts in soil and water are known as salinization. In irrigated agricultural systems, soil salinity is an enormous problem. There are two main types of soil salinity: primary and secondary (Qadir and Schubert 2002). Primary salinity refers to natural processes of salt formation in soil and water. Development of secondary salinity results from anthropogenic activities such as land development, agriculture, irrigation, and industrial development (Rengasamy 2006). Common causes of secondary salinity are rising groundwater tables due to excessive irrigation or use of poor-quality water, clearance of vegetation, and changes in land use. Soils in hot and dry regions of the world are frequently saline with low agricultural potential. Secondary salinization of land and water resources in arid and semiarid conditions results from major anthropogenic activities such as agricultural irrigation (Chandra and Enespa 2019a; Machado and Serralheiro 2017). Anthropic salinization occurs in arid and semiarid areas because of waterlogging and mismanagement of irrigated water (Singh 2015). Worldwide, more than 45 million hectares of irrigated land, representing about 20% of all irrigated land and about 2% of all dryland agriculture, has already been damaged by salt (Carillo et al. 2011). Poor irrigation systems causing loss of once productive agricultural land represent the most serious salinity threat (Machado and Serralheiro 2017). Calcium (Ca2+), magnesium (Mg2+), and sodium (Na+) salts are found in irrigation water. Evapotranspiration plays a very significant role in pedogenesis of saline soils in arid and semiarid regions. Ions of calcium (Ca2+) and magnesium (Mg2+) salts released after evaporation often precipitate into carbonates, leaving Na+ dominant in the soil (Acosta et al. 2011; Qadir et al. 2007). Therefore, high concentrations of Na+ in the soil solution may put a brake on nutrient ion activities and produce extreme Na+:Ca2+ or Na+:K+ ratios (Guan et al. 2017; Antoniadis et al. 2015). During the last century, physical, chemical, and/or biological land degradation processes have resulted in

106

P. Chandra et al.

serious concerns about compaction, inorganic/organic contamination, and diminished microbial activity/diversity in natural soil resources worldwide (Mondal and Kaur 2017). As a result of introduction of irrigation, the areas of soils affected by these problems continue to increase each year. In India, saline soil mostly occurs in the Indo-Gangetic plain, which covers the states of Punjab, Haryana, Uttar Pradesh, and Bihar, and some parts of Rajasthan. Semiarid tracts in Gujarat, Madhya Pradesh, Maharashtra, Karnataka, and Andhra Pradesh are also largely affected by saline soils, as are arid tracts in Gujarat and Rajasthan (Chandra and Singh 2014; Shinde 2018; Silva et al. 2019).

4.3  Nature and Diversity of Plant Growth–Promoting Fungi Plant growth–promoting fungi are a heterogeneous group of nonpathogenic fungi associated with plants and mediate improvements in plant growth and health (Hossain et al. 2017; Rana et al. 2019b; Yadav et al. 2020a; Yadav et al. 2018c). Individual PGPF may differ conspicuously from one another in terms of their taxonomy, habitats, physiology, and interactions with plants, as observed in various studies (Bhattacharyya et al. 2016; Venturi and Keel 2016). A fungus that stimulates the growth of a given plant may not have the same effect upon the growth of another plant, or the effect may vary under a different set of environmental conditions (Hardoim et al. 2015; Vejan et al. 2016; Yadav et al. 2019d). Not all fungi that promote plant growth are considered to be PGPF, in the same way that symbiotic mycorrhizal fungi are known to improve plant growth but are not considered to be PGPF (Baum et al. 2015; Hossain et al. 2017). Mycorrhizal fungi behave as obligate biotrophs and establish an intimate association with the roots of most host plants (Hiruma et al. 2018). On the other hand, PGPF are nonsymbiotic saprotrophic fungi, which live freely on the root surface, in the interior of the root itself, or in the rhizosphere (Kour et al. 2019a). Fungal microbial flora identified as PGPF have diverse taxonomy (Chagas et al. 2018). The majority of true fungi characterized as PGPF primarily belong to the phylum Ascomycota (Aspergillus, Aureobasidium, Chaetomium, Cladosporium, Colletotrichum, Exophiala, Fusarium, Gliocladium, Penicillium, Phoma, Phomopsis, Purpureocillium, Talaromyces, and Trichoderma), and a few of them belong to Basidiomycota (Limonomyces, Rhizoctonia, Rhodotorula, and sterile fungi) and Zygomycota (Mucor and Rhizopus), according to the literature (Hossain et al. 2017; Rana et al. 2019a; Sharma et al. 2019; Yadav 2019; Zhang et al. 2018a, b). Fusarium oxysporum, Colletotrichum, and binucleate Rhizoctonia are phylogenetically related to plant pathogens but lack functional virulence determinants for many of the plant hosts from which they can be recovered (Lorenzo-Gutiérrez et al. 2019; Jiang et al. 2018). The members of the Oomycota are mostly virulent plant pathogens, while some are nonpathogenic (Hassani et al. 2018). Pythium oligandrum and Phytophthora cryptogea, which colonize root ecosystems and act as PGPF, are nonpathogenic oomycetes (Hossain et al. 2017). PGPF mostly have origins either in the soil or in the roots of a large range of hosts.

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

107

Commonly, 44% of rhizospheric fungal isolates are PGPF (Compant et al. 2010). The occurrence of PGPF in the rhizospheric region differs between different crop plants. Various fungi that live inside the root tissues or endophytes also have miscellaneous positive effects on plant growth and are PGPF (Cardoso Filho 2019). Fusarium, Penicillium, and Alternaria are the most dominant endophytes (Barsainya et al. 2016; Khalmuratova et al. 2015).

4.4  Effects of Salinity on Crops The growth of various plant species, particularly glycophytes (which are salt-­ sensitive rather than salt-tolerant halophyte species), is greatly impacted by high soil salinity. Most agricultural crops come under the category of glycophytes, which exhibit a spectrum of responses under salt stress (Volkmar et al. 1998; Hester et al. 2001). Salinity affects the physicochemical properties and ecological balance of the land, leading to low economic returns, soil erosion, and decreased crop productivity (Karami et al. 2012). The particular effects of salinity include the following: • Excessive accumulation of sodium ions in cell walls results in osmotic stress and cell death (Flowers and Yeo 1986; Munns and Passioura 1984). • Higher concentrations of salt in soil can interrupt nutrient stability in plants or interfere with uptake of some nutrients (Bernstein and Hayward 1958). • Extensive decreases in leaf area, chlorophyll content, and stomatal conductance occur, leading to a less competent photosystem II (PS-II) (Hura et al. 2007). • A substantial reduction in phosphorus uptake by plants occurs as a result of precipitation of phosphate ions in the form of calcium phosphate (Wendling et al. 2013). • Salinity inhibits the development of fertilization by weakening microsporogenesis and stamen filament elongation, causing ovule abortion and senescence of fertilized embryos (Gómez et al. 2015). • The supply of photosynthetic assimilates or hormones to growing tissues becomes impaired (Weber 2009). • Salt stress is a result of ion toxicity in which the K+:Na+ ratio changes, leading to replacement of K+ by Na+ in biochemical reactions. Because of this, quite a few enzymatic activities, as well as binding of transfer RNA (tRNA) to ribosomes— and consequently protein synthesis, in which K+ is a requisite—are inhibited (Almeida et al. 2017). Furthermore, high levels of Na+ and Cl− induce conformational changes in proteins. Recent reports have also shown that salinity adversely affects plant growth and development by hindering enzyme activity (Rani et al. 2019), DNA, RNA, protein synthesis, and mitosis (Atieno et al. 2017). • Osmotic stress and ion toxicity can cause metabolic imbalance, which in turn leads to oxidative stress (Liang et al. 2018).

108

P. Chandra et al.

• Cyclin-dependent kinases and cyclin activities are reportedly hindered by soil salinity, resulting in fewer cells in the meristem and limited growth. The activity of cyclin-dependent kinase is also reduced by posttranslational inhibition during salinity stress (Chandra and Enespa 2019c; Raines et al. 2016).

4.5  Arbuscular Mycorrhizal Fungi Endophytic and biotrophic fungi are known as mycorrhizal fungi and form mutualistic symbiosis with several plant species (Rana et al. 2019a; Verma et al. 2017). Various types of mycorrhizal fungi among the endomycorrhizal fungi (arbuscular mycorrhizal fungi) and ectomycorrhizal fungi are important in agriculture and forestry (Fesel and Zuccaro 2016). AMF are well known for their efficiency in plant growth promotion, especially in arid and semiarid regions. AMF may have appeared on earth more than 400  million years ago and are grouped into the phylum Glomeromycota (Berruti et  al. 2016). For their growth and reproduction, AMF mainly depend on host plants. Various researchers have reported that AMF improve plant growth and productivity by increasing the supply of phosphorus to host plants (Baum et al. 2015).

4.5.1  Arbuscular Mycorrhizal Fungi in Saline Soils AMF have been known to occur naturally in saline environments, in spite of the low mycorrhizal affinity of halophytes (Latef et al. 2016). In saline areas, the average density of spores has been reported to be low by some investigators but not others (Yang et al. 2018a, b). The most predominant species of AMF in the severely saline soils of the Tabriz plains (with an electrical conductivity (ECe) of 162 dS m−1) were found to be Glomus intraradices, Glomus versiform, and Glomus etunicatum (Becerra et al. 2019; Sheng et al. 2019). Increases in AMF spore numbers in the presence of soil salinity (defined as a mean of 100 spores per 10 g of soil) have been observed by various investigators (Bencherif et al. 2019a, b). Sporulation is stimulated under salt stress in saline soil with a high fungal spore density (Kissoudis et al. 2015). It has also been revealed that in severely saline ecosystems with low root colonization levels, AMF may produce spores (Sheng et al. 2019). One study found that saline soils with ECe of approximately 45 dS m−1 had zero spore inhabitants, in contrast to other observations (Kong et al. 2017; Lee et al. 2015). A 150 mM NaCl concentration inhibited hyphal growth and spore germination of AMF.  An abundance of AMF spores were found in highly alkaline soils with a pH of up to 11; the degree of colonization varied between individual AMF, independently of the soil type and salt type (NaCl, Na2CO3, Na2SO4, or CaSO4) (Hage-Ahmed et al. 2019; Latef et al. 2016; Porcel et al. 2016). AMF spore distribution was evaluated in two salt marshes (Powell and Rillig 2018). Greater AMF biodiversity was observed in

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

109

soil samples from both sites on the basis of morphological analysis of spores, but the overall biodiversity was lower in the roots at both sites, according to sequencing analysis (Faggioli et al. 2019; Berruti et al. 2017). AMF interactions were found to have valuable effects on water status, addition of osmolytes, and growth of Phragmites australis plants in a saline environment (Pereira et al. 2016). In mycorrhizal Aster tripolium plants in saline soil, an amended water relationship was observed. It was reported that the most common AMF observed in salt-­ stressed soil were Glomus spp., and one species, Glomus geosporum, produced 80% of the spores detected by biological molecular techniques (Mahmood et al. 2019; Plouznikoff et al. 2016). In the primary stage of growth, Glomus mosseae, Glomus intraradices, and Glomus claroideum were found to ameliorate salt stress in olive trees (Yasmeen et al. 2019). In terms of olive tree performance, Glomus mosseae was the most proficient fungus in acting against unfavorable effects of salinity, particularly in terms of the protection it offered (Kour et al. 2019). The negative properties of salinity stress may be contingent on the behavior of each species of AMF and its capability in protecting the plants, as suggested by these observations (Igiehon and Babalol 2018). Various observations have revealed that AMF increase the growth and productivity of plants through ingredient uptake, but the exact apparatus used by AMF to alleviate the reduction of growth in saline conditions is not yet clear (Vangelisti et al. 2018). In severely saline soil conditions, Glomus intraradices, Glomus versiforme, and Glomus etunicatum were found to be the most predominant species (Chun and Chandrasekaran 2018). Hyphal growth, spore germination, and colonization capability are adversely affected by extremely saline conditions, and salt can reduce formation of arbuscular mycorrhizae (Wang et  al. 2017; Venneman et  al. 2017). However, spore germination is not prevented or inhibited in severely saline ecosystems, although it may be delayed (Nagler et al. 2015). Multiple biochemical pathways such as ion homeostasis and retention and/or acquisition of water help to protect chloroplast functions in salt-tolerant plants (Suo et al. 2017). 4.5.1.1  Interactions Between Arbuscular Mycorrhizal Fungi and Plants Approximately 80% of terrestrial plant species and 92% of terrestrial plant families form symbiotic or mutualistic associations through colonization of plant roots by AMF (Asmelash et  al. 2016). Intraradical or extraradical hyphae are formed by AMF spores present in the soil. Plant roots are infected by intraradical hyphae penetrating their epidermal cells and colonizing their cortical cells (Yang et al. 2018a, b; Javeria et al. 2017). In the infected cortical cells, the formation of arbuscules is a unique property of AMF.  This colonization benefits both the host and the AMF, which have no negative effects on each other (Chen et al. 2018). Intercellular and intracellular hyphae are formed by the AMF inside the root, and the intercellular hyphae between the cortical cells form vesicles, which store nutrients (Walker et al. 2018). Glomus spores are known to form these vesicles (Oehl and Körner 2014).

110

P. Chandra et al.

The arbuscules formed inside the cortical cells are used by the plant and fungi to exchange nutrients such as phosphorus and nitrogen (Cosme et al. 2018). 4.5.1.2  I mportance of Arbuscular Mycorrhizal Fungi Under Stress Conditions AMF are used in cultivars mainly for improvement of plant growth and crop productivity. Salinity stress decreases nutrient supply and uptake by roots (Ilangumaran and Smith 2017). In most soils, the ionic form of phosphate is poorly transferred. A phosphate-depleted soil zone forms around plant roots over time, as a result of continuous nutrient uptake by the roots (York et al. 2016; Hinsinger et al. 2018). The extraradical hyphae of AMF play a dynamic part in nutrient uptake from soil after colonization is successfully completed (Hodge et al. 2010). In the undepleted nutrient zone, extraradical hyphae infiltrate the soil and extend more widely (Bücking and Kafle 2015). From the undepleted nutrient zone, the hyphae absorb nutrients and supply them to the plant via the arbuscular membrane (Jakobsen and Hammer 2015). Under salinity stress, mycorrhizal plants absorb and accumulate more nutrients (such as phosphorus) from the soil than nonmycorrhizal plants do (Parihar and Bora 2019). Macromolecules such as lignin, chitin, protein, and nucleic acid are broken down into simple monomers, which are hydrolyzed by the hydrolytic enzymes produced by extraradical hyphae in the soil. Nutrients are absorbed as monomers more efficiently by AMF (Ma et al. 2015). 4.5.1.3  Genera of Arbuscular Mycorrhizal Fungae Arbuscular mycorrhizal fungi have been found to occur naturally in saline ecosystems. Glomus, belonging to the family Glomeromycota, is the genus most commonly observed in saline soil, but the specificity of its ecology was not demonstrated until recently (Oehl et al. 2017). Only morphological characterization was used to identify AMF spores in earlier studies (Öpik et al. 2013; Wang et al. 2010). However, studies of fatty acid methyl ester (FAME), using polymerase chain reaction (PCR) and restriction fragment length polymorphism (RFLP) molecular techniques, have helped to provide better and more precise accounts of fungal diversity in NaCl-­ affected areas (Hinojosa et  al. 2010). AMF genera with potential for salt stress amendment are Glomus (Glomus intraradices, Glomus versiform, Glomus etunicatum (Pagano et al. 2016; Vályi et al. 2016), Glomus fasciculatum, Glomus macrocarpum, Glomus geosporum, and Glomus coronatum (Bhattacharjya et al. 2018)), Gigaspora (Gigaspora gigantean and Gigaspora margarita (de Souza Moreira et  al. 2015)), Acaulospora, Archaeospora (Muhammad and Setyaningrum 2017), Funneliformis (Funneliformis mosseae, Funneliformis geosporum, and Funneliformis coronatum), and Rhizophagus (Rhizophagus fasciculatus) (Bhattacharjya et al. 2018).

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

111

4.5.1.4  Nitrogen Fixation and Nodulation Nitrogen-fixing bacteria, which form nodules through symbiosis, are a soft target for salt stress, and the density of these bacteria is reduced by salinity stress (Garg and Chandel 2015; Yadav et  al. 2018b). This is due to early nodule senescence prompted by salinity stress (Matamoros et al. 2017), changes in formation of green pigments from leghemoglobin, damage to nitrogen fixation, and consequent acceleration of lytic activities (Savitha et  al. 2016). The detrimental effects of salt on nodulation and nitrogen fixation in legumes is counteracted by application of AMF (Mia et al. 2014). It has been observed that AMF interaction can ameliorate drought stress–induced premature nodule senescence (Zahir et al. 2019). A resilience effect of a mycorrhizal booster on nodule development under salinity stress has been observed (Choudhary et al. 2016). The number of nodules and the colonization of legumes was observed to be increased by AMF (Mahdhi et  al. 2017). A positive boost from AMF collaboration with nitrogen-fixing bacteria was observed in leguminous plants (Montaño et al. 2012). In mycorrhizal plants, higher leghemoglobin content was observed (Khatabi et al. 2019; Chandra and Singh 2016). In the synthesis of green pigments from leghemoglobin, a change of color in the nodule from pink to brownish pink was used to estimate the leghemoglobin content (Shahid et al. 2019). Higher nitrogenase activity occurs in mycorrhizal plants. Nodule interaction and mycorrhiza act synergistically to influence the infection rate, mineral nourishment, and plant growth (Muleta 2017; Zarea et al. 2011), which fulfill the requirement for both N and P, and improving plant tolerance of salt stress (Zhang et al. 2016a, b; Porcel et al. 2016). 4.5.1.5  Plant Growth and Biomass Saline stress hinders the growth of plants and biomass. The toxic effects of NaCl in disbursement of energy and unavailability of nutrients are the main reasons (Pollastri et al. 2018; Hussein et al. 2017). The fitness of the host plant is increased by mycorrhization, augmenting its growth and biomass (Garcia et al. 2014). Various research studies have observed that AMF-inoculated plants grow better than noninoculated plants under salt stress (Lone et al. 2017; Talaat and Shawky 2017; Sellitto et al. 2019). Mycorrhizal Acacia nilotica seedlings had higher root and shoot dry weights than nonmycorrhizal seedlings (Porcel et  al. 2016; Santander et  al. 2017). Fruit weight, fruit number, shoot and root dry weights, and fresh fruit yield were higher in mycorrhizal tomato plants than in nonmycorrhizal plants (Shinde and Singh 2017). During exposure to salinity stress, Glomus intraradices colonization of Cucurbita pepo plants improved plant growth, fruit quality, water status, and nutrient content (Bowles et al. 2016; Latef et al. 2016; Bona et al. 2017).

112

P. Chandra et al.

4.5.2  A  rbuscular Mycorrhizal Fungi and Salinity Stress Alleviation Salt stress alleviation by host plants’ interaction with AMF results from several mechanisms (Wang et  al. 2015; Hashem et  al. 2018). The protection against salt stress conferred by AMF has been attributed to increased uptake of nutrients as the result of interaction (Wu et al. 2010), osmoregulator accumulation, and increases in both water-use efficiency (WUE) and the rate of photosynthesis through a combination of nutritional effects (Waraich et al. 2011; Gattward et al. 2012), biochemical effects, and physiological effects, resulting in observations of salt stress alleviation in various studies (Katschnig et al. 2013). During salinity stress, alterations at the cellular, anatomical, and morphological levels are initiated by the plant itself to increase its capability to tolerate or avoid stress (Fahad et al. 2015a, b; Julkowska and Testerink 2015). These adaptations are not common in plants and are a dynamic consequence in several species of plants (Lämke and Bäurle 2017). To combat these stresses, in addition to inherent adaptations that can alleviate the effects of stress, several rhizospheric soil microorganisms display interactions (Singh et al. 2011). Photosynthetic efficiency, membrane integrity, and water status are physiological mechanisms that are disrupted by salinity effects (Evelin et al. 2009; Van Oosten et al. 2017). Salinity stress can be alleviated by enrichment of the physiological processes of plants by AMF, in addition to the aforementioned mechanisms (Parray et  al. 2016; Bhandari and Garg 2017). Colonization, spore germination, hyphal elongation, and growth of AMF (as well as that of host plants) have been shown to be hindered by salt stress (Lenoir et al. 2016; Mostofa et al. 2018). However, various studies have observed increased colonization and sporulation (Le Fevre et al. 2016). In saline and alkaline stress in soil, plant biomass, growth, elongation of roots and shoots, productivity, transformation of nutrients (Pii et al. 2015; Yadav et al. 2019d), production of phytohormones, water status, and various physiological and biochemical properties of plants can be increased by the interaction of mycorrhizal associations (Evelin et al. 2009; Chandra and Singh 2016). To protect plants from the adverse effects of salt stress, various approaches have been recommended (Fahad et al. 2015a, b; Jorge et al. 2016). Nutrient enrichment in colonized plants is attributable not only to nutrient uptake via the mycorrhizal pathway but also to morphological and biophysical modifications that are indirectly due to root colonization (Delian et  al. 2011; Chen et  al. 2016). The rate of carbon dioxide exchange, transpiration, stomatal conductance, and WUE boost nutrient absorbency with truncated mobility of P, Zn, and Cu related to changes in physiological processes associated with upgraded halotolerance in mycorrhizal plants (Elhindi et  al. 2017; Augé et  al. 2016). Various studies have reported that plants that are not inoculated with AMF contain less water than those inoculated with AMF (Symanczik et al. 2018; Santander et al. 2017), in which low water potential is enhanced by the hydraulic conductivity of the root (Robbins and Dinneny 2015).

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

113

A change in the morphogenetic atmosphere of the roots is associated with upgraded root conductance (Forni et al. 2017; Yadav et al. 2020d). The meristem activity of the root apexes is decreased by AMF, leading to an increase in the formation of adventitious roots, and these AMF-facilitated amendments in the morphology of roots may contribute to sustaining nutrient absorbance and water stability in the host plant under salt stress (Bahadur et al. 2019). Alterations in root systems in response to AMF- predominantly augmentations in branching and root system volume- have been reviewed (Sánchez-Bel et al. 2018; Schmidt and Gaudin 2017). In a salt-stressed ecosystem, water absorbency was augmented per unit of root length in colonized plants (Metwally and Abdelhameed 2018). Mycorrhizal colonization helps host plants to use water more efficiently and also allows maintenance of lower concentrations of carbon dioxide intercellularly, as manifested by several parameters (Yooyongwech et al. 2016). Consequently, in mycorrhizal plants, the capability for gas exchange increases (Romero-Munar et al. 2017), and fungi are considered to be bioameliorators of saline soils (Al-Amri et al. 2016).

4.5.3  A  meliorative Mechanisms Involved in Abatement of Salt Stress in Crops Salinity stress causes severe setbacks in plant growth, nutrient uptake behavior, physiological processes, and productivity (Beckles and Thitisaksakul 2014). Most observations have shown that the role of AMF in alleviating salt stress in plants has positive outcomes (Latef et al. 2016; Chandrasekaran et al. 2019). Different mechanisms used by AMF for reduction of salt stress in crops are summarized in Figure 4.1.

Fig. 4.1  Ameliorative mechanisms involved in alleviation of salt stress in crops

114

P. Chandra et al.

4.5.4  Improved Nutrient Uptake In plants grown in salt-stressed ecosystems, AMF have shown positive effects on mineral nutrient composition by improving selective absorbance of mineral nutrients (Gosling et al. 2006; Pii et al. 2015). Increased transport (absorption and/or translocation) and supply of minerals and ions to the root system are regulated primarily by AMF (Jeffries et  al. 2003). With increases in salt concentrations, the mycorrhizal dependency increases, and different fungal isolates have different effects in the same plant species (Tian et  al. 2004). The impacts of mycorrhizal fungi on diverse mineral nutrients are described in the following subsections. 4.5.4.1  Phosphorus Absorption of mineral nutrients, particularly phosphorus (P), is reduced significantly by soil salinity because phosphate ions are precipitated with Ca2+, Mg2,+ and Zn2+ ions and become unavailable to plants growing in saline soil (Grattan and Grieve 1999; Termaat and Munns 1986). Thus, solubilization of phosphorus to overcome the P-binding capacity of the soil is necessary for the growth of the plant and helps to alleviate salt stress (Kour et al. 2020; Reynolds and Davies 2001; Reef et al. 2010). Phosphate concentrations in plants are increased by mycorrhizal inoculation, which augments uptake. This is facilitated by the widespread hyphae of the fungus, giving mycorrhizal plants access to a greater soil volume than nonmycorrhizal plants (Casieri et al. 2013). It has been estimated that up to 80% of a plant’s phosphorus requirement is fulfilled by external hyphae (Tarafdar and Marschner 1994). In saline soil with various levels of soil salinity (1.2, 4, 6.5, and 9.5 dS m−1), higher P content was observed in mycorrhizal Acacia nilotica plants (1.2, 1.2, 0.9, and 0.6%, respectively) than in nonmycorrhizal plants (0.6, 0.5, 0.2, and 0.1%, respectively) (Giri et al. 2007; Soliman et al. 2012). The concentration of phosphorus in Trifolium alexandrium plants was found to be reduced with increasing levels of salinity (Shokri and Maadi 2009). It was also determined that as soil salinity increased from 2.2 to 5 and 10 dS m−1, P concentrations in shoots of nonmycorrhizal Trifolium alexandrium plants decreased from 0.41 to 0.36 and 0.28 mg L−1, respectively, while the respective concentrations in mycorrhizal plants were 0.68, 0.62, and 0.47 mg L−1 (Navarro et al. 2014; Alqarawi et al. 2014). In mycorrhizal plants, higher P absorption at all salinity levels showed that AMF increased P uptake in plants under saline conditions (Frosi et al. 2017; Evelin et al. 2009). In legumes, AMF-inoculated plants increased their growth rate, antioxidant production, and nodulation when the supply of phosphate nutrition was increased (Ashrafi et al. 2014; Veselaj et al. 2018). In AMF-inoculated plants grown in saline ecosystems, phosphate uptake was increased and vacuolar membrane integrity was maintained, while compartmentalization within vacuoles and ion uptake were selectively enhanced and negative effects of Na+ and Cl2 ions were

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

115

reduced (Evelin et al. 2012; Zhang et al. 2014), thereby precluding those ions from interfering in growth via metabolic pathways. 4.5.4.2  Nitrogen Uptake and reduction of NO3− and protein synthesis influence the various stages of nitrogen acquisition and utilization after interference by salinity (Zahran 1999; Tischner 2000). AMF can enhance absorption of nitrogen in host plants (Verzeaux et al. 2017), as shown by greater N accumulation in shoots of mycorrhizal Sesbania grandiflora and Sesbania aegyptiaca plants than in nonmycorrhizal control plants (Giri and Mukerji 2004) (Yadav et  al. 2020b, c). Inorganic nitrogen is absorbed from the soil in the form of nitrate by extraradical mycelia and assimilated by nitrate reductase sites on arbuscule cells (Toussaint et  al. 2004), and arginine formation occurs via the glutamine synthetase–glutamine oxoglutarate aminotransferase (GS-GOGAT) cycle. In primary nitrogen fixation in extraradical mycelia, these processes are consistent with increased expression of enzymes involved in arginine catabolism (Bücking et al. 2012; Azcón-Aguilar and Barea 2015). Metabolism of nitrogen is changed by alterations in enzyme processes when absorption of nitrogen is increased in plants with AMF (Burns et al. 2013; Van Der Heijden et al. 2008). The toxic effects of Na+ ions are decreased with upgraded nitrogen nutrition and this indirectly helps to maintain chlorophyll content (Friedman 2002). Plants absorb nitrogen in the form of nitrate (NO32−) and ammonium (NH4+) ions, strongly affecting accumulation of Na+ ions (Giri and Mukerji, 2004; Kaushal and Wani 2016). However, nitrogen uptake mechanisms in salt-stressed environments have not yet been clearly described (Dodd and Pérez-Alfocea 2012). 4.5.4.3  The K+:Na+ Ratio Plants have a tendency to take up more Na+ ions when the concentration of NaCl is increased in soil and the absorbency of K+ ions is decreased. K+ ions are essential for various cellular functions and compete with Na+ ions (Rejili et al. 2007; Khan and Panda 2008). In plant metabolism, K+ activates a range of enzymes and plays a dynamic role in protein synthesis and the movement of stomata (Martinoia et al. 2006). In protein synthesis, K+ ions bind tRNA to ribosomes in high concentrations (Weinger et al. 2004). A high Na+:K+ ion ratio caused by salinity disrupts the ionic balance in the cytoplasm, disturbing various metabolic pathways (Tuteja 2007; Tester and Davenport 2003). The effect of salinity on K+ and Na+ nutrition in plants with AMF can be reversed through mycorrhizal colonization, improving the uptake of K+ ions in saline ecosystems (Tester and Davenport 2003; Estrada et al. 2013a, b, c) while preventing Na+ translocation to shoot tissues. Synthesis and storage of polyphosphate influence uptake of Na+ ions and other cations (Giri and Mukerji 2004) by amending expression and movement of K+ and Na+ transporters and of H+ pumps that produce the driving force for transportation of ions (Matsui and

116

P. Chandra et al.

Homareda 1982). The transfer of Na+ out of the cytoplasm into either vacuoles or the apoplasm is catalyzed through Na+/H+ antiporters (Bassil et al. 2012; Ouziad et al. 2006). Interruption of various K-mediated enzymatic developments and protein synthesis is prevented by a higher K+:Na+ ion ratio. The ionic balance of the cytoplasm or Na+ efflux from plants influences the high K+:Na+ ion ratio (Maathuis and Amtmann 1999; Wishnia et al. 1975). In mycorrhizal plants, in comparison with nonmycorrhizal plants, lower Na+ ion concentrations are also attributable to the dilution effect due to growth enhancement (Garg and Manchanda 2009). In mycorrhizal plants, Na+ concentrations are increased with increasing salinity up to a certain level but then successively diminish at higher concentrations of salinity (Chartzoulakis and Klapaki 2000). These observations suggest that AMF promote a buffering effect on uptake of Na+ ions when the Na+ content is within an acceptable limit (Onofre et al. 2015). This also indicates an opportunity for a regulatory mechanism to function in the plant to contain Na+ ions. However, the uptake of P by mycorrhizal plants is diminished when salt concentrations are too high (9.5 dS m−1), because of the toxic effects of Na+ ions on fungal growth (Wang et  al. 2019), suggesting that mycorrhizal responses are only influential up to a certain level of salinity (4.7 dS m−1) (Elhindi et al. 2017). 4.5.4.4  Chloride Ions In saline ecosystems, root cells absorb Cl2 from the soil solution through anion channels and also through H+/Cl2 symporters (White and Broadley 2001). Chloride ions pass through the root via a simplistic pathway and are released from cells within the stele through specific anion channels to reach the xylem and then the shoots (Clarkson 1993). Accumulation of chloride ions greatly increases at high salt concentrations but remains constant in the root (Schachtman et al. 1989; Chen et al. 2002). High chloride ion concentrations can be toxic to crop plants and may restrict agriculture in saline regions where concentrations are higher (Chartzoulakis 2005). AMF can tackle this problem by reducing uptake of Cl2 ions (Evelin et al. 2009). In vacuolar membranes, Cl2 ions can be clustered in a way that inhibits them from interfering with metabolic pathways in the plant. However, some reports have indicated that Cl2 accumulation can actually be increased as a result of mycorrhizal colonization. This may be due to the carbon drain imposed by mycorrhizal hyphae on plants, which enhances translocation of highly mobile anions such as Cl2 from the soil (Elhindi et al. 2017; Evelin et al. 2009). 4.5.4.5  Calcium To transduce signals during salt stress, concentrations of Ca2+ are increased, and it acts as a second messenger (Kader and Lindberg 2010). Mycorrhization strongly affects Ca2+ in the plant, as shown in various studies. In mycorrhizal lettuce, Ca2+

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

117

uptake was increased (Ruiz-Lozano and Azcón 1997; Hajiboland et al. 2010), and nonmycorrhizal banana plants were shown to have lower Ca2+ concentrations than mycorrhizal plants (Azcón et al. 2003). Furthermore, it was reported that colonization and sporulation of AMF were promoted by higher concentrations of Ca2+ (Doubková et al. 2013). However, in contrast to the above observations, the concentration of Ca2+ ions was found to remain unchanged in shoot tissues of mycorrhizal and nonmycorrhizal Acacia auriculiformis plants (Kaya et al. 2009). This suggests that AMF may not be as important to movement of nutrients to plant roots by mass flow as it is to nutrient movement by diffusion (Jakobsen et al. 2003). 4.5.4.6  Magnesium Chlorophyll biosynthesis is reduced by saline stress, which also inhibits light harvesting and causes photosynthesis to diminish (Singh et al. 2018). Mycorrhizae can support higher chlorophyll concentrations by improving magnesium ion concentrations (Giri and Mukerji 2004). It has been reported that salt interferes with chlorophyll synthesis less in mycorrhizal plants than in nonmycorrhizal plants (Giri and Mukerji, 2004; Feng et al. 2002). The efficiency of photosynthesis and plant growth increase after sufficient absorption of Mg2+ ions, which also increases concentrations of chlorophyll (Gattward et al. 2012). 4.5.4.7  Other Micronutrients Plants’ access to micronutrients (Zn, Cu, and Fe) is profoundly affected by salinity (Viets Jr 1962). The solubility and mobility of micronutrients such as Cu and Fe is reduced in saline environments, where a depletion zone is created all around the root; therefore, the plant’s absorption of micronutrients is reduced (Kaur et al. 2020; Rastegari et al. 2020b; Welch and Shuman 1995). However, higher concentrations of these micronutrients are found in plants inoculated with rhizospheric fungi than in noninoculated plants (Richardson et al. 2009; Wu et al. 2013). This may be attributable to (1) a widespread root–hyphal system that shortens the path of nutrients entry into the plant; (2) the mycelium of fungi acting as a substrate for nutrients to bind to; (3) changes in the rhizosphere after introduction of AMF, influencing the solubility of nutrients and their ability to be absorbed; (4) an increase in the sink size of Cu and Zn due to higher shoot P concentrations, successively instigating uptake of nutrients and their translocation to the shoots (Maathuis et al. 2011); or (5) upregulation of expression of transporter genes for these nutrients. As an example, a plasma membrane Zn transporter gene, MtZIP2, is upregulated upon colonization by AMF (Cavagnaro 2008). The ionic balance maintained by rhizospheric fungi is now being interpreted at the molecular level. However, much remains to be elucidated regarding AMF-influenced increases in Ca2+:Na+ and Ca2+:Mg2+ ratios, as well as uptake of micronutrients (Elhindi et al. 2017; Chandra and Enespa 2019b; Chandra and Enespa 2020).

118

P. Chandra et al.

4.5.5  Morphological and Physiological Alterations The potential of soil and water becomes more negative in dry soil; to maintain a favorable gradient for water flow from the soil into the roots, the water potential must be decreased by the plants (Ruiz-Lozano 2003). A plethora of mechanisms have been developed by plants to achieve such an effect, the most essential being osmotic modification or osmoregulation, requiring a reduction in the plant osmotic potential, which is mitigated by active accumulation of organic ions or solutes (Yeo 1983). In plants exposed to saline stress, a number of nitrogen-containing compounds accumulate. Amino acids, amide, and proteins are the most common, along with quaternary ammonium compounds (betaines) and polyamines (Mansour 2000). When plants are not under salt stress, these compounds are generally present in low concentrations (Glick 2004). In saline ecosystems, the specific nitrogen-­ containing compounds that accumulate vary between plant species (Rare 1990). 4.5.5.1  Chlorophyll Content The chlorophyll content is decreased by increasing salinity suppressing specific enzymes that are responsible for synthesis of photosynthetic pigments (Parida and Das 2005). Chlorophyll biosynthesis also reduces chlorophyll concentrations in leaves after a reduction in the uptake of minerals that are required for the process (Pal and Laloraya 1972). In the leaves of mycorrhizal plants in saline ecosystems, higher chlorophyll content has been observed by various authors (Beltrano et  al. 2013). This suggests that salt interferes with synthesis of chlorophyll less in mycorrhizal plants than in nonmycorrhizal plants (Zhu et al. 2012). The antagonistic effect of Na+ on Mg2+ uptake is well controlled and suppressed in mycorrhizal plants (Allen and Shachar-Hill 2009). Under salt stress, inoculated plants reach levels of photosynthetic capacity (estimated by chlorophyll content) that are even superior to those seen with relative permeability (Shabala et al. 2012). 4.5.5.2  Water Status In the rhizospheric region, high concentrations of salt cause physiological drought for plants. Salts put water out of action and make it unobtainable by plants (Carillo et  al. 2011). In Malus hupehensis, mycorrhizal inoculation resulted in relatively higher leaf turgidity being maintained by seedlings, with lower leaf osmotic potential, in comparison with nonmycorrhizal plants in salt stress conditions (Yang et al. 2014a, b). Higher relative water content was observed in mycorrhizal Robinia pseudoacacia plants than in nonmycorrhizal plants under salt stress (Stratu et al. 2016). The improved hydraulic conductivity in mycorrhizal plants was attributed to AMF-­ induced transformation of root morphology and the capability of mycorrhizal plants to source macroelements well beyond the depletion zone, facilitated by the

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

119

extensive extrametrical mycelium of AMF (Bitterlich et  al. 2018). Additionally, more compatible solutes were accumulated by mycorrhizal plants to adjust the osmotic potential and enable efficient water usage by the host plants (Juniper and Abbott 1993). In salt-stressed mycorrhizal plants, improved water status may be due to AMF-regulated expression of aquaporin genes present in the leaves and roots (Rapparini and Peñuelas 2014). However, each aquaporin gene in the roots of mycorrhizal plants may react differently to salt stress (Bárzana et  al. 2014). For instance, the LePIP1 gene was downregulated with AMF colonization in Lycopersicon esculentum, while the same gene was upregulated in Lactuca sativa (Ouziad et al. 2006; Jahromi et al. 2008). The expression profiles of aquaporin genes (RpPIP1;1, RpPIP1;3, RpPIP2;1, RpTIP1;1, RpTIP1;3, and RpTIP2;1) were described in the leaves and roots of mycorrhizal and nonmycorrhizal Robinia pseudoacacia plants exposed to saline stress (Chen et al. 2017; Li et al. 2014). The AMF symbiosis effect on transcription of aquaporin genes varies between different plant species, the type of plant tissue in which they are expressed, and the level of salinity (Ruiz-Lozano et  al. 2012). In addition, the potential of various aquaporin genes to influence transport of water and other solutes may fluctuate and may be contingent on their location in the cell (Tyerman et al. 2002). 4.5.5.3  Osmoregulation Lowering the turgor pressure in plant cells under salinity stress causes cellular dehydration. Plants use osmoregulation as a mechanism to tolerate salt stress to counteract this effect (Shabala and Lew 2002). The water potential of the soil decreases after formation of Na+ and Cl− in the soil (Chao-Yin et  al. 2011). The plants must respond to the lower water potential to sustain a favorable gradient for water flow from the soil into the roots and to prevent dehydration of cells in this situation (Ruiz-Lozano et  al. 2006, 2012). Proline, betaine, polyamines, sugars, organic acids, amino acids, and osmolytes such as trehalose start to accumulate in the plants (Mansour 2000). Small organic solutes are osmolytes (i.e., nontoxic and water soluble) at high concentrations and are known as compatible solutes (Gibon et al. 1997; Low 1985). These osmolytes contribute to osmotic adjustment (Augé et al. 2014). Furthermore, they are involved in ROS quenching and in maintaining membrane integrity, the enzyme balance, and the protein balance; thus, they are also known as osmoprotectants (Xiao et al. 2008). 4.5.5.4  Relative Permeability Mycorrhizal fungal inoculation of host plants empowers the plants to maintain higher concentrations of electrolytes than nonmycorrhizal plants through enhanced membrane integrity and immovability (Franken and Bui 2018). Consequently, the electrical conductivity of mycorrhizal roots has been shown to be greater than that

120

P. Chandra et al.

of nonmycorrhizal roots (Sands et al. 1982). The roots of Cajanus cajan with fungi displayed higher relative permeability than those of nonmycorrhizal plants at various levels of soil salinity (ECe 4, 6, and 8 dS m−1). The leakage of electrolyte in leaves of Capsicum annum treated with 50  mM and 100  mM concentrations of NaCl were 31.66 and 42.45 mM. respectively, while AMF-inoculated plants had relatively lower electrolyte leakage values of 26.87 and 30.98 mM respectively (Parihar and Rakshit 2016). This suggests that the mycorrhizal plants had considerably lower root plasma membrane electrolyte permeability than the nonmycorrhizal plants. The membrane stability increase has been attributed to mycorrhiza-mediated increased uptake of phosphorus and increased antioxidant production (Chang et al. 2018; Evelin and Kapoor 2014).

4.5.6  Biochemical Alterations Plants must decrease their water potential to maintain a favorable gradient for water flow from the soil into the roots when the soil dries and the water potential reduces (Cook and Papendick 1972; Sharp and Davies 1985). Osmotic adjustment is promoted by the plants through active accumulations of organic ions or solutes, which mitigate the osmotic potential and counteract adverse effects (Eisa et al. 2012; Blum 2017). In plants grown in saline ecosystems, compatible osmolytes are commonly found—for example, nitrogen-holding complexes such as amino acids, amides, imino acids, ectoine (1,4,5,6-tetrahydro-2-methyl-4-carboxylpyrimidine), proteins, quaternary ammonium complexes, low molecular weight sugars, organic acids, and polyols (Ciulla et  al. 1997; Slama et  al. 2015). Various biochemical changes are discussed briefly here. In plants’ reactions to salt stress, several compounds that accumulate are nitrogen-containing ones such as quaternary ammonium compounds (betaines) and polyamines, and also amino acids, amides, and proteins (Rhodes and Hanson 1993). These compounds are generally present in low concentrations when the plant is not under salt stress (Edreva et al. 2008; Sudha and Ravishankar 2002). The compounds that accumulate in saline ecosystems vary from species to species (Al Hassan et al. 2016) and are present in very low concentrations in the absence of salt stress (Wu et al. 1988). To maintain turgor and turgor-dependent processes such as photosynthesis and stomatal opening, growth and cellular expansion occur in cells by osmoregulation (Daie and Patrick 1988; Hsiao 1973). 4.5.6.1  Proline Accumulation of the amino acid proline, induced by abiotic salinity stress, is the most frequently reported alteration in plants (de Carvalho et al. 2013). Proline is a nontoxic and defensive osmolyte, which maintains an osmotic balance under a lower water potential in saline ecosystems and is accumulated by various plants under saline conditions (Hayat et al. 2012; Hare et al. 1998). During salt stress, it

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

121

acts as a pool of energy and nitrogen for utilization (Mansour 2000). When a plant is inoculated with AMF, proline accumulation has been found to increase. Vigna radiata and Glycine max (L.) mycorrhizal plants were shown to have higher proline content than nonmycorrhizal plants (Nadeem et  al. 2014; Kim et  al. 2012), and higher concentrations of proline were found in the roots and shoots of the plants. The osmotic balance between water-absorbing root cells and external media is maintained by the roots, which are the primary sites of water absorption (Bernstein and Hayward 1958; Sharifi et al. 2007). In contrast, more proline was found to accumulate in nonmycorrhizal Vicia faba plants than in mycorrhizal plants at various salinity levels (0–6 dS m−1). In less-salinity-tolerant plant species, proline accumulation may be a symptom of stress and its involvement in the adjustment of osmotic may be insignificant and associated with potassium ions (Chun and Chandrasekaran 2018). Accumulation of proline in response to salinity may not necessarily be due to mycorrhizal colonization (Porcel et al. 2012). In response to salinity, high levels of proline were shown to accumulate in Lotus glaber (Sanchez et  al. 2005), and AMF influenced this proline accumulation. To determine the salt tolerance mechanisms operating in different plant systems, better explanations are needed (Andrade et al. 2009). 4.5.6.2  Betaines Under salinity stress, betaine accumulation is a common occurrence (Hossain and Fujita 2010). Betaines are N-methylated derivatives of amino acids, and quaternary ammonium compounds are metabolized infrequently after their formation (D’Agostino and Mabury 2013; Annunziata et al. 2019). They are also used as an indicator of salt stress (Juan et al. 2005; Tramontano and Jouve 1997). Betaines are simple nontoxic cellular osmolytes, improve the construction and actions of enzymes and complexes of proteins, and also maintain membrane integrity against the destructive effects of excess salt (Burg and Ferraris 2008; Papageorgiou and Murata 1995). When a plant is colonized by fungi, the accumulation of betaines is found to increase under salinity stress (Hameed et al. 2014). At higher salinity levels, the glycine betaine content of fungi-associated plants was found to be about twice that of plants not associated with fungi (Papageorgiou and Murata 1995; Kumar et al. 2014). 4.5.6.3  Polyamines Free polyamines are small organic cations, which are essential for growth of eukaryotic cells. Putrescine (Put), spermidine (Spd), and spermine (Spm) are the three main polyamines in plants (Galston and Sawhney 1990). As a result of sequential accumulation of amino propyl groups, spermidine and spermine are synthesized from putrescine (Pál et al. 2018; Moschou et al. 2008). Putrescine is manufactured indirectly via decarboxylation of arginine and directly from ornithine decarboxylase

122

P. Chandra et al.

(Panagiotidis et  al. 1987). A significant role is played by these cations in plant responses to a wide collection of ecological stressors such as salt stress (Urano et al. 2004), high osmolarity (Rajam et  al. 1998), and antioxidative stress. Under salt stress conditions, they have been suggested to regulate root development (Sannazzaro et al. 2007) and pools of free polyamine have been observed to be reduced (Talaat and Shawky 2013). However, host plant inoculation with rhizofungi increases concentrations of free polyamines (Barea et al. 2005). In Lotus glaber plants colonized by Glomus intraradices, the total free polyamine pools were increased, as observed by Sannazzaro et al. (2007). Individual polyamines determine variations in response to salinity and mycorrhization, contingent on the genotype of the plant and the organ (root/shoot) being considered. Salt-tolerant genotypes of mycorrhizal Lotus glaber plants displayed higher levels of root spermine than nonmycorrhizal plants (Abdel-Fattah et al. 2016). Under salt stress, salt-sensitive Lotus glaber mycorrhizal plants exhibited higher root spermine, lower shoot and root putrescine, and lower spermidine levels than nonmycorrhizal plants (Talaat and Shawky 2015). Polyamine pool modulations may be one of the apparatuses used by AMF to increase plants’ adaptation to saline soils (Acosta-Motos et al. 2017; Augé et al. 2014). 4.5.6.4  Carbohydrates A significant plant protection mechanism formed against the salt stress using to addition of soluble sugars counter to that stress by the osmotic potential of plants. Using the addition of soluble sugars a significant plant protection mechanism formed by the osmotic potential of plants against salt stress (Ashraf and Harris 2004). With increased concentrations of NaCl, the soluble sugar content in Phragmites australis was found to be expressively increased (Li et al. 2019; Vilela and Barbosa 2019). Phragmites australis plants inoculated with Glomus fasciculatum had higher levels of soluble sugars than nonmycorrhizal plants (Nasim 2010). Sugar concentrations were increased in soybean roots inhabited by Glomus intraradices (St-Arnaud et al. 1995). The presence of mycorrhizae and sugar content were positively correlated as a result of the sink effect of the fungus obtaining sugars from the shoot tissues (Abbaspour et al. 2012; Ruiz-Lozano et al. 2012). The presence of carbon compounds in the root system of mycorrhizal host plants habitually leads to increased rates of photosynthesis involvement in the development process (Fitter 2002). As a result of hydrolysis of starch to sugars in seedlings immunized with mycorrhizae, sugar accumulation was found to be increased (Conrath 2009). Correlations between sugar accumulation and P concentration were observed in host plants grown in saline conditions (Hammer et al. 2011; Flowers et al. 2010). Soluble sugar concentrations were found to be higher in the roots of mycorrhizal maize plants than in those of nonmycorrhizal plants in spite of similar P concentrations (Feng et al. 2002). It was suggested that the higher soluble sugar concentrations in mycorrhizal roots were due to AMF settlement and not to an enhancement in the P status of the plants (Délano-Frier and Tejeda-Sartorius 2008; Mohammadi et al. 2011). Trehalose carbohydrate is a nonreducing disaccharide stored in AMF

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

123

and plays a significant role as an abiotic stress protectant, stabilizing dehydrated enzymes and membranes, and protecting biological structures from drying damage (Redillas et al. 2012; Moussaid et al. 2015). It is also present in spores and in the extraradical mycelium of AMF (Hajiboland 2013). Trehalose is a rare sugar involved in AMF settlement and helps to defend plant roots against saline stress in higher vascular plants (Iordachescu and Imai 2011; Kosar et al. 2019). It is believed to possibly play a role in defending plants against abiotic stresses, as shown by the effect of salinity stress on trehalose content and metabolism in the extraradical hyphae of Glomus intraradices (Kaushal 2019). After treatment with 0.5 M NaCl in Glomus intraradices, no alteration in trehalose content was observed (Bencherif et al. 2019a, b; Liu et  al. 2014). Trehalose-6-phosphate phosphatase activations of moderate transient and neutral trehalase actions not associated with any transcriptional changes have been detected (Zhou et al. 2014). In extraradical hyphae and mycorrhizal roots, trehalose accumulation is of interest and may influence the response of AMF to stress environments, with trehalose being used as a stress defense agent (Kravić et al. 2013; Maralian et al. 2010). A substantial role in alteration of hyperosmotic conditions in symbiotic bacteria is played by trehalose metabolism (Reina-Bueno et al. 2012). This molecule plays a part in initiating tolerance of salt stress (Ghosh et  al. 2011). Consequently, the potential of trehalose in protecting cells from salt stress needs to be determined (Mostofa et al. 2015). A reduction in carbohydrate concentrations with proliferation in the percentage of root colonization has been determined (Zangaro et al. 2012). In the responses to salinity of soybean plants colonized by Glomus etunicatum, no role of soluble carbohydrates was detected (Dodd and Pérez-Alfocea 2012). 4.5.6.5  Antioxidants Singlet oxygen, superoxide anions, hydrogen peroxide, and hydroxyl radicals are activated oxygen species and expected by-products of the interface between oxygen and electrons trickling from electron transport chains during normal aerobic metabolism in chloroplasts and mitochondria (Phaniendra et al. 2015). Proteins, lipids, and DNA react with all activated oxygen species and when defensive mechanisms are deficient, cell structure and function can be damaged (Birben et al. 2012). Plants released antioxidants and enzymes from oxidative destruction which used as defense mechanisms. Thus, defensive mechanisms are found in plants outflow from oxidative destruction connecting antioxidant fragments and enzymes (Grassi et al. 2010). Correlations between antioxidant capability and NaCl tolerance have been established in various plant species (Arbona et al. 2013; Ashraf et al. 2012). Maximum antioxidant concentrations providing plants with more resistance to oxidative impairment have been determined (de Bernonville et  al. 2010). Superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APOX), glutathione reductase (Wang 2011), dehydroascorbate, monodehydroascorbate reductase (Yin et al. 2010; Eltelib et  al. 2011), guaiacol peroxidase, oxidized glutathione (Bela et  al.

124

P. Chandra et al.

2015), glutathione peroxidase, and enzymes involved in the ascorbate–glutathione cycle are considered to be antioxidants (Caverzan et al. 2012; Joseph et al. 2011). Activated oxygen species such as carotenoids, glutathione, tocopherols, and ascorbic acid are scavenged by nonenzymatic compounds (Carocho and Ferreira 2013). AMF symbiosis helps plants to alleviate salt stress by enhancing the activities of antioxidant enzymes, as shown by various observations (Estrada et al. 2013a, b, c; Ruiz-Lozano et al. 2012). In mycorrhizal plants, these advanced antioxidant enzymes indomitable comparison to the non-mycorrhizal plants observed in various studies (Zhu et  al. 2010). Higher antioxidant activities of SOD, peroxidase, and APOX have been observed in mycorrhizal soybean plants than in nonmycorrhizal plants (Gong et al. 2015). SOD helps to detoxify superoxide into hydrogen peroxide (Rodrigues and Gomes 2010). CAT and peroxidase detoxify hydrogen peroxide (Ramos et al. 2014). Detoxification of hydrogen peroxide produced in the chloroplasts of stressed host plants by APOX has also been reported (Liang et al. 2013). Increased glutathione reductase activity may assist nicotinamide adenine dinucleotide phosphate (NADP+) to receive electrons resulting from photosynthetic electron transport, thereby attracting electrons away from oxygen and reducing the production of O2 (Jing et al. 2011; Yamamori et al. 2012). 4.5.6.6  Hormonal Regulation Phytohormones (also known as growth regulators) are known to regulate plant growth under both ambient and stress conditions (Fahad et al. 2015a, b). They are derived via biosynthetic pathways in plants and can act at the site of production or away from it. Abscisic acid (ABA), auxins, brassinosteroids (BRs), cytokinins (CKs), gibberellins (GAs), jasmonic acid (JA), salicylic acid (SA), strigolactones (SLs), nitric oxide (NO), and triazoles are phytohormones known to play substantial roles in communicating salt stress tolerance in plants (Hilbert et al. 2012). Hormonal interactions between them modify biological and physiological processes, translating into mediation of growth, development, nutrient allocation, and source/sink transitions in response to environmental stimuli (Lüttge 2013). Furthermore, ABA, auxins, JA, and SA are known to act as signaling molecules in AMF symbiosis (Miransari et al. 2014; Martínez-Medina et al. 2011). Consequently, it is assumed that these hormones reduce soil salinity and play significant roles in improving plant growth (Paul and Lade 2014; Yaish et al. 2015). A newly recognized class of phytohormones is strigolactones, which are involved in various characteristics of plant development such as root growth coordination and shape, access to soil nutrients, secondary branch suppression in shoots, influence on internode length in cross talk with auxin, leaf senescence regulation, and induction of AMF symbiosis (Koltai and Kapulnik 2011). H2O2 accumulation depends on reduced NADP+ (NADPH) oxidase activities, which play an important role in ABA signaling (Ishibashi et al. 2010). In Solanum lycopersicum and Cicer arietinum, exogenous applications of GA and SA, respectively, have been shown to boost salinity tolerance (Hasanuzzaman et  al. 2013).

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

125

Greater nutrient access and manifold increases in GA concentrations in mycorrhizal Solanum lycopersicum indicated that GA can stimulate salinity tolerance as a result of foliar spraying of gibberellic acid (GA3) (Maggio et al. 2010; Peleg and Blumwald 2011). AMF colonization was shown to have a positive influence on endogenous concentrations of GA (Kiers et al. 2010; Jung et al. 2012). The phytohormone JA, which belongs to the octadecanoid family, is involved in plant responses to both biotic and abiotic stresses (Santino et al. 2013; Avanci et al. 2010).

4.5.7  Molecular and Ultrastructural Changes In the root cells of Sorghum plants, salinity stress cause increases in membrane surfaces and vesicle quantities (Beltrano et al. 2013; Grover et al. 2011). In response to salt stress in the shoot apical meristems of canola, increases in plasmodesmata numbers, cytoplasm vacuolization, and thickening of cell walls have been observed (Rewald et al. 2013). In Arabidopsis thaliana, as a result of dissipation of mitochondrial membranes, potential disruptions in thylakoid and thylakoid membranes and induction of ovule abortion have been observed (Waraich et al. 2012; Cossani and Reynolds 2012). Consequently, ROS accumulate in the cells of gametophytes, gradually leading to programmed cell death (Xie et al. 2014; Wang et al. 2013). Aborting gametophytes are produced from the concentric rings of endoplasmic reticulum, surrounding chloroplasts, mitochondria, microbodies, and cytoplasm due to the accumulation of ROS (Perry et al. 2011). The cytoplasmic content and organelles were invaginated into the vacuole. Antioxidant activities are increased in plants by inoculation with AMF (Yang et al. 2014a, b; Hoeksema et al. 2010), and AMF can be applied to neutralize the actions of ROS and alleviate salt stress (Estrada et al. 2013a, b, c; Filippou et al. 2013). Expression of a few proteins such as Na+/H+ antiporters, D1-pyrroline-5-­ carboxylate synthetase (LsP5CS), late embryogenesis abundant protein (LsLea), and ABA (Lsnced) has been the focus of various molecular inventions (Vaseva et al. 2010; Shu et al. 2013). Aquaporins are major intrinsic proteins (MIPs), belonging to the family of transmembrane channels, which permit the passage of water and a few other compounds (but not H+ and other ions) via selective membranes (Hachez et al. 2014) controlled by tonoplast aquaporins (TIPs) and plasmalemma aquaporins (PIPs) (Obroucheva 2013). Abiotic factors such as salt stress influence the expression of aquaporins, most probably via the phytohormones ABA and GA (Popko et  al. 2010; Skirycz and Inzé 2010). In salt-stressed AMF plants, analysis of the expression of aquaporin genes revealed antagonistic consequences. AMF expressively reduced messenger RNA (mRNA) transcription of LePIP1 and LeTIP but not LePIP2 in salt-stressed roots of untreated control plants (Li et  al. 2013; Gu et al. 2010).

126

P. Chandra et al.

4.6  Conclusion and Future Prospects Salinity stress in soil causes adverse effects on growth and physiology at the molecular level. However, plant growth–promoting fungi (PGPF) and arbuscular mycorrhizal fungi associated with the rhizospheric region of the plant effectively improve plant growth and crop productivity through accumulation of different solutes and greater uptake of water and nutrients in saline ecosystems. Ongoing improvements in molecular tools are improving our comprehension of cellular procedures and signaling mechanisms associated with development and resistance due to PGPF– plant interactions. The benefits of high-performing PGPF can be obtained by application of innovative biotechnological procedures to form genetically modified strains with amended features, such as functional articulation of PGPF genes in plants to yield beneficial results. Diverse rhizofungi such as Trichoderma viride, Trichoderma harzianum, Trichoderma longibrachiatum T6, Claroideoglomus etunicatum, Rhizophagus intraradices, Aspergillus aculeatus, Glomus fasciculatum, Glomus mosseae, Piriformospora indica, Claroideoglomus etunicatum, Rhizophagus intraradices, Funneliformis mosseae, and Rhizophagus intraradices increase the activity of soil enzymes, which helps to enhance plant growth hormones. These activities improve plant growth and productivity with the help of osmoregulation in saline soil. Acknowledgements  Prem Chandra would like to acknowledge the Department of Environmental Microbiology, Babasaheb Bhimrao Ambedkar University, and Dr. Enespa thanks the Department of Plant Pathology, Sri Mahesh Prasad Degree College, University of Lucknow, for assistance in the preparation of this chapter manuscript.

References Abbaspour H, Saeidi-Sar S, Afshari H, Abdel-Wahhab MA (2012) Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169(7):704–709 Abdel-Fattah GM, Rabie GH, Lamis DS, Rabab AM (2016) The impact of the arbuscular mycorrhizal fungi on growth and physiological parameters of cowpea plants grown under salt stress conditions. Int J Appl Sci Biotechnol 4(3):372–379 Abdelhamid MT, El-Masry RR, Darwish DS, Abdalla MM, Oba S, Ragab R (2019) The mechanisms involved in improving the tolerance of plants to salt stress using arbuscular mycorrhizal fungi. In: Microorganisms in saline environments: strategies and functions. Springer, Cham, pp 303–327 Acosta JA, Faz A, Jansen B, Kalbitz K, Martínez-Martínez S (2011) Assessment of salinity status in intensively cultivated soils under semiarid climate, Murcia, SE Spain. J Arid Environ 75(11):1056–1066 Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7(1):18 Al Hassan M, Pacurar A, López-Gresa MP, Donat-Torres MP, Llinares JV, Boscaiu M, Vicente O (2016) Effects of salt stress on three ecologically distinct Plantago species. PLoS One 11(8):e0160236

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

127

Al-Amri SM, Elhindi KM, El-Din AFS (2016) Effects of arbuscular mycorrhizal fungus Glomus mosseae and phosphorus application on plant growth rate, essential oil content and composition of coriander (Coriander sativum L.). Prog Nutr 18(4):443–454 Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10(2):51–54 Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149(1):549–560 Almeida DM, Oliveira MM, Saibo NJ (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Gen Mol Biol 40(1):326–345 Alqarawi AA, Abd Allah EF, Hashem A (2014) Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J Plant Interact 9(1):802–810 Andrade SA, Gratão PL, Schiavinato MA, Silveira AP, Azevedo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing Zn concentrations. Chemosphere 75(10):1363–1370 Annunziata MG, Ciarmiello LF, Woodrow P, Dell’Aversana E, Carillo P (2019) Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Front Plant Sci 10:230 Antoniadis V, Koutroubas SD, Fotiadis S (2015) Nitrogen, phosphorus, and potassium availability in manure- and sewage sludge–applied soil. Commun Soil Sci Plant Anal 46(3):393–404 Arbona V, Manzi M, Ollas CD, Gómez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14(3):4885–4911 Arora S, Sahni D (2019) Halophilic microbe interactions with plants to mitigate salt stress. In: Akhtar M (ed) Salt stress, microbes, and plant interactions: causes and solution. Springer, Singapore Ashraf MPJC, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166(1):3–16 Ashraf MA, Ashraf M, Shahbaz M (2012) Growth stage–based modulation in antioxidant defense system and proline accumulation in two hexaploid wheat (Triticum aestivum L.) cultivars differing in salinity tolerance. Flora-Morphol Distrib Funct Ecol Plants 207(5):388–397 Ashrafi E, Zahedi M, Razmjoo J (2014) Co-inoculations of arbuscular mycorrhizal fungi and rhizobia under salinity in alfalfa. Soil Sci Plant Nutr 60(5):619–629 Asmelash F, Bekele T, Birhane E (2016) The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7:1095 Atieno J, Li Y, Langridge P, Dowling K, Brien C, Berger B, Sutton T (2017) Exploring genetic variation for salinity tolerance in chickpea using image-based phenotyping. Sci Rep 7(1):1300 Augé RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front Plant Sci 5:562 Augé RM, Toler HD, Saxton AM (2016) Mycorrhizal stimulation of leaf gas exchange in relation to root colonization, shoot size, leaf phosphorus and nitrogen: a quantitative analysis of the literature using meta-regression. Front Plant Sci 7:1084 Avanci NC, Luche DD, Goldman GH, Goldman MHS (2010) Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet Mol Res 9(1):484–505 Azcón R, Ambrosano E, Charest C (2003) Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci 165(5):1137–1145 Azcón-Aguilar C, Barea JM (2015) Nutrient cycling in the mycorrhizosphere. J Soil Sci Plant Nutr 15(2):372–396 Bahadur A, Batool A, Nasir F, Jiang S, Mingsen Q, Zhang Q, Feng H (2019) Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int J Mol Sci 20(17):4199 Baluška F, Šamaj J, Wojtaszek P, Volkmann D, Menzel D (2003) Cytoskeleton–plasma membrane–cell wall continuum in plants. Emerging links revisited. Plant Physiol 133(2):482–491

128

P. Chandra et al.

Banjara M, Zhu L, Shen G, Payton P, Zhang H (2012) Expression of an Arabidopsis sodium/ proton antiporter gene (AtNHX1) in peanut to improve salt tolerance. Plant Biotechnol Rep 6(1):59–67 Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56(417):1761–1778 Barsainya M, Chandra P,  Singh D P (2016) Investigation of Cr (VI) uptake in saline condition using psychrophilic and mesophilic Penicillium sp. Int J Curr Microbiol Appl Sci 5:274–288 Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant-Microbe Interact 27(4):349–363 Bassil E, Coku A, Blumwald E (2012) Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot 63(16):5727–5740 Baum C, El-Tohamy W, Gruda N (2015) Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Scientia Hortic 187:131–141 Becerra AG, Cofré MN, García I (2019) Arbuscular mycorrhizal symbiosis in salt-tolerance species and halophytes growing in salt-affected soils of South America. In: Mycorrhizal fungi in South America. Springer, Cham, pp 295–314 Beckles DM, Thitisaksakul M (2014) How environmental stress affects starch composition and functionality in cereal endosperm. Starch-Stärke 66(1–2):58–71 Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201 Beltrano J, Ruscitti M, Arango MC, Ronco M (2013) Effects of arbuscular mycorrhiza inoculation on plant growth, biological and physiological parameters and mineral nutrition in pepper grown under different salinity and P levels. J Soil Sci Plant Nutr 13(1):123–141 Bencherif K, Dalpé Y, Hadj-Sahraoui AL (2019a) Arbuscular mycorrhizal fungi alleviate soil salinity stress in arid and semiarid areas. In: Microorganisms in saline environments: strategies and functions. Springer, Cham, pp 375–400 Bencherif K, Dalpé Y, Sahraoui ALH (2019b) Influence of native arbuscular mycorrhizal fungi and Pseudomonas fluorescens on Tamarix shrubs under different salinity levels. In: Microorganisms in saline environments: strategies and functions. Springer, Cham, pp 265–283 Benito B, Haro R, Amtmann A, Cuin TA, Dreyer I (2014) The twins K+ and Na+ in plants. J Plant Physiol 171(9):723–731 Bernstein L, Hayward HE (1958) Physiology of salt tolerance. Ann Rev Plant Physiol 9(1):25–46 Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559 Berruti A, Demasi S, Lumini E, Kobayashi N, Scariot V, Bianciotto V (2017) Wild Camellia japonica specimens in the Shimane Prefecture (Japan) host previously undescribed AMF diversity. Appl Soil Ecol 115:10–18 Besharati H, Aliasgharzad N, Khavazi K, Rahmani HA (2018) Soil biology and biotechnology. In: The soils of Iran. Springer, Cham, pp 189–211 Bhandari P, Garg N (2017) Arbuscular mycorrhizal symbiosis: a promising approach for imparting abiotic stress tolerance in crop plants. In: Plant–microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 377–402 Bhattacharjya S, Bhaduri D, Sahu A (2018) Arbuscular mycorrhizal fungi: a potential tool for enhancing crop productivity in salt affected soil. Int J Agric Env Biotechnol 11(6):871–880 Bhattacharyya PN, Goswami MP, Bhattacharyya LH (2016) Perspective of beneficial microbes in agriculture under changing climatic scenario: a review. J Phytology 8:26–41 Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5(1):9–19

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

129

Bitterlich M, Franken P, Graefe J (2018) Arbuscular mycorrhiza improves substrate hydraulic conductivity in the plant available moisture range under root growth exclusion. Front Plant Sci 9:301 Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40(1):4–10 Bona E, Cantamessa S, Massa N, Manassero P, Marsano F, Copetta A, Berta G (2017) Arbuscular mycorrhizal fungi and plant growth–promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza 27(1):1–11 Bowles TM, Barrios-Masias FH, Carlisle EA, Cavagnaro TR, Jackson LE (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci Total Env 566:1223–1234 Bücking H, Kafle A (2015) Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5(4):587–612 Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. Plant Sci 4:108–132 Burg MB, Ferraris JD (2008) Intracellular organic osmolytes: function and regulation. J Biol Chem 283(12):7309–7313 Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234 Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168(4):521–530 Cardoso Filho JA (2019) Production and application of novel bio-active compounds by endophytic microbes. In: Natural bio-active compounds. Springer, Singapore, pp 1–40 Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. Abiotic Stress Plant Mech Adapt 1:21–38 Carocho M, Ferreira IC (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 51:15–25 Casieri L, Lahmidi NA, Doidy J, Veneault-Fourrey C, Migeon A, Bonneau L, Brun A (2013) Biotrophic transportome in mutualistic plant–fungal interactions. Mycorrhiza 23(8):597–625 Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304(1–2):315–325 Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35(4):1011–1019 Chagas FO, de Cassia PR, Caraballo-Rodríguez AM, Pupo MT (2018) Chemical signaling involved in plant–microbe interactions. Chem Soc Rev 47(5):1652–1704 Chandra P, Singh DP (2014) Removal of Cr (VI) by a halotolerant bacterium Halomonas sp. CSB 5 isolated from sāmbhar salt lake Rajastha (India). Cell Mol Biol 60(5): 64–72 Chandra P, Enespa (2019a) Mycoremediation of environmental pollutants from contaminated soil. In Mycorrhizosphere and Pedogenesis (pp 239–274). Springer, Singapore Chandra P, Enespa (2019b) Soil–Microbes–Plants: interactions and ecological diversity. In plant microbe interface (pp 145–176). Springer, Cham Chandra P, Enespa (2019c) Fungal enzymes for bioremediation of contaminated soil. In Recent advancement in white biotechnology through fungi (pp 189–215). Springer, Cham Chandra P, Enespa, Kumar M (2020) Contribution of microbes in the renovation of wetlands. In: Upadhyay A, Singh R, Singh D (eds) Restoration of wetland ecosystem: a trajectory towards a sustainable environment. Springer, Singapore Chandra P, Singh E (2016) Applications and mechanisms of plant growth–stimulating rhizobacteria. In: Choudhary D, Varma A, Tuteja N (eds) Plant–microbe interaction: an approach to sustainable agriculture. Springer, Singapore

130

P. Chandra et al.

Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T (2019) Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress—a meta-analysis. Front Plant Sci 10:457 Chang W, Sui X, Fan XX, Jia TT, Song FQ (2018) Arbuscular mycorrhizal symbiosis modulates antioxidant response and ion distribution in salt-stressed Elaeagnus angustifolia seedlings. Front Microbiol 9:652 Chao-Yin DOU, Yao-Hu KANG, Shu-Qin WAN, Wei HU (2011) Soil salinity changes under cropping with Lycium barbarum L. and irrigation with saline–sodic water. Pedosphere 21(4):539–548 Chartzoulakis KS (2005) Salinity and olive: growth, salt tolerance, photosynthesis and yield. Agric Water Manag 78(1–2):108–121 Chartzoulakis K, Klapaki G (2000) Response of two greenhouse pepper hybrids to NaCl salinity during different growth stages. Scientia Hortic 86(3):247–260 Chen S, Li J, Fritz E, Wang S, Hüttermann A (2002) Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. Forest Ecol Manag 168(1–3):217–230 Chen W, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proc Nat Acad Sci 113(31):8741–8746 Chen J, Zhang H, Zhang X, Tang M (2017) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front Plant Sci 8:1739 Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi—from ecology to application. Front Plant Sci 9:1270 Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, Varma A (2016) Bacterial-­ mediated tolerance and resistance to plants under abiotic and biotic stresses. J Plant Growth Regul 35(1):276–300 Chun SC, Chandrasekaran M (2018) Proline accumulation influenced by osmotic stress in arbuscular mycorrhizal symbiotic plants. Front Microbiol 9:2525 Ciulla RA, Diaz MR, Taylor BF, Roberts MF (1997) Organic osmolytes in aerobic bacteria from Mono Lake, an alkaline, moderately hypersaline environment. Appl Environ Microbiol 63(1):220–226 Clarkson DT (1993) Roots and the delivery of solutes to the xylem. Phil Trans R Soc Lond Ser B 341(1295):5–17 Compant S, Van Der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plant– microorganism interactions. FEMS Microbiol Ecol 73(2):197–214 Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395 Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149(3):1579–1592 Cook RJ, Papendick RI (1972) Influence of water potential of soils and plants on root disease. Annu Rev Phytopathol 10(1):349–374 Cosme M, Fernández I, Van der Heijden MG, Pieterse CM (2018) Non-mycorrhizal plants: the exceptions that prove the rule. Trend Plant Sci 23(7):577–587 Cossani CM, Reynolds MP (2012) Physiological traits for improving heat tolerance in wheat. Plant Physiol 160(4):1710–1718 D’Agostino LA, Mabury SA (2013) Identification of novel fluorinated surfactants in aqueous film forming foams and commercial surfactant concentrates. Environ Sci Technol 48(1):121–129 Dagar JC (2016) Agroforestry: four decades of research development. Indian J Agrofor 18:1–32 Daie J, Patrick JW (1988) Mechanism of drought-induced alterations in assimilates partitioning and transport in crops. Crit Rev Plant Sci 7(2):117–137

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

131

de Bernonville TD, Guyot S, Paulin JP, Gaucher M, Loufrani L, Henrion D, Brisset MN (2010) Dihydrochalcones: implication in resistance to oxidative stress and bioactivities against advanced glycation end-products and vasoconstriction. Phytochemistry 71(4):443–452 de Carvalho K, de Campos MKF, Domingues DS, Pereira LFP, Vieira LGE (2013) The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol Biol Rep 40(4):3269–3279 de Souza Moreira FM, Ferreira PAA, Vilela LAF, Carneiro MAC (2015) Symbioses of plants with rhizobia and mycorrhizal fungi in heavy metal-contaminated tropical soils. In: Heavy metal contamination of soils. Springer, Cham, pp 215–243 Délano-Frier JP, Tejeda-Sartorius M (2008) Unraveling the network: novel developments in the understanding of signaling and nutrient exchange mechanisms in the arbuscular mycorrhizal symbiosis. Plant Signal Behav 3(11):936–944 Delian E, Chira A, Chira L, Savulescu E (2011) Arbuscular mycorrhizae: an overview. S West J Hortiv Biol Environ 2:167–192 Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63(9):3415–3428 Doubková P, Vlasáková E, Sudová R (2013) Arbuscular mycorrhizal symbiosis alleviates drought stress imposed on Knautia arvensis plants in serpentine soil. Plant Soil 370(1–2):149–161 Ebrahim MKH, Saleem AR (2017) Alleviating salt stress in tomato inoculated with mycorrhizae: photosynthetic performance and enzymatic antioxidants. J Taibah Univ Sci 11(6):850–860 Edreva A, Velikova V, Tsonev T, Dagnon S, Gürel A, Aktaş L, Gesheva E (2008) Stress-protective role of secondary metabolites: diversity of functions and mechanisms. Gen Appl Plant Physiol 34(1–2):67–78 Eisa S, Hussin S, Geissler N, Koyro HW (2012) Effect of NaCl salinity on water relations, photosynthesis and chemical composition of quinoa (Chenopodium quinoa Willd.) as a potential cash crop halophyte. Aust J. Crop Sci 6(2):357 Elhindi KM, El-Din AS, Elgorban AM (2017) The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.). Saudi J Biol Sci 24(1):170–179 Eltelib HA, Badejo AA, Fujikawa Y, Esaka M (2011) Gene expression of monodehydroascorbate reductase and dehydroascorbate reductase during fruit ripening and in response to environmental stresses in acerola (Malpighia glabra). J P Physiol 168(6):619–627 Enespa, Chandra P (2017) Microbial volatiles as chemical weapons against pathogenic fungi. In: Choudhary D, Sharma A, Agarwal P, Varma A, Tuteja N (eds) Volatiles and food security. Springer, Singapore, pp 227–254 Enespa, Chandra P (2019) Fungal community for novel secondary metabolites. In: Yadav A, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi. Fungal biology. Springer, Cham, pp 249–283 Enespa, Prakash J, Chandra P (2020) Halophilic microbes from plant growing under the hypersaline habitats and their application for plant growth and mitigation of salt stress. In: Yadav AN, Singh J, Rastegari AA, Yadav N (eds) Plant Microbiomes for Sustainable Agriculture. Springer, Cham, pp 317–349. https://doi.org/10.1007/978-3-030-38453-1_11 Estrada B, Aroca R, Azcón-Aguilar C, Barea JM, Ruiz-Lozano JM (2013a) Importance of native arbuscular mycorrhizal inoculation in the halophyte Asteriscus maritimus for successful establishment and growth under saline conditions. Plant Soil 370(1–2):175–185 Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM (2013b) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201:42–51 Estrada B, Aroca R, Maathuis FJ, Barea JM, Ruiz-Lozano JM (2013c) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36(10):1771–1782 Evelin H, Kapoor R (2014) Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza 24(3):197–208

132

P. Chandra et al.

Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104(7):1263–1280 Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22(3):203–217 Faggioli VS, Cabello MN, Grilli G, Vasar M, Covacevich F, Öpik M (2019) Root colonizing and soil borne communities of arbuscular mycorrhizal fungi differ among soybean fields with contrasting historical land use. Agric Ecosyst Environ 269:174–182 Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D, Tabassum MA (2015a) Potential role of phytohormones and plant growth–promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ Sci Pollut Res 22(7):4907–4921 Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Faiq M (2015b) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75(2):391–404 Feng G, Zhang F, Li X, Tian C, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12(4):185–190 Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Curr Opin Microbiol 32:103–112 Fileccia V, Ruisi P, Ingraffia R, Giambalvo D, Frenda AS, Martinelli F (2017) Arbuscular mycorrhizal symbiosis mitigates the negative effects of salinity on durum wheat. PLoS One 12(9):e0184158 Filippou P, Tanou G, Molassiotis A, Fotopoulos V (2013) Plant acclimation to environmental stress using priming agents. In: Plant acclimation to environmental stress. Springer, New York, pp 1–27 Fitter A (2002) Characteristics and functions of root systems. In: Plant roots. CRC Press, Boca Raton, pp 49–78 Flowers TJ, Yeo AR (1986) Ion relations of plants under drought and salinity. Funct Plant Biol 13(1):75–91 Flowers TJ, Gaur PM, Gowda CL, Krishnamurthy L, Samineni S, Siddique KH, Colmer TD (2010) Salt sensitivity in chickpea. Plant Cell Environ 33(4):490–509 Forni C, Duca D, Glick BR (2017) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 410(1–2):335–356 Franken P, Bui VC (2018) Acclimatisation of Rhizophagus irregularis enhances Zn tolerance of the fungus and the mycorrhizal plant partner. Front Microbiol 9:3156 Friedman M (2002) Tomato glycoalkaloids: role in the plant and in the diet. J Agric Food Chem 50(21):5751–5780 Frosi G, Barros VA, Oliveira MT, Santos M, Ramos DG, Maia LC, Santos MG (2017) Arbuscular mycorrhizal fungi and foliar phosphorus inorganic supply alleviate salt stress effects in physiological attributes, but only arbuscular mycorrhizal fungi increase biomass in woody species of a semiarid environment. Tree Physiol 38(1):25–36 Galston AW, Sawhney RK (1990) Polyamines in plant physiology. Plant Physiol 94(2):406–410 Garcia K, Delteil A, Conéjéro G, Becquer A, Plassard C, Sentenac H, Zimmermann S (2014) Potassium nutrition of ectomycorrhizal Pinus pinaster: overexpression of the Hebeloma cylindrosporum HcTrk1 transporter affects the translocation of both K+ and phosphorus in the host plant. New Phytol 201(3):951–960 Garg N, Chandel S (2015) Role of arbuscular mycorrhiza in arresting reactive oxygen species (ROS) and strengthening antioxidant defense in Cajanus cajan (L.) Mill sp. nodules under salinity (NaCl) and cadmium (Cd) stress. Plant Growth Regul 75(2):521–534 Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Mill sp. (pigeonpea). J Agron Crop Sci 195(2):110–123 Gattward JN, Almeida AAF, Souza JO Jr, Gomes FP, Kronzucker HJ (2012) Sodium–potassium synergism in Theobroma cacao: stimulation of photosynthesis, water-use efficiency and mineral nutrition. Physiol Plant 146(3):350–362

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

133

Gemenet DC, Leiser WL, Beggi F, Herrmann LH, Vadez V, Rattunde HF, Haussmann BI (2016) Overcoming phosphorus deficiency in West African pearl millet and sorghum production systems: promising options for crop improvement. Front Plant Sci 7:1389 Ghorbani A, Razavi SM, Omran VOG, Pirdashti H (2018) Piriformospora indica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russian J Plant Physiol 65(6):898–907 Ghosh N, Adak MK, Ghosh PD, Gupta S, Gupta DS, Mandal C (2011) Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep 5(1):89–103 Gibon Y, Bessieres MA, Larher F (1997) Is glycine betaine a non-compatible solute in higher plants that do not accumulate it? Plant Cell Environ 20(3):329–340 Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14(5):307–312 Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54(4):753–760 Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312 Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57(11):876–891 Gong M, You X, Zhang Q (2015) Effects of Glomus intraradices on the growth and reactive oxygen metabolism of foxtail millet under drought. Ann Microbiol 65(1):595–602 Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113(1–4):17–35 Grassi D, Desideri G, Ferri C (2010) Flavonoids: antioxidants against atherosclerosis. Nutrients 2(8):889–902 Grattan SR, Grieve CM (1999) Mineral nutrient acquisition and response by plants grown in saline environments. Handb Plant Crop Stress 2:203–229 Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotech 27(5):1231–1240 Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138(2):226–237 Guan F, Xia M, Tang X, Fan S (2017) Spatial variability of soil nitrogen, phosphorus and potassium contents in Moso bamboo forests in Yong’an City, China. Catena 150:161–172 Hachez C, Veljanovski V, Reinhardt H, Guillaumot D, Vanhee C, Chaumont F, Batoko H (2014) The Arabidopsis abiotic stress–induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2; 7 through protein–interactions and autophagic degradation. Plant Cell 26(12):4974–4990 Hage-Ahmed K, Rosner K, Steinkellner S (2019) Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manag Sci 75(3):583–590 Hajiboland R (2013) Role of arbuscular mycorrhiza in amelioration of salinity. In: Ahmad P, Azooz MM, Prasad MNV (eds) Salt Stress in Plants: Signalling, Omics and Adaptations. Springer, New York, pp 301–354. https://doi.org/10.1007/978-1-4614-6108-1_13 Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331(1–2):313–327 Hameed A, Dilfuza E, Abd-Allah EF, Hashem A, Kumar A, Ahmad P (2014) Salinity stress and arbuscular mycorrhizal symbiosis in plants. In: Miransari M (ed) Use of Microbes for the Alleviation of Soil Stresses, Volume 1. Springer New York, New York, NY, pp 139–159. https:// doi.org/10.1007/978-1-4614-9466-9_7 Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21(2):117–129

134

P. Chandra et al.

Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79(3):293–320 Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21(6):535–553 Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87 Hashem A, AbdAllah EF, Alqarawi AA, Aldubise A, Egamberdieva D (2015) Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J Plant Interact 10(1):230–242 Hashem A, Alqarawi AA, Radhakrishnan R, Al-Arjani ABF, Aldehaish HA, Egamberdieva D, Abd_Allah EF (2018) Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 25(6):1102–1114 Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6(1):58 Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466 Hester MW, Mendelssohn IA, McKee KL (2001) Species and population variation to salinity stress in Panicum hemitomon, Spartina patens, and Spartina alterniflora: morphological and physiological constraints. Environ Exp Bot 46(3):277–297 Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol 196(2):520–534 Hinojosa MB, García-Ruiz R, Carreira JA (2010) Utilizing microbial community structure and function to evaluate the health of heavy metal polluted soils. In: Soil heavy metals. Springer, Berlin, pp 185–224 Hinsinger P, Herrmann L, Lesueur D, Robin A, Trap J, Waithaisong K, Plassard C (2018) Impact of roots, microorganisms and microfauna on the fate of soil phosphorus in the rhizosphere. Ann Plant Rev 48:377–407 Hiruma K, Kobae Y, Toju H (2018) Beneficial associations between Brassicaceae plants and fungal endophytes under nutrient-limiting conditions: evolutionary origins and host–symbiont molecular mechanisms. Curr Opin Plant Biol 44:145–154 Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3(4):267–273 Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Wilson GW (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13(3):394–407 Hossain MA, Fujita M (2010) Evidence for a role of exogenous glycine betaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. Physiol Mol Biol Plants 16(1):19–29 Hossain MM, Sultana F, Islam S (2017) Plant growth-promoting fungi (PGPF): phytostimulation and induced systemic resistance. In: Plant–microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 135–191 Hsiao TC (1973) Plant responses to water stress. Ann Rev Plant Physiol 24(1):519–570 Hu L, Li H, Pang H, Fu J (2012) Responses of antioxidant gene, protein and enzymes to salinity stress in two genotypes of perennial ryegrass (Lolium perenne) differing in salt tolerance. J Plant Physiol 169(2):146–156 Hura T, Hura K, Grzesiak M, Rzepka A (2007) Effect of long-term drought stress on leaf gas exchange and fluorescence parameters in C3 and C4 plants. Acta Physiol Plant 29(2):103

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

135

Hussein M, Embiale A, Husen A, Aref IM, Iqbal M (2017) Salinity-induced modulation of plant growth and photosynthetic parameters in faba bean (Vicia faba) cultivars. Pak J Bot 49(3):867–877 Igiehon NO, Babalol OO (2018) Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. Int J Environ Res Public Health 15(4):574 Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1768 Iordachescu M, Imai R (2011) Trehalose and abiotic stress in biological systems. Abiotic stress in plants—mechanisms and adaptations. InTech, Rijeka, pp 215–234 Ishibashi Y, Tawaratsumida T, Zheng SH, Yuasa T, Iwaya-Inoue M (2010) NADPH oxidases act as key enzyme on germination and seedling growth in barley (Hordeum vulgare L.). Plant Prod Sci 13(1):45–52 Jackson SK, Hancock JT, James PE (2007) Biological free radicals and biomedical applications of EPR spectroscopy. Electron Paramagn Reson 20:192–244 Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbl Ecol 55(1):45 Jakobsen I, Hammer EC (2015) Nutrient dynamics in arbuscular mycorrhizal networks. In: Mycorrhizal networks. Springer, Dordrecht, pp 91–131 Jakobsen I, Smith SE, Smith FA (2003) Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. In: Mycorrhizal ecology. Springer, Berlin, pp 75–92 Javeria S, Kumar V, Sharma P, Prasad L, Kumar M, Varma A (2017) Mycorrhizal symbiosis: ways underlying plant–fungus interactions. In: Mycorrhiza—eco-physiology, secondary metabolites, nanomaterials. Springer, Cham, pp 183–207 Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37(1):1–16 Jiang C, Zhang X, Liu H, Xu JR (2018) Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLoS Pathog 14(3):e1006875 Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, Lombard D, Kahn CR (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Nat Acad Sci 108(35):14608–14613 Jorge TF, Rodrigues JA, Caldana C, Schmidt R, van Dongen JT, Thomas-Oates J, António C (2016) Mass spectrometry–based plant metabolomics: metabolite responses to abiotic stress. Mass Spectrom Rev 35(5):620–649 Joseph B, Jini D, Sujatha S (2011) Development of salt stress–tolerant plants by gene manipulation of antioxidant enzymes. Asian J Agric Res 5(1):17–27 Juan M, Rivero RM, Romero L, Ruiz JM (2005) Evaluation of some nutritional and biochemical indicators in selecting salt-resistant tomato cultivars. Environ Exp Bot 54(3):193–201 Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trend Plant Sci 20(9):586–594 Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38(6):651–664 Juniper S, Abbott L (1993) Vesicular–arbuscular mycorrhiza and soil salinity. Mycorrhiza 4(2):45–57 Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5(3):233–238 Karami A, Homaee M, Afzalinia S, Ruhipour H, Basirat S (2012) Organic resource management: impacts on soil aggregate stability and other soil physico-chemical properties. Agric Ecosyst Environ 148:22–28 Katschnig D, Broekman R, Rozema J (2013) Salt tolerance in the halophyte Salicornia dolichostachya Moss: growth, morphology and physiology. Environ Exp Bot 92:32–42

136

P. Chandra et al.

Kaur T, Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Dhaliwal HS, Saxena AK (2020) Microbe-mediated biofortification for micronutrients: present status and future challenges. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 1–17. https://doi.org/10.1016/B978-0-12-820528-0.00002-8 Kaushal M (2019) Microbes in cahoots with plants: MIST to hit the jackpot of agricultural productivity during drought. Int J Mol Sci 20(7):1769 Kaushal M, Wani SP (2016) Rhizobacterial–plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agric Ecosyst Environ 231:68–78 Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic 121(1):1–6 Khalmuratova I, Kim H, Nam YJ, Oh Y, Jeong MJ, Choi HR, Yoon H (2015) Diversity and plant growth promoting capacity of endophytic fungi associated with halophytic plants from the west coast of Korea. Mycobiol 43(4):373–383 Khan MH, Panda SK (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant 30(1):81 Khatabi B, Gharechahi J, Ghaffari MR, Liu D, Haynes PA, McKay MJ, Salekdeh GH (2019) Plant–microbe symbiosis: what has proteomics taught us. Proteomic 19(16):1800105 Kiers ET, Adler LS, Grman EL, Van Der Heijden MG (2010) Manipulating the jasmonate response: how do methyl jasmonate additions mediate characteristics of aboveground and belowground mutualisms. Funct Ecol 24(2):434–443 Kim YC, Glick BR, Bashan Y, Ryu CM (2012) Enhancement of plant drought tolerance by microbes. In: Plant responses to drought stress. Springer, Berlin, pp 383–413 Kissoudis C, Chowdhury R, van Heusden S, van de Wiel C, Finkers R, Visser RG, van der Linden G (2015) Combined biotic and abiotic stress resistance in tomato. Euphytica 202(2):317–332 Koltai H, Kapulnik Y (2011) Strigolactones as mediators of plant growth responses to environmental conditions. Plant Signal Behav 6(1):37–41 Kong CC, Ren CG, Li RZ, Xie ZH, Wang JP (2017) Hydrogen peroxide and strigolactones signaling are involved in alleviation of salt stress induced by arbuscular mycorrhizal fungus in Sesbania cannabina seedlings. J Plant Growth Regul 36(3):734–742 Kosar F, Akram NA, Sadiq M, Al-Qurainy F, Ashraf M (2019) Trehalose: a key organic osmolyte effectively involved in plant abiotic stress tolerance. J Plant Growth Regul 38(2):606–618 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Recent advancement in white biotechnology through fungi. Springer, Cham, pp 1–64 Kour D, Rana KL, Yadav N, Yadav AN, Kumar A, Meena VS, et al. (2019a) Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: Kumar A, Meena VS (eds) Plant growth promoting rhizobacteria for agricultural sustainability: from theory to practices. Springer, Singapore, pp 19–65. https:// doi.org/10.1007/978-981-13-7553-8_2 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019b) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, volume 2: perspective for value-added products and environments. Springer, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kour D, Rana KL, Yadav AN, Sheikh I, Kumar V, Dhaliwal HS, Saxena AK (2020) Amelioration of drought stress in Foxtail millet (Setaria italica L.) by P-solubilizing drought-tolerant microbes with multifarious plant growth promoting attributes. Environ Sustain 3:23–34. https://doi. org/10.1007/s42398-020-00094-1 Kravić N, Marković K, Anđelković V, Šukalović VHT, Babić V, Vuletić M (2013) Growth, proline accumulation and peroxidase activity in maize seedlings under osmotic stress. Acta Physiol Plant 35(1):233–239

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

137

Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2014) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Rev Biotechnol 35(4):461–474 Kumar A, Chaturvedi AK, Yadav K, Arunkumar KP, Malyan SK, Raja P, Kumar R, Khan SA, Yadav KK, Rana KL, Kour D, Yadav N, Yadav AN (2019a) Fungal phytoremediation of heavy metal-contaminated resources: current scenario and future prospects. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 3: perspective for sustainable environments. Springer, Cham, pp  437–461. https://doi. org/10.1007/978-3-030-25506-0_18 Kumar M, Saxena R, Rai PK, Tomar RS, Yadav N, Rana KL, Kour D, Yadav AN (2019b) Genetic diversity of methylotrophic yeast and their impact on environments. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 3: perspective for sustainable environments. Springer, Cham, pp  53–71. https://doi. org/10.1007/978-3-030-25506-0_3 Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18(1):124 Laouane RB, Meddich A, Bechtaoui N, Oufdou K, Wahbi S (2019) Effects of arbuscular mycorrhizal fungi and rhizobia symbiosis on the tolerance of Medicago sativa to salt stress. Gesunde Pflanzen 71(2):135–146 Latef AAHA, Hashem A, Rasool S, Abd_Allah EF, Alqarawi AA, Egamberdieva D, Ahmad P (2016) Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. J Plant Biol 59(5):407–426 Le Fevre R, O’Boyle B, Moscou MJ, Schornack S (2016) Colonization of barley by the broad-host hemibiotrophic pathogen Phytophthora palmivora uncovers a leaf development–dependent involvement of Mlo. Mol Plant-Microbe Interact 29(5):385–395 Lee Y, Krishnamoorthy R, Selvakumar G, Kim K, Sa T (2015) Alleviation of salt stress in maize plant by co-inoculation of arbuscular mycorrhizal fungi and Methylobacterium oryzae CBMB20. J Korean Soc Appl Biol Chem 58(4):533–540 Lenoir I, Fontaine J, Sahraoui ALH (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15 Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197(2):617–630 Li G, Santoni V, Maurel C (2014) Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 1840(5):1574–1582 Li X, Han S, Wang G, Liu X, Amombo E, Xie Y, Fu J (2017) The fungus Aspergillus aculeatus enhances salt-stress tolerance, metabolite accumulation, and improves forage quality in perennial ryegrass. Front Microbiol 8:1664 Li X, Sun X, Wang G, Amombo E, Zhou X, Du Z, Fu J (2019) Inoculation with Aspergillus aculeatus alters the performance of perennial ryegrass under phosphorus deficiency. J Am Soc Horticult Sci 144(3):182–192 Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011 Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun 495(1):286–291 Liu Z, Ma L, He X, Tian C (2014) Water strategy of mycorrhizal rice at low temperature through the regulation of PIP aquaporins with the involvement of trehalose. Appl Soil Ecol 84:185–191 Lone R, Shuab R, Khan S, Ahmad J, Koul KK (2017) Arbuscular mycorrhizal fungi for sustainable agriculture. In: Probiotics and plant health. Springer, Singapore, pp 553–577 Lorenzo-Gutiérrez D, Gómez-Gil L, Guarro J, Roncero MIG, Fernández-Bravo A, Capilla J, López-Fernández L (2019) Role of the Fusarium oxysporum metallothionein Mt1 in resistance to metal toxicity and virulence. Metallomic 11(7):1230–1240

138

P. Chandra et al.

Low PS (1985) Molecular basis of the biological compatibility of nature’s osmolytes. In: Transport processes, iono and osmoregulation. Springer, Berlin, pp 469–477 Lüttge U (2013) Whole-plant physiology: synergistic emergence rather than modularity. In: Progress in botany. Springer, Berlin, pp 165–190 Ma L, Sun X, Kong X, Galvan JV, Li X, Yang S, Hu X (2015) Physiological, biochemical and proteomics analysis reveals the adaptation strategies of the alpine plant Potentilla saundersiana at altitude gradient of the northwestern Tibetan plateau. J Proteom 112:63–82 Maathuis FJ, Amtmann ANNA (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84(2):123–133 Maathuis FJ, Podar D, Hawkesford MJ, Barraclough P (2011) Uptake, distribution, and physiological functions of potassium, calcium, and magnesium. In: The molecular and physiological basis of nutrient use efficiency in crops. Wiley, Chichester, pp 265–293 Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulture 3(2):30 Maggio A, Barbieri G, Raimondi G, De Pascale S (2010) Contrasting effects of GA 3 treatments on tomato plants exposed to increasing salinity. J Plant Growth Regul 29(1):63–72 Mahdhi M, Mahmoudi N, Msaadek A, Rejili M, Mars M (2017) Natural nodulation and AMF colonization of Retama raetam and their impact on soil microbial properties in arid regions of Tunisia. Res J Microbiol 12:82–89 Mahmood A, Kataoka R, Turgay OC, Yaprak AE (2019) Halophytic microbiome in ameliorating the stress. In: Eco physiology, abiotic stress responses and utilization of halophytes. Springer, Singapore, pp 171–194 Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43(4):491–500 Maralian H, Ebadi A, Haji-Eghrari B (2010) Influence of water deficit stress on wheat grain yield and proline accumulation rate. Afr J Agric Res 5(4):286–289 Martínez-Medina A, Roldán A, Albacete A, Pascual JA (2011) The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72(2–3):223–229 Martinoia E, Maeshima M, Neuhaus HE (2006) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58(1):83–102 Matamoros MA, Dalton DA, Becana M (2017) Ascorbate metabolism and nitrogen fixation in legumes. In: Ascorbic acid in plant growth, development and stress tolerance. Springer, Cham, pp 471–490 Matsui H, Homareda H (1982) Interaction of sodium and potassium ions with Na+, K+-ATPase. I.  Ouabain-sensitive alternative binding of three Na+ or two K+ to the enzyme. J Biochem 92(1):193–217 Metwally RA, Abdelhameed RE (2018) Synergistic effect of arbuscular mycorrhizal fungi on growth and physiology of salt-stressed Trigonella foenum-graecum plants. Biocatal Agric Biotechnol 16:538–544 Mia S, Van Groenigen JW, Van de Voorde TFJ, Oram NJ, Bezemer TM, Mommer L, Jeffery S (2014) Biochar application rate affects biological nitrogen fixation in red clover conditional on potassium availability. Agric Ecosyst Environ 191:83–91 Miransari M, Abrishamchi A, Khoshbakht K, Niknam V (2014) Plant hormones as signals in arbuscular mycorrhizal symbiosis. Critic Rev Biotech 34(2):123–133 Mohammadi K, Khalesro S, Sohrabi Y, Heidari G (2011) A review: beneficial effects of the mycorrhizal fungi for plant growth. J Appl Environ Biol Sci 1(9):310–319 Mondal HK, Kaur H (2017) Effect of salt stress on medicinal plants and its amelioration by plant growth promoting microbes. Int J Bio-Res Stress Manag 8(2):316–326 Montaño NM, Alarcón A, Camargo-Ricalde SL, Hernández-Cuevas LV, Álvarez-Sánchez J, González-Chávez MDCA, Maldonado-Mendoza IE (2012) Research on arbuscular mycorrhizae in Mexico: an historical synthesis and future prospects. Symbiosis 57(3):111–126

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

139

Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism: the state of the art. Plant Signal Behav 3(12):1061–1066 Mostofa MG, Hossain MA, Fujita M (2015) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasm 252(2):461–475 Mostofa MG, Li W, Nguyen KH, Fujita M, Tran LSP (2018) Strigolactones in plant adaptation to abiotic stresses: an emerging avenue of plant research. Plant Cell Environ 41(10):2227–2243 Moussaid S, Domínguez-Ferreras A, Muñoz S, Aurag J, Sanjuán J (2015) Increased trehalose biosynthesis improves Mesorhizobium ciceri growth and symbiosis establishment in saline conditions. Symbiosis 67(1–3):103–111 Muhammad M, Setyaningrum H (2017) Exploration and application of mycorrhiza as input of biological fertilizer technology to increase growth and melon quality. J Agroqua Media Inf Agron Budid Perair 15(2):1–12 Muleta D (2017) Legume response to arbuscular mycorrhizal fungi inoculation in sustainable agriculture. In: Microbes for legume improvement. Springer, Cham, pp 227–260 Munns R, Passioura JB (1984) Effect of prolonged exposure to NaCl on the osmotic pressure of leaf xylem sap from intact, transpiring barley plants. Funct Plant Biol 11(6):497–507 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681 Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32(2):429–448 Nagler K, Setlow P, Reineke K, Driks A, Moeller R (2015) Involvement of coat proteins in Bacillus subtilis spore germination in high-salinity environments. Appl Environ Microbiol l81(19):6725–6735 Nasim G (2010) The role of arbuscular mycorrhizae in inducing resistance to drought and salinity stress in crops. In: Plant adaptation and phytoremediation. Springer, Dordrecht, pp 119–141 Navarro JM, Pérez-Tornero O, Morte A (2014) Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the rootstock salt tolerance. J Plant Physiol 171(1):76–85 Obroucheva NV (2013) Aquaporins in seeds. Seed Sci Res 23(4):213–216 Oehl F, Körner C (2014) Multiple mycorrhization at the coldest place known for angiosperm plant life. Alp Bot 124(2):193–198 Oehl F, Laczko E, Oberholzer HR, Jansa J, Egli S (2017) Diversity and biogeography of arbuscular mycorrhizal fungi in agricultural soils. Biol Fertil Soil 53(7):777–797 Onofre SB, Santos ZM, Kagimura FY, Mattiello SP (2015) Cellulases produced by the endophytic fungus Pycnoporus sanguineus (L.) Murrill. Afr J Agric Res 10(13):1557–1564 Öpik M, Davison J, Moora M, Zobel M (2013) DNA-based detection and identification of Glomeromycota: the virtual taxonomy of environmental sequences. Botany 92(2):135–147 Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exp Bot 57(1–2):177–186 Pagano MC, Oehl F, Silva GA, Maia LC, Silva DK, Cabello MN (2016) Advances in arbuscular mycorrhizal taxonomy. In: Recent advances on mycorrhizal fungi. Springer, Cham, pp 15–21 Pal RN, Laloraya MM (1972) Effect of calcium levels on chlorophyll synthesis in peanut and linseed plants. Biochem Physiol Pflanz 163(5):443–449 Pál M, Tajti J, Szalai G, Peeva V, Végh B, Janda T (2018) Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants. Sci Report 8(1):12839 Panagiotidis CA, Blackburn S, Low KB, Canellakis ES (1987) Biosynthesis of polyamines in ornithine decarboxylase, arginine decarboxylase, and agmatine ureohydrolase deletion mutants of Escherichia coli strain K-12. Proc Natl Acad Sci 84(13):4423–4427 Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 44(3):243–252

140

P. Chandra et al.

Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349 Parihar P, Bora M (2019) Plants growing under salinity stress can be eased through mycorrhizal association. In: Salt stress, microbes, and plant interactions: causes and solution. Springer, Singapore, pp 237–248 Parihar M, Rakshit A (2016) Arbuscular mycorrhiza: a versatile component for alleviation of salt stress. Nat Environ Pollut Technol 15(2):417 Parray JA, Jan S, Kamili AN, Qadri RA, Egamberdieva D, Ahmad P (2016) Current perspectives on plant growth-promoting rhizobacteria. J Plant Growth Regul 35(3):877–902 Paul D (2013) Osmotic stress adaptations in rhizobacteria. J Basic Microbiol 53(2):101–110 Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34(4):737–752 Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14(3):290–295 Pereira SI, Moreira H, Argyras K, Castro PM, Marques AP (2016) Promotion of sunflower growth under saline water irrigation by the inoculation of beneficial microorganisms. Appl Soil Ecol 105:36–47 Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA (2011) Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotech 50(2):98–115 Phaniendra A, Jestadi DB, Periyasamy L (2015) Free radicals: properties, sources, targets, and their implication in various diseases. Ind J Clin Biochem 30(1):11–26 Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth–promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soil 51(4):403–415 Plouznikoff K, Declerck S, Calonne-Salmon M (2016) Mitigating abiotic stresses in crop plants by arbuscular mycorrhizal fungi. In: Belowground defence strategies in plants. Springer, Cham, pp 341–400 Pollastri S, Savvides A, Pesando M, Lumini E, Volpe MG, Ozudogru EA, Fotopoulos V (2018) Impact of two arbuscular mycorrhizal fungi on Arundo donax L. response to salt stress. Planta 247(3):573–585 Popko J, Hänsch R, Mendel RR, Polle A, Teichmann T (2010) The role of abscisic acid and auxin in the response of poplar to abiotic stress. Plant Biol 12(2):242–258 Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32(1):181–200 Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26(7):673–684 Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220(4):1059–1075 Qadir M, Schubert S (2002) Degradation processes and nutrient constraints in sodic soils. Land Degrad Dev 13(4):275–294 Qadir M, Oster JD, Schubert S, Noble AD, Sahrawat KL (2007) Phytoremediation of sodic and saline–sodic soils. Adv Agron 96:197–247 Raines T, Shanks C, Cheng CY, McPherson D, Argueso CT, Kim HJ, Schaller GE (2016) The cytokinin response factors modulate root and shoot growth and promote leaf senescence in Arabidopsis. Plant J 85(1):134–147 Rajam MV, Dagar S, Waie B, Yadav JS, Kumar PA, Shoeb F, Kumria R (1998) Genetic engineering of polyamine and carbohydrate metabolism for osmotic stress tolerance in higher plants. J Biosci 23(4):473–482 Ramos AS, Correia AT, Antunes SC, Gonçalves F, Nunes B (2014) Effect of acetaminophen exposure in Oncorhynchus mykiss gills and liver: detoxification mechanisms, oxidative defence system and peroxidative damage. Environ Toxicol Pharmacol 37(3):1221–1228

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

141

Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Springer, Cham, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rani S, Sharma MK, Kumar N (2019) Impact of salinity and zinc application on growth, physiological and yield traits in wheat. Curr Sci (00113891) 116(8):1324–1330 Rapparini F, Peñuelas J (2014) Mycorrhizal fungi to alleviate drought stress on plant growth. In: Use of microbes for the alleviation of soil stresses, vol 1. Springer, New York, pp 21–42 Rare E (1990) Stress physiology: the functional significance of the accumulation of nitrogen-­ containing compounds. J Hortic Sci 65(3):231–243 Rastegari AA, Yadav AN, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam Rastegari AA, Yadav AN, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam Redillas MC, Park SH, Lee JW, Kim YS, Jeong JS, Jung H, Kim JK (2012) Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnol Rep 6(1):89–96 Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30(9):1148–1160 Reina-Bueno M, Argandoña M, Nieto JJ, Hidalgo-García A, Iglesias-Guerra F, Delgado MJ, Vargas C (2012) Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli. BMC Microbiol 12(1):207 Rejili M, Vadel AM, Guetet A, Neffatti M (2007) Effect of NaCl on the growth and the ionic balance K+/Na+ of two populations of Lotus creticus (L.) (Papilionaceae). S Afr J Bot 73(4):623–631 Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57(5):1017–1023 Rewald B, Shelef O, Ephrath JE, Rachmilevitch S (2013) Adaptive plasticity of salt-stressed root systems. In: Ecophysiology and responses of plants under salt stress. Springer, New  York, pp 169–201 Reynolds CS, Davies PS (2001) Sources and bioavailability of phosphorus fractions in freshwaters: a British perspective. Biol Rev 76(1):27–64 Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Biol 44(1):357–384 Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321(1–2):305–339 Robbins NE, Dinneny JR (2015) The divining root: moisture-driven responses of roots at the micro- and macro-scale. J Exp Bot 66(8):2145–2154 Rodrigues JV, Gomes CM (2010) Enhanced superoxide and hydrogen peroxide detection in biological assays. Free Radic Biol Med 49(1):61–66 Romero-Munar A, Del-Saz NF, Ribas-Carbó M, Flexas J, Baraza E, Florez-Sarasa I, Gulías J (2017) Arbuscular mycorrhizal symbiosis with Arundo donax decreases root respiration and increases both photosynthesis and plant biomass accumulation. Plant Cell Environ 40(7):1115–1126 Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13(6):309–317 Ruiz-Lozano JM, Azcón R (1997) Effect of calcium application on the tolerance of mycorrhizal lettuce plants to polyethylene glycol. Symbiosis 23(1):9–22 Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes. New Phytol 171(4):693–698

142

P. Chandra et al.

Ruiz-Lozano JM, Porcel R, Azcón C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63(11):4033–4044 Sakamoto A, Murata N (2001) The use of bacterial choline oxidase, a glycine-betaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiol 125(1):180–188 Sanchez DH, Cuevas JC, Chiesa M, Ruiz OA (2005) Free spermidine and spermine content in Lotus glaber under long-term salt stress. Plant Sci 168(2):541–546 Sánchez-Bel P, Sanmartín N, Pastor V, Mateu D, Cerezo M, Vidal-Albalat A, Flors V (2018) Mycorrhizal tomato plants fine tune the growth–defence balance upon N depleted root environments. Plant Cell Environ 41(2):406–420 Sands R, Fiscus EL, Reid CPP (1982) Hydraulic properties of pine and bean roots with varying degrees of suberization, vascular differentiation and mycorrhizal infection. Funct Plant Biol 9(5):559–569 Sannazzaro AI, Echeverría M, Albertó EO, Ruiz OA, Menéndez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol Biochem 45(1):39–46 Santander C, Aroca R, Ruiz-Lozano JM, Olave J, Cartes P, Borie F, Cornejo P (2017) Arbuscular mycorrhiza effects on plant performance under osmotic stress. Mycorrhiza 27(7):639–657 Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32(7):1085–1098 Savitha MM, Anitha P, Sumalatha BS, Tejavathi DH (2016) Effect of mycorrhizal association on nodule number, mass, leghaemoglobin and free proline content in Macrotyloma uniflorum (lam.) Verdc. under PEG induced water stress. Int J Curr Microbiol Appl Sci 5(4):165–174 Schachtman DP, Bloom AJ, Dvořák J (1989) Salt-tolerant Triticum × Lophopyrum derivatives limit the accumulation of sodium and chloride ions under saline-stress. Plant Cell Environ 12(1):47–55 Schmidt JE, Gaudin AC (2017) Toward an integrated root ideotype for irrigated systems. Trend Plant Sci 22(5):433–443 Sellitto VM, Golubkina NA, Pietrantonio L, Cozzolino E, Cuciniello A, Cenvinzo V, Caruso G (2019) Tomato yield, quality, mineral composition and antioxidants as affected by beneficial microorganisms under soil salinity induced by balanced nutrient solutions. Agriculture 9(5):110 Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669 Shabala SN, Lew RR (2002) Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol 129(1):290–299 Shabala L, Mackay A, Tian Y, Jacobsen SE, Zhou D, Shabala S (2012) Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiol Plant 146(1):26–38 Shahid M, Khan MS, Kumar M (2019) Kitazin-pea interaction: understanding the fungicide induced nodule alteration, cytotoxicity, oxidative damage and toxicity alleviation by Rhizobium leguminosarum. RSC Adv 9(30):16929–16947 Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. J Plant Physiol 164(9):1144–1151 Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P, Thakur S, Thakur N, Sudheer S, Yadav N, Yadav AN, Rastegari AA, Singh K (2019) Trichoderma: biodiversity, ecological significances, and industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Springer, Cham, pp 85–120. https://doi.org/10.1007/978-3-030-10480-1_3 Sharp RE, Davies WJ (1985) Root growth and water uptake by maize plants in drying soil. J Exp Bot 36(9):1441–1456

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

143

Sheng M, Zhang X, Chen X, Hamel C, Huang S, Tang M (2019) Biogeography of arbuscular mycorrhizal fungal communities in saline ecosystems of northern China. Appl Soil Ecol 143:213–221 Shinde P (2018) Effect of seed polymer coating with micronutrients on seed quality of chickpea (Cicer arietinum L.). J Pharm Phytochem 7(6):1152–1155 Shinde BP, Singh N (2017) Effect of arbuscular mycorrhizal fungi on growth parameters of sweet corn under NaCl salinity. Int J Curr Microbiol App Sci 6(2):1317–1325 Shokri S, Maadi B (2009) Effects of arbuscular mycorrhizal fungus on the mineral nutrition and yield of Trifolium alexandrinum plants under salinity stress. J Agron 8(2):79–83 Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216 Silva FC, Cruz NC, Tarelho LA, Rodrigues SM (2019) Use of biomass ash–based materials as soil fertilizers: critical review of the existing regulatory framework. J Clean Prod 214:112–124 Singh A (2015) Soil salinization and waterlogging: a threat to environment and agricultural sustainability. Ecol Indic 57:128–130 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140(3–4):339–353 Singh R, Upadhyay AK, Chandra P, Singh DP (2018) Sodium chloride incites reactive oxygen species in green algae Chlorococcum humicola and Chlorella vulgaris: implication on lipid synthesis, mineral nutrients and antioxidant system. Bioresour Technol 270:489–497 Singh A, Kumari R, Yadav AN, Mishra S, Sachan A, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–16. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Skirycz A, Inzé D (2010) More from less: plant growth under limited water. Curr Opin Biotechnol 21(2):197–203 Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115(3):433–447 Soliman AS, Shanan NT, Massoud ON, Swelim DM (2012) Improving salinity tolerance of Acacia saligna (Labill.) plant by arbuscular mycorrhizal fungi and Rhizobium inoculation. Afr J Biotechnol 11(5):1259–1266 Sotiropoulos TE (2007) Effect of NaCl and CaCl2 on growth and contents of minerals, chlorophyll, proline and sugars in the apple rootstock M4 cultured in vitro. Biol Plant 51(1):177–180 St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1995) Altered growth of Fusarium oxysporum f. sp. chrysanthemi in an in  vitro dual culture system with the vesicular arbuscular mycorrhizal fungus Glomus intraradices growing on Daucus carota transformed roots. Mycorrhiza 5(6):431–438 Stratu A, Costică N, Costică M (2016) Wooden species in the urban green areas and their role in improving the quality of the environment. Environ Sustain Dev 10(2):173–184 Sudha G, Ravishankar G (2002) Involvement and interaction of various signaling compounds on the plant metabolic events during defense response, resistance to stress factors, formation of secondary metabolites and their molecular aspects. Plant Cell Tissue Organ Cult 71:181 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh D, Abhilash P, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, research perspectives. Springer-Verlag, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7 Suo J, Zhao Q, David L, Chen S, Dai S (2017) Salinity response in chloroplasts: insights from gene characterization. Int J Mol Sci 18(5):1011

144

P. Chandra et al.

Symanczik S, Lehmann MF, Wiemken A, Boller T, Courty PE (2018) Effects of two contrasted arbuscular mycorrhizal fungal isolates on nutrient uptake by Sorghum bicolor under drought. Mycorrhiza 28(8):779–785 Syvertsen JP, Garcia-Sanchez F (2014) Multiple abiotic stresses occurring with salinity stress in citrus. Environ Exp Bot 103:128–137 Talaat NB, Shawky BT (2013) Modulation of nutrient acquisition and polyamine pool in salt-­ stressed wheat (Triticum aestivum  L.) plants inoculated with arbuscular mycorrhizal fungi. Acta Physiol Plant 35(8):2601–2610 Talaat NB, Shawky BT (2015) Plant–microbe interaction and salt stress tolerance in plants. Managing salt tolerance in plants: molecular and genomic perspectives. CRC Press/Taylor & Francis Group, Boca Raton, pp 267–289 Talaat NB, Shawky BT (2017) Microbe-mediated induced abiotic stress tolerance responses in plants. In: Plant–microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 101–133 Tarafdar JC, Marschner H (1994) Phosphatase activity in the rhizosphere and hyphosphere of VA mycorrhizal wheat supplied with inorganic and organic phosphorus. Soil Biol Biochem 26(3):387–395 Termaat A, Munns R (1986) Use of concentrated macronutrient solutions to separate osmotic from NaCl-specific effects on plant growth. Funct Plant Biol 13(4):509–522 Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527 Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecol 26(2):143–148 Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant Cell Environ 23(10):1005–1024 Tofighi C, Khavari-Nejad RA, Najafi F, Razavi K, Rejali F (2017) Responses of wheat plants to interactions of 24-epibrassinolide and Glomus mosseae in saline condition. Physiol Mol Biol Plant 23(3):557–564 Toussaint JP, St-Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck and Smith and Ri T-DNA roots of Daucus carota L. in an in vitro compartmented system. Can J Microbiol 50(4):251–260 Tramontano WA, Jouve D (1997) Trigonelline accumulation in salt-stressed legumes and the role of other osmoregulator as cell cycle control agents. Phytochemistry 44(6):1037–1040 Tuteja N (2007) Mechanisms of high salinity tolerance in plants. In: Methods in enzymology, vol 428. Academic Press, Cambridge, MA, pp 419–438 Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25(2):173–194 Uhlmann E, Görke C, Petersen A, Oberwinkler F (2006) Arbuscular mycorrhizae from arid parts of Namibia. J Arid Environ 64(2):221–237 Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313(2):369–375 Vályi K, Mardhiah U, Rillig MC, Hempel S (2016) Community assembly and coexistence in communities of arbuscular mycorrhizal fungi. ISME J 10(10):2341–2351 Van Der Heijden MG, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296–310 Van Oosten MJ, Pepe O, De Pascale S, Silletti S, Maggio A (2017) The role of biostimulants and bio effectors as alleviators of abiotic stress in crop plants. Chem Biol Technol Agric 4(1):5 Vangelisti A, Natali L, Bernardi R, Sbrana C, Turrini A, Hassani-Pak K, Giordani T (2018) Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots. Sci Rep 8(1):4

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

145

Vaseva II, Grigorova BS, Simova-Stoilova LP, Demirevska KN, Feller U (2010) Abscisic acid and late embryogenesis abundant protein profile changes in winter wheat under progressive drought stress. Plant Biol 12(5):698–707 Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecule 21(5):573 Venneman J, Audenaert K, Verwaeren J, Baert G, Boeckx P, Moango AM, Haesaert G (2017) Congolese rhizospheric soils as a rich source of new plant growth–promoting endophytic Piriformospora isolates. Front Microbiol 8:212 Venturi V, Keel C (2016) Signaling in the rhizosphere. Trend Plant Sci 21(3):187–198 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017) Beneficial plant–microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant–microbe interactions in agro-­ ecological perspectives: volume 2: microbial interactions and agro-ecological impacts. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22 Verzeaux J, Hirel B, Dubois F, Lea PJ, Tétu T (2017) Agricultural practices to improve nitrogen use efficiency through the use of arbuscular mycorrhizae: basic and agronomic aspects. Plant Sci 264:48–56 Veselaj E, Sallaku G, Balliu A (2018) Tripartite relationships in legume crops are plant-­ microorganism-­specific and strongly influenced by salinity. Agriculture 8(8):117 Viets FG Jr (1962) Micronutrient availability, chemistry and availability of micronutrients in soils. J Agric Food Chem 10(3):174–178 Vilela LAF, Barbosa MV (2019) Contribution of arbuscular mycorrhizal fungi in promoting cadmium tolerance in plants. In: Cadmium tolerance in plants. Academic Press, Cambridge, MA, pp 553–586 Volkmar KM, Hu Y, Steppuhn H (1998) Physiological responses of plants to salinity: a review. Can J Plant Sci 78(1):19–27 Walker C, Harper CJ, Brundrett MC, Krings M (2018) Looking for arbuscular mycorrhizal fungi in the fossil record: an illustrated guide. In: Transformative paleobotany. Academic Press, Cambridge, MA, pp 481–517 Wang CQ (2011) Water-stress mitigation by selenium in Trifolium repens L. J Plant Nutr Soil Sci 174(2):276–282 Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218(1):1–14 Wang Y, Qiu Q, Yang Z, Hu Z, Tam NFY, Xin G (2010) Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 331(1–2):181–191 Wang S, Zhao F, Wei X, Lu B, Duan D, Wang G (2013) Preliminary study on flg22-induced defense responses in female gametophytes of Saccharina japonica (Phaeophyta). J Appl Phycol 25(4):1215–1223 Wang J, Meng Y, Li B, Ma X, Lai Y, Si E, Wang DI (2015) Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus. Plant Cell Environ 38(4):655–669 Wang Y, Zhang Z, Zhang P, Cao Y, Hu T, Yang P (2016) Rhizobium symbiosis contribution to short-term salt stress tolerance in alfalfa (Medicago sativa L.). Plant Soil 402(1–2):247–261 Wang S, Augé RM, Toler HD (2017) Arbuscular mycorrhiza formation and its function under elevated atmospheric O3: a meta-analysis. Environ Pollut 226:104–117 Wang J, Fu Z, Ren Q, Zhu L, Lin J, Zhang J, Yue J (2019) Effects of arbuscular mycorrhizal fungi on growth, photosynthesis, and nutrient uptake of Zelkova serrata (Thunb.) makino seedlings under salt stress. Forests 10(2):186 Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4(3):162–176 Waraich EA, Ahmad R, Ashraf MY, Saifullah Ahmad M (2011) Improving agricultural water use efficiency by nutrient management in crop plants. Acta Agric Scand Sect B Soil Plant Sci 61(4):291–304

146

P. Chandra et al.

Waraich EA, Ahmad R, Halim A, Aziz T (2012) Alleviation of temperature stress by nutrient management in crop plants: a review. J Soil Sci Plant Nutr 12(2):221–244 Weber DJ (2009) Adaptive mechanisms of halophytes in desert regions. In: Ashraf M, Ozturk M, Athar H (eds) Salinity and water stress. Tasks for vegetation sciences, vol 44. Springer, Dordrecht Weinger JS, Parnell KM, Dorner S, Green R, Strobel SA (2004) Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat Struct Mol Biol 11(11):1101 Welch RM, Shuman L (1995) Micronutrient nutrition of plants. Critic Rev Plant Sci 14(1):49–82 Wendling LA, Blomberg P, Sarlin T, Priha O, Arnold M (2013) Phosphorus sorption and recovery using mineral-based materials: sorption mechanisms and potential phytoavailability. Appl Geochem 37:157–169 White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot 88(6):967–988 Wishnia A, Boussert A, Graffe M, Dessen PH, Grunberg-Manago M (1975) Kinetics of the reversible association of ribosomal subunits: stopped-flow studies of the rate law and of the effect of Mg2+. J Mol Biol 93(4):499–515 Wu L, Huang ZZ, Burau RG (1988) Selenium accumulation and selenium-salt tolerance in five grass species. Crop Sci 28(3):517–522 Wu QS, Zou YN, He XH (2010) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32(2):297–304 Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Scientia Hortic 164:77–87 Xiao X, Xu X, Yang F (2008) Adaptive responses to progressive drought stress in two Populus cathayana populations. Silva Fennica 42(5):705–719 Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26(5):2007–2023 Yadav AN (2019) Fungal white biotechnology: conclusion and future prospects. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 3: perspective for sustainable environments. Springer, Cham, pp 491–498. https://doi. org/10.1007/978-3-030-25506-0_20 Yadav AN, Saxena AK (2018) Biodiversity and biotechnological applications of halophilic microbes for sustainable agriculture. J Appl Biol Biotechnol 6:48–55 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018a) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, New York, pp 305–332 Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP, Saxena AK, Dhaliwal HS (2018b) Actinobacteria from rhizosphere: molecular diversity, distributions and potential biotechnological applications. In: Singh B, Gupta V, Passari A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, New York, pp 13–41. https://doi.org/10.1016/ B978-0-444-63994-3.00002-3 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018c) Biodiversity of the genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering, Penicillium system properties and applications. Elsevier, Amsterdam, pp  3–18. https://doi.org/10.1016/ B978-0-444-63501-3.00001-6 Yadav AN, Gulati S, Sharma D, Singh RN, Rajawat MVS, Kumar R, Dey R, Pal KK, Kaushik R, Saxena AK (2019a) Seasonal variations in culturable Archaea and their plant growth promoting attributes to predict their role in establishment of vegetation in Rann of Kutch. Biologia 74:1031–1043. https://doi.org/10.2478/s11756-019-00259-2 Yadav AN, Mishra S, Singh S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. Volume 1: diversity and enzymes perspectives. Springer, Cham

4  Soil Salinity and Its Alleviation Using Plant Growth–Promoting Fungi

147

Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi. Volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019d) Recent advancement in white biotechnology through fungi. Volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N, Kour D (2020b) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020d) Plant microbiomes for sustainable agriculture. Springer, Cham Yaish MW, Antony I, Glick BR (2015) Isolation and characterization of endophytic plant growth– promoting bacteria from date palm tree (Phoenix dactylifera  L.) and their potential role in salinity tolerance. Anton Van Leeuwenhoek 107(6):1519–1532 Yamamori T, Yasui H, Yamazumi M, Wada Y, Nakamura Y, Nakamura H, Inanami O (2012) Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by up regulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic Biol Med 53(2):260–270 Yang G, Liu N, Lu W, Wang S, Kan H, Zhang Y, Chen Y (2014a) The interaction between arbuscular mycorrhizal fungi and soil phosphorus availability influences plant community productivity and ecosystem stability. J Ecol 102(4):1072–1082 Yang SJ, Zhang ZL, Xue YX, Zhang ZF, Shi SY (2014b) Arbuscular mycorrhizal fungi increase salt tolerance of apple seedlings. Bot Stud 55(1):70 Yang H, Schroeder-Moreno M, Giri B, Hu S (2018a) Arbuscular mycorrhizal fungi and their responses to nutrient enrichment. In: Root biology. Springer, Cham, pp 429–449 Yang L, Sui X, Liu Y, Wang J, Wu Y, Zhang T, Ni H (2018b) Abundance and diversity of arbuscular mycorrhizal fungi (AMF) in Calamanrostis angustifolia wetlands of the Sanjiang Plain, China. Int J Agric Biol 20(6):1424–1432 Yasmeen T, Tariq M, Iqbal S, Arif MS, Riaz M, Shahzad SM, Li T (2019) Ameliorative capability of plant growth promoting rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) against salt stress in plant. In: Plant abiotic stress tolerance. Springer, Cham, pp 409–448 Yeo AR (1983) Salinity resistance: physiologies and prices. Physiol Plant 58(2):214–222 Yin L, Wang S, Eltayeb AE, Uddin MI, Yamamoto Y, Tsuji W, Tanaka K (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231(3):609–621 Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-Um S (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Scientia Hortic 198:107–117 York LM, Carminati A, Mooney SJ, Ritz K, Bennett MJ (2016) The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots. J Exp Bot 67(12):3629–3643 Zahir ZA, Nadeem SM, Khan MY, Binyamin R, Waqas MR (2019) Role of halotolerant microbes in plant growth promotion under salt stress conditions. In: Saline soil–based agriculture by halotolerant microorganisms. Springer, Singapore, pp 209–253 Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989 Zangaro W, Alves RA, Lescano LE, Ansanelo AP, Nogueira MA (2012) Investment in fine roots and arbuscular mycorrhizal fungi decrease during succession in three Brazilian ecosystems. Biotropica 44(2):141–150

148

P. Chandra et al.

Zarea MJ, Karimi N, Goltapeh EM, Ghalavand A (2011) Effect of cropping systems and arbuscular mycorrhizal fungi on soil microbial activity and root nodule nitrogenase. J Saudi Soc Agric Sci 10(2):109–120 Zhang HS, Qin FF, Qin P, Pan SM (2014) Evidence that arbuscular mycorrhizal and phosphate-­ solubilizing fungi alleviate NaCl stress in the halophyte Kosteletzkya virginica: nutrient uptake and ion distribution within root tissues. Mycorrhiza 24(5):383–395 Zhang M, Smith JAC, Harberd NP, Jiang C (2016a) The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 91(6):651–659 Zhang S, Gan Y, Xu B (2016b) Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front Plant Sci 7:1405 Zhang J, Chen J, Jia R, Ma Q, Zon Z, Wang Y (2018a) Suppression of plant wilt diseases by nonpathogenic Fusarium oxysporum Fo47 combined with Actinomycetes strains. Biocontrol Sci Technol 28(6):562–573 Zhang T, Hu Y, Zhang K, Tian C, Guo J (2018b) Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crop Prod 117:13–19 Zhou ML, Zhang Q, Sun ZM, Chen LH, Liu BX, Zhang KX, Wu YM (2014) Trehalose metabolism–related genes in maize. J Plant Growth Regul 33(2):256–271 Zhu X, Song F, Xu H (2010) Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20(5):325–332 Zhu XC, Song FB, Liu SQ, Liu TD, Zhou X (2012) Arbuscular mycorrhiza improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58(4):186–191

Chapter 5

Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense Shomaila Sikandar, Asfand Yar Saqib, and Imran Afzal

Contents 5.1  Introduction 5.2  Fungi as Biological Control Agent 5.3  Sesquiterpenes 5.3.1  Sources and Their Function 5.3.2  Synthesis 5.4  Polyketides 5.4.1  Source and Function 5.4.2  Synthesis 5.5  Alkaloids 5.5.1  Source and Function 5.6  Conclusion and Future Prospects References

 149  152  153  154  156  158  158  163  164  164  167  172

5.1  Introduction The relation between the variety of plants, ecosystem, ecological stability, and overall productivity is of utmost importance to nature organization. Pathogens causing disease in plants affect such a relationship by influencing plant defense, fitness, hindering plant growth, and sustainability greatly impacting plant ecosystem and population (Creissen et  al. 2016). Over 100 different diseases affect crop plants. While, only a single pathogen under given circumstances multiplies enough to become a disease causing agent. These crop plant diseases falls among the biggest hurdles limiting the production of large and adequate quantities of food (Savary et al. 2012). It is estimated that various plant diseases at different planting stages and plant pests are responsible for half of the total agricultural production loss in the world (Khan 2008).

S. Sikandar (*) · A. Y. Saqib · I. Afzal (*) Department of Biology, Lahore Garrison University, Lahore, Pakistan © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_5

149

150

S. Sikandar et al.

Plant disease can be defined as “a physiological disorder or structural abnormality that is harmful to the plant or to any of its parts or products that reduces the economic value” (Stalkman and Harrar 1957). Phytopathogenic agents are responsible for significant loss of crops resulting from plant diseases. In order to sustain the standard and diversity of feed, food and fiber all over the globe, plant diseases need to be eradicated and controlled. For this purpose, various approaches for plant disease control have been proposed. Apart from efficient horticulture and agronomical applications, often producers are heavily reliant upon chemically synthesized pesticides and fertilizers, while, the environmental pollution and fluctuations resulting from these synthetic pesticides, fertilizers, and agrochemicals have caused significant changes over their use in agriculture, plant disease control and prevention (Kaur et al. 2020; Kour et al. 2020; Singh and Yadav 2020). Biological control of fungal plant pathogens is of great interest and in recent times, more emphasis is provided as potential alternatives to the chemical use (Rastegari et al. 2020b; Yadav et al. 2020b, e; Vinale et al. 2014). Synthetically produced pesticides are expensive, pollutants of environment and hazardous to humans and animals as well. Moreover, repeated exposure of such chemicals enhances the stride of resistant pathogenic strains. Pest management mediated by microbes is among the most efficient and inexpensive biological control applications in agriculture (Rana et al. 2019; Verma et al. 2017; Yadav 2019). Outcome of such an approach is largely based upon the choice of microbial strain. The benefits for the plant associated involve: (1) plant growth promotion; (2) establishment of microbial community within the rhizosphere involving antagonistic activity; (3) pathogen elimination; (4) plant health benefits; (5) greater uptake and availability of nutrients, and (6) improved biotic and abiotic stress resistance to host (Harman et  al. 2004; Vinale et  al. 2008; Yadav et  al. 2017). Advantageous microbes have been known to have various mode of action such as: pathogen inhibition or parasitism using antibiotics sometimes in conjugation with cell wall decomposing extracellular enzymes; contention for nutrients (i.e., carbon, iron or nitrogen) in sites of colonization; onset of plant developmental and resistance phenomenon (Kour et al. 2020; Howell 2003; Whipps 2001). Microbial species, particularly of fungi, secrete diverse range of secondary metabolites involving a variety of industrially and economically important compounds (Herbert 1989; Yadav et al. 2019b). Chemically, secondary metabolites are naturally different compounds characterized by low molecular weight usually, less than 3 kDa. Secondary metabolites are assigned to each specific genera, strain or species being mainly synthesized by plants and microorganisms (Rastegari et  al. 2019b; Yadav et  al. 2019a). Their biosynthesis involves primary metabolites in specific pathways such as mevalonate or polyketide pathways driven through amino acids or Acetyl Coenzyme A along with a few clustered genes. Some global regulators appear to be the gene expression inducers of such genes (Herbert 1989; Rastegari et  al. 2019a). Secondary metabolites exhibit several biological functions in relevance to survival of organisms (Yadav et al. 2020a). For instance, metal transportation, symbiotic association, and contention with both micro and macroorganisms. Secondary metabolite synthesis in fungi is often held parallel to distinct phases of

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

151

structural differentiation along with active growth phase (Keller et al. 2005). Their range of distribution varies from among a few related species to individual strains emphasizing diverse activities of each metabolite in contrast to a universal activity (Keller et al. 2005). Secondary metabolites of fungal origin display various biological features while offering essential regulatory interactions among organisms (Hanson 2003; Yadav et al. 2019b). For example, mycotoxins (toxic secondary metabolite produced by fungi colonizing crops causing disease and death in animals and humans), phytotoxins (secondary metabolite that invades the plant defense), antibiotics (compounds possessing inhibitory and antimicrobial activities), and pigments (colored compounds involving antioxidant features) (Chiang et al. 2009; Vinale et al. 2014; Yadav et al. 2019c) (Fig. 5.1). However, interestingly, a few secondary metabolites of fungal origin possess the ability to alter plant growth and metabolism while others act on specialized fungal phenomenon including hyphal elongation, growth, and sporulation (Keller et al. 2005). Soil borne fungal species thrive in extremely competent environments. Virtually every fungal community is known to have antagonistic relationship among natural competing fungal species (Ghisalberti 2002). Fungi known to be invasive function indirectly or directly towards fungal phytopathogens. Indirectly by facing contention for physical space and nutrient availability, altering

Fig. 5.1  Schematic diagram of biologically active secondary metabolites and their major classes involved in the plant defense mechanisms

152

S. Sikandar et al.

environmental circumstances or by enhancing plant growth. Fungi are also known by its defense and antibiosis mechanisms and by the processes like mycoparasitism against phytopathogens (Yadav et al. 2019d, 2020d). This influence is attained by production of a great variety of secondary metabolites, evolving a wide array of natural and xenobiotics, developing altered degradative enzymes like chitinase (Gloer 1997; Kumar et al. 2019a). Biological activities having integral impact on crop regulation and production are greatly influenced by fungal metabolites.

5.2  Fungi as Biological Control Agent Biocontrol agents are the microorganisms that suppress the effects of pests or pathogens by a variety of mechanisms or induce stimulatory effects on the plants growth. Currently, various microbial biocontrol agents are present. Bacterial biocontrol agents include Pseudomonas spp., Bacillus spp., and Agrobacterium sp., while, biocontrol agents of fungal origin are Aspergillus spp., Candida sp., Ampelomyces sp., Coniothyrium sp., Trichoderma spp., and Gliocladium sp. (Atehnkeng et al. 2008; Gilardi et al. 2008; Koumoutsi et al. 2004; Mavrodi et al. 2002; Papavizas 1985). Among these, Trichoderma sp. stands out as the most versatile and diverse fungal biocontrol agent mainly towards pathogenic fungi. Various studies claimed Trichoderma spp. as an effective biocontrol weapon against pant diseases (Sharma et al. 2019; Yadav et al. 2020c). Commercially available Trichoderma products as biopesticides are in use presently that alter the soil properties enhancing plant growth promotion (Chet 1987; Harman et al. 2004; Papavizas 1985; Vinale et al. 2008). In 1934, Trichoderma lignorum was utilized as biocontrol agent against the fungal plant pathogen Rhizoctonia solani by Weindling (1934). Similarly, Trichoderma lignorum displayed mycoparasitic features towards Rhizopus, Phytophthora, Sclerotium rolfsii, and Pythium (Wells 1988). Many diverse secondary metabolites are also reported from Trichoderma spp., which has therefore drawn great interest in fungus being designated as a biocontrol model (Chet 1993; Chet et al. 1981; Rastegari et al. 2020a) (Table 5.1). Presently, mankind faces huge challenges in the form of environmental degradation, deterioration of land, water and loss of biological diversity (Kour et al. 2019; Kumar et al. 2019b). Secondary metabolites, therefore, hold great potential in rectifying these challenges of nature. Fungi secrete a great number of diverse bioactive secondary metabolites with broad range of functions (Fig. 5.2). Major categories of natural products from fungal origin include antioxidants, antidiabetics, antibiotics, insecticides, and immunosuppressant of various chemical characters (Rana et  al. 2020; Singh et al. 2020). The present chapter focuses on the three major and most abundant classes of secondary metabolites synthesized by fungi along with their functions and complex interactions in response with phytopathogens.

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

153

Table 5.1  Plant crop diseases controlled by fungal biocontrol agents Crop disease Blight of Sesamum

Pathogen Phytophthora sp.

Root rot of Sesamum

M. phaseolina

Root rot chilli Dieback of chilli

S. rolfsii Colletotrichum capsici

Wilt of eggplant

F. solani

Damping-off of eggplant

P. aphanidermatum

Wilt of tomato Root knot of tomato

F. oxysporum Meloidogyne incognita M. javanica Pythium spp. Alternaria helianthi Fusarium udum

Wilt of okra Leaf blight of sunflower Wilt of pigeon pea

Wilt of chickpea

F. oxysporum f.sp. ciceri

Dry root rot of soybean

M. phaseolina

Stem rot of groundnut Damping-off of mustard

Sclerotium rolfsii Pythium aphanidermatum

Root rot of mung bean

M. phaseolina

Biocontrol agents T. harzianum T. viride Trichoderma sp. Gliocladium sp. T. harzianum T. viride T. harzianum T. viride T. koningii T. viride T. koningii T. harzianum T. harzianum A. niger T. virens T. viride T. hamatum T. harzianum T. koningii T. viride T. harzianum T. virens T. viride T. harzianum T. harzianum T. harzianum T. viride T. harzianum T. viride

Source: Gawai (2018)

5.3  Sesquiterpenes Sesquiterpenes are the most abundant sub-class of terpenoids group of fungal secondary metabolites that involves an arrangement of three isoprene units with a molecular formula of C15H24. Their classification is based upon the presence or absence of carbon rings acyclic in nature or monocyclic, bicyclic, tri-cyclic and onwards. Sesquiterpenes are known to be anti-inflammatory with characteristic bactericidal properties involving strong odors (Waterman 1993).

154

S. Sikandar et al.

Fig. 5.2  Broad classification of fungal bioactive secondary metabolites

5.3.1  Sources and Their Function Daucane, a class of sesquiterpenes which is also referred as carotanes are rarely known fungal metabolites. A novel daucane (carotene) metabolite (1) (Fig.  5.3) from one of the strains of T. virens showed antifungal properties against a number of dermatophytes and yeast with significant effect recorded on C. albicans (Watanabe et al. 1990). T. virens was also reported as a source of four novel metabolites with carotene backbone, trichocaranes A, B, C, and D (2–5) (Fig. 5.3). The structure of each trichocarane was confirmed by mass spectroscopy and NMR emphasizing each compound remarkably inhibited the growth rate of etiolated wheat coleoptiles (Macias et al. 2000). Numerous sesquiterpenes from endophytic fungi have also been identified. Two caryophyllene (pestalotiopsin A and B) along with a novel 2α-hydroxydimeninol (6–8) (Fig. 5.4) sesquiterpenes from Pestalotiopsis spp. that forms an endophytic relationship with Taxus brevifolia evaluated by spectral and X-ray diffraction analysis (Pulici et  al. 1996a, b). Sesquiterpenes are also known to exhibit insecticidal properties. For instance, toxicity against the larvae of spruce budworm (Choristoneura fumiferana) of Phyllosticta sp., that involves an endophytic association with Abies balsamea from the family Pinaceae by the action of heptelidic and hydroheptelidic acid (9–10) (Fig. 5.5) (Calhoun et al. 1992). Epichloë typhina, a species of fungus of cool season grass that is endophytic in nature on plant Phleum pretense. It has been reported to elicit sesquiterpenes chokols A–G (Fig. 5.6) involving antifungal activity against the pathogen of leaf spot disease Cladosporium phlei (Koshino et al. 1989). Trichoderma sp. PR-35 exhibiting endophytic association with Paeonia delavayi provided three compounds cyclonerodiol, cyclonerodiol oxide, and sorbicillin (11–13) with two new

155

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

Fig. 5.3  Chemical structure of: 1 carotane-type metabolite; 2, 3, 4, 5 trichocaranes A, B, C, and D 13 AcO 2 H3C 1 O 4 H3C 14 CH3 RO 5 6 OCH3

RO 6

AcO H3C H3C OH HOH2C

HO CH3 OCH3

7

HO

CH3

O

H H3C CH3 8

Fig. 5.4  Chemical structure of: 6 pestalotiopsin A; 7 pestalotiopsin B; 8 2α-hydroxydimeninol

sesquiterpene: trichoderic acid and 2β-hydroxytrichoacorenol (14–15), a bisabolane type and acorane type sesquiterpene (Fig.  5.7), respectively. Most of these compounds displayed varying levels of both antibacterial and antifungal characteristics against different types of pathogens (Wu et al. 2011). The medicinal plant Costus speciosus is host to fungal endophyte Bipolaris sorokiniana identified to yield helminthosporal acid (16) and helminthosporol (17), two quite rare sesquiterpenes (Fig.  5.8). Compound 16 exhibited antifungal activity (Qader et  al. 2017). Helminthosporol (17) has also been reported from Drechslera dematioidea obtained from Liagora viscida, red algae of marine origin (Osterhage et  al. 2002). Helminthosporol (17) is also experimented to show elongation effect upon the shoots of rice seedlings (Tamura et al. 1965).

156

S. Sikandar et al. O

4

6

8 9

O

7 H

HO

O H

O

O

5

10

H

H 13 15

OH

3

11 2 1

COOH

COOR

H

14

9

10 R = H

Fig. 5.5  Chemical structure of: 9 heptelidic and 10 hydroheptelidic acid

OH

OH

R2

RO

R1

A

R=H

F R=Ac C

R1=OH, R2=H

D

R1=H, R2=OH

14

OH

7 6

15 HO

OR

B R=H

12

10 OH

OH 2

1

3

13

E

OH HO

G Fig. 5.6  Chemical structure of: chokols A–G

5.3.2  Synthesis Biosynthesis of metabolites belonging to the class of terpenoids are synthesized via the CoA derived C-5-isopentenyl-diphosphate intermediate products isopentenyl and dimethylallyl-diphosphate. The isoprene units are processed through prenyl

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

157

H

HO

OH

H OH

O OH

HO OH

11

13

12 13

14 5 H 7 15

3

O

6 1

H

12

11 COOH

O

H

9 13

HO

11

12

10

1

9 15

3

5 7

14

14

OH

15

Fig. 5.7  Chemical structure of: 11 cyclonerodiol; 12 cyclonerodiol oxide; 13 sorbicillin; 14 trichoderic acid; 15 2β-hydroxytrichoacorenol

Fig. 5.8 Chemical structure of: 16 helminthosporal acid and helminthosporol 17

12

14

OHC 11

3

10

H

1R

2

9 4R

7

6

15

R

5S

8S 13

H

16 R=COOH 17 R=CH2OH

synthases with post synthetic modifications by the action of numerous enzymes, producing different classes of terpenoids from lesser isoprene units (SchmidtDannert 2015). The genome of C. rosea comprises eight of the terpene synthase genes (Karlsson et al. 2015). While E. weberi involves six terpene synthase genes and three of these genes are known to exist at the biosynthetic clusters of secondary metabolite (de Man et al. 2016). In comparison to T. reesei and T. atroviride, the genome of T. virens contains enriched region of terpene cyclase genes (Bansal and Mukherjee 2016). The terpene class of cyclase gene vir4 was determined to be involved in greater than 20 sesquiterpene biosynthesis volatile in nature (Crutcher et al. 2013).

158

S. Sikandar et al.

5.4  Polyketides Polyketides are generated from coenzyme A esters such as acetyl CoA or malonyl CoA by polyketide synthases decarboxylation condensation and post-synthetic modification (Pfeifer et al. 2001). Polyketide synthases of fungal origin are complex interchangeable enzymes with characteristic inclusion of ketoacyl CoA synthase, involved in the generation of long chain fatty acids belonging to the enzyme family, acyltransferase (Keller et al. 2005). Polyketides are diverse in nature while being the core class of secondary metabolites produced from the kingdom of fungi including antibiotics, toxins, antiparasitics to antifungals, insecticides (Karlsson et al. 2017).

5.4.1  Source and Function 6-pentyl-a-pyrone (18) (Fig. 5.9) is among the characteristic metabolite of the genus Trichoderma first discovered in 1972 (Collins and Halim 1972) from T. viride growth culture broth. In the same way, T. koningii and T. harzianum have also been reported as the metabolite producer (Claydon et al. 1987; Simon et al. 1988). Plate tests evaluation effects against Fusarium oxysporum f. sp. Lycopersici and Rhizoctonia solani have also been investigated. An addition of this compound in agar medium resulted in growth reduction of F. oxysporum and R. solani within 48 h by 69.6% and 31.7%, respectively, to an amount of 0.3  mg/ml. Complete spore germination was halted at 0.45 mg/ml when spore germination tests were performed against the spores of Fusarium. Similarly, Poole et al. identified the control against Botrytis cinerea causing rots of stored kiwi fruits (Poole et al. 1998). Massoilactone and delta-decanolactone (19–20) (Fig.  5.9) have been patented (Hill et al. 1995) due to their broad range of controlling plant disorders caused by Phytophthora and Botrytis species as they involve the ability to halt the growth at 62–250 μg/ml of S. aureus and at 31–125 μg/ml of A. niger and C. albicans. This is

Fig. 5.9  Chemical structure of: 18 6-pentyl-a-pyrone; 19 massoilactone; 20 delta-decanolactone; 21 viridepyronone; 22 6-(1′-pentenyl)-2H-pyran-2-one; 23 cytosporone S

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

159

achieved by adopting 96 well equipped microbioassay and agar dilution method (Kishimoto et al. 2005). T. viridae has been identified as a source of viridepyronone (21) (Fig. 5.9) showing in vitro inhibitory effects of over 90% against Sclerotium rolfsii (Evidente et al. 2003). Studies conducted on 6-(1′-pentenyl)-2H-pyran-2-one (22) (Fig. 5.9) displayed inhibitory effects to Cryptococcus neoformans, Candida albicans, Penicillium spp., and Aspergillus fumigatus isolated from two strains of T. harzianum (Claydon et al. 1987; Parker et al. 1997). In vitro antibiotic response from cytosporone S (pyrone) (23) (Fig.  5.9) has been reported against numerous fungi and bacteria as well from a Trichoderma sp. strain as the source (Ishii et al. 2013). Similarly, novel polyketide terpene metabolites (24–26) (Fig.  5.10) from endolichenic fungus belonging to Pestalotiopsis sp. showed potential as antifungal agents capable of being employed in crop and agricultural protection practices. Compounds 24 and 25 inhibited the plant pathogen fungus F. oxysporum, while compounds 25 and 26 inhibited the growth of F. gramineum at an MIC of 8 ug/ml (Yuan et al. 2017). Hormonema dematioides endophytic to balsam fir, produces a quinone compound rugulosin (27) (Fig.  5.11) exhibiting insecticidal activity (Calhoun et  al. 1992). A quinone 1′,5′-trihydroxy-3′,4′dihydro-1′H-[2,4′]binaphthalenyl-1,4,2′trione (28) (Fig. 5.11) elicited from an endophytic fungi of Larix laricina needle displays toxicity towards the larvae of spruce budworm (Findlay et  al. 1997). Similarly, Alternaria spp. and Phoma sp. in conjugation with plants secrete hydroxyl quinone altersolanol A (29) (Fig.  5.11) with antibacterial characteristics (Yang et al. 1994). Anthraquinones pachybasin, chrysophanol, and emodin (30–32) (Fig. 5.11) have been reported from wild T. viridae strain sampled from soil (Slater et al. 1967). The mixture of these compounds along with their O-acetyl and O-methyl derivatives towards two F. annosus strains resulted in a linear reduction of fungal growth in particular when O-acetyl derivatives were employed (Donnelly and Sheridan 1986).

Fig. 5.10  Chemical structures of novel polyketide terepene metabolites 24, 25, and 26

160

S. Sikandar et al.

Fig. 5.11  Chemical structure of: 27 rugulosin; anthraquinones 30 pachybasin; 31 chrysophanol; 32 emodin

Fig. 5.12  Chemical structure of: 33 secalonic acid B; 34, 35, 36, 37 blennolides A, B, D, and E

Emodin (32) is known to have the activities of tyrosine kinase (Jayasuriya et  al. 1992; Kumar et al. 1998) and monoamine oxidase (Fujimoto et al. 1998). Blennoria sp. exhibiting endophytic relation to Carpobrotus edulis has been reported as a source of secalonic acid B (33) (Fig. 5.12), blennolides A, B, D, and E

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

161

(34–37) (Fig. 5.12). Compounds 33–35 show antialgal, antibacterial, and antifungal properties, while compound 33 was antagonistic against Bacillus megaterium and M. violaceum. Compounds 36 and 37 showed appreciable antialgal and antifungal properties (Zhang et al. 2008). Compounds 38 and 39 (Fig. 5.13) obtained from fungal culture of Coniothyrium sp., an endophyte of Salsola oppostifolia is known to have notable effects against Botrytis cinerea and M. violaceum (Sun et al. 2013). Javanicin (40), a naphthoquinone counterpart (Fig.  5.13), was identified from Fusarium sp. (Kornsakulkarn et al. 2011) and as well as Chloridium sp. It is known to inhibit the fungal growth of Verticillium dahliae, Fusarium oxysporum, Rhizoctonia solani, and Cercospora arachidicola (Kharwar et al. 2009). Similarly, Delitschia corticola secretes a series of naphthoquinone 6-ethyl-7-hydroxyl-2-methoxyjuglone (41), 6-ethyl-2,7-dimethoxyjuglone (42), and 6-(1-hydroxyethyl)-2,7-dimethoxyjuglone (43) (Fig. 5.13) displaying antifungal activity against Fusarium sp., Alternaria sp., and Sclerotium sp. (Sun et al. 2011). The depsidones called cordycepsidone A (44) (Fig. 5.13) was reported to exhibit strong antifungal characteristics against fungus known to be plant pathogens viz., Gibberella fujikuroi with intermediate effects towards Pythium ultimum with the fungus Cordyceps dipterigena as a source (Varughese et al. 2012). Pyrenocine analogs called phomopsinones A and D (45–46) (Fig. 5.14) are reported from Phomopsis sp. that resides as an endophytic fungus on Santolina chamaecyparissus (Hussain et al. 2012b). Phomopsinone A (45) showed strong antifungal properties against plant and crop pathogens Pyricularia oryzae, Septoria tritici, and

Fig. 5.13  Chemical structure of: 38 1,6-dihydroxy-3-methyl-9,10-anthraquinone (phomarin); 39 coniothyrinone A; 40 javanicin; 41 6-ethyl-7-hydroxyl-2-methoxyjuglone; 42 6-ethyl-2,7-dimethoxyjuglone; 43 6-(1-hydroxyethyl)-2,7-dimethoxyjuglone; 44 cordycepsidones A

162

S. Sikandar et al.

Fig. 5.14  Chemical structure of: 45, 46 phomopsinones A and D; pyrenocines 47, 48, 49  J, K, and M Fig. 5.15 Chemical structure of: 50, 51 phomochromone A and B

B. cinerea. Phomopsinone D (46) is reported to only inhibit the growth of B. cinerea and S. tritici. In the same way, four pyrocine counterparts were isolated from the fungus belonging to Phomopsis sp., endophyte of Cistus salvifolius (Hussain et al. 2012a). Out of these four, pyrenocines K (48) and M (49) (Fig.  5.14) displayed antifungal effects against M. violaceum and S. tritici, whereas, pyrenocine J (47) (Fig. 5.14) was antifungal only against S. tritici. Phomochromone A (50) and B (51) (Fig.  5.15), two novel chromones were reported from Phomopsis sp. displaying appreciable antifungal, antibacterial, and antialgal properties when tested against S. tritici, B. cinerea, B. megaterium, M. violaceum and also against E. coli and C. fusca (Ahmed et al. 2011). Mellein (52) (Fig.  5.14), an isocoumarin analog isolated from Pezicula sp., inhibits B. cinerea and Fulvia fulva with EC50 values of less than 50 μg/ml (Wang et  al. 2014). Palmarumycin C8 (53) (Fig.  5.14) obtained from the fungal species Berkleasmium inhibits and antifungal in spore germination with 9.1  μg/ml IC50 value against Magnaporthe oryzae (Shan et al. 2014). Seimatoporic acid A and B (54–55) (Fig. 5.16) obtained from fungus Seimatosporium sp., endophytic in association exhibits strong antifungal effects towards S. tritici, P. oryzae, and B. cinerea (Hussain et al. 2012c).

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

163

Fig. 5.16  Chemical structure of: 52 mellein; 53 palmarumycin C8; 54, 55 seimatoporic acid A and B

5.4.2  Synthesis In comparison to T. reesei, the genomes of T. virens and T. atroviridae contain 60% polyketide synthase genes (Kubicek et  al. 2011). T. ophioglossoides involves 15 polyketide synthases in its genome (Quandt et al. 2016), while C. rosea contains 31 polyketide synthase genes (Karlsson et  al. 2015). C. rosea imparts antibacterial activity due to the action of TMC-151 type polyketides (Zhai et al. 2016). On the other hand, T. ophioglossoides is responsible for eliciting two antibacterial and antifungal compounds: the NRPS/PKS enzyme hybrid driven ophiosetin and polyketide ophiocordin (Kneifel et al. 1977; Putri et al. 2010; Quandt et al. 2016). The pks4 deletion in Fusarium spp. which codes for aurofusarin and bikaverin orthologue for polyketides synthases, resulted in considerable alterations of metabolism, morphology, and physiology in T. reesei. Inhibition of teleomorph structures and conidia pigmentation were evaluated along with reduced stability of cell wall in conidia in delta-pks4 mutants. Deletion of the of the mutant Pks4 caused a decrease in hostile characteristics in confrontation estimation assays of T. reesei, decreased the antifungal properties induced by polar soluble and resilient metabolites along with altered gene expression of other polyketide synthases (Atanasova et al. 2013).

164

S. Sikandar et al.

5.5  Alkaloids Alkaloids consists of a diverse molecular class pertaining nitrogen and amino acid containing molecular entities representing wide functions in nature, while occurring in animals, plants, and microorganisms (Pelletier 1983).

5.5.1  Source and Function Pyrrolizidines are organic compounds heterocyclic in nature biosynthesized by plants as a defense mechanism against herbivores (Macel 2011). 1-aminopyrrolizidine, also known as lolines (56) (Fig. 5.17), have been reportedly secreted by endophytic fungi residing on grasses. Neither endophytic fungal cultures nor the infected grasses separately produced lolines in vitro (Schardl and Phillips 1997). Emphasizing, secretion only took place during plant-endophyte interaction. Lolines are diverse insecticides playing the role of metabolic toxicants and feeding repellents. The allelopathic phenomenon when grasses reside as host is credited to certain endophyte secreted loline counterparts (Bush et  al. 1997). For instance, F. pratensis when infected by N. uncinatum and N. coenophialum infecting Festuca arundinacea distinctively produces lolines (56). These are also

Fig. 5.17  Chemical structure of: 56 lolines; 57 peramine; 58 1-N-methylalbonoursin; indole alkaloids 59 elymoclavine; 60 agroclavine; 61 chanoclavine

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

165

relatively lesser toxicants when made a comparison with indole diterpene alkaloids and ergot alkaloids. Secondary metabolites classified under amine and amides have been identified from Neotyphodium, also referred as Epichloë and the grass endophytes from the genus Acremonium (Glenn et al. 1996; Schardl and Phillips 1997). Peramine (57), a pyrrolopyrazine (Fig. 5.15) classified alkaloid is reportedly secreted by E. typhina, Neotyphodium coenophialum, N. lolli, and Epichloë festucae within the culture, in leaves of taller fescue, ryegrass and as well as in plants having association with the stem while being a toxicant against insects such as Argentine stem weevil having no hazardous influence on mammals (Dew et al. 1990; Rowan and Latch 1994). Ras farnesyl transferase is known to be inhibited due to the production of 1-N-methylalbonoursin (58) (Fig. 5.17) from Phoma sp. (Ishii et al. 2000). Secretion of Indole alkaloids like elymoclavine, agroclavine, and chanoclavine (59–61) (Fig. 5.17) providing toxicity against some insects and mammals are reported from Neotyphodium (Powell and Petroski 1992; Schardl and Phillips 1997). Neotyphodium endophytes provides plant hosts with numerous advantages like enhanced growth rate, increased reproduction, and herbivores resistance using endophyte alkaloids (Clay and Schardl 2002; Faeth 2009; Müller and Krauss 2005). Cavendishia pubescens tree bark isolated Phomopsis sp. and indole byproducts like tremorgenic aspalitrems A (62) and C (63) (Fig.  5.18) of Aspergillus flavus are produced by the endophyte (Bills et al. 1992). Similarly, 3-IAA (64) (Fig. 5.18) of auxin class is produced by Artemisia annua residing Epicoccum purpurascens, Aureobasidium pullulans, Colletotrichum sp., and Acremonium coenophialum endophytes. Tobacco isolated strains of Hypoxylon serpens elicites IAA, cytokinins with 3-indoleacetonitrile (65) (Fig.  5.18) (Petrini 1991).

Fig. 5.18  Chemical structure of: 62, 63 aspalitrems A and C; 64 indole-3-acetic acid; 65 3-indoleacetonitrile; 66 6-isoprenylindole-3-carboxylic acid

166

S. Sikandar et al.

6-isoprenylindole-3-carboxylic acid (66), an indole byproduct (Fig. 5.18), has been identified from Colletotrichum sp. endophyte to Artemisia. annua. This derivative is hostile towards pathogenic bacteria and as well as phytopathogenic fungi such as Rhizoctonia cerealis, Gaeumannomyces graminis var. tritici, and Phytophthora capsici (Lu et al. 2000). A 4-year long field experiment examined alkaloids associated infection on Achnatherum robustum, the sleepygrass. Results emphasized the potential of alkaloidal infection in protection from extreme winter circumstances and underground herbivore antagonism (Faeth et al. 2010). Pyridine ring containing metabolites of fungal origin exist with 2,3-dimethoxy4-pyridinol structure (Fig.  5.19). For example, harzianopyridone (67) (Fig.  5.19) obtained from T. harzianum whose racemic structure display huge antifungal potential towards Pythium ultimum, Gaeumannomyces graminis var. tritici, Botrytis cinerea, and Rhizoctonia solani (Dickinson et al. 1989; Vinale et al. 2006). On the other hand, remarkable phytotoxic effects were observed in etiolated wheat coleoptile bioassay with marginal antibacterial and antifungal characteristics from the laevorotatory form Cutler and Jacyno (1991). This form of compound 67 was also shown to elicit necrosis among corn, tobacco, and bean in accordance to the concentration. Thus, signifying the potential of harzianopyridone (67) enantiomers to exhibit altering characteristics (Sivasithamparam and Ghisalberti 1998). Penta-substituted ring structure of pyridine is reportedly involved in WF-16775 A2 (68) (Fig.  5.19) obtained by Chaetasbolisia erysiophoides (Otsuka et  al. 1992), piericidin A (69) (Fig.  5.19) isolated from Streptomyces mobaraensis and S. pactum (Jansen and Höfle 1983; Takahashi et  al. 1965) and atpenin compounds (70–72) (Fig.  5.19) secreted from Penicillium sp. (Kumagai et  al. 1990; Omura et  al. 1988; Oshino et al. 1990).

Fig. 5.19  Chemical structure of: 67 harzianopyridone; 68 WF-16775 A2; 69 piericidin A; 70–72 atpenin compounds

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

167

Oxazole derivatives and pirrolidindione ring structures of fungal origin have been reported. ATF-451 strain of Trichoderma was reported to produce melanoxadin (73) and melanoxazal (74), oxazole byproducts (Fig. 5.20) from the post fermentation cultural broth. Significant inhibition potential has been reported towards mushroom tyrosinase from melanoxazal (74) while the silkworm Bombyx mori had inhibited melanin production within the hemolymph larval fluid from both compounds (73–74) (Hashimoto et al. 1995; Takahashi et al. 1965). Harzianic acid (75) (Fig. 5.20) consisting of a pirrolidindione ring structure is identified from a strain of T. harzianum subjected to fermentation (Sawa et al. 1994). Harzianic acid have also been found from F-1531 fungal strain along with dimethyl harzianic (76) and homoharzianic (77) acids (Fig. 5.20) (Kawada et al. 2004). Compounds (75–77) showed similar function of inhibiting PP2A (protein phosphatase type 2A) (Sivasithamparam and Ghisalberti 1998). Fungal bioactive secondary metabolites and their role in plant defense along with their activities have been enlisted in Table 5.2.

5.6  Conclusion and Future Prospects Secondary metabolites are the microbial products play a major role in the controlling of pest and phytopathogens harmful for agricultural crops. Different secondary metabolites produced by beneficial fungi have been commercially used for the plant defense mechanisms. The fungal secondary metabolites involved in the interactions with phytopathogenic agents used various mechanisms due to their complex nature of chemical composition and their synthesis based on their source of isolation. The quality of the synthesized secondary metabolites depends on the species and the strains, their growth conditions, the occurrence of the other organisms, and the absence and presence of the pathogenic agents. Therefore, the applications of fungal secondary metabolites to induce resistance against phytopathogens may be an interesting alternative to the chemical pesticides.

Fig. 5.20  Chemical structure of: 73 melanoxadin; 74 melanoxazal; 75 harzianic acid; 76 demethylharzianic; 77 homoharzianic acid

168

S. Sikandar et al.

Table 5.2  Secondary metabolites; sesquiterpenes, polyketides and alkaloids from fungal species Source T. virens

Secondary metabolites Carotane-type metabolite

Activity Antifungal

Class References Sesquiterpenes Watanabe et al. (1990) Sesquiterpenes Macias et al. (2000)

Trichocaranes A, B, C and Inhibition of D etiolated wheat coleoptiles Sesquiterpenes Calhoun et al. Heptelidic and Toxic to Phyllosticta sp. (1992) hydroheptelidic acid spruce (endophyte of budworm Abies balsamea) larvae Antifungal to Sesquiterpenes Koshino et al. Epichloë typhina Chokols A–G (1989) pathogen of (endophyte of leaf spot Phleum pretense) disease Antibacterial Sesquiterpenes Wu et al. Cyclonerodiol, Trichoderma sp. and antifungal (2011) PR-35 (endophyte cyclonerodiol oxide and sorbicillin of Paeonia delavayi) Trichoderma sp. 2β-hydroxytrichoacorenol Antibacterial Sesquiterpenes Wu et al. PR-35 and trichoderic acid and antifungal (2011) Helminthosporal acid Antifungal Sesquiterpenes Qader et al. Bipolaris (2017) sorokiniana (endophyte of Costus speciosus) Sesquiterpenes Osterhage Helminthosporol Shoot Bipolaris et al. (2002), elongation of sorokiniana, Tamura et al. rice seedlings Drechslera (1965) dematioidea Sesquiterpenes Vinale et al. T. harzianum, T. Cyclonerodiol Inhibits (2014) koningii growth of etiolated wheat coleoptiles Trichodermin Antifungal Sesquiterpenes Shentu et al. T. harzianum, T. Nematicidal (2014), Shi brevicompactum, et al. (2009), Trichoderma Yang et al. sp.YMF1.02647 (2010) Collins and 6-pentyl-a-pyrone Antifungal to Polyketides T. viride, T. Halim (1972) F. oxysporum koningii, T. and R. solani harzianum Poole et al. 6-pentyl-a-pyrone Antifungal to Polyketides T. viride, T. (1998) Botrytis koningii, T. cinerea harzianum Trichoderma spp. Massoilactone and Antifungal Polyketides Kishimoto delta-decanolactone et al. (2005) T. virens

(continued)

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

169

Table 5.2 (continued) Source T. viridae

T. harzianum

Secondary metabolites Viridepyronone

Activity Antifungal to Sclerotium rolfsii 6-(1′-pentenyl)-2H-pyran- Antifungal 2-one

Trichoderma sp.

Cytosporone S

T. viride, T. atroviride, T. koningii, T. harzianum

6-pentyl-2H-pyran-2-one

Pestalotiopsis sp.

Polyketide terpene metabolites

Hormonema dematioides endophyte of balsam fir Endophytic fungus of Larix laricina needle

Rugulosin

Antibacterial and antifungal Antifungal, anti-nematode and enhances growth in tomato and Arabidopsis thaliana Antifungal to F. oxysporum and F. gramineum Insecticidal

1′,5′-trihydroxy3′,4′dihydro-1′H-[2,4′] binaphthalenyl-1,4,2′trione Altersolanol A

Toxic to spruce budworm larvae Antibacterial

Alternaria spp., Phoma sp. T. viridae

Blennoria sp. endophyte of Carpobrotus edulis

Class Polyketides

References Evidente et al. (2003)

Polyketides

Claydon et al. (1987), Parker et al. (1997) Ishii et al. (2013) GarnicaVergara et al. (2016)

Polyketides Polyketides

Polyketides

Yuan et al. (2017)

Polyketides

Calhoun et al. (1992)

Polyketides

Findlay et al. (1997)

Polyketides

Yang et al. (1994) Donnelly and Sheridan (1986) Zhang et al. (2008)

Polyketides Pachybasin, chrysophanol Growth and emodin reduction of F. annosus Secalonic acid B Antimicrobial Polyketides to Bacillus megaterium and M. violaceum Blennolides A, B, D and E Antimicrobial Polyketides

Blennoria sp. endophyte of Carpobrotus edulis Coniothyrium sp., Phomarin and coniothyrinone A endophyte of Salsola oppostifolia

Antifungal to Botrytis cinerea and M. violaceum

Polyketides

Zhang et al. (2008)

Sun et al. (2013)

(continued)

170

S. Sikandar et al.

Table 5.2 (continued) Source Fusarium sp., Chloridium sp.

Secondary metabolites Javanicin

Delitschia corticola

6-ethyl-7-hydroxyl-2methoxyjuglone, 6-ethyl-2,7dimethoxyjuglone and 6-(1-hydroxyethyl)-2,7dimethoxyjuglone Cordycepsidone A

Cordyceps dipterigena

Phomopsis sp. endophyte of Santolina chamaecyparissus Phomopsis sp. endophyte of Santolina chamaecyparissus Phomopsis sp., endophyte of Cistus salvifolius Phomopsis sp., endophyte of Cistus salvifolius Phomopsis sp.

Pezicula sp.

Berkleasmium sp.

Seimatosporium sp.

Phomopsinone A

Phomopsinone D

Pyrenocines K and M

Pyrenocine J

Activity Class Antifungal to Polyketides V. dahliae, F. oxysporum, R. solani, and C. arachidicola Antifungal to Polyketides Fusarium sp., Alternaria sp. and Sclerotium sp. Antifungal to Polyketides G. fujikuroi and P. ultimum Antifungal to Polyketides P. oryzae, S. tritici, and B. cinerea Antifungal to Polyketides B. cinerea and S. tritici Antifungal to M. violaceum and S. tritici Antifungal to S. tritici.

Phomochromone A and B Antifungal to S. tritici, B. cinerea, B. megaterium, M. violaceum Mellein Antifungal to B. cinerea and Fulvia fulva Palmarumycin C8 Antifungal to Magnaporthe oryzae Seimatoporic acid A and Antifungal to B S. tritici, P. oryzae and B. cinerea

References Kornsakulkarn et al. (2011)

Sun et al. (2011)

Varughese et al. (2012)

Hussain et al. (2012b)

Hussain et al. (2012c)

Polyketides

Hussain et al. (2012a)

Polyketides

Hussain et al. (2012a)

Polyketides

Ahmed et al. (2011)

Polyketides

Wang et al. (2014)

Polyketides

Shan et al. (2014)

Polyketides

Hussain et al. (2012b)

(continued)

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

171

Table 5.2 (continued) Source N. uncinatum and N. coenophialum endophyte of F. pratensis F. arundinacea E. typhina, N. coenophialum, N. lolli, E. festucae

Secondary metabolites Lolines

Activity Insecticides and feeding deterrents

Class Alkaloids

References Schardl and Phillips (1997)

Peramine

Insecticidal to Alkaloids Argentine stem weevil

Dew et al. (1990), Rowan and Latch (1994) Powell and Petroski (1992), Schardl and Phillips (1997) Clay and Schardl (2002), Faeth (2009), Müller and Krauss (2005) Bills et al. (1992)

Neotyphodium

Insecticide Indole alkaloids: elymoclavine, agroclavine and chanoclavine

Alkaloids

Neotyphodium endophytes

Endophyte alkaloids

Alkaloids

Phomopsis sp. from Cavendishia pubescens tree bark, Aspergillus flavus E. purpurascens, A. pullulans, Colletotrichum sp., A. coenophialum endophytes of Artemisia annua Hypoxylon serpens

Aspalitrems A and C

Enhanced growth rate, reproduction and herbivores resistance Toxic to insects and vertebrates

Alkaloids

Indole-3-acetic acid

Major plant growth promoting hormone

Alkaloids

Petrini (1991)

IAA and 3-indoleacetonitrile

Alkaloids Major plant growth promoting hormones Alkaloids Stimulates adventitious root formation in Arabidopsis thaliana Alkaloids Influences root growth in Arabidopsis thaliana

Petrini (1991)

T. atroviride, T. virens

Indole-3-carboxaldehyde

T. atroviride, T. virens

Indole-3-acetaldehyde

ContrerasCornejo et al. (2011)

ContrerasCornejo et al. (2009) (continued)

172

S. Sikandar et al.

Table 5.2 (continued) Source Secondary metabolites Colletotrichum sp. 6-isoprenylindole-3carboxylic acid endophyte to Artemisia. annua

Activity Antifungal to R. cerealis, G. graminis var. tritici and P. capsici T. harzianum Racemic harzianopyridone Antifungal to P. ultimum, G. graminis var. tritici, B. cinerea and R. solani T. harzianum Laevorotatory form of Phytotoxic to harzianopyridone etiolated wheat coleoptile S. mobaraensis, S. Piericidin A Insecticide pactum

Class Alkaloids

References Lu et al. (2000)

Alkaloids

Dickinson et al. (1989), Vinale et al. (2006)

Alkaloids

Cutler and Jacyno (1991)

Alkaloids

Jansen and Höfle (1983), Takahashi et al. (1965) Kumagai et al. (1990), Omura et al. (1988) Hashimoto et al. (1995), Takahashi et al. (1965)

Penicillium sp.

Atpein compounds

Antifungal

Alkaloids

Trichoderma sp. ATF-451

Melanoxadin and melanoxazal

T. harzianum, T. arundinaceum,

Harzianic acid

Inhibition of Alkaloids melanin in larval hemolymph of Bombyx mori Antimicrobial Alkaloids and plant growth regulation

Malmierca et al. (2013), Sawa et al. (1994)

References Ahmed I, Hussain H, Schulz B, Draeger S, Padula D, Pescitelli G, van Ree T, Krohn K (2011) Three new antimicrobial metabolites from the endophytic fungus Phomopsis sp. Eur J Org Chem 15:2867–2873 Atanasova L, Knox BP, Kubicek CP, Druzhinina IS, Baker SE (2013) The polyketide synthase gene pks4 of Trichoderma reesei provides pigmentation and stress resistance. Eukaryot Cell 12:1499–1508 Atehnkeng J, Ojiambo PS, Ikotun T, Sikora RA, Cotty PJ, Bandyopadhyay R (2008) Evaluation of atoxigenic isolates of Aspergillus flavus as potential biocontrol agents for aflatoxin in maize. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25:1264–1271 Bansal R, Mukherjee PK (2016) The terpenoid biosynthesis toolkit of Trichoderma. Nat Prod Commun 11:1934578X1601100401 Bills GF, Giacobbe RA, Lee SH, Peláez F, Tkacz JS (1992) Tremorgenic mycotoxins, paspalitrem A and C, from a tropical Phomopsis. Mycol Res 96:977–983

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

173

Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1–7 Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286 Chet I (1987) Trichoderma-application, mode of action, and potential as a biocontrol agent of soilborne pathogenic fungi. In: Chet I (ed) Innovative approaches to plant disease control. Wiley, New York, pp 137–160 Chet I (1993) Biological control of soil-borne plant pathogens with fungal antagonists in combination with soil treatments. In: Hornby D (ed) Biological control of soil borne plant pathogens. CABI Publishers, London, p 15 Chet I, Harman GE, Baker R (1981) Trichoderma hamatum: its hyphal interaction with Rhizoctonia solani and Pythium spp. Microbial Ecol 7:29–38 Chiang YM, Lee KH, Sanchez JF, Keller NP, Wang CC (2009) Unlocking fungal cryptic natural products. Nat Prod Commun 4:1505–1510 Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160(Suppl 4):S99–s127 Claydon N, Allan M, Hanson JR, Avent AG (1987) Antifungal alkyl pyrones of Trichoderma harzianum. Trans Br Mycol Soc 88:503–513 Collins RP, Halim AF (1972) Characterization of the major aroma constituent of the fungus Trichoderma viride. J Agric Food Chem 20:437–438 Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol, 149(3), 1579–1592. https://doi.org/10.1104/pp.108.130369 Contreras-Cornejo HA, Macias-Rodriguez L, Beltran-Pena E, Herrera-Estrella A, Lopez-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal- and camalexindependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal Behav, 6(10), 1554–1563. https://doi.org/10.4161/ psb.6.10.17443 Creissen HE, Jorgensen TH, Brown JK (2016) Impact of disease on diversity and productivity of plant populations. Funct Ecol 30:649–657 Crutcher FK, Parich A, Schuhmacher R, Mukherjee PK, Zeilinger S, Kenerley CM (2013) A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens. Fungal Genet Biol 56:67–77 Cutler HG, Jacyno JM (1991) Biological activity of (−)-harzianopyridone isolated from Trichoderma harzianum. Agric Biol Chem 55:2629–2631 de Man TJ, Stajich JE, Kubicek CP, Teiling C, Chenthamara K, Atanasova L, Druzhinina IS, Levenkova N, Birnbaum SS, Barribeau SM, Bozick BA, Suen G, Currie CR, Gerardo NM (2016) Small genome of the fungus Escovopsis weberi, a specialized disease agent of ant agriculture. Proc Natl Acad Sci U S A 13:3567–3572 Dew RK, Boissonneault GA, Gay N, Boling JA, Cross RJ, Cohen DA (1990) The effect of the endophyte (Acremonium coenophialum) and associated toxin (s) of tall fescue on serum titer response to immunization and spleen cell flow cytometry analysis and response to mitogens. Vet Immunol Immunopathol 26:285–295 Dickinson JM, Hanson JR, Hitchcock PB, Claydon N (1989) Structure and biosynthesis of harzianopyridone, an antifungal metabolite of Trichoderma harzianum. J Chem Soc Perkin Trans 1:1885–1887 Donnelly DMX, Sheridan MH (1986) Anthraquinones from Trichoderma polysporum. Phytochemistry 25:2303–2304 Evidente A, Cabras A, Maddau L, Serra S, Andolfi A, Motta A (2003) Viridepyronone, a new antifungal 6-substituted 2H-pyran-2-one produced by Trichoderma viride. J Agric Food Chem 51:6957–6960

174

S. Sikandar et al.

Faeth SH (2009) Asexual fungal symbionts alter reproductive allocation and herbivory over time in their native perennial grass hosts. Am Nat 173:554–565 Faeth SH, Hayes CJ, Gardner DR (2010) Asexual endophytes in a native grass: tradeoffs in mortality, growth, reproduction, and alkaloid production. Microb Ecol 60:496–504 Findlay JA, Buthelezi S, Li GQ, Seveck M, Miller JD (1997) Insect toxins from an endophytic fungus from wintergreen. J Nat Prod 60:1214–1215 Fujimoto H, Satoh Y, Yamaguchi K, Yamazaki M (1998) Monoamine oxidase inhibitory constituents from Anixiella micropertusa. Chem Pharm Bull 46:1506–1510 Garnica-Vergara A, Barrera-Ortiz S, Munoz-Parra E, Raya-Gonzalez J, Mendez-Bravo A, Macias-Rodriguez L, Lopez-Bucio J (2016) The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ETHYLENE INSENSITIVE 2 functioning. New Phytol, 209(4), 1496–1512. https://doi. org/10.1111/nph.13725 Gawai DU (2018) Role of fungi as biocontrol agents for the control of plant diseases in sustainable agriculture. In: Gehlot P, Singh J (eds) Fungi and their role in sustainable development: current perspectives. Springer, Singapore, pp 283–291 Ghisalberti EL (2002) Anti-infective agents produced by the hyphomycetes general Trichoderma and Glioclaudium. Curr Med Chem 1:343–374 Gilardi G, Manker DC, Garibaddi A, Gullino ML (2008) Efficacy of the biocontrol agents Bacillus subtilis and Ampelomyces quisqualis applied in combination with fungicides against powdery mildew of zucchini. J Plant Dis Prot 115:208–213 Glenn AE, Bacon CW, Price R, Hanlin RT (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88:369–383 Gloer J (1997) Environmental and microbial relationships. In: Wicklow DT (ed) The mycota, vol IV. Springer, Berlin, p 249 Hanson JR (2003) Natural products: the secondary metabolites, vol 17. Royal Society of Chemistry, London Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56 Hashimoto R, Takahashi S, Hamano K, Nakagawa A (1995) A new melanin biosynthesis inhibitor, melanoxadin from fungal metabolite by using the larval haemolymph of the silkworm, Bombyx mori. J Antibiot 48:1052–1054 Herbert RB (1989) The biosynthesis of secondary metabolites, 2nd edn. Chapman & Hall, London Hill RA, Cutler HG, Parker SR (1995) Trichoderma and metabolites as control agents for microbial plant diseases. PCT Int Appl 9520879, 10 Aug 1995 Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10 Hussain H, Ahmed I, Schulz B, Draeger S, Krohn K (2012a) Pyrenocines J-M: four new pyrenocines from the endophytic fungus, Phomopsis sp. Fitoterapia 83:523–526 Hussain H, Krohn K, Ahmed I, Draeger S, Schulz B, Di Pietro S, Pescitelli G (2012b) Phomopsinones A–D: four new pyrenocines from endophytic fungus Phomopsis sp. Eur J Org Chem 9:1783–1789 Hussain H, Krohn K, Schulz B, Draeger S, Nazir M, Saleem M (2012c) Two new antimicrobial metabolites from the endophytic fungus, Seimatosporium sp. Nat Prod Commun 7:293–294 Ishii T, Hayashi K, Hida T, Yamamoto Y, Nozaki Y (2000) TAN-1813, a novel Rasfarnesyltransferase inhibitor produced by Phoma sp. J Antibiot 53:765–778 Ishii T, Nonaka K, Suga T, Masuma R, Ōmura S, Shiomi K (2013) Cytosporone S with antimicrobial activity, isolated from the fungus Trichoderma sp. FKI-6626. Bioorg Med Chem Lett 23:679–681 Jansen R, Höfle G (1983) Revised stereochemistry of piericidin A1. Tetrahedron Lett 24:5485–5486 Jayasuriya H, Koonchanok NM, Geahlen RL, McLaughlin JL, Chang CJ (1992) Emodin, a protein tyrosine kinase inhibitor from Polygonum cuspidatum. J Nat Prod 55:696–698

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

175

Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G, Tzelepis GD, Nygren K, Dubey MK, Kamou N, Levasseur A, Zapparata A, Wang J, Amby DB, Jensen B, Sarrocco S, Panteris E, Lagopodi AL, Pöggeler S, Vannacci G, Collinge DB, Hoffmeister D, Henrissat B, Lee YH, Jensen DF (2015) Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biol Evol 7:465–480 Karlsson M, Atanasova L, Jensen DF, Zeilinger S (2017) Necrotrophic mycoparasites and their genomes. Microbiol Spectr 5:FUNK-0016 Kaur T, Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Dhaliwal HS, Saxena AK (2020) Microbe-mediated biofortification for micronutrients: present status and future challenges. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 1–17. https://doi.org/10.1016/B978-0-12-820528-0.00002-8 Kawada M, Yoshimoto Y, Kumagai H, Someno T, Momose I, Kawamura N, Isshiki K, Ikeda D (2004) PP2A inhibitors, harzianic acid and related compounds produced by fungal strain F-1531. J Antibiot 57:235–237 Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol 3:937–947 Khan MR (2008) Plant nematodes: methodology, morphology, systematics, biology and ecology. Science Publishers, Enfield, p 360 Kharwar RN, Verma VC, Kumar A, Gond SK, Harper JK, Hess WM, Lobkovosky E, Ma C, Ren Y, Strobel GA (2009) Javanicin, an antibacterial naphthaquinone from an endophytic fungus of neem, Chloridium sp. Curr Microbiol 58:233–238 Kishimoto N, Sugihara S, Mochida K, Fujita T (2005) In vitro antifungal and antiviral activities of γ-and δ-lactone analogs utilized as food flavoring. Biocontrol Sci 10:31–36 Kneifel H, Konig WA, Loeffler W, Muller R (1977) Ophiocordin, an antifungal antibiotic of Cordyceps ophioglossoides. Arch Microbiol 113:121–130 Kornsakulkarn J, Dolsophon K, Boonyuen N, Boonruangprapa T, Rachtawee P, Prabpai S, Kongsaeree P, Thongpanchang C (2011) Dihydronaphthalenones from endophytic fungus Fusarium sp. BCC14842. Tetrahedron 67:7540–7547 Koshino H, Yoshihara T, Sakamura S, Shimanuki T, Sato T, Tajimi A (1989) A ring B aromatic sterol from stromata of Epichloë typhina. Phytochemistry 28:771–772 Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franhe P, Vater J, Borris R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bactriol 186:1084–1096 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Perspective for value-added products and environments, vol 2. Springer, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal HS, Saxena AK (2020) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi.org/10.1016/j. bcab.2019.101487 Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M, Kredics L, Alcaraz LD, Aerts A, Antal Z, Atanasova L, Cervantes-Badillo MG, Challacombe J, Chertkov O, McCluskey K, Coulpier F, Deshpande N, von Döhren H, Ebbole DJ, Esquivel-Naranjo EU, Fekete E, Flipphi M, Glaser F, Gómez-Rodríguez EY, Gruber S, Han C, Henrissat B, Hermosa R, HernándezOñate M, Karaffa L, Kosti I, Le Crom S, Lindquist E, Lucas S, Lübeck M, Lübeck PS, Margeot A, Metz B, Misra M, Nevalainen H, Omann M, Packer N, Perrone G, Uresti-Rivera EE, Salamov A, Schmoll M, Seiboth B, Shapiro H, Sukno S, Tamayo-Ramos JA, Tisch D, Wiest A, Wilkinson HH, Zhang M, Coutinho PM, Kenerley CM, Monte E, Baker SE, Grigoriev IV

176

S. Sikandar et al.

(2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40 Kumagai H, Nishida H, Imamura N, Tomoda H, Omura S, Bordner J (1990) The structures of atpenins A4, A5 and B, new antifungal antibiotics produced by Penicillium sp. J Antibiot 43:1553–1558 Kumar A, Dhawan S, Aggarwal BB (1998) Emodin (3-methyl-1,6,8-trihydroxy-anthraquinone) inhibits TNF-induced NF-kB activation, IkB degradation, and expression of cell surface adhesion proteins in human vascular endothelial cells. Oncogene 17:913–918 Kumar A, Chaturvedi AK, Yadav K, Arunkumar KP, Malyan SK, Raja P, Kumar R, Khan SA, Yadav KK, Rana KL, Kour D, Yadav N, Yadav AN (2019a) Fungal phytoremediation of heavy metal-contaminated resources: current scenario and future prospects. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Perspective for sustainable environments, vol 3. Springer, Cham, pp  437–461. https://doi. org/10.1007/978-3-030-25506-0_18 Kumar M, Saxena R, Rai PK, Tomar RS, Yadav N, Rana KL, Kour D, Yadav AN (2019b) Genetic diversity of methylotrophic yeast and their impact on environments. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Perspective for sustainable environments, vol 3. Springer, Cham, pp  53–71. https://doi. org/10.1007/978-3-030-25506-0_3 Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151(1):67–73 Macel M (2011) Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochem Rev 10:75–82 Macias FA, Varela RM, Simonet AM, Cutler HG, Cutler SJ, Eden MA, Hill RA (2000) Bioactive carotanes from Trichoderma virens. J Nat Prod 63:1197–1200 Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Collado IG, Hermosa R, . . . Gutiérrez S (2013) Relevance of trichothecenes in fungal physiology: Disruption of tri5 in Trichoderma arundinaceum. Fungal Genet Biol, 53, 22–33. https://doi.org/10.1016/j.fgb.2013.02.001 Mavrodi DV, Mavrodi OV, McSpaddenss-Gardener BB, Landa BB, Weller DM, Thomashow LS (2002) Identification of differences in genome content among phID-positive Pseudomonas fluorescens strains by using PCR based substractive hybridization. Appl Environ Microbiol 68:5170–5776 Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456 Omura S, Tomoda H, Kimura K, Zhen DZ, Kumagai H, Igarashi K, Imamura N, Takahashi Y, Tanaka Y, Iwai Y (1988) Atpenins, new antifungal antibiotics produced by Penicillium sp. Production, isolation, physico-chemical and biological properties. J Antibiot 41:1769–1773 Oshino K, Kumagai H, Tomoda H, Omura S (1990) Mechanism of action of atpenin B on Raji cells. J Antibiot 43:1064–1068 Osterhage C, König GM, Höller U, Wright AD (2002) Rare sesquiterpenes from the algicolous fungus Drechslera dematioidea. J Nat Prod 65:306–313 Otsuka T, Takase S, Terano H, Okuhara M (1992) New angiogenesis inhibitors, WF-16775 A1 and A2. J Antibiot 45:1970–1973 Papavizas GC (1985) Trichoderma and Glioclaudium: biology, ecology and potential for biocontrol. Annu Rev Phytopathol 23:23–54 Parker RS, Cutler HG, Jacyno JM, Hill RA (1997) Biological activity of 6-pentyl-2H-pyran-2-one and its analogs. J Agric Food Chem 45:2774–2776 Pelletier SW (ed) (1983) The nature and definition of an alkaloid. In: Alkaloids: chemical and biological perspectives, vol 1. Wiley, New York, pp 1–31 Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Brock/Springer series in contemporary bioscience. Springer, New  York, pp 179–197

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

177

Pfeifer BA, Admiraal SJ, Gramajo H, Cane DE, Khosla C (2001) Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 291:1790–1792 Poole PR, Ward BG, Whitaker G (1998) The effects of topical treatments with 6-pentyl-2-pyrone and structural analogs on stem end post-harvest rots in kiwi fruit due to Botrytis cinerea. J Agric Food Chem 77:81–86 Powell RG, Petroski RJ (1992) Alkaloid toxins in endophyte-infected grasses. Nat Toxins 1:163–170 Pulici M, Sugawara F, Koshino H, Uzawa J, Yoshida S, Lobkovsky E, Clardy J (1996a) Pestalotiopsins A and B: new caryophyllenes from an endophytic fungus of Taxus brevifolia. J Org Chem 61(6):2122–2124 Pulici M, Sugawara F, Koshino H, Uzawa J, Yoshida S, Lobkovsky E, Clardy J (1996b) A new isodrimeninol from Pestalotiopsis sp. J Nat Prod 59:47–48 Putri SP, Kinoshita H, Ihara F, Igarashi Y, Nihira T (2010) Ophiosetin, a new tetramic acid derivative from the mycopathogenic fungus Elaphocordyceps ophioglossoides. J Antibiot 63:195–198 Qader MM, Kumar NS, Jayasinghe L, Araya H, Fujimoto Y (2017) Bioactive sesquiterpenes from an endophytic fungus Bipolaris sorokiniana isolated from a popular medicinal plant Costus speciosus. Mycology 8:17–20 Quandt CA, Di Y, Elser J, Jaiswal P, Spatafora JW (2016) Differential expression of genes involved in host recognition, attachment, and degradation in the Mycoparasite Tolypocladium ophioglossoides. G3 (Bethesda) 6:731–741 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rana KL, Kour D, Yadav N, Yadav AN (2020) Endophytic microbes in nanotechnology: current development, and potential biotechnology applications. In: Kumar A, Singh VK (eds) Microbial endophytes. Woodhead Publishing, Cambridge, pp 231–262. https://doi.org/10.1016/ B978-0-12-818734-0.00010-3 Rastegari AA, Yadav AN, Yadav N (2019a) Genetic manipulation of secondary metabolites producers. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  13–29. https://doi.org/10.1016/ B978-0-444-63504-4.00002-5 Rastegari AA, Yadav AN, Yadav N, Tataei Sarshari N (2019b) Bioengineering of secondary metabolites. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  55–68. https://doi.org/10.1016/ B978-0-444-63504-4.00004-9 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge Rowan DD, Latch GCM (1994) In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, pp 169–183 Savary S, Ficke A, Aubertot J-N, Hollier C (2012) Crop losses due to diseases and their implications for global food production losses and food security. Food Secur 4:519–537 Sawa R, Mori Y, Iinuma H, Naganawa H, Hamada M, Yoshida S, Furutani H, Kajimura Y, Fuwa T, Takeuchi T (1994) Harzianic acid, a new antimicrobial antibiotic from a fungus. J Antibiot 47:731–732 Schardl CL, Phillips TD (1997) Protective grass endophytes: where are they from and where are they going? Plant Dis 81:430–438 Schmidt-Dannert C (2015) Biosynthesis of terpenoid natural products in fungi. Adv Biochem Eng Biotechnol 148:19–61

178

S. Sikandar et al.

Shan T, Tian J, Wang X, Mou Y, Mao Z, Lai D, Dai J, Peng Y, Zhou L, Wang M (2014) Bioactive spirobisnaphthalenes from the endophytic fungus Berkleasmium sp. J Nat Prod 77:2151–2160 Shentu X, Zhan X, Ma Z, Yu X, Zhang C (2014) Antifungal activity of metabolites of the endophytic fungus Trichoderma brevicompactum from garlic. Brazilian J Micro: [publication of the Brazilian Society for Microbiology], 45(1), 248–254. https://doi.org/10.1590/ s1517-83822014005000036 Shi Y, Shentu X, Yu X (2009) Identification of an endophytic fungus isolated from Ilex cornuta and the biocontrol effects of its secondary metabolite. Acta Phyto Sinica, 39(4), 362–367 Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P, Thakur S, Thakur N, Sudheer S, Yadav N, Yadav AN, Rastegari AA, Singh K (2019) Trichoderma: biodiversity, ecological significances, and industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Diversity and enzymes perspectives, vol 1. Springer, Cham, pp 85–120. https://doi.org/10.1007/978-3-030-10480-1_3 Simon A, Dunlop RW, Ghisalberti EL, Sivasithamparam K (1988) Trichoderma koningii produces a pyrone compound with antibiotic properties. Soil Biol Biochem 20:263–264 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Singh A, Kumari R, Yadav AN, Mishra S, Sachan A, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–16. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Sivasithamparam K, Ghisalberti EL (1998) Secondary metabolism in Trichoderma and Glioclaudium. In: Kubicek CP, Harman GE (eds) Trichoderma and Glioclaudium, vol 1. Taylor & Francis Ltd, London Slater GP, Haskins RH, Hogge LR, Nesbitt LR (1967) Metabolic products from a Trichoderma viride. Can J Chem 45:92–96 Stalkman EC, Harrar JG (1957) Principles of plant pathology. Ronald Press, New York Sun R, Gao Y-X, Shen K-Z, Xu Y-B, Wang C-R, Liu H-Y, Dong J-Y (2011) Antimicrobial metabolites from the aquatic fungus Delitschia corticola. Phytochem Lett 4:101–105 Sun P, Huo J, Kurtan T, Mandi A, Antus S, Tang H, Draeger S, Schulz B, Hussain H, Krohn K, Pan W, Yi Y, Zhang W (2013) Structural and stereochemical studies of hydroxyanthraquinone derivatives from the endophytic fungus Coniothyrium sp. Chirality 25:141–148 Takahashi N, Suzuki A, Tamura S (1965) Structure of piericidin A. J Am Chem Soc 87:2066–2068 Tamura S, Sakurai A, Kainuma K, Takai M (1965) Isolation of helminthosporol, as a natural plant growth regulator and its chemical structure. Agric Biol Chem 29:216–221 Varughese T, Riosa N, Higginbotham S, Arnold AE, Coley PD, Kursar TA, Gerwick WH, Cubilla Rios L (2012) Antifungal depsidone metabolites from Cordyceps dipterigena, an endophytic fungus antagonistic to the phytopathogen Gibberella fujikuroi. Tetrahedron Lett 53:1624–1626 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agroecological perspectives, Microbial interactions and agro-ecological impacts, vol 2. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22 Vinale F, Marra R, Scala F, Ghisalberti E, Lorito M, Sivasithamparam K (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148 Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma– plant–pathogen interactions. Soil Biol Biochem 40:1–10 Vinale F, Sivasithamparam K, Ghisalberti EL, Woo SL, Nigro M, Marra R, Lombardi N, Pascale A, Ruocco M, Lanzuise S (2014) Trichoderma secondary metabolites active on plants and fungal pathogens. Open Mycol J 8:127–139 Wang J, Wang G, Zhang Y, Zheng B, Zhang C, Wang L (2014) Isolation and identification of an endophytic fungus Pezicula sp. in Forsythia viridissima and its secondary metabolites. World J Microbiol Biotechnol 30:2639–2644

5  Fungal Secondary Metabolites and Bioactive Compounds for Plant Defense

179

Watanabe N, Yamagishi M, Mizutani T, Kondoh H, Omura S, Hanada K, Kushida K (1990) CAF-603: a new antifungal carotane sesquiterpene. Isolation and structure elucidation. J Nat Prod 53:1176–1181 Waterman PG (1993) The chemistry of volatile oils. In: Hay R (ed) Volatile oil crops: their biology, biochemistry and production. Longman Scientific and Technical, Essex, pp 47–61 Weindling R (1934) Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 24:1153–1179 Wells DH (1988) Trichoderma as a biocontrol agent. In: Mukerji KG, Garg KL (eds) Biocontrol and plant diseases. CRC Press, Florida, p 73 Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511 Wu SH, Zhao LX, Chen YW, Huang R, Miao CP, Wang J (2011) Sesquiterpenoids from the endophytic fungus Trichoderma sp. PR-35 of Paeonia delavayi. Chem Biodivers 8:1717–1723 Yadav AN (2019) Fungal white biotechnology: conclusion and future prospects. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Perspective for sustainable environments, vol 3. Springer, Cham, pp  491–498. https://doi. org/10.1007/978-3-030-25506-0_20 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan V, Dhaliwal HS, Saxena AK (2017) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Kour D, Rana KL, Yadav N, Singh B, Chauhan VS, Rastegari AA, Hesham AE-L, Gupta VK (2019a) Metabolic engineering to synthetic biology of secondary metabolites production. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  279–320. https://doi.org/10.1016/ B978-0-444-63504-4.00020-7 Yadav AN, Mishra S, Singh S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. In: Diversity and enzymes perspectives, vol 1. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi. In: Perspective for value-added products and environments, vol 2. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019d) Recent advancement in white biotechnology through fungi. In: Perspective for value-added products and environments, vol 3. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, Perspective for diversity and crop productivity, vol 1. Springer, Cham Yadav AN, Rastegari AA, Yadav N (2020b) Microbiomes of extreme environments: biodiversity and biotechnological applications. CRC Press/Taylor & Francis, Boca Raton Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020d) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020e) Plant microbiomes for sustainable agriculture. Springer, Cham Yang X, Strobel G, Stierle A, Hess WM, Lee J, Clardy J (1994) A fungal endophyte-tree relationship: Phoma sp. in Taxus wallichiana. Plant Sci 102:1–9 Yang Z, Li G-H, Zhao P, Zheng X, Luo S-L., Li L., Zhang K-Q (2010) Nematicidal activity of Trichoderma spp. and isolation of an active compound. World J Microbiol Biotechnol 26, 2297–2302. https://doi.org/10.1007/s11274-010-0410-y Yuan C, Ding G, Wang H-Y, Guo Y-H, Shang H, Ma X-J, Zou Z-M (2017) Polyketide-Terpene hybrid metabolites from an endolichenic fungus Pestalotiopsis sp. Biomed Res Int 2017:10 Zhai MM, Qi FM, Li J, Jiang CX, Hou Y, Shi YP, Di DL, Zhang JW, Wu QX (2016) Isolation of secondary metabolites from the soil-derived fungus Clonostachys rosea YRS-06, a biological control agent, and evaluation of antibacterial activity. J Agric Food Chem 64:2298–2306 Zhang W, Krohn K, Zia U, Flörke U, Pescitelli G, Di Bari L, Antus S, Kurtán T, Rheinheimer J, Draeger S, Schulz B (2008) New mono- and dimeric members of the secalonic acid family: blennolides A–G isolated from the fungus Blennoria sp. Chem Eur J 14:4913–4923

Chapter 6

Fungal Endophytes: A Source for Biological Control Agents Hiran Kanti Santra and Debdulal Banerjee

Contents 6.1  6.2  6.3  6.4 

Introduction Detection of Antifungal Activity Biocontrol of Nematodes Reduction in Number of Gall Formation of Meloidogyne Incognita by Lolium perenne Endophytes 6.5  Control of European Pepper Moth by Endophytes of Strawberry 6.6  Biocontrol of Sirex Wood-Wasp by Endophytic Isolates 6.7  Endophytic Fungal Isolates Against Cotton Leaf Worm (Spodoptera littoralis (Boisd.) 6.8  Endophyte Mediated Plant Volatiles Restrict Planococcus ficus Infection 6.9  Biocontrol of Radopholus similis (Root Burrowing Nematode) by Banana Endophytes 6.10  Muscodor Albus Volatiles Control Codling Moth in Storage Conditions 6.11  Biological Control of PTM-Potato Tuber Moth (Sc. Name: Phthorimaea operculella) 6.12  Entomopathogenic Fungi Affecting Aphis gossypii Infections on Melon Plants (Cucumis melo var. cantalupensis) 6.13  Biological Control of Agricultural Fungal Pathogens by Endophytic Isolates 6.13.1  Citrus Endophytes Protect the Host from Citrus Black Spot Pathogen 6.13.2  Biocontrol of Verticillium Wilts by Cotton Root Endophytes 6.13.3  Biocontrol of Moniliophthora spp. by Endophytes of Theobroma cacao (Malvaceae) 6.13.4  Biocontrol of Potato Tuber Pathogen Rhizoctonia solani 6.13.5  Endophytic Fungi Mediated Control of Rice Blast Disease 6.13.6  Biocontrol of Vascular Streak Disease 6.13.7  Wheat Endophytes in the Control of Fusarium Head Blight 6.13.8  Reduction of Gibberella Ear Rot (GER) by Epicoccum nigrum and Sordaria fimicola 6.13.9  Biocontrol of Tan Spot Disease

 182  183  184  187  188  188  189  190  191  192  192  193  195  195  195  196  197  199  200  201  201  202

H. K. Santra · D. Banerjee (*) Microbiology and Microbial Biotechnology, Department of Botany and Forestry, Vidyasagar University, Midnapore, West Bengal, India © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_6

181

182

H. K. Santra and D. Banerjee

6.13.10  Biocontrol of Ginseng Pathogens by Ginseng Endophytes  203 6.13.11  Biocontrol of Root Rot of Pepper  204 6.13.12  Mycofumigation by M. albus Reduces Verticillium Wilt of Egg-Plant  204 6.13.13  M. albus Controlling the Post-Harvest Decay  208 6.13.14  Volatiles of Endophytic Daldinia cf concentrica Control Aspergillus niger 208 6.14  Conclusion and Future Prospects  211 References  211

6.1  Introduction Endophytes are the hidden microflora that live inside the plant for a part or lifetime within the plant tissue and promote the plant to fight against odd conditions like physiological stress, microorganism attacks, thus produce a wide range of bioactive compounds with deep industrial or agricultural application (Yadav et al. 2020a, d). Endophytes have been exploited for their novel bioactive compound production for a long time but in recent past emphasis has been given by the endophyte biologist regarding their use in agricultural sectors for minimizing the crop loss caused by fungal pathogenic attack as well as insect, burrowing nematode, flies, and moth infections (Rana et al. 2019). It has been evidenced by scientists from all over the world that endophyte has been proved to be an appropriate agent in this respect and due to its organic origin the products are found to be biodegradable and does not hamper the natural sustainability at all (Yadav et al. 2019a, b). So nowaday the trend has been shifted to endophytes with mycofumigating or biocontrol ability for minimizing the use of chemical insecticides or fungicides. Some endophytic genus like Muscodor albus is reported to be the storehouse of a wide and diverse range of volatile bioactive product with anti-pathogenic activity and this volatile antimicrobial producing endophyte is widely used in agricultural lands for minimizing fungal pathogen mediated crop loss or for reducing the economic loss caused by the fungal toxins during food transport or storage. The isolation of novel endophyte is dependent on the screening of plant as plants with particular odor or inhabiting in tropical rain forest are known to harbor greater diversity of endophytic genus as those environments are supportive for endophytes survival. As they share necessary characters with their host plants they are easy to exploit for bioactive compound production (Rastegari et al. 2020a, b; Yadav et al. 2020b, c). The crying need of this modern era of science is the maintenance of sustainability on the one hand and development of biological tools with no negative impact on environment for solving the fungal pathogenesis issues on the other hand. Fungal pathogens are known to be the prime agent for agricultural crop loss. This chapter summarizes the remarkable scientific works related to the endophytic fungi with their biocontrol ability on common and severe dreadful agricultural pathogens in vitro and in vivo conditions.

6  Fungal Endophytes: A Source for Biological Control Agents

183

6.2  Detection of Antifungal Activity Plants of medicinal importance or with special characters are selected for endophytic fungi isolation and plant parts are washed in tap water thoroughly for the avoidance of surface microbes. Plant parts are cut into small pieces and surface sterilized using sodium hypochlorite or 80% ethanol and immediately flamed in spirit lamp for 5–10 s. Then they are plated on water agar medium supplemented with 2% of agar (Fig. 6.1). After proper incubation at 28 °C for 24–72 h when the first hyphae comes out from the plant segments they are immediately transferred to a medium containing selective media supplemented with antibacterial streptomycin

Fig. 6.1 (a) Selaginella sp., a pteridophytic genus; a source of endophytic fungus. (b) Water agar plate with the explants; an endophytic fungus emerges out from that explant. (c) Plate morphology of the pure culture of the endophytic isolate. (d) Light microscopic view of the endophytic isolate showing the spores. (e) Scanning electron microscopic view of the fungal spores. (f) Round fungal colony in culture broth. (g) Antagonistic activity of the endophytic isolate against the pathogen in dual culture assay. (h) Split plate showing the inhibition of the pathogen by endophytic volatiles. (i) Fungal morphology in liquid culture. (j) Crude extract put into column for purification of active compounds

184

H. K. Santra and D. Banerjee

and potato dextrose agar as growth substance. After successful isolation they are identified by their microscopic morphology (scanning electron micrographs are also taken), colony characters, and using molecular biology methods (Fig.  6.1). The endophytic isolates are then tested for their antagonistic ability by dual culture plate assay and the diameters of the both the pathogen and the fungal growth are recorded and the clear zone of inhibition is recorded, this is called as antagonistic activity of the endophytic fungal isolates (Fig. 6.1). Next the potent isolates are screened for their culture broth assay. The fungal blocks are transferred to the culture broth provided with potato dextrose medium and agitated in 120 rotations per minute (rpm) in shaker incubator. The culture broth are filtrated and mixed with ethyl acetate and bioactive compounds are extracted. The extracted liquid is tested for their antifungal activity in agar well diffusion technique and the clear zone of inhibition is measured immediately after 12 h of incubation. The antifungal compounds are isolated using purification techniques based on column chromatographic procedures and further identification is done by IR spectral analysis and using HPLC technique (Fig. 6.1). For the detection of volatile antifungal emissions of the endophytic isolates split plate assay is performed where at one side endophytes is placed and on the other side the targeted pathogen is inoculated and on successful volatile emission the pathogen growth would be inhibited (Fig.  6.1). The volatile organic compounds (VOCs) are recorded using the GC-MS instrument. The volatiles are detected by growing the fungal mycelium on specialized GC vials and then finally comparing the chromatographic spectra with the NIST library (Fig. 6.2). The chemical compounds are checked in vitro or in vivo using standards and they are noted as the bioactive chemicals of endophytic origin (Fig. 6.3).

6.3  Biocontrol of Nematodes Endophytic microorganism especially fungus not only inhibits the growth of the pathogenic fungus in vitro but also in in vivo conditions. Reports include the inhibition of mycelial growth of the Fusarium oxysporum F.sp. Cubense, the causal agent of panama disease by the endophytes (Pocasangre 2000). The endophytes are also reported to inhibit the growth of the burrowing nematode Radopholus similis that causes potential damage in banana plant crop production. So use of endophyte for the control of nematode and pathogenic fungus is a new approach. Pederson and his co-workers in the year of 1988 worked on the effect of endophytic fungus (Acremonium coenophialum Morgan-Jones and Gams) of tall fescue on the behavior of the nematodes associated with the host plant’s infection. They reported that the removal of endophyte from the plant Festuca arundinacea Schreb. (Tall fescue) is increasing the susceptibility of the nematodal (lower spiral [Helicotylenchus dihystera (Cobb) Sher.] and stubby root [Paratrichodorus minor (Colbran) Siddiqi]) infection. They performed experiments taking soybean plants and tall fescue plants with rye grass cultivars (annual and perennial). Finally there

6  Fungal Endophytes: A Source for Biological Control Agents

185

Fig. 6.2  Endophytic isolates is grown on specialized GC vials and the volatile compounds emitted are detected in GC-MS resulting in the development of complete chromatogram of 12 min run

motto was to check the ability of the double cropping system (nematode susceptible soybean cultivars and annual rye grass) to eliminate the nematodal infection. They experimented with 13 annual rye grass cultivars, nematode susceptible soybean, and tall fescue plants with or without Acremonium coenophialum infection. After 7 weeks of continuous growth in pots of green house with a soil of sandy or fine loam infected with huge numbers of phytonematodes they ended up with the conclusion that nematode infection sensitive soybean plants are not affected and their growth or annual production is not affected but tall fescue stand decline has occurred.

186

H. K. Santra and D. Banerjee

CH2

CH3

CH3

CH3

CH2 H3C

O H2C

H

CH2

H3C

CH3

H CH3

H3C

CH3 Caryophyllene

β-elemene

Eucalyptol CH3

CH3

CH3 CH3

H2C

O CH3

β-selinine

Napthalene

CH3

α- -selinine

1,8-cineole

Azulene

Thujopsene

CH3

H3C

CH2 CH3 N H3C

CH2 β-phellandrene

CH3

CH3 N-methyl pyrrolidine

Chamigrene

Fig. 6.3  Chemical structures of the volatiles emitted by the endophytic volatiles

6  Fungal Endophytes: A Source for Biological Control Agents

187

6.4  R  eduction in Number of Gall Formation of Meloidogyne Incognita by Lolium perenne Endophytes Stewart and his scientific partners in the year of 1993 worked on the infection of Meloidogyne naasi Franklin on endophyte infected as well as non-endophyte infected perennial rye grass and evaluated the gall formation (in quantitative measurement) and proliferation of this gall forming nematode. Lolium perenne L. is globally called as the Perennial rye grass and has been a major plant of New Zealand. Earlier reports include that this plant is susceptible to the infection of gall forming nematode (Sheridan and Grbavac 1979). Acremonium spp. has been reported to protect rye grass from Argentine stem weevil pathogen but there had been no previous report on the effect of this endophytic species on gall formation mediated by M. naasi (Popay and Mainland 1991). Seeds of the experimental grass were sown in 5 cm pots filled with 50:50 mixtures of silt-loam soil and sand (pasteurized) and thinned to individual pots after germination. Occurrence of endophyte was confirmed microscopically by staining of leaf sheath with lacto-phenol cotton blue. Infection procedure includes the application of 3  mL water to all the plants by syringe into a pencil hole made on the plant body after 21 days of complete emergence. Ten endophyte infected and ten free pots were provided with nematode inoculum and the other set got only water. Final observation was made after the proper supply of nutrients and maintenance of the plants in glass house at 18–24 °C and separation of root from soil followed by the counting of number of galls per root sample. Not only the number of gall decreased but also the number of females present in each root sample of the endophyte treated plants was lesser in number in comparison to the endophyte treated one. Absence of juvenile ones was also a remarkable observation. This type of observation supports the results of experiments on similar area performed by Pederson et al. (1988), Kimmons et al. (1990), and Kirkpatrick et al. (1990). The results are of complete conclusion with Cook et al. (1991). The probable explanation of the deviation of the result could be drawn from observations of Kirkpatrick et al. (1990) that differences among endophytes isolates or in interactions between host genotype and fungal isolate are important. The occurrence of lower number of galls and females support the fact that endophytes resistance occurred early in the plant and nematode interaction. The probable explanation of this type of enhanced resistance like reduced invasion and increased emigration of juveniles or death of nematodes in the roots is due to the toxins produced by the endophytic fungus produced in the roots that repel or kill nematodes. This concept is also supported by the investigations of Siegel et al. (1989) that emphasized the production of toxins by the endophytic fungus and also the presence of endophytic fungus increased resistance.

188

H. K. Santra and D. Banerjee

6.5  C  ontrol of European Pepper Moth by Endophytes of Strawberry Fragaria ananassa (Sc, name of the strawberry plant) is an economically important fruit plant worldwide and is affected by a large number of bacterial, fungal, viral, and nematodal pathogens. Such an example is the occurrence of nematodal pest Duponchelia fovealis Zeller, 1847, a member of Lepidoptera: Crambidae (the European pepper moth). Being native to marshy habitats of Southern Europe and eastern part of Mediterranean region this nematode is a green-house pest of flowers, fruits, and vegetables of aquatic and terrestrial plants found abundantly in Europe and Canada (CABI 2016) and recent reports include its invasion on strawberry plants (Bonsignore and Vacante 2009; Franco and Baptista 2010; Efil et al. 2014; Zawadneak et al. 2016). The popular control measures include chemical and physical controls with huge amount of side effects and natural enemies are also not effective against this nematode as this is considered to be an exotic species (Zawadneak et al. 2015). So focus is on endophytic fungus being the best suitable method in this respect. Endophyte isolated from strawberry plant is used as a biological control agent against the strawberry nematode pathogen (Amatuzzia et al. 2018). In total 400 leaves of the strawberry cultivar “Albion” collected from four different commercial farms were placed into potato dextrose agar Petri-dishes after proper disinfection of the explants and maintained in incubation for 30 days with tetracycline supplemented media. Out of 517 fungal colonies some of them are identified as Alternaria sp., Aspergillus sp., Bipolaris sp., Cladosporium sp., Chaetomium sp., Diaporthe sp., Fusarium sp., Nigrospora sp., Paecilomyces sp., Penicillium sp., Phoma sp., Trichoderma sp., and Ulocladium sp. Eight isolates (belonging to genera Aspergillus, Cladosporium, Diaporthe, and Paecilomyces) were found to be effective against third instar larvae of Duponchelia fovealis. Isolates Paecilomyces sp. exhibited highest effectivity against the nematodal larvae.

6.6  Biocontrol of Sirex Wood-Wasp by Endophytic Isolates Sirex noctilio also called as Sirex wood-wasp is a horntail species generally found as a native one to Asia, Europe, and northern parts of Africa. This wasp species is involved in a symbiotic relationship with a fungus Amylostereum areolatum that promotes the invasion of the wasp into the tree trunk by boring the trunk and the larvae are generally feed on the fungal hypha. Fungus also helps the invasion by secreting mucus like materials. Wang et al. in the year of 2019 selected nine species of Pinus in China; Pinus tabuliformis, Pinus sylvestris, var. mongolica, Pinus koraiensis, Picea koraiensis, Larix gmelinii, Pinus yunnanensis, Pinus massoniana, Pinus taeda, Pinus elliottii and evaluated the effect of endophyte diversity on the Sirex noctilio infection in terms of their oviposition behavior. They isolated a total number of 1626 endophytic fungi from 2025 explants (wooden blocks) of nine

6  Fungal Endophytes: A Source for Biological Control Agents

189

selected coniferous tree species and identified them by ITS (internal transcribed spacer) sequencing system. Each host plant is characterized by a unique structure of endophytic community and that varies from one host plant to another and from one region to another. The isolates belong to 61 species under 34 genera. Fifty-one out species (83.40%) were confirmed through molecular identification and ten species (16.60%) were identified by microscopic morphological characters. The isolates belong to the genera of Alternaria sp., Arthrinium sp., Ascocoryne sp., Aspergillus sp., Capronia sp., Chaetomium sp., Coprinopsis sp., Cylindrobasidium sp., Cytospora sp., Diaporthe sp., Fusarium sp., Gliocladium sp., Gliomastix sp., Lasiodiplodia sp., Mucor sp., Ophiostoma sp., Paecilomyces sp., Paraconiothyrium sp., Penicillium sp., Pestalotiopsis sp., Peyronellaea sp., Phaeomollisia sp., Phoma sp., Phomopsis sp., Pythium sp., Schizophyllum sp., Seiridium sp., Sphaeropsis sp., Sydowia sp., Trichoderma sp., and Umbelopsis sp. CR (colonization rate) and IR (isolation rate) of endophytes from Pinus tabuliformis were the lowest and were the highest for Pinus elliottii. CR and IR values for other species were of no such significant deviation. The endophytic community also varied from different portions of the same species like base portion, central part, and also upper portions of the trunk of the Pine tree. The chances of getting infected by this wasp is negatively proportionate to the diversity of the endophytic fungus in Pinus plant as the higher occurrence of infection is due to the poor diversity of endophytic fungus in the host plant. Results are indicative that out of the nine tested coniferous plant the highest chances of getting infected by wasp is in case of Pinus tabuliformis and lowest in case of Pinus elliottii and intermediate in case of others due to the lower occurrence of endophytic species in case of P. tabuliformis.

6.7  E  ndophytic Fungal Isolates Against Cotton Leaf Worm (Spodoptera littoralis (Boisd.) Saad et  al. (2019) isolated ten endophytic fungus from four angiospermic plants (two were medicinal plants and two were weeds); Pelargonium graveolens (Geraniaceae), Melia azedarach (Meliaceae), Chenopodium album (Chenopodiaceae), and Malva parviflora (Malvaceae). The isolates of C. album were identified as Fusarium chlamydosporum saad3 MG786540, Alternaria alternata saad5 MG786542, Alternaria alternata saad8 MG786545, Fusarium oxysporum saad4 MG786541, Phoma sp. Two endophytes were identified from each of the plants (Melia azedarach and Malva parviflora) as Curvularia lunata and Nigrospora sphaerica saad1 MF113055 and F. equiseti saad7 MG786544 and Stemphylium sp., respectively. And only one is isolated from aromatic plant species of P. graveolens identified as Alternaria solani saad6 MG786543. They tested the spore suspension of A. alternata, A. solani, C. lunata, N. sphaerica, and Stemphylium sp. against the third instar larvae of cotton leaf worm scientifically named as Spodoptera littoralis (Boisd.) belonging to order Lepidoptera and family Noctuidae. Two popular

190

H. K. Santra and D. Banerjee

techniques were used for this assay that includes either dipping in spore suspension or residual film technique. The endophytes were screened having their insecticidal capacity by calculating the mortality rates of the larvae. In residual film technique no such endophytic fungus yielded positive results. Secondary metabolites were subjected to isolation from the endophytic isolates in order to evaluate their insecticidal property using ethyl acetate as a standard organic solvent for the effective extraction. Dipping assay revealed the insecticidal property of the isolates named C. lunata, followed by A. solani and A. alternata, respectively, with a mortality percentage of 60% as highest among all the tested ones, 40% and 33.3%. This type of study strongly evidences the fact that endophytic secondary metabolites are effective in vivo against the larval infection.

6.8  E  ndophyte Mediated Plant Volatiles Restrict Planococcus ficus Infection A unique study had been performed in recent past by Moloinyane and Nchu (2019) on the effect of endophytic fungus on insect (Planococcus ficus) infection. They actually tested the efficiency of the fungus to modify the host plant in terms of volatile compounds production with insecticidal activity. Beauveria bassiana (Hypocreales), an entomopathogenic fungus is a common parasite of insects and is distributed worldwide. They isolated B. bassiana from soil sample of grape vineyard and inoculated the fungus (1 × 108 conidia mL−1) on grape vine (Vitis vinifera) and again re-isolated the fungal species from the grape plant leaves after 25 days from the first inoculation. The effect of inoculation has led to production of unique volatile compounds with insecticidal compounds like benzaldehyde (Paulraj et al. 2011), limonene (Hebeish et al. 2008), geraniol (Chen and Viljoen 2010), geranylacetone (Maia and Moore 2011), gamma-terpinene (Wang et al. 2006), beta-Pinene (Dambolena et al. 2016), napthelene (Daisy et al. 2002), M-Cymene (Chang et al. 2002), Citral, naphthalene, 2-hexanoic acid, terpinolene, benzene, benzofuranone, heptadecane, nerolidol, pentanoic acid. The occurrences of these insecticidal compounds increase the plants’ resistance by reducing the number of female nematodes and their infestation activity. The re-isolation confirms the endophytic nature of the phytophagous fungus and inoculation is done before the artificial inoculation of Planococcus ficus on Vitis vinifera. Though plant growth parameters were not (N, P, K, Na, Mn, Fe, Cu, Zn, B contents of leaf) sharply deviating from the fungus treated and untreated Vitis plant but there was a change in (calcium) Ca and (magnesium) Mg content of the plant leaf tissues. This type of study elaborates the fact that endophytic fungi are effective against insects of economically important plants also, thus, enhancing the plants’ protection.

6  Fungal Endophytes: A Source for Biological Control Agents

191

6.9  Biocontrol of Radopholus similis (Root Burrowing Nematode) by Banana Endophytes Radopholus similis also known as the burrowing nematode is a devastating pathogen of banana (Musa paradisiaca) and has led to qualitative and quantitative decrease of the yield. It is an agent of root rot causing reddish brown lesions in the cortical portions of the root and hampering the water conduction, nutrient uptake leading to the lengthy vegetative cycle and finally to the death of the plant (Gowen and Quénéhérvé 1990). Chemical control measures being too much expensive and non-eco-friendly lead to hazardous problems of human health. Till date a very few reports include development of complete resistant banana species against the banana plant (Gowen 1995). Scientist has moved to biological methods for this reason (Kerry 1990 and Sikora 1992). Endophytes could be an alternative solution in this respect (Hallmann and Sikora 1994; Schuster et al. 1995). Some fungal species are reported to be anti-endoparasitic (Sikora 1992; Schuster et  al. 1995). Previously endophytic fungus isolated from banana root tissue has been checked for the anti-­ nematodal activity in vitro by culture filtrate assay (Schuster et al. 1995). Niere et al. (1999) investigated the in vivo and in vitro effectivity of the Fusarium oxysporum isolates (from banana root) against burrowing nematode and also their influence on plant growth. They prepared PDB (potato dextrose broth) culture extracts with spore suspensions (1.4–3.2 × 106 spores/ml) of 4 selected isolates V4w5, III3w3, III4w1, and V5w2 and inoculated them on the previously tested (in vitro) banana seedling (Musa AAA, cv. Gros Michel) raised through tissue culture techniques (Vuylsteke 1989). The plantlets were potted in 100 ml cups with sterilized soil filled in it and after 4 weeks transferred to carry bags containing 2 l of sterilized soil. Two set of experiments were carried out just having the difference between the time (one setup of 13 weeks aged and another of 32 weeks aged). Plants were removed from the polythene bags and after gentle wash of the roots they were inoculated with 10 Radopholus similis females singly collected from soil populations and kept directly on the root surface. Then they are infected with fungal endophytes for the observation of their morphological changes at 4  weeks constant interval. Beginning 6 weeks after nematode inoculation (plant age 19 and 38 weeks, respectively), the root segments inoculated with the nematode in the cup were cut free from the intact root and the nematodes extracted overnight by the extraction dish method (Oostenbrink 1960). All nematodes extracted were concentrated on a 20 μm sieve and counted. Endophyte treated plants are reported to be enhanced in their growth parameters by 11–25%. After the complete removal of soil, transplantation of the plant and nematodal infection Fo1 is known to be promoting plant height by 29% in relation to the control plant. The nematode multiplication rate is reduced in plants treated with endophytic isolates. The reduction rate varied but Fo4 is proved to be the potent one regarding the reduction in number (26% than the control, i.e., untreated plant) of nematode population in a 19-weeks-old root segment whereas the nematode population increased up to 33% (in comparison to the initial number of nematode) in a

192

H. K. Santra and D. Banerjee

38-week-old control (without any endophyte inoculation) plant. The nematode populations were reduced from 51% to 99% after the endophytic treatment.

6.10  M  uscodor Albus Volatiles Control Codling Moth in Storage Conditions Codling moth (Sc. Name—Cydia pomonella (L)) belongs to the group Lepidoptera and class Torticidae is known to be a harmful pest pathogen of apple fruit (Malus spp.). It is one of the giant causes of worldwide severe economic loss in pome fruit marketing. Chemical fumigants like methyl bromide are restricted due to quarantine issues in case of international import and export. So there is an urgent need for the discovery of effective moth inhibiting agents with minimum amount of side effects. In this regard endophytic fungus from medicinal plant has been an effective alternative. Such a remarkable work had been done by Lacey and his co-workers in the year of 2009. They collected the endophytic Muscodor albus Worapong, Strobel, and Hess (A member of Ascomycota; family—Xylariaceae) and evaluated the bioactivity of the volatile compounds emitted by the endophytic isolates against the growth and development of the different stages (codling moth adults, diapausing cocooned larvae, larvae in infested apple, neonate larvae) of codling moth. The fumigation of the adult moths with M. albus VOCs for a continuous exposure of 72 h and immediate incubation in fresh open air for 24 h time at a temperature of 25 °C leads to 81% mortality of the total larvae. When the time of treatment or exposure is enhanced to 48 h or 120 h the mortality increased from 84% to 100%. The control apple fruits were also found to be with dead moths due to their short life span. Treatment of neonate larvae for 72 h on apple fruits and then immediate incubation for 7  days resulted in 86% of mortality. The larvae were mostly of third instars stage and when apples infested (for 5  days) with moth larvae exposed to volatiles for 3 continuous days 71% mortality occurred. Not only that the diapausing cocooned moth larvae when exposed to volatile organic compounds for one or 2 weeks resulted in 31% to 100% of mortality. So this type of biocontrol ability of endophytic M. albus opens up new popular angles of environment friendly techniques for the broad spectrum protection of economically important plants like apple from pest devastation.

6.11  B  iological Control of PTM-Potato Tuber Moth (Sc. Name: Phthorimaea operculella) Potato tubers are one of the major vegetable products of the world with several uses in the food and junk food industry. Solanum tuberosum (potato) is a plant of Solanaceae family and has been subjected to a large number of fungal, bacterial,

6  Fungal Endophytes: A Source for Biological Control Agents

193

and viral pathogens leading to mass destruction of potato farms. One such pathogen is PTM (potato tuber moth) scientifically named as Phthorimaea operculella (Lepidoptera: Gelechiidae) found all over the world as a serious pest of potato tubers on field and in storage conditions in the countries especially where potato tubers are grown. Biological control of this serious pest has been performed by the unique volatiles of the novel endophytic fungus Muscodor albus (Lacey and Neven 2006). The volatile antimicrobial includes alcohols, esters, ketones, acids, and lipids and shows insecticidal activity. They exposed adult and neonate larvae to the VOCs generated by M. albus sterile mycelium (15 g or 30 g) for 72 h at 24 °C in a sealed 28.3 L chambers. When the mycelial weight of M. albus is increased from 0 to 15 g and finally to 30  g as a source of volatile exposure the mortality increased from 84.6% to 90.6%, respectively. When the pupal stages were exposed to 15 g and 30 g of M. albus culture their growth reduced by 61.8% and 72.8% in relation to control conditions. The time of exposure is also a valuable parameter for the control of PTM. Though the higher exposure leads to the accumulation of excess CO2 generated by the respiration of the endophytic fungus M. albus which is harmful for tuber storage but still exposure for 3 days, 7 days, and 14 days and incubation at 27 °C leads to the increased mortality of 84.2%, 95.5%, and 99.6%, respectively. Increased exposure significantly affected on mortality of larvae; determined in terms of percentage as larvae fail to survive to the adult stage. Temperature for incubation has a direct effect on larval death and studies are indicative that lower temperature leads to reduced mortality, so this type of biological control measure is effective in warm and humid countries where potato tubers grow generally at 25–35  °C.  When the temperature are fluctuated from 10 °C to 15 °C and finally to 24 °C with an exposure of 7 days followed by clean air incubation at 27 °C the mortality rates are 50.8%, 76.8%, and 95.4%, respectively (Lacey et al. 2008). Storage conditions and degree of cooling are also valuable factors for using this biocontrol method. So this study clearly states the fact that if some correction could be made like the excess CO2 production M. albus volatiles could be an effective tool in this respect. Proper detection of volatiles in GC-MS and preparation of artificial mixtures of those chemicals could replace the harmful side effects of other measures of pest control.

6.12  E  ntomopathogenic Fungi Affecting Aphis gossypii Infections on Melon Plants (Cucumis melo var. cantalupensis) Aphid control has been a grave problem for the farmers and agriculturalists as they not only involve direct damage of crops but also are effective agents of transmission of economically important plant virus (Van Emden and Harrington 2007). Aphids are characterized with high fecundity rates and short lifetimes as a result they grow rapidly (Dixon 1998). Chemical control leads to development of resistance.

194

H. K. Santra and D. Banerjee

Entopathogenic fungi here play a vital role for biological control measure (Brodeur et  al. 2018). A high percentage of fungus that infects aphids belongs to Entomopthoromycota and Ascomycota (Order Hypocreales) and the Ascomycota members are highly commercialized due to their fast mass production in vitro and easy spray formulation (Burges 1998). The myco-insecticides are environmentally safe and meet the guidelines of legislation requirements (Lacey et al. 2005). They are not only used in spraying, drenching, and seed dressing but also as endophyte for protecting the plant (Quesada-Moraga et  al. 2009; Sánchez-Rodríguez et  al. 2018). Using entomopathogenic fungi as a tool for the biological control of aphids is one of the possible measures of plant protection especially in green house conditions. González-Mas et al. (2019) study on the behavior of entomopathogenic fungi as an endophyte of those treated plant and evaluated the enhancement of resistance against the aphid attack. Generally Beauveria bassiana and Metarhizium brunneum acts as common entomopathogens of serious pest like aphid; Aphis gossypii and protect the economically important vegetable crops that are largely affected worldwide regarding their quality and quantity of production due to this type of pathogenic aphid attack. They studied that when the entomopathogen is sprayed on the leaves of the host melon plant (Cucumis melo var. cantalupensis; Family-­ Cucurbitaceae) they acted as endophyte and infected the host plants leaf tissues. This statement was confirmed by the successful isolation (100% for infected leaves and 20–40% for non-sprayed leaves) of that fungus again from leaf tissues as an endophytic one. These herbivores’ life table parameters and behavior are drastically affected by the endophytic nature of this fungus. Investigations were made on lethal and pre-mortality rates of those two entomopathogens on the cotton aphid (Aphis gossypii). The effect of endophyte on the mortality rates were determined either by feeding the aphid population on endophyte colonized leaves or on endophytic fungus sprayed leaves. The comparison were made by feeding the larvae on un-colonized leaves. Mortality rates of this Hemiptera aphid were found to be between the values of 37.70–50.00% in case of endophyte colonized leaves and in comparison to fungus sprayed leaves where the values ranged between 48.2% and 56.9%. The nymph productions were also affected by endophytic colonization. Though endophytic colonization had no drastic effect on aphid control but plants are benefitted by indirect methods like defense enhancement, resistance development to plant pathogens, and also abiotic stress tolerance. Endophytic colonization on plants largely affects the volatile emissions of those plant tissues in contrast to the controlled or untreated plants. The VOCs were recorded using GC-MS and by comparing with standards. The volatiles emitted by the crushed homogenized melon plant tissues fall under several chemical classes like aldehyde, alcohols, ketones. The major aldehydes are 2-pentenal, 2-heptenal, 2-octenal, 2-nonenal, 2-hexenal, 2,4-hexadienal, 2,4-heptadienal, 2,6-nonadienal, 3-methyl-hexanal, 3-methyl-­ butanal, 4-heptenal, 4-oxohex-2-enal, 5-methyl-hexanal, 6-nonenal, butanal, hexanal, heptanal, nonanal, octanal, pentanal. The predominant alcohols include ethanol, 1-octen-3-ol, 1-penten-3-ol, 2-hexen-1-ol, 2-propyl-1-pentanol,

6  Fungal Endophytes: A Source for Biological Control Agents

195

2-ethyl-­ 1-hexanol, 3-hexen-1-ol, 4-methyl-1-pentanol. The keton bodies are 6-methyl-2-heptanone, 3-octanone, 6-methyl-5-hepten-2-one, 3,5-octadien-2-one. Chemical compounds like 2,2,6-trimethyl-cyclohexanone, β-cyclocitral, β-citral, β-ionone, eucarvone, geranial, isomethyl-α-ionone were also recorded. Phenolic derivatives include 2-phenyl-isopranol, acetophenone, benzaldehyde, benzophenone, benzyl alcohol, phenol, toluene. In spite of such huge production of different types of volatiles by the endophyte infected leaf tissues the host selection of aphid population (confirmed by choice based assays) has not been affected by the blend of volatiles emitted. This type of biological control is environment friendly and does not develop resistance, so should be adopted in large scale and is one of the unique applications of endophyte as biological control agent.

6.13  B  iological Control of Agricultural Fungal Pathogens by Endophytic Isolates 6.13.1  C  itrus Endophytes Protect the Host from Citrus Black Spot Pathogen Citrus fruit is a common economically plant species found all over the World. Tran et al. (2019) isolated 33 endophytic fungus from different citrus plants (Citrus reticulata, C. maxima, C. aurantium, C. australasica, C. wintersii, C. japonica, C. hystrix, C. limon) found in Queensland of Australia and studied their diversity on citrus plants and also their bioactivity in terms of antifungal activity. The endophytes were identified as species of Phyllosticta capitalensis and Phyllosticta paracapitalensis. These endophytes are tested for their in vitro antifungal activity against citrus black spot pathogen Phyllosticta citricarpa. For the first time these species are reported from Australia (Queensland) and proved through the principles of Koch’s postulate that these endophytic isolates are non-pathogenic to the host citrus species, thus could be confirmed as a true endophyte of citrus and providing protection against one of the dreadful diseases of these economically important plants. In vivo test also shows reduction of P. citricarpa pathogen on citrus fruits after inoculation of endophytic isolate P. capitalensis 14  days before the pathogen inoculation. So it is a classic example of biological control by endophytic fungus.

6.13.2  Biocontrol of Verticillium Wilts by Cotton Root Endophytes Verticillium wilt is caused by the fungus Verticillium dahliae and hugely impacts on the growth of the cotton plant (Gossypium herbaceum) as it is generally pathogenic to cotton plant species and leads to qualitative and quantitative deterioration of the

196

H. K. Santra and D. Banerjee

cotton yield. Yuan et al. (2017) isolated four endophytic fungi (CEF-818 (Penicillium simplicissimum), CEF-714 (Leptosphaeria sp.), CEF-642 (Talaromyces flavus.), and CEF-193 (Acremonium sp.) from different portions of the cotton plant collected from Anyang region of Henan province of China. The phytopathogen was isolated from infected soils of Xinji of Hebei province of China. They used two upland cotton cultivars named Gossypium hirsutum Jimian 11 and Lumianyan 21 which were susceptible and tolerant to the disease, respectively. The isolates were tested for their disease control activity in vivo in green house condition where the tested plants were maintained and results indicated the control efficacy of the isolates ranged from 26% (Talaromyces flavus) to 67% (Penicillium simplicissimum) after a treatment of 25 days from the time of inoculation. In comparison to the controls of the disease nursery the isolates showed a better level of protection efficiency of 69.5%, 69.2%, 54.6%, and 45.7% by Penicillium simplicissimum, Acremonium sp., and Leptosphaeria sp., Talaromyces flavus, respectively. Reports include that endophytic isolates CEF-818 and CEF-714 offer protection to the host plant even in the heavily infected cases (during the time of early July; the first peak of the disease). These types of result are indicative that endophytic isolates not only delayed the wilt symptoms but they reduced the symptoms on the host plants. The treatment with endophyte causes the enhancement of harvest up to 13.1 and 12.2% increase from the untreated ones. When the seeds are treated with the isolates the production increased (7.3%) from 3207.51 kg/ha to 3442.04 kg/ha. Study up to molecular details included that treatment of endophytes increased the transcript level of PAL (phenylalanine ammonia lyase), PPO (polyphenol oxidase), and POD (peroxidase) that results in the increase of defense reactions in the cotton plant. So the summary of the performed experiment is that the endophytic treatment in vitro conditions improved the yield of cotton seed in cotton fields and also results in the enhancement of the disease resistance ability of this plant. So it will be a great chance of biological control against the verticillium wilt of cotton.

6.13.3  Biocontrol of Moniliophthora spp. by Endophytes of Theobroma cacao (Malvaceae) Theobroma cacao, a plant of Malvaceae family is commonly known as the cocoa tree and the seeds are commercially exploited in chocolate industry for making of chocolate liquor, cocoa solids, and cocoa butter. The economically important taxon is affected largely by frosty pod rot and witches’ broom diseases caused by the aggressive fungal pathogens Moniliophthora roreri and Moniliophthora perniciosa, respectively. M. roreri affects the development of fruits leading to severe yield loss up to 30–100% (Bowers et al. 2001; Sánchez et al. 2015) and M. perniciosa affects the leaves, branches, shoots, flowers (Parra and Sánchez 2005). Villavicencio-­ vásquez and his co-workers in the year of 2018 tried the biological control methods

6  Fungal Endophytes: A Source for Biological Control Agents

197

for the reduction of these dreadful fungal pathogenic attacks using endophytic fungal flora of the host plant (T. cacao) itself as a tool. They isolated 17 fungal strains from leaves of T. cacao collected from two different parts of Ecuador; Balao and Naranjal of Guayas province and Molleturo of Azuay province. Out of 17 endophytic fungal isolates seven were identified as Lasiodiplodia theobromae, three isolates are known as Pestalotiopsis microspora, two proved to be Colletotrichum gloeosporioides, others are identified as Phanerochaete chrysosporium, Xylaria feejeensis, Daldinia eschscholtzii, Xylaria sp., Hypoxylon investiens, and Nigrospora sphaerica. The biocontrol ability of these isolates were determined by two ways; by detecting the mycoparasitism of foliar endophytic fungus against Moniliophthora spp., antifungal activity by the crude extracts containing secondary metabolites. The true endophytic nature was confirmed by the re-inoculation test. Three strains of L. theobromae (Ec098, Ec151, Ec157) were found to effective antifungal agent in both the cases of direct antagonism and crude extract tests. They were successfully recolonized onto the host plant for almost 80–100%. The strains of L. theobromae were all square in all the three formats whereas other isolates were magnificent in only one parameter each like Ec035 (identified as L. theobromae) is an effective agent for mycoparasitism against both of the indicator organism when both the colonies were brought into contact but is the second best in antifungal activity shown by the crude extracts and moreover they were unable to re-infect host plant. Another strain of endophytic fungus Ec059 identified as Xylaria feejeensis has the 100% of re-inoculation but is negative in antagonistic tests. Colletotrichum gloeosporioides (Ec107) inhibited Moniliophthora roreri but also stimulated the growth of another phytopathogen Moniliophthora perniciosa. So the fungal endophytes of T. cacao could be largely exploited as biological control agent. Alternative biological control of the above said two pathogens were already done by antagonistic native microorganisms such as bacteria and fungi (Hebbar 2007; Bailey et al., 2008; Hernández-Rodríguez et al. 2014). This study focuses on the ability of the endophyte on the above said purpose as they help the plant to defend against pathogenic attack (Arnold et al. 2003). Previously scientists have tried integrated management system with the use of biological agent like Trichoderma spp., chemicals like azoxystrobin, chlorothalonil, cupric oxide, copper sulfate and also physical techniques like pruning and removal of diseased fruits. But endophytes were not explored widely for this purpose.

6.13.4  B  iocontrol of Potato Tuber Pathogen Rhizoctonia solani Rhizoctonia solani, a pathogenic fungus of Basidiomycota is a serious tuber and stem colonizer of potato plant (Scientifically known as Solanum tuberosum under the family Solanaceae) that causes stem canker and tuber blemishes. This soil borne pathogen is one of the prime causes of qualitative and quantitative damage of potato

198

H. K. Santra and D. Banerjee

crop production worldwide (Woodhall et al. 2007). Previous techniques include the control through chemical fungicide or by physical separation of affected individuals. But nowaday focus has been totally shifted to the alternative mode of biological control measures maintaining the sustainability of the environment. The use of mycoparasites or antagonists leading to interhyphal physical interference using the volatile or non-volatile secondary metabolites has already been studied in large scale (Benítez et al. 2004). Verticillium biguttatum (an obligate mycoparasite) and Trichoderma sp. have been used as biological control agent of R. solani (Van Den Boogert & Jager). Earlier researchers have confirmed the anti-Rhizoctonia activity of Ampelomyces, Coniothyrium, and Trichoderma (Berg 2009). Lahlali and Hijri (2010) isolated six fungal endophytes from Acer platanoides (Family Sapindaceae), commonly called as Norway maple and identified them (by microscopic morphology and ITS rDNA sequences) as Trichoderma atroviride, Epicoccum nigrum (E1, E8, E18), Alternaria longipes (E13), and Phomopsis sp. (R24). They evaluated the antifungal activity of the isolates against the potato tuber pathogen Rhizoctonia solani in vitro and in green house conditions by direct confrontation methods. It has been found that endophytic fungal isolate T. atroviride and E. nigrum inhibited the pathogenic fungus in vitro in dual culture assays having the highest zone of inhibition of mycelial growth among the tested individuals. Evaluation of antifungal ability includes the screening by secondary metabolites production. The highest inhibition zone was displayed by the culture filtrates of T. atroviride. The inhibitory effect of the fungal isolates was further studied in detail using confocal microscopy that confirmed that Trichoderma atroviride acts as mycoparasite and competitor. Epicoccum nigrum covers the mycelium of R. solani and causes the lysis of cell wall leading to loss of turgidity of the cells of the pathogen. The fungal hyphae of Trichoderma atroviride rolls up and penetrates into the mycelium of tuber pathogen leading to the formation of dense coils tightly encircling the fungal hyphae. Phomopsis sp. invades the pathogen colony and competes for nutrients finally limiting its growth and the fungal hyphal densities are found to be higher than R. solani. Though hyphae of A. longipes were of more density than R. solani and hyphae of the pathogen were of abnormal morphology in comparison to the control or untreated one but endophytic Alternaria shows no hyphal penetration or inhibition of the pathogen. So it could be drawn that Phomopsis sp. causes loss of turgor. The fungal isolates were recorded for the antifungal volatile emissions in split plate method and the remarkable antagonistic properties are shown by T. atrovirde, Phomopsis sp., A. longipes, E. nigrum E18, E1, and E8 with an inhibition percentage of 81.81, 38.63, 21.02, 20.73, 11.36, and 10.22, respectively. In vivo tests performed in green house conditions confirmed the endophytic fungal isolates T. atroviride and E. nigrum enhanced the yield of potato tuber and significantly reduced the stem disease caused by the pathogens. So this endophytic genus could be used in large-scale as a biocontrol agent of stem and tuber pathogens.

6  Fungal Endophytes: A Source for Biological Control Agents

199

6.13.5  E  ndophytic Fungi Mediated Control of Rice Blast Disease Magnaporthe grisea is known as the causative agent of blast disease of rice (Oryza sativa) leading to irreparable crop loss worldwide. Chemical fungicides are found to be ineffective due to development of resistance. In this occasion biological control is the best effective way. Atugala and Deshappriya (2015) for the first time isolated 41 fungal endophytes from 160 explants of leaves, stems, seeds, roots of two rice plant varieties Suwandel (35 endophytic fungal isolates from 80 explants) and Kaluheenati (31 endophytic fungal isolates from 80 explants) grown in Sri Lanka. The isolates were identified as Cylindrocladium sp., Absidia sp., Aspergillus sp.1, Cladosporium sp., Penicillium sp., Paecilomyces sp., Phoma sp., Gliocladium sp., Acremonium sp., Aspergillus sp. 2, Rhizoctonia sp., Aspergillus sp. 3, Varicosporium sp., Rhizopus sp., Arthroderma sp., Aureobasidium sp. Most of the fungal endophytes belonged to Ascomycetes group and only one genus fall under Basidiomycetes and two under Zygomycetes. Absidia sp. and Cylindrospermum sp. were the dominant fungi found in Suwandel and Kaluheenati, respectively. They selected the two most commonly occurring endophyte and tested their effect on crop plants’ growth and also antagonistic or antifungal ability against the pathogen. Results include that the treated plants show remarkable enhancement of plant height and plant weight (dry weight and fresh weight). They screened 22 endophytic isolates with antifungal activity checked in dual culture assay. The potent isolates inhibited the pathogenic fungal growth (M. grisea) by coiling their hyphae around pathogenic fungal hyphae and forming loops and clamps. Absidia sp. and Acremonium sp. were the best agents for growth inhibition of the pathogenic one by their inhibitory structures. Thirteen endophytic fungi were cultured in broth medium and were checked for the presence of antifungal secondary metabolites by diffusion plate method. In vivo studies were performed with three endophytic fungi (Acremonium sp., Absidia sp., Penicillium sp.) against M. grisea. A set of plant was kept separate and designated as control and other three sets were inoculated by the endophytic fungus first then by pathogenic fungus. The control plant only received the spore suspension as inoculum of the pathogen in an amount of 1 × 107 spores/ mL. Plants pre-inoculated with endophytic fungi and next infected with pathogen show no disease symptoms. Only endophytic Penicillium sp. treated plants showed the occurrence of disease symptoms. So, endophytic Absidia sp., Acremonium sp. could be used commercially in field trials for the protection of rice plants from pathogenic fungal attack.

200

H. K. Santra and D. Banerjee

6.13.6  Biocontrol of Vascular Streak Disease Indonesia represents the third highest producers of Cacao (ICCO Annual Report 2014/2015). Sulawesi Island of this Southeast Asian country is the prime producer and is reported to be largely affected by the systemic VSD (vascular streak disease). This vascular streak disease leads to the loss of almost 774 million US dollar (Abdurrahman (2017)). The causal agent is named as Ceratobasidium theobromae (earlier known as Oncobasidium theobromae), belongs to the basidiomycete (Guest and Keane 2007; Samuels et al. 2012). It not only hampers the cacao production but also questions its existence in the affected areas especially in small-scale farms. Wind-borne spores matures during midnight to early morning time, penetrate the unhardened leaves at terminal portions of the branch, and grow through the cuticular portions just above the veins of the leaves finally infecting the xylem and stem tissues after 3 or 5  months of first penetration through ramification of the hypha (Prior 1979). Being a systemic disease the control measures are tough including the application of fungitoxic triadimefon, triazole, triadimenol, and propiconazole that protect the leaves from the germination of the basidiospores on it. Chemical methods are avoided due to their high cost and cultural or biological control measures are focused in this respect. Asman et al. (2018) isolated ten fungal endophytes from the healthy branch of vascular streak disease resistance cacao plants. The fungal identification was done by comparing the colony characters with standard literature and identified as Aspergillus-like colony, Curvularia-like colony, Colletotrichum-like colony, Fusarium-like colony, Gliocladium-like colony, Geotrichum-like colony, another four isolates due to the absence of their reproductive structures are known as mycelia sterilia 1–4. The fungal isolates were infected to a 2.5-months-old cacao seedling and after 30 days the fungal pathogen was inoculated and the seedlings were placed in a region surrounded by the cacao infected plants for the facilitation of the secondary infection. They started recording the disease incidence after 30 days, 60 days, 90 days, and 120 days of disease incidence. The results proved that endophytic fungi when pre-inoculated to the cacao plants can reduce infection occurrence but vary from days (60, 90, 120  days) after detection. The incidence occurrence were reduced after 60 days when the treatment was done by Curvularia-like colony, followed by Geotrichum-like colony, Fusariumlike colony, mycelia sterilia isolate 4 and the results were better than the standard antifungal antibiotic copper fungicide. After 90  days still Curvularia-like colony was found to be best effective followed by mycelia sterilia isolate 1 which was equal or better than the copper fungicide treatment. Final tests were again done using the 120-days-old plants and the results include Curvularia-like colony showed higher degree of resistance even higher than the standard copper fungicide followed by sterile mycelia (isolate no. 1), colony resembling Gliocladium, colony similar with Fusarium-, Geotrichum-like colony, sterile mycelia 3, Colletotrichum-like colony, Aspergillus-like colony and lastly control (no application), sterile mycelia 2, sterile mycelia 4 with percentage of 3.0, 8.3, 9.5, 11.3, 15.8, 18.0, 19.0, 19.3, 21.3, 26.5,

6  Fungal Endophytes: A Source for Biological Control Agents

201

30.5, respectively. So the disease incidence will increase as the days goes by. The re-isolation of the endophytes from the infected plants was made and it was found that after 150 days no endophyte was potentially re-isolated from root, stem, or leaf but after 30 days all the endophytic isolates were found to be reappeared from leaf tissues but not from the root or stem tissues except Colletotrichum-like colony morphology showing endophyte. This type of experimental result can conclude that endophytes could be used for biological control of dreadful fungal diseases.

6.13.7  W  heat Endophytes in the Control of Fusarium Head Blight Comby et al. (2017) isolated 86 endophytic fungi from the inner tissues of Triticum aestivum (wheat plant). They were screened for their ability to inhibit the growth of pathogenic fungus Fusarium graminearum and Fusarium culmorum in vitro in dual culture assays. A group consisting of 22 fungal isolates was found to very effective in the control (30–51% inhibition) of F. graminearum and these strains were known to be effective controller (15–53% inhibition) of F. culmorum also globally. New findings of this study include the identification of three previously unknown species with anti-Fusarium head blight activity. They confirmed Phoma glomerata, Aureobasidium proteae, and Sarocladium kiliense to be antifungal by screening on a detached spikelet inflorescence of the wheat plant. This was the first report from wheat endophyte that these three species are effective biocontrol agent of the dreadful pathogen Fusarium culmorum and F. graminearum. Authors pointed out a significant difference among the antifungal ability of the endophytic fungal isolates in the two different types of in  vitro screening approaches applied in this study. Findings emphasizes on the procedure that includes the use of detached wheat spikelet which potentially points out the pathogenicity of the endophyte and also growth ability of the endophytic isolate on the targeted host plant. So, proper screening procedure is needed in search of biocontrol agent before trying them on the whole plant.

6.13.8  R  eduction of Gibberella Ear Rot (GER) by Epicoccum nigrum and Sordaria fimicola Fusarium graminearum is known as a serious pathogen of wheat causing Gibberella ear rot and blight disease of seedlings. Not only that the huge production of mycotoxins but also accumulation of those toxins like zearalenone, trichothecenes, and deoxynivalenol (its acetylated forms also) causes destructive loss of global wheat production and transport or consumption. Abdallah et al. (2018) isolated five endophytic fungi; four from soil sample and one from maize stubble. They were

202

H. K. Santra and D. Banerjee

identified as Clonostachys rosea, Sordaria fimicola, and Epicoccum nigrum (three species) according to their macroscopic and microscopic morphology along with their nucleotide sequencing. Sordaria fimicola is found to be a potent inhibitor of the pathogenic fungal growth in vitro tested by dual culture assay for 4 days in a sharp comparison with other well-known biocontrol agent like Trichoderma harzianum. Other isolates Clonostachys rosea and Epicoccum nigrum showed similar antifungal activity whereas the control Piriformospora sp. was not efficient in this respect. The absolute mycotoxin levels were variable in PDA plates of different endophytic genus and between different strains of the same endophytic species especially for reduction in deoxynivalenol (DON) and 15-acetyldeoxynivalenol (15-ADON) production. Sordaria fimicola and one isolate of E. nigrum could decrease the DON levels in comparison to the reference strains of biological control agents. Though the results were of high variation after repeated replication Clonostachys rosea was average in mycotoxin reduction. Endophytic Sordaria fimicola UG 106, Epicoccum nigrum UG 1703 reduced completely the ZEN (Zearalenone) production. These isolates were consistent in their reduction ability against ZEN production. It is concluded from the above mycotoxin reduction studies that DON and 15-ADON levels are related to reduction of fungal hyphal growth. The more the fungal growth is reduced more the mycotoxin levels are reduced. In case of ZEN synthesis the hyphal growth in one way and in another way the mycotoxins are inhibited by the endophytes directly. The volatiles of Sordaria fimicola reduced the fungal growth up to 60–70% in comparison to the control. In vivo tests revealed the reduction of DON levels in maize plant after endophytic treatment. Except E. nigrum UG 11703 the other endophytic isolates Sordaria fimicola, E. nigrum UG 11701, E. nigrum 11702, and Clonostachys rosea cause significant reduction in 15-ADON levels. These type of results highlight the unique potential of some selected endophytic fungal strains as new and novel biocontrol agents in agricultural science and technology.

6.13.9  Biocontrol of Tan Spot Disease Larran et al. (2016) isolated endophytes from cultivars of wheat found in Buenos Aires province of Argentina. The endophytes were tested for their antifungal activity against Pyrenophora tritici-repentis (Died.) Drechsler (anamorph Drechslera tritici-repentis) (Died.) Shoem (Dtr), the causal agent of tan spot disease of wheat using dual culture assay. The endophytes were identified as Alternaria alternata, Chaetomium globosum, Cladosporium herbarum, Epicoccum nigrum, Fusarium sp., Penicillium sp., Paecilomyces lilacinus, Rhodotorula rubra, and Trichoderma hamatum. They were evaluated for their pathogenicity on 30-day-old wheat plant (susceptible cultivar Buck Poncho) in green house conditions. Except Rhodotorula rubra all the other endophytic fungal isolates reduced the pathogenic fungal growth. Penicillium sp., Trichoderma hamatum and Paecilomyces lilacinus reduced the diameter of the colony of the pathogenic fungus. The endophytes showed sharp

6  Fungal Endophytes: A Source for Biological Control Agents

203

morphological changes in the conidia or the vegetative mycelium of Drechslera tritici-repentis. Endophytic Fusarium sp. reduced the spore germination percentage (6.82–52%). In in vivo green-house tests using Trichoderma hamatum, Chaetomium globosum and Fusarium sp. significantly reduce the disease severity on all the three leaves treated with endophytic isolate and infected with the fungal pathogen. Trichoderma hamatum is reported to be the best effective in in vitro plate assay as well as in vivo green-house experiments. So from this experiment it could be drawn that endophytic T. hamatum is a potent biological control agent of tan spot pathogen of wheat.

6.13.10  B  iocontrol of Ginseng Pathogens by Ginseng Endophytes Park et al. (2015) isolated 1300 endophytic fungus from root, stem, and leaf tissues from mountain cultivated ginseng tree (Panax ginseng Meyer) collected from 24 different geographical locations in Korea. One hundred and twenty-nine fungal endophytes were identified using internal transcribed spacer sequences. Phyllogenetic analysis revealed that endophytic isolates belonged to group of Ascomycota, Basidiomycota, Zygomycota with a percentage of 81.7%, 7.08%, 10%, respectively. Fifty-nine genera were found to be unknown. The endophytes are tested for their biocontrol or antifungal ability against destructive pathogen of gingseng known as Alternaria panax, Botrytis cinerea, Cylindrospermum destructans, Pythium sp., Rhizoctonia solani. The endophytic diversity was determined using Shannon diversity index that revealed that root tissues are colonized by endophytic fungal isolates more than stem or leaf tissues. The cause might be due to the rhizospheric nature of the soil. Diversity of the endophytic fungus are totally dependent on geographical locations and the environmental factors of that particular area in reference to its temperature, rainfall, humidity, and soil type or other physical or abiotic factors. Some fungal isolates are found to be tissue specific extremely. The fungal isolates were grown in culture broth and extraction of the bioactive compounds is made by using ethyl acetate organic solvent. The ethyl acetate extracts were tested for their antifungal ability and results revealed that only one endophytic fungal isolates identified as Trichoderma polysporum shows broad spectrum antifungal activity against all the 5 fungal pathogens of ginseng. Other isolates Tricharina ochroleuca, Lachnum virgineum, Phoma sp., Alternaria longissima, unknown fungal endophyte, Penicillium chrysogenum inhibited the growth of at least one pathogenic fungi but not all. So from this study it could be concluded that endophytic Trichoderma polysporum could be used as an alternative approach for the biocontrol of ginseng pathogens reducing the worldwide huge economic loss.

204

H. K. Santra and D. Banerjee

6.13.11  Biocontrol of Root Rot of Pepper Fungal root rot pathogens causing severe disease symptoms are the main reason of destruction of bell pepper production in United States even when the environmental factors are favorable (Kelley et al. 2009; Kelly et al. 2010). The prime destructive fungal pathogens are Phytophthora capsici, Phytophthora nicotianae var parasitica, Fusarium solani, Fusarium oxysporum, Verticillium spp., Rhizoctonia solani, Pythium aphanidermatum, Macrophomina phaseolina. In spite of chemical and biological control measures still it is a grave problem for economic earning based on pepper production but endophytes are being introduced in these respects nowadays with a high degree of success rates. Mmbaga et al. (2018) isolated 16 endophytic fungi from stem tissues of Cornus florida (flowering dogwood). Endophytes were identified as Dothideomycetes sp., Cornus florida, Hypoxylon howeanum, Hypoxylon sp., Nigrospora sphaerica, Entonaema sp., Whalleya microplaca, Hypoxylon submonticulosum, Hypoxylon rubiginosum, Hypoxylon sp., Dothideales sp, Hypoxylon submonticulosum, Botryosphaeria dothidea. These endophytes were screened for their antifungal activity against fungal pathogen Fusarium solani, Fusarium oxysporum, Macrophomina phaseolina, Phytophthora nicotianae, Phytophthora irrigate, Phytophthora cryptogea, Phytophthora capsici (Lt6745, OP97, and Lt263), Cercospora nicotianae causing root rot of Capsicum annum L. Most of the endophytes exhibited antifungal potency in dual culture assay and one isolate A22F1 (Nigrospora sphaerica) was tested in green house conditions for their disease inhibiting ability in vivo in three separate cultivars of pepper (California Wonder, Pepper Cayenne and Numex Primavera). So this endophytic A22F1 could be exploited commercially for root rot pathogen control of Bell pepper.

6.13.12  Mycofumigation by M. albus Reduces Verticillium Wilt of Egg-Plant Volatiles from endophytic fungus are a promising source of new and novel bioactive compounds for agricultural exploitation in terms of their antifungal activity and biocontrol ability. A very potent genus Muscodor plays an important role in this respect and is commercially exploited worldwide for their broad spectrum anti-­ pathogenic activity that has open up new areas of agricultural research on microbial volatiles. Muscodor species has been isolated as a true endophyte worldwide by several workers from different type of plants residing in diverse environments and they have checked for their biocontrol (mycofumigating) ability in vitro (Table 6.1). Usually the identity of the genus is confirmed by molecular means, also supporting evidences are collected from their channel tests and specialized microscopic structure unique for this genus. One such application is documented here. Mycofumigation with the two agents; Muscodor albus and M. roseus has effectively enhanced the Sugar beet (Beta vulgaris L.) stand establishment and reduced the disease severity

6  Fungal Endophytes: A Source for Biological Control Agents

205

Table 6.1  Biocontrol ability of volatile organic compounds of different types of Muscodor species Muscodor species Volatile compounds Muscodor albus 1-butanol, 3-methyl-acetate, naphthalene, tetrohydrofuran, 2-methyl furan, 2-butanone, aciphyllene, azulene, germacrene B, acetic acid, methyl ester, 1-Butanol, benzeneethanol, acetate, Pyrrolidine, 2-Heptanoic acid, 4-cyclopropyl-, Bicyclo[3.1.1] heptane, 6-methyl-2- propanoic acid

Muscodor roseus Muscodor vitigenus

2-butenoic acid, ethyl ester, 1,2,4-trimethylbenzene, 2,3-nonadiene Naphthalene, azulene, 3-methylbutan-1-ol, 3-methylbutyl acetate

Muscodor fengyangensis

Naphthalene derivatives; α-phellandrene; β-phellandrene; 2-cyclohexen; propionic acid, its 2-methyl-, and methyl ester

Muscodor sutura (Xylariaceae)

Thujopsene, chamigrene, isocaryophyllene, butanoic acid, 2-methyl

Biocontrol ability Mycofumigating agent for the control of storage insects like potato tuber moth and coddling moth. A biological control agent of Aphanomyces cochliodiodes, Aspergillus fumigatus, Fusarium culmorum, and Glomerella cingulata

Antifungal activity

References Worapong et al. (2001) Ezra and Strobel (2003) Ezra et al. (2004) Strobel et al. (2007) Banerjee et al. (2010a, b) Worapong et al. (2002)

Insect repellent of a crop Daisy et al. pest C. cinctus (2002) Siri-udom et al. (2016) Zhang et al. Antifungal against (2010) Botrytis cinerea, Aspergillus clavatus, Colletotrichum fragariae, Didymella bryoniae, Magnaporthe oryzae, Pythium ultimum, Rhizoctonia solani, Sclerotium rolfsii, Verticillium dahlia, Penicillium digitatum Kudalkar Antifungal activity et al. (2012) against pathogenic fungus A. fumigatus, Botrytis cinerea, Colletotrichum lagenarium, Ceratocystis ulmi, Cercospora beticola, Geotrichum candidum, Mycosphaerella fijiensis, Phytophthora cinnamomi, Phytophthora palmivora, Pythium ultimum, Rhizoctonia solani, Sclerotinia sclerotiorum, Verticillium dahlia (continued)

206

H. K. Santra and D. Banerjee

Table 6.1 (continued) Muscodor species Muscodor cinnamomi Muscodor equiseti Muscodor musae

Muscodor kashayum

Volatile compounds Azulene; butanoic acid, 2-methyl, methyl ester, propanoic acid, 2-methyl, methyl ester Isobutyric acid, C4H8O2 2-methylpropanoic acid, 3,7-dimethyl-1,6-octadiene, 6-nitro-2-picoline, Ethyl 2-methylpropanoate, Methyl 2-methylbutanoate, 2-Methylpropyl acetate, Methyl 3-methylbutanoate, 2-Methylpropyl propanoate, 2-Methylpropan-1-ol, 3-Methylbutanoyl acetate, 2-Methylbutyl 2-methylpropanoate, 3-Methylbutan-1-ol, Ethyl 2-hydroxy-2-methylpropanoate

Biocontrol ability Biocontrol agent for Rhizoctonia solani

Antifungal activity against pathogenic fungus like Alternaria porri, Alternaria solani, Aspergillus flavus Botrytis cinerea, Colletotrichum capsici, Colletotrichum gloeosporioides, Colletotrichum musae, Fusarium oxysporum, Fusarium solani, Nigrospora oryzae, Penicillium digitatum, Penicillium expansum, Rhizoctonia solani, Sclerotium rolfsii 3-cyclohexen-1-ol,1-(1,5-dimethyl-­ Antifungal against a wide range of fungus 4-hexenyl)-4-methyl; Alternaria alternate, 1,6-dioxacyclododecane-7,12-­ dione; 2,6-bis(1,1-dimethylethyl)- Aspergillus flavus, Aspergillus japonicas, 4-(1-oxopropyl) phenol; Bionectria ochroleuca, 2,4-di-tert-butylthiophenol and Botrytis cinerea, 4-octadecylmorpholine Cercospora beticola, Chaetomium heterosporum, Colletotrichum gloeosporioides, Curvularia lunata, Fusarium equiseti, Fusarium oxysporum, Lasiodiplodia theobromae, Mycosphaerella fijiensis Penicillium citreonigrum, Penicillium marneffei, Rhizoctonia solani, Trichderma viridae, Agaricus bisporus, Pleurotus flabellatus

References Suwannarach et al. (2010, 2012) Suwannarach et al. (2013) Siri-udom et al. (2016)

Meshram et al. (2013)

(continued)

6  Fungal Endophytes: A Source for Biological Control Agents

207

Table 6.1 (continued) Muscodor species Muscodor strobelii

Volatile compounds Viridiflorol, tetraoxapropellan, terpinolene, octadec-9-enoic acid, aspidofractinine-3-methanol

Biocontrol ability Antifungal against Penicillium citreonigrum, Botrytis cinerea, Aspergillus japonicas, Mycosphaerella fijiensis, Cercospora beticola, Rhizoctonia solani, Colletotrichum gloeosporioides, Fusarium oxysporum, Lasiodiplodia theobromae Muscodor 2, 6-Bis (1,1-dimethylethyl)-4-(1-­ Inhibits the growth of fungal pathogen Candida darjeelingensis oxopropyl) phenol, 1, 6-Dioxacyclododecane-7, 12-dione species and 4-octadecylmorpholine Inhibits the growth of Muscodor 4-octadecylmorpholine, tigerii 1-tetradecanamine, N,N-dimethyl fungal pathogens and 1,2-Benzenedicarboxylic acid, Cercospora beticola, Penicillium marneffei, mono(2-ethylhexyl) ester Rhizoctonia solani, Candida albicans M. suthepensis 2-methylpropanoic acid, by Myco-fumigant agent to 3-methylbutan-1-ol control tangerine fruit rot caused by Penicillium digitatum Muscodor 3-methylbutan-1-ol, 3-methylbutyl Antifungal to pathogenic fungi Phellinus noxius heveae acetate, 2 methyl propanoic acid and Rigidoporus and azulene derivatives microporus Mycofumigating agent Tetracontane, Muscodor against ghoomensis, M. 4-octadecylmorpholine, N,N-­ Cercospora beticola, dimethyl-­1-pentadecanamine and indica, M. Penicillium marneffei, cis-9-hexadecena, camphora and Colletotrichum 4-octadecylmorpholine; gloeosporioides 1,6-dioxacyclododecane-7,12-­ dione, 1,4-dimethyl-7-prop-1-en-2-yl-­ 2,3,3a,5,6,7,8,8a-octahydro-1H-­ azulen-4-ol

References Meshram et al. (2014)

Saxena et al. (2014)

Saxena et al. (2015)

Suwannarach et al. (2015)

Siri-udom et al. (2016)

Meshram et al. (2015, 2017)

when these two mycofumigating agents are applied in autoclaved sterilized soil prior infested with severe pathogens like Rhizoctonia solani, Pythium ultimum, Aphanomyces cochlioides (Stinson et al. 2003). Experiment with egg-plant seedlings include the mycofumigation of the autoclaved soil previously inoculated with pathogens that significantly reduces the disease incidence on Solanum melongena

208

H. K. Santra and D. Banerjee

after 4–5  weeks when compared with non-fumigated but Verticillium pathogen infested soil. Damping off disease (caused by Pythium ultimum) is controlled effectively by Muscodor roseus volatiles but in case of sugar beet pathogen Fusarium sp. (Causal agent of Fusarium wilt of sugar beet) mycofumigation was not effective. The common formulations include potato dextrose agar strips with fungal mycelium, alginate capsules having hyphae, barley grains infected with M. roseus or M. albus, stabilize or Pesta granules with fungal inoculum. The best control of Aphanomyces cochliodes (causal agent of damping off) was obtained by Stabileze formulation and Rhizoctonia solani damping off was minimized by agar strip method coupled with barley grain inoculation technique. None of the fungal volatiles affected the plant growth or external morphological appearance. So it could be said that mycofumigation using M. albus and M. roseus is a new way for control of soil-borne pathogens P. ultimum, A. cochlioides, R. solani, and V. dahliae.

6.13.13  M. albus Controlling the Post-Harvest Decay Mercier and Jiménez (2004) worked on the ability of the fungal volatiles of M. albus for the control of decay on economically important fruits apple and peach. They assessed the mycofumigating property of the Muscodor albus in vitro and in vivo. In vitro tests resulted in death of a wide range of storage pathogens like Botrytis cinerea, Colletotrichum acutatum, Geotrichum candidum, Monilinia fructicola, Penicillium digitatum, and Rhizopus sp. In vivo tests include the treatment of apples for 7 days with the culture of M. albus and resulted in complete inhibition of blue and gray mold growth (P. expansum and B. cinerea, respectively). The fruits were inoculated with pathogen and M. albus culture is not in direct contact with the fruit but exposed to its volatiles. In case of wound inoculated peach fruits 24–72 h of fumigation controlled the brown rot disease (Monilinia fructicola). Shorter fumigation time also resulted in complete control of mold and gray mold. Headspace GC-FID detection showed the maximum occurrence of 2-methyl-1-butanol, isobutyric acid.

6.13.14  Volatiles of Endophytic Daldinia cf concentrica Control Aspergillus niger Other than Muscodor species a lots of endophytes have been isolated those are efficient producers of volatile bioactive compounds with antifungal activity (Table 6.2). One of such example includes the biocontrol of Aspergillus niger and other food pathogens or agricultural pathogens (Alternaria alternata pathotype tangelo, Alternaria alternate, Aspergillus niger, Botrytis cinerea, Colletotrichum sp., Coniella sp., Fusarium euwallaceae, Fusarium mangiferae, Fusarium oxysporum,

6  Fungal Endophytes: A Source for Biological Control Agents

209

Table 6.2  Biocontrol activity of endophytic isolates by their volatile organic compounds Endophytic isolates Gliocladium sp.

Colletotrichum gloeosporioides, Clonostachys rosea, Botryosphaeria ribis

Prime VOCs emitted Butanol, 3-methyl-octene, 1-propanol, 2-methyl-1-butanol, 2-methyl-propanoic acid, octanone, 1,3,5,7-cyclooctatetraene (azulene), acetic acid, 2-phenylethyl ester, phenylethyl alcohol None

Biocontrol ability Pythium ultimum, Verticillium dahliae

References Stinson et al. (2003)

Controls the frosty pod rot, black pod rot, and witches broom pathogen Moniliophthora roreri, Phytophthora palmivora, Moniliophthora perniciosa, respectively Rhizoctonia fragariae, Fuasrium oxysporum, Sclerotium rolfsii Verticillium dahlia, Colletotrichum acutatum Pythium ultimum.

Mejıa et al. (2008)

Nodulisporium sp.2 Nodulisporium sp.3

1,3,8-p-menthatriene; caryophyllene; eucalyptol

Oidium sp.

Butanoic acid, 3-methyl-,methyl ester; butanoic acid, 3-methyl-ethyl ester 5-pentyl-2-furaldehyde Controls post-harvest apple decay and Rhizoctonia sp. root rot on moth orchid Butane-2-methyl; β-butyrolactone, Fusarium oxysporum 2-butenedinitrile Butane-2-methyl, 1-propanol Biocontrol potential 2-methyl against phytopathogen Fusarium oxysporum Biocontrol of Pythium 3-octanone, 3-octanol, 7-octen-­ ultimum and Sclerotinia 4-ol, cyclo hexane, 1,4-cyclo sclerotiorum hexadiene, β-elemene, β-selinene, α-selinene; Post-harvest biocontrol 1-methyl-1,4-cyclohexadiene agent of apple and a potent bio-fumigant agent 1-butanol, 3-methyl; Biocontrol potential β-butyrolactone; 2-butenedinitrile against phytopathogen Fusarium oxysporum 1,3,5,7-cyclooctatetraene; Post-harvest control 3-methyl-1-butanol agent for strawberry against Botrytis fruit rot

Oxyporus latemarginatus

Botrytis sp. BTF 21 Cladosporium sp. MIF01 Myrothecium inundatum Nodulisporium sp.

Penicillium sp. BTF08 Candida intermedia

Mann et al. (2008)

Strobel et al. (2008) Lee et al. (2009)

Ting et al. (2010) Ting et al. (2010) Banerjee et al. (2010a, b) Park et al. (2010)

Ting et al. (2010) Huang et al. (2011) (continued)

210

H. K. Santra and D. Banerjee

Table 6.2 (continued) Endophytic isolates Phomopsis sp.

Prime VOCs emitted Sabinene (monoterpene), 1-butanol, 3-methyl, benzeneethanol, 1-propanol, 2-methyl, 2-propanone Alpha-humulene (sesquiterpene); alcohols, reduced naphthalene derivatives, trans-caryophyllene

Biocontrol ability Biocontrol of Sclerotinia sp., Botrytis sp.

Minimize the growth of Verticillium sp., Ceratocystis sp., Cercospora sp., Sclerotinia sp. Biological control of Nodulisporium sp., Series of ketones, including acetone; 2-pentanone, 3-hexanone, plant pathogen Daldina sp., Phytophthora 4-methyl, 3-hexanone, Hypoxylon spp. cinnamomi 2,4-dimethyl, 2-hexanone, 4-methyl and 5-hepten, 2-one, 1,8-cineole, 1-butanol, 2-methyl and phenylethanol alcohol, cyclohexane, propyl Antifungal agent against Nodulisporium sp. Mono and sesquiterpenes, GS4d2llla especially eucalyptol and limonene Pythium aphanidermatum Inhibits the growth of Xylaria sp. 3-methyl-1-butanol, thujopsene, pathogenic Pythium 2-methyl-1-butanol, aphanidermatum, 2-methyl-1-propanol Phytophthora capsici, Alternaria solani, Fusarium oxysporum Fusarium Caryophyllene, a potent post-harvest oxysporum 4-methyl-2,6-di-tert-butylphenol biocontrol agent for tomato plant from pathogenic Fusarium oxysporum Phoma sp.

References Singh et al. (2011)

Strobel et al. (2011)

UL-Hassan et al. (2013)

Fernández et al. (2016) Sánchez-­ Ortiz et al. (2016)

Romero et al. (2017)

Lasiodiplodia theobromae, Neoscytalidium dimidiatum, Penicillium digitatum, Phoma tracheiphila, Pythium aphanidermatum, Pythium ultimum, Rhizoctonia solani, Sclerotinia sclerotiorum) by D. concentrica endophyte isolated from olive tree (Olea europaea) (Liarzi et al. 2016). In total 27 volatiles (3-methyl-1-butanol, 2-methyl-1-butanol, 1-methyl-1,3-cyclohexadiene, 1-methyl-1,4-cyclohexadiene, 4-heptanone, isoamyl acetate, 4-heptyn-2-ol, 2-octenal, octanal, 4,4-dimethyl1,3-cyclopentanedione, 2, 2, 5-trimethylcyclopentanone, phenyl ethyl alcohol, β-elemene,-α-funebrene, α-guaiene, 2-(4-hydroxyphenyl)ethanol, terpenes, β-selinene, α-selinene, α-bulnesene, germacrene,α-selinene, veratryl acetone, 3-methoxy-2-naphthol, pogostol) have been identified from its unique mixture of volatiles that have immense importance in food processing and storage industry as they are proved to be inhibiting the growth of the one of the common food pathogen or contaminant Aspergillus niger.

6  Fungal Endophytes: A Source for Biological Control Agents

211

6.14  Conclusion and Future Prospects The vast nature of the Science could be interpreted by its definition “to know the unknown and to see the unseen” and it is a quite obvious fact that a lots of knowledge are still to be explored even in the high tech time of the twenty-first century. Sustainability maintenance in one hand and assuring the optimum pace of development finding fast solution to the leading problems is the crying need of this era. In this respect dependence on endophytic microorganism solely as a tool for biological control of agricultural pest or pathogens not only assures the nature’s longevity but also a step ahead towards our secured future. This is just a try to sum up all the recent or past remarkable discoveries on endophytic bioactivity but it is quite obvious that it is of very little percentage of the huge arena of endophyte biology. After going through all the popular discoveries it could be sum up that still we use endophytic biocontrol as the last step or alternative step for the survival of crops or protection from pests but in true sense the sustainability of our agricultural policies along with our environment would be maintained when endophytes would be used as a common and frequently used most dominant mode of protection against agricultural disease related issues.

References Abdallah MF, Boevre MD, Landschoot S, Saeger SD, Haesaert G, Audenaert K (2018) Fungal endophytes control Fusarium graminearum and reduce trichothecenes and zearalenone in Maize. Toxins 10:493 Abdurrahman (2017) Penerapan Budidaya Tanaman Sehat dalam Rangka Peningkatan Produksi Kakao di Sulawesi Selatan Pertem. Entomol. Indones. dan Fitopatol. Indonesia Sulawesi Selatan di Balitsereal Maros Amatuzzia RF, Cardosob N, Poltronieria AS, Poitevina CG, Dalzotoa P, Zawadeneaka MA, Pimentela IC (2018) Potential of endophytic fungi as biocontrol agents of Duponchelia fovealis (Zeller) (Lepidoptera:Crambidae). Braz J Biol 78(3):429–435 Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci 100(26):15649–15654 Asman A, Amin N, Rosmana A, Abdulla T (2018) Endophytic fungi associated with cacao branch and their potential for biocontrol vascular streak dieback disease on cacao seedling. IOP Conf Ser Earth Environ Sci 157:012039 Atugala DM, Deshappriya N (2015) Effect of endophytic fungi on plant growth and blast disease incidence of two traditional rice varieties. J Natn Sci Found 43(2):173–187 Bailey BA, Bae H, Strem MD, Crozier J, Thomas SE, Samuels GJ (2008) Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biol Control 46(1):24–35 Banerjee D, Strobel GA, Booth E, Geary B, Sears J, Spakowicz D, Busse S (2010a) An endophytic Myrothecium inundatum producing volatile organic compounds. Mycosphere 1(3):229–240 Banerjee D, Strobel GA, Geary B, Sears J, Ezra D, Liarzi O, Coombs J (2010b) Muscodor albus strain GBA, an endophytic fungus of Ginkgo biloba from United States of America, produces volatile antimicrobials. Mycology 1(3):179–186

212

H. K. Santra and D. Banerjee

Benítez T, Rincón AM, Limón MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7(4):249–260 Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84 (1):11–18 Bonsignore CP, Vacante V (2009) Emerging insects and pests in southern Italy. Prot Colture 4:25–31 Bowers JH, Bailey BA, Hebbar PK, Sanogo S, Lumsden RD (2001) The impact of plant diseases on world chocolate production. Plant Health Prog 2:12 Brodeur J, Abram P, Heimpel GE, Messing RH (2018) Trends in biological control: public interest, international networking and research direction. Biocontrol 63:11–26 Burges HD (1998) Formulation of mycoinsecticides. In: Burges HD (ed) Formulation of microbial biopesticides. Kluwer Academic Publishes, Dordercht, pp 131–185 CABI (2016) Duponchelia fovealis (Southern European marshland pyralid) Chang KS, Shin EH, Park C, Ahn YJ (2002) Contact and fumigant toxicity of Cyperus rotundus steam distillate constituents and related compounds to insecticide-susceptible and -resistant Blattella germanica. J Med Entomol 49:631–639 Chen W, Viljoen AM (2010) Geraniol—a review of a commercially important fragrance material. S Afr J Bot 76:643–651 Comby M, Gacoin M, Robineau M, Rabenoelina F, Ptas S, Dupont J, Profizi C, Baillieul F (2017) Screening of wheat endophytes as biological control agents against Fusarium head blight using two different in vitro tests. Microbiol Res 202:11–20 Cook R, Lewis GC, Mizen KA (1991) Effects on plant-parasitic nematodes of infection of perennial ryegrass, Lolium perenne, by the endophytic fungus, Acremonium lolii. Crop Prot 10:403–407 Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741 Dambolena JS, Zunino MP, Herrera JM, Pizzolitto RP, Areco VA, Zygadlo JA (2016) Terpenes: natural products for controlling insects of importance to human health—a structure-activity relationship study. Psyche 2016:4595823 Dixon AFG (1998) Aphid ecology: an optimization approach, 2nd edn. Chapman & Hall, London Efil L, Efil F, Atay E (2014) New pest Duponchelia fovealis Zeller (Lepidoptera: Pyralidae) in peanut field. J Appl Biol Sci 5:65–67 Ezra D, Strobel GA (2003) Effect of substrate on the bioactivity of volatile antimicrobials produced by Muscodor albus. Plant Sci 165:1229–1238 Ezra D, Hess WM, Strobel GA (2004) New endophytic isolates of Muscodor albus, a volatile-­ antibiotic-­producing fungus. Microbiology 150:4023–4031 Fernández RES, Diaz D, Duarte G, Oliveras PS, Sánchez S, Macías-Rubalcava ML (2016) Antifungal volatile organic compounds from the endophyte Nodulisporium sp. strain GS4d2II1a: a qualitative change in the intraspecific and interspecific interactions with Pythium aphanidermatum. Microb Ecol 71(2):347–364 Franco CM, Baptista M (2010) Duponchelia fovealis Zeller: nova praga em Portugal. Rev Frutas 110:34–35 González-Mas N, Sánchez-Ortiz A, Valverde-García P, Quesada-Moraga E (2019) Effects of endophytic entomopathogenic ascomycetes on the life-history traits of Aphis gossypii glover and its interactions with melon plants. Insects 10:165 Gowen S (1995) The source of nematodes resistance, the possible mechanisms and the potential for nematode tolerance in Musa. In: Frison EA, Horry J-P, DeWaele D (eds) Proceedings of a workshop on New Frontiers in resistance breeding for Nematode, Fusarium and Sigatoka. INIBAP, Montpellier, pp 45–48 Gowen S, Quénéhérvé P (1990) Nematode parasite of banana, plantains and abaca. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp 431–460 Guest D, Keane P (2007) Vascular-streak dieback: a new encounter disease of cacao in Papua New Guinea and Southeast Asia caused by the obligate basidiomycete Oncobasidium theobromae. Phytopathology 97:1654–1657

6  Fungal Endophytes: A Source for Biological Control Agents

213

Hallmann J, Sikora RA (1994) Occurrence of plant parasitic nematodes and non-pathogenic species of Fusarium in tomato plants in Kenya and their role as mutualistic synergists for biological control of root-knot nematodes. Int J Pest Manage 40:321–325 Hebbar PK (2007) Cacao diseases: important threats to chocolate production worldwide cacao diseases: a global perspective from an industry point of view. Phytopathology 97(12):1658–1663 Hebeish A, Fouda MMG, Hamdy IA, El-Sawy SM, Abdel-Mohdy FA (2008) Preparation of durable insect repellent cotton fabric: Limonene as insecticide. Carbohydr Polym 74:268–273 Hernández-Rodríguez A, Ruíz-Beltrán Y, Acebo-Guerrero Y, Miguélez-Sierra Y, Heydrich-­ Pérez M (2014) Antagonistas microbianos para el manejo de la pudrición negra del fruto en Theobroma cacao L: estado actual y perspectivas de uso en Cuba. Rev Prot Veg 29(1):11–19 Huang R, Li GQ, Zhang J, Yang L, Che HJ, Jiang DH, Huang HC (2011) Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101:859–869 Kelley WT, Boyhan GE, Harrison KA, Granberry DM, Langston DB (2009) Commercial pepper production handbook. The University of Georgia, Athens Kelly G, Wilson E, Sandoz K, Kitchens J (2010) The valued living questionnaire: defining and measuring valued action within a behavioral framework. Psychol Rec 60:249–272 Kerry BR (1990) An assessment of progress toward microbial control of plant-parasitic nematodes. Suppl J Nematol 22:621–631 Kimmons CA, Gwinn KD, Bernard EC (1990) Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis 74:757–761 Kirkpatrick TL, Barham JD, Bateman RJ (1990) Host status for Meloidogyne graminis of tall fescue selections and clones with and without the endophyte Acremonium coenophialum. In: Quisenberry SS, Joost RE (eds) Proceedings of the international symposium on Acremonium/ grass interactions. Louisiana Agricultural Experimental Station, Baton Rouge, pp 154–156 Kudalkar P, Strobel G, Ul-Hassan SR, Geary B, Sears J (2012) Muscodor sutura, a novel endophytic fungus with volatile antibiotic activities. Mycoscience 53:319–325 Lacey LA, Neven LG (2006) The potential of the fungus, Muscodor albus, as a microbial control agent of potato tuber moth (Lepidoptera: Gelechiidae) in stored potatoes. J Invertebr Pathol 9:195–198 Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2005) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41 Lacey LA, Horton DR, Jones DC (2008) The effect of temperature and duration of exposure of potato tuber moth (Lepidoptera: Gelechiidae) in infested tubers to the biofumigant fungus Muscodor albus. J Invertebr Pathol 97:159–164 Lahlali R, Hijri M (2010) Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants. FEMS Microbiol Lett 311:152–159 Larran S, Simón MR, Moreno MV, Santamarina Siurana MP, Perelló A (2016) Endophytes from wheat as biocontrol agents against tan spot disease. Biol Control 92:17–23 Lee SO, Kim HY, Choi GJ, Lee HB, Jang KS, Choi YH, Kim JC (2009) Mycofumigation with Oxyporus latemarginatus EF069 for control of postharvest apple decay and Rhizoctonia root rot on moth orchid. J Appl Microbiol 106:1213–1219 Liarzi O, Bar E, Lewinsohn E, Ezra D (2016) Use of the endophytic fungus Daldinia cf. concentrica and its volatiles as bio-control agents. PLoS ONE 11(12):0168242 Maia MF, Moore SJ (2011) Plant-based insect repellents: a review of their efficacy, development and testing. Malar J 10:11 Mann R, Mattner S, Allen D, Porter I, Edwards J (2008) Bioprospecting for endophytes from Australian flora with mycofumigation potential. In: 3rd International biofumigation symposium. CSIRO Discovery Centre, Canberra, p 80 Mejıa LC, Rojas EI, Maynard Z, SV AAE, Hebbar P, Samuels GJ, Robbins N, Herre EA (2008) Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol Control 46(1):4–14

214

H. K. Santra and D. Banerjee

Mercier J, Jiménez JI (2004) Control of fungal decay of apples and peaches by the biofumigant fungus Muscodor albus. Postharvest Biol Technol 31:1–8 Meshram V, Kapoor N, Saxena S (2013) Muscodor kashayum sp. nov.  – a new volatile anti-­ microbial producing endophytic fungus. Mycology 4(4):196–204 Meshram V, Saxena S, Kapoor N (2014) Muscodor strobelii, a new endophytic species from South India. Mycotaxon 128:93–104 Meshram V, Gupta M, Saxena S (2015) Muscodor ghoomensis and Muscodor indica: new endophytic species based on morphological features, molecular and volatile organic analysis from Northeast India. Sydowia 67:133–146 Meshram V, Kapoor N, Chopra G, Saxena S (2017) Muscodor camphora, a new record from Cinnamomum camphora. Mycosphere 8(4):568–582 Mmbaga MT, Gurung S, Maheshwari A (2018) Screening of plant endophytes as biological control agents against root rot pathogens of pepper (Capsicum annum L.). J Plant Pathol Microbiol 9:3 Moloinyane S, Nchu F (2019) The effects of endophytic Beauveria bassiana inoculation on infestation level of Planococcus ficus, growth and volatile constituents of potted greenhouse grapevine (Vitis vinifera L.). Toxins 11:72 Niere BI, Speijer PR, Gold CS, Sikora RA (1999) Fungal endophytes from bananas for the biocontrol of Radopholus similis. Review of IPM research activities. pp 313–318 Oostenbrink M (1960) Estimating nematode populations by some selected methods. In: Sasser JN, Jenkins WR (eds) Nematology. University of North Carolina, Chapel Hill, pp 85–102 Park MS, Ahn J, Choi GJ, Choi YH, Jang KS, Kim JC (2010) Potential of the volatile producing fungus Nodulisporium sp. CF016 for the control of postharvest diseases of apple. Plant Pathol J 26:253–259 Park YH, Kim Y, Mishra RC, Bae H (2015) Fungal endophytes inhabiting mountain-cultivated ginseng (Panax ginseng Meyer): Diversity and biocontrol activity against ginseng pathogens. Sci Rep 7:16221 Parra D, Sánchez L (2005) El control de la moniliasis en el cacao. INIA Divulga 6:23–26 Paulraj MG, Reegan AD, Ignacimuthu S (2011) Toxicity of benzaldehyde and propionic acid against immature and adult stages of aedes aegypti (Linn.) and Culex quinquefasciatus (Say) (Diptera: Culicidae). J Entomol 8:539–547 Pederson JF, Rodriguez-Kabana R, Shelby RA (1988) Ryegrass cultivars and endophyte in tall fescue affect nematodes in grass and succeeding soybean. Agron J 80:811–814 Pocasangre LE (2000) Biological enhancement of banana tissue culture plantlets with endophytic fungi for the control of the burrowing nematode Radopholus similis and the Panama disease (Fusarium oxysporum f. sp. cubense). Ph.D. thesis, University of Bonn, Germany, p 107 Popay AJ, Mainland RA (1991) Seasonal damage by Argentine stem weevil to perennial ryegrass pastures with different levels of Acremonium lolii. In: Proceedings of the 44th New Zealand weed and pest control conference. pp 171–175 Prior C (1979) Resistance of cocoa to vascular-streak dieback disease. Ann Appl Biol 92:369–376 Quesada-Moraga E, Muñoz-Ledesma FJ, Santiago-Alvarez C (2009) Systemic protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environ Entomol 38:723–730 Rana KL, Kour D, Yadav AN (2019) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge Romero YMM, Flores GR, Rubalcava MLM (2017) Volatile organic compounds from endophytic fungi as innovative postharvest control of Fusarium oxysporum in cherry tomato fruits. Appl Microbiol Biotechnol 101:8209–8222

6  Fungal Endophytes: A Source for Biological Control Agents

215

Saad MMG, Ghareeb RY, Saeed AA (2019) The potential of endophytic fungi as bio-control agents against the cotton leafworm, Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). Egyptian J Biol Pest Control 29:7 Samuels GJ, Ismaiel A, Rosmana A, Junaid M, Guest D, Mcmahon P, Keane P, Purwantara A, Lambert S, Rodriguez-Carres M, Cubeta MA (2012) Vascular streak dieback of cacao in Southeast Asia and Melanesia: in planta detection of the pathogen and a new taxonomy. Fungal Biol 116:11–23 Sánchez M, Jaramillo E, Ramírez I (2015) Enfermedades del cacao, 1st edn. Editorial UTMACH, Machala, p 80 Sánchez-Ortiz BL, Sánchez-Fernandez RE, Duarte G, Lappe-Oliveras P, Macias-Rubalcava ML (2016) Antifungal, anti-oomycete and phytotoxic effects of volatile organic compounds from the endophytic fungus Xylaria sp. strain PB3f3 isolated from Haematoxylon brasiletto. J Appl Microbiol 120(5):1313–1325 Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreño ÁM, García-Mina JM, Del Campillo MC, Quesada-Moraga E (2018) An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae. Biol Control 116:90–102 Saxena S, Meshram V, Kapoor N (2014) Muscodor darjeelingensis, a new endophytic fungus of Cinnamomum camphora collected from northeastern Himalayas. Sydowia 66(1):55–67 Saxena S, Meshram V, Kapoor N (2015) Muscodor tigerii sp. nov.-volatile antibiotic producing endophytic fungus from the Northeastern Himalayas. Ann Microbiol 65(1):47–57 Schuster RP, Sikora RA, Amin N (1995) Potential of endophytic fungi for the biological control of plant parasitic nematodes. Med Fac Landbouww Univ Gent 60:1047–1052 Sheridan JE, Grbavac N (1979) Cereal root knot nematode, Meloidogyne naasi Franklin, on barley in New Zealand. Australas Plant Pathol Newsl 8:53–54 Siegel MR, Dahlman DL, Bush LP (1989) The role of endophytic fungi in grasses: new approaches to biological control of pests. In: Leslie AR, Metcalf RL (eds) Integrated pest management for turfgrass and ornamentals. US-EPA, Washington, DC, pp 169–186 Sikora RA (1992) Management of the antagonistic potential in agricultural ecosystems for the control of plant parasitic nematodes. Annu Rev Phytopathol 30:245–270 Singh SK, Strobel GA, Knighton B, Geary B, Sears J, Ezra D (2011) An Endophytic Phomopsis sp. possessing bioactivity and fuel potential with its volatile organic compounds. Microb Ecol 61(4):729–739 Siri-udom S, Suwannarach N, Lumyong S (2016) Existence of Muscodor vitigenus, M. equiseti and M. heveae sp. nov. in leaves of the rubber tree (Hevea brasiliensis Müll.Arg.), and their biocontrol potential. Ann Microbiol 66:437–448 Stinson AM, Zidack NK, Strobel GA, Jacobsen BJ (2003) Mycofumigation with Muscodor albus and Muscodor roseus for control of seedling diseases of sugar beet and Verticillium Wilt of eggplant. Plant Dis 87:1349–1354 Strobel GA, Kluck K, Hess WM, Sears J, Ezra D, Vargas PN (2007) Muscodor albus E-6, an endophyte of Guazuma ulmifolia making volatile antibiotics: isolation, characterization and experimental establishment in the host plant. Microbiology 153:2613–2620 Strobel GA, Spang S, Kluck K, Hess WM, Sears J, Livinghouse T (2008) Synergism among volatile organic compounds resulting in increased antibiosis in Oidium sp. FEMS Microbiol Lett 283:140–145 Strobel G, Singh SK, Riyaz-Ul-Hassan S, Mitchell AM, Geary B, Sears J (2011) An endophytic/ pathogenic Phoma sp. from creosote bush producing biologically active volatile compounds having fuel potential. FEMS Microbiol Lett 320:87–94 Suwannarach N, Bussaban B, Hyde KD, Lumyong S (2010) Muscodor cinnamomi, a new endophytic species from Cinnamomum bejolghota. Mycotaxon 15(114):15–23 Suwannarach N, Kumla J, Bussaban B, Lumyong S (2012) Biocontrol of Rhizoctonia solani AG-2, the causal agent of damping-off by Muscodor cinnamomi CMU-Cib 461. World J Microbiol Biotechnol 28:3171–3177

216

H. K. Santra and D. Banerjee

Suwannarach N, Kumla J, Bussaban B, Hyde KD, Matsui K, Lumyong S (2013) Molecular and morphological evidence support four new species in the genus Muscodor from northern Thailand. Ann Microbiol 63:1341–1351 Suwannarach N, Bussaban B, Nuangmek W, Pithakpol W, Jirawattanakul B, Matsui K, Lumyong S (2015) Evaluation of Muscodor suthepensis strain CMU-Cib462 as a postharvest biofumigant for tangerine fruit rot caused by Penicillium digitatum. J Sci Food Agric 96(1):339–345 Ting ASY, Mah SW, Tee CS (2010) Identification of volatile metabolites from fungal endophytes with biocontrol potential towards Fusarium oxysporum F. sp. cubense race 4. Am J Agric Biol Sci 5(2):177–182 Tran NT, Miles AK, Dietzgen RG, Drenth A (2019) Phyllosticta capitalensis and P. paracapitalensis are endophytic fungi that show potential to inhibit pathogenic P. citricarpa on citrus. Australas Plant Path 48(3):281–296 Ul-Hassan R, Strobel G, Geary B, Sears J (2013) An Endophytic Nodulisporium sp. from Central America producing volatile organic compounds with both biological and fuel potential. J Microbiol Biotechnol 23(1):29–35 Van Emden HF, Harrington R (2007) Aphids as crop pests, 2nd edn. Cabi, Wallingford Vuylsteke D (1989) Shoot-tip culture for the propagation, conservation, and exchange of Musa germplasm. Practical manuals for handling crop germplasm in vitro 2. International Board for Plant Genetic Resources, Rome, p 56 Wang SY, Lai WC, Chu FH, Lin CH, Shen SY, Chang ST (2006) Essential oil from the leaves of Cryptomeria japonica acts as a silverfish (Lepisma saccharina) repellent and insecticide. J Wood Sci 52:522–526 Woodhall JW, Lees AK, Edwards SG, Jenkinson P (2007) Characterization of Rhizoctonia solani from potato in Great Britain. Plant Pathol 56:286–295 Worapong J, Strobel GA, Ford EJ, Li JY, Baird G, Hess WM (2001) Muscodor albus anam. sp. nov. an endophyte from Cinnamomum zeylanicum. Mycotaxon 79:67–79 Worapong J, Strobel G, Daisy B, Castillo UF, Baird G, Hess WM (2002) Muscodor roseus anam. sp. nov., an endophyte from Grevillea pteridifolia. Mycotaxon 81:463–475 Yadav AN, Singh S, Mishra S, Gupta A (2019a) Recent advancement in white biotechnology through fungi. volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N, Kour D (2020b) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020d) Plant microbiomes for sustainable agriculture. Springer, Cham Yuan Y, Feng H, Wang L, Li Z, Shi Y, Zhao L (2017) Potential of endophytic fungi isolated from cotton roots for biological control against verticillium wilt disease. PLoS One 12(1):0170557 Zawadneak MAC, Vidal HR, Santos B (2015) Lagarta-da-coroa, Duponchelia fovealis (Lepidoptera: Crambidae). In: Villela E, Zucchi RA (eds) Pragas introduzidas: insetos e ácaros. ESALQ/FEALQ, Piracicaba, pp 216–231 Zawadneak MAC, Goncalves RB, Pimentel IC, Schuber JM, Santos B, Poltronieri AS, Solis MA (2016) First record of Duponchelia fovealis (Lepidoptera: Crambidae) in South America. Idesia 34(3):1–5 Zhang CL, Wang GP, Mao LJ, Komon-Zelazowska M, Yuan ZL, Lin FC, Drzhinina IS, Kubicek CP (2010) Muscodor fengyangensis sp. nov. from Southeast China: morphology, physiology and production of volatile compounds. Fungal Biol 114:797–808

Chapter 7

Aspergillus Mycotoxins: Potential as Biocontrol Agents Fatma A. Abo Nouh, Sara A. Gezaf, and Ahmed M. Abdel-Azeem

Contents 7.1  I ntroductions 7.2  A  flatoxin 7.2.1  Historical Perspective and Producing Aspergillus Species 7.2.2  Occurrence and Common Food Products Involved 7.3  Ochratoxin A 7.3.1  Historical Perspective and Producing Aspergillus Species 7.3.2  Occurrence and Common Food Products Involved 7.4  Fumonisins 7.4.1  Historical Perspective and Producing Aspergillus Species 7.4.2  Occurrence and Common Food Products Involved 7.5  Patulin 7.5.1  Historical Perspective and Producing Aspergillus Species 7.5.2  Occurrence and Common Food Products Involved 7.6  Gliotoxin 7.6.1  Historical Perspective and Producing Aspergillus Species 7.6.2  Occurrence and Common Food Products Involved 7.7  Cyclopiazonic Acid 7.7.1  Historical Perspective and Producing Aspergillus Species 7.7.2  Occurrence and Common Food Products Involved 7.8  Aspergillus Mycotoxins as Biocontrol Agents References

 217  218  218  219  220  220  221  223  223  223  224  224  225  225  225  226  227  227  228  228  230

7.1  Introductions Aspergillus species are widespread in nature; they are regarded as soil fungi, frequently colonizing plant debris and decaying agricultural crops, and are among the commonest airborne fungi. They occur with high frequency as saprophytes on a wide range of substrates, including foods and feeds, and several species are among F. A. Abo Nouh · A. M. Abdel-Azeem (*) Systematic Mycology Laboratory, Botany Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt S. A. Gezaf Botany Department, Faculty of Science, Al-Arish University, North Sinai, Egypt © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_7

217

218

F. A. Abo Nouh et al.

the typical pathogens of harvested fruits and vegetables (Barkai-Golan 2008). Mycotoxins are a group of secondary metabolites characterized by both a diversity of chemical structures and biological activities. Mycotoxigenic species can be found in all major taxonomic groups of fungi, but the genus Aspergillus is undoubtedly one of the most important (Abarca et al. 2001; Rana et al. 2019b; Yadav et al. 2017). The Aspergillus species that produce mycotoxins are more common in the warmer, subtropical, and tropical areas than in the temperate areas of the world (Wilson et al. 2002). Some of the Aspergillus species and teleomorphs that potentially produce mycotoxins include A. candidus, A. clavatus, A. flavus, A. fumigatus, A. niger, A. nomius, A. ochraceus, A. parasiticus, A. restrictus, A. tamarii, A. terreus, A. versicolor, Emericella nidulans, and Eurotium amstelodami (Wilson et al. 2002; Rana et al. 2019a; Yadav et al. 2020a). The term mycotoxin was first used in the 1960s to describe the toxin associated with contaminated peanuts in animal feed and the loss of turkeys in England (Turkey X disease). This mycotoxin was later identified as the Aspergillus flavus toxin (aflatoxin B1) (Ismaiel and Papenbrock 2015). Mycotoxins are defined as natural products produced by fungi that evoke a toxic response when introduced in low concentration to higher vertebrates and other animals by natural route (Alshannaq and Yu 2017(. Mycotoxins produced by Aspergillus have a serious impact on the health of humans and animals. The main mycotoxins produced by species belonging to Aspergillus genus are aflatoxins (B1, B2, G1, G2); ochratoxin A (OTA); fumonisins (B2 and B4); patulin (PAT); cyclopiazonic acid (CPA); gliotoxin (GT) (Abarca et al. 2001; Wilson et al. 2002; Varga et al. 2015; Perrone and Gallo 2017). Although OTA and aflatoxins are the most important Aspergillus mycotoxins in fruits, other mycotoxins synthesized by Aspergillus, such as cyclopiazonic acid, fumonisins, patulin, gliotoxin, and other secondary metabolites, may also elicit toxicological effects (Barkai-Golan 2008).

7.2  Aflatoxin 7.2.1  H  istorical Perspective and Producing Aspergillus Species The toxin of aflatoxin was first discovered in 1960 when there were increase deaths from liver disease of turkeys in England followed by deaths of other farm animals; more than 100,000 turkeys died within a few months. Scientists first called the new disease “Turkey X Disease” because they did not know its reason. It was finally founded that all birds affected had been fed with fodder prepared with contaminated groundnut meal; examination of the incriminated groundnut meal revealed the presence of mold (Liu et al. 2004). They were first identified from peanut samples in 1961 as responsible for Turkey X disease. The main causative agent was A. flavus. Since then, aflatoxin is considered as one of the most harmful mycotoxins in the world (Varga et al. 2015).

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

219

Aflatoxin term is derived from three source words, “a” from Aspergillus, “fla” from flavus, with toxin added (Obioha 1979). The aflatoxins are a group of mycotoxins structurally have related to many secondary metabolites of fungi produced by certain Aspergillus species (Gourama and Bullerman 1995), especially Aspergillus flavus, A. parasiticus, and A. nominus (Garber and Cotty 1997; Fente et al. 2001). Recently, A. ochraceoroseus and A. pseudotamari are also aflatoxin-producing species in nature, but they are less encountered with them (Li et al. 2011). The aflatoxins are extremely potent carcinogenic, teratogenic, mutogenic, hepatotoxin, with hepatocarcinogenic effects and immunosuppressive agents that cause significant damage to human and animal health (Brown et al. 1991; Razzaghi-Abyaneh et al. 2005). Aflatoxins are decaketide-derived secondary metabolites produced by a complex biosynthetic pathway which could lead to different metabolites: aflatoxin M1, M2 (Murphy et al. 2006; Amalaradjou 2008), B1, B2, G1, and G2 (Perrone and Gallo 2017). The most potent and frequently occurring of these compounds is aflatoxin B1 (Richard et al. 1993; Amalaradjou 2008). Mainly AFB1 is the most toxic and carcinogenic naturally occurring mycotoxins, and exhibits hepatocarcinogenic and hepatotoxic properties, and epidemiological data implicating AFB1 as a component of liver cancer in humans in certain parts of the world (Kocsubé et al. 2013). The International Agency for Research on Cancer (IARC) assigned all aflatoxins to group 1 (carcinogenic to humans) (Varga et al. 2015). Aflatoxins are produced in nature only by A. flavus, A. parasiticus, and a recently described species A. nomius. A. flavus is ubiquitous. A. parasiticus is apparently less widely distributed, but the extent of its occurrence may be obscured by the tendency for A. flavus and A. parasiticus to be reported only as A. flavus. A. nomius is not of practical importance (Pitt 2000). Among 18 different types of aflatoxins produced by A. flavus strains (Ismaiel and Papenbrock 2015) these toxins are produced by at least 14 species assigned to three sections of the genus Aspergillus: section Flavi (A. flavus, A. pseudotamarii, A. parasiticus, A. nomius, A. bombycis, A. parvisclerotigenus, A. minisclerotigenes, A. arachidicola, A. togoensis) (Kocsubé et al. 2013), and several other species whose importance and ecology; less importance has some aflatoxin-producing species belonging to section Nidulantes (Emericella astellata, E. venezuelensis, E. olivicola) and section Ochraceorosei (A. ochraceoroseus, A. rambellii) (Perrone and Gallo 2017). Recent data indicate that aflatoxins are produced by at least 20 species assigned to three sections of the genus Aspergillus: sections Flavi, Nidulantes, and Ochraceorosei including the newly described A. pseudonomius, A. pseudocaelatus, A. togoensis, A. mottae, A. sergii, A. transmontanensis, and A. novoparasiticus (Varga et al. 2015).

7.2.2  Occurrence and Common Food Products Involved Aflatoxins many times occur naturally on crops in the field before to harvest. Post-­ harvest contamination of foods and crops can occur if crop drying is delayed and the moisture content is allowed to exceed critical values supporting mold growth during

220

F. A. Abo Nouh et al.

storage (Amalaradjou 2008; Yadav et  al. 2019a). Aflatoxins have been found in milk, cheese, corn, peanuts, cottonseed, nuts, almonds, figs, spices, and a variety of other foods and feeds. Milk, eggs, and meat products are contaminated due to the ingestion of aflatoxin-contaminated feed by animals and birds (Amalaradjou 2008). Natural contamination of cereals (maize, wheat, and rice principally), oilseeds (cotton, peanut, rapeseed, coconut, sunflowers, and others), cassava, tobacco, and a long list of other commodities is a common occurrence (Detroy et al. 1971; Diener et al. 1987; Bennett and Klich 2003; Rizzi et al. 2003; Azziz-Baumgartner et al. 2005; Saleemullah et al. 2006; Strosnider et al. 2006; Masoero et al. 2007; Wild and Gong 2010). However, the commodities with the highest risk of aflatoxin contamination are corn, peanuts, and cottonseed. Corn attracted the attention as a commodity of greatest concern worldwide, because it is grown in climates that are likely to contaminate with aflatoxin (Heathcote and Hibbert 1978). Feeding of aflatoxin-contaminated corn and cottonseed meal to dairy cattle can result in aflatoxin M1 contaminated-milk and milk products, including non-fat dry milk, cheese, and yogurt (Amalaradjou 2008). Due to climatic factors, aflatoxins are mainly detected in products imported (e.g., Brazil nuts, pistachio nuts, peanuts, and figs) into Central Europe (Kocsubé et al. 2013). A. flavus and A. parasiticus have a particular affinity for nuts and oilseeds. Peanuts, maize, and cottonseed are the three most important crops affected (Pitt 2000). A. flavus, which is primarily known as a producer of the aflatoxins, is a frequent contaminant of corn, peanuts (Domer 2002), stored wheat, onions, grapes, rice, cattle feed, sunflower flour, and spices (Kocsubé et al. 2013).

7.3  Ochratoxin A 7.3.1  H  istorical Perspective and Producing Aspergillus Species OTA was originally isolated as a secondary metabolite from a strain of Aspergillus ochraceus in a corn meal in South Africa in 1965 (Abarca et  al. 1994; Zinedine 2010; Malir et al. 2016). Its isolation was part of a large-scale screening for aflatoxins, during the “mycotoxin gold rush” that followed the discovery of aflatoxins (Bayman and Baker 2006). In the following years, the OTA production of six other species from section Circumdati (A. melleus, A. sulphureus (Lai et al. 1970), A. ostianus, A. petrakii, A. sclerotiorum, and A. alliaceus) was reported (Hesseltine et al. 1972; Tsubouchi et  al. 1995), but A. alliaceus is now placed in section Flavi (Bayman and Baker 2006). The economically most important OTA producers belong to Aspergillus sections Circumdati and Nigri, with only two minor OTA-producing species in section Flavi (ochratoxins are produced by a range of Aspergillus species assigned to sections Circumdati, Nigri, and Flavi (Kocsubé et al. 2013; Perrone and Gallo 2017). Section

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

221

Circumdati, named also Aspergillus ochraceus group responsible for production of several mycotoxins harmful for animals and humans. The most important mycotoxin is OTA, named after the producer A. ochraceus. Some species of the section are utilized for the biochemical transformation of steroids and alkaloids, or as sources of proteolytic enzymes; while other produces several promising anticancer compounds (Frisvad et al. 2004; Perrone and Gallo 2017). Many species produce large amounts of OTA: A. pseudoelegans, A. sulphureus (Kocsubé et  al. 2013); A. steynii, A. westerdijkiae (Ismaiel and Papenbrock 2015); A. cretensis, A. fresenii, A. flocculosus (syn: A. ochraceopetaliformis), A. muricatus, A. ochraceus, A. pseudoelegans, A. pulvericola, A. roseoglobulosus, A. sclerotiorum (Perrone and Gallo 2017). In section, section Nigri OTA is produced by A. niger (Abarca et al. 1994); A. awamori, A. carbonarius (Teren et al. 1996); A. lacticoffeatus, and A. sclerotioniger (Kocsubé et al. 2013). Members of Aspergillus section Nigri are widely distributed throughout the world. Some are used in the food industry because they are good producers of organic acids and hydrolytic enzymes (Abarca et al. 2001). OTA production in A. niger is alarming because this species is used in fermentations for food and enzyme production; industrial strains should be tested for OTA production (Bayman and Baker 2006). While in Flavi, A. lanosus (Bayman and Baker 2006); A. alliaceus and A. albertensis produce OTA (Kocsubé et al. 2013; Majeed et al. 2013). The ochratoxin family consists of three members A, B, and C which differ slightly from each other in chemical structures (Ciconova et al. 2010). OTA is the most toxic mycotoxin in the group of ochratoxins (Anjorin et al. 2013). OTA may also exhibit teratogenic, genotoxic, mutagenic (Barkai-Golan 2008); carcinogenic and nephrotoxic effects, and also has been regarded as an immunosuppressive agent (Kocsubé et al. 2013).

7.3.2  Occurrence and Common Food Products Involved OTA is a mycotoxin that is a common contaminant of a wide variety of food products (plant products and animal products). The molecular structure comprises a chlorinated polyketide dihydroisocoumarin ring linked to phenylalanine and, as shown in different producing fungal species, a polyketide synthase (PKS) is a major part of the biosynthetic pathway (Wang et  al. 2016). Because of its widespread occurrence on a large variety of agricultural commodities and the potential health risks, mainly toward humans, OTA has been classified as a possible human carcinogen (group 2B) by the International Agency for Research on Cancer (Ismaiel and Papenbrock 2015; Frisvad et al. 2018). OTA have been detected in several agricultural products from temperate and tropical zones (Adegoke and Letuma 2013). OTA is found mainly in cereal and cereal products starting in the 1960s (Abarca et  al. 2001; Barkai-Golan 2008; Kocsubé et  al. 2013; Perrone and Gallo 2017). Higher amounts of OTA were produced on wheat than on other substrates (Zinedine

222

F. A. Abo Nouh et al.

2010; Wang et al. 2016). OTA is found in wheat, barley, rye corn, oats (Abarca et al. 2001; Wilson et al. 2002; Stoev 2013; Adegoke and Letuma 2013), maize (Abarca et al. 2001), rice (Abarca et al. 2001; Stoev 2013; Alshannaq and Yu 2017), and cassava flour (Zain 2011; Adegoke and Letuma 2013). More recently, besides cereals and cereal products OTA is found in a range of other food commodities, including legumes (Abarca et al. 2001; Bayman et al. 2002; Bayman and Baker 2006; Barkai-­ Golan 2008; Perrone and Gallo 2017), coffee beans (Nakajima et al. 1997; Bucheli et al. 2000), cocoa beans, dried fruits (Pitt 2000; Bayman et al. 2002; Aish et al. 2004; Barkai-Golan 2008), peanuts (Pitt 2000; Zain 2011; Adegoke and Letuma 2013; Kocsubé et  al. 2013; Stoev 2013; Perrone and Gallo 2017). Grapes, wine (Abarca et  al. 2001; Wilson et  al. 2002; Battilani and Pietri 2002; Adegoke and Letuma 2013; Stoev 2013; Ostry et al. 2017; Perrone and Gallo 2017), beers, spices (Aziz et al. 1998; Bayman and Baker 2006; Aish et al. 2004), baby foods, crackers, raisins, pecans, figs (Wilson et  al. 2002); raisins (Abarca et  al. 2001); pulses (Kocsubé et al. 2013; Perrone and Gallo 2017), and oilseeds (Wang et al. 2016). OTA can also contaminate animal-derived products, such as meat (Pitt 2000; Bayman et  al. 2002; Wilson et  al. 2002; Perrone and Gallo 2017), pork, poultry meat (Nakajima et al. 1997; Bucheli et al. 2000), milk (Barkai-Golan 2008; Stoev 2013), fish and eggs (Adegoke and Letuma 2013). The fungi responsible for OTA contamination vary from crop to crop and from place to place. OTA found in cereals in storage is primarily produced by growth of Penicillium verrucosum, and perhaps the associated Aspergillus species, A. ochraceus and A. ostianus (Wilson et al. 2002). A. ochraceus is likely the most important Aspergillus species involved with OTA contamination in storage (Wilson et  al. 2002). In contrast, A. ochraceus is most commonly found in dried and stored foods, such as smoked and salted dried fish, soya beans, chick peas, nuts, pepper, and dried fruit. It has been reported infrequently in cereals and green coffee beans. A. ochraceus is generally present at low levels and rarely causes spoilage (Aish et al. 2004). The most important toxin of the group is OTA; generally A. ochraceus prefers to grow in hot-tropical regions (Alshannaq and Yu 2017). OTA is produced by A. carbonarius in grapes, wines, and vine fruits, and by A. ochraceus sometimes in coffee beans (Pitt 2000; Bayman and Baker 2006). A. carbonarius its major habitat is dried vine fruit. It is therefore the main source of OTA in grapes and grape products, such as raisins and wine. A. niger is often found in association with A. carbonarius and is commonly isolated from nuts, fresh fruit, and some vegetables in warm climates (Aish et  al. 2004). The most important species regarding potential OTA production in coffee, rice, beverages, and other foodstuffs are A. ochraceus, A. westerdijkiae, and A. steynii (Frisvad et al. 2004); and recently, in two newly described species from coffee A. lacticoffeatus and A. sclerotioniger (Samson et al. 2004; Bayman and Baker 2006). Aspergillus species producing OTA in fruits include: A. ochraceus, A. carbonarius, A. niger, A. tubingensis, A. sclerotiorum, A. sulphureus, A. aculeatus, A. japonicus var. aculeatus, A. alliaceus, A. melleus (Barkai-Golan 2008).

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

223

7.4  Fumonisins 7.4.1  H  istorical Perspective and Producing Aspergillus Species Fumonisins were discovered only recently as the result of many years of study of the disease known as leukoencephalomalacia (LEM) (Pitt 2000). Fumonisins were first isolated in 1988 from cultures of F. verticillioides strain MRC 826 at the Programme on Mycotoxins and Experimental Carcinogenesis (PROMEC) of the Medical Research Council (MRC) in South Africa (Jackson and Jablonski 2004). Fumonisins are mycotoxins produced by group of Fusarium fungi commonly found on crops, produced mainly by Fusarium verticillioides and F. proliferatum, and producing by group of Aspergillus fungi. The most common species are A. flavus and A. niger, A. welwitschiae, A. parasiticus, A. ochraceus, A. carbonarius, A. tubingensis, A. nomius, A. alliaceus, and recently also A. westerdijkiae and A. steynii (Perrone and Gallo 2017). Most of these reports claimed that A. niger produced only fumonisins B2 and B4 (Kocsubé et al. 2013). Fumonisin B (FB) analogs are the most common among which FB1 predominates on FB2 and FB3, while FB4 is detected in insignificant amounts (Gelderblom et  al. 1988; Munkvold and Desjardins 1997; Pagliuca et  al. 2005; Afolabi et  al. 2007; Dall’Asta et al. 2009; Gazzotti et al. 2011; Bryła et al. 2013). FB1 can cause two diseases to animals: leucoencephalomalacia in horses and porcine pulmonary edema. It is also carcinogenic, hepatotoxic, and embryotoxic in laboratory animals. In humans fumonisins can cause esophageal cancer and neural tube defects (Marasas 2001; Missmer et al. 2006; Scott 2012). The IARC evaluated FB1 as a Group 2B carcinogen. However FB2 was reported as more cytotoxic than FB1 (Perrone and Gallo 2017).

7.4.2  Occurrence and Common Food Products Involved Fumonisins are natural contaminants of cereal grains worldwide and are mostly found in corn and products derived from corn (Jackson and Jablonski 2004). Fumonisins are mycotoxins which frequently contaminate maize and maize products worldwide. Limits for total fumonisins B1 and B2 have been set for cereals and cereal-based products (Perrone and Gallo 2017). Findings of fumonisins in grains (other than maize and sorghum) and grain-based products and found in a wide variety of other foods such as garlic bulbs (Seefelder et al. 2002; Scott 2012), black tea (Martins et al. 2001; Omurtag and Yazicioglu 2004; Scott 2012), garlic (powder), onion powder (Boonzaaijer et al. 2008; Scott 2012), fig (Senyuva and Gilbert 2008; Scott 2012), peanuts (Sangare-Tigori et al. 2006; Liu et al. 2008; Njobeh et al. 2010; Scott 2012), and soybeans (Scott 2012). While FB1 has been detected in cow’s milk (Gazzotti et al. 2009; Scott 2012). Fumonisins have been found in medicinal wild

224

F. A. Abo Nouh et al.

plants in South Africa (Sewram et al. 2006; Scott 2012). Found also in mint and stinging nettle in Turkey (Omurtag and Yazicioglu 2004; Scott 2012) and sage leaves, valerian root (Santos et al. 2009; Scott 2012). Of particular note and interest is that for some foods, FB1 is not the major fumonisin as it is for maize and other grains. Of current concern is the occurrence of FB2 in wine (Logrieco et al. 2010), in beer (Romero-González et al. 2009) and, together with FB4, in coffee (Noonim et al. 2009; Scott 2012). In recent years, FB2 produced by Aspergilli was detected in coffee beans, beer, other grain-based products, barley, and wheat (Perrone and Gallo 2017). Black Aspergilli were suspected to be responsible for fumonisin contamination of grape-derived products, figs, and onions (Kocsubé et  al. 2013). Among Aspergilli, A. niger and A. welwitschiae are fumonisin producers. A. niger is frequently detected on grape-derived products, while A. welwitschiae infects onions and Welwitschiae mirabilis (Varga et al. 2015).

7.5  Patulin 7.5.1  H  istorical Perspective and Producing Aspergillus Species Patulin (PAT) was originally isolated and named as claviformin due to its isolation from Penicillium claviforme, later it was renamed PAT according to the PAT-­ producing mold, P. patulum (now P. griseofulvum) (Ismaiel and Papenbrock 2015). PAT is a water-soluble lactone first isolated as an antibiotic during the 1940s. Owing to co-discovery of the compound by various groups, it has historically been known by names such as clavicin, clavitin, expansin, gigantic acid, leucopin, mycoin, penicidin, and tercinin. Initially isolated as a broadspectrum antifungal antibiotic, it was later found to inhibit more than 75 different bacterial species including both Gram-­ positive and Gram-negative bacteria (Moake et  al. 2005). The early findings that PAT had antibiotic activity led to its testing against the common cold in humans. PAT was soon found almost useless in curing the common cold and was too toxic for use as an antimicrobial agent (Ismaiel and Papenbrock 2015). During the 1960s it was found to be toxic to biological systems comprising of bacteria, mammalian cell cultures, higher plants, and animals. The adverse effects of patulin in biological systems are genotoxicity, carcinogenicity, embryotoxicity, and teratogenicity, immunotoxicity, and genotoxicity (Erdoğan et al. 2014). PAT is a fungal secondary metabolite that produced by some Penicillium, Aspergillus, and Byssochlamys mold species (Kadakal and Nas 2002). PAT has been isolated from Aspergillus terreus (Jiménez et al. 1991), A. clavatus, A. giganteus, A. longivesica (Varga et al. 2007). Several Aspergillus species are also able to produce patulin, including species assigned to Aspergillus sections Clavati and Terrei (Kocsubé et al. 2013). Among the Aspergillus species, the number of patulin producing species is limited to three of the Clavati group: A. clavatus, A. giganteus, and A. longivesica (Puel et al. 2010).

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

225

7.5.2  Occurrence and Common Food Products Involved Patulin is first of all found in pomaceous foods like apples and pears, but also in other fruits (Frisvad 2018). In nature, PAT is found commonly in different products and especially in apples and apple products in which these molds can grow. The results of experiments on animals have shown that patulin is mutagenic, carcinogenic, and teratogenic (Kadakal and Nas 2002). While it predominantly contaminates apples, apple juice, and apple products, other fruit including pears, peach, and grapes may also be vulnerable to patulin contamination (Moake et al. 2005). Several studies have shown that patulin is stable in dry cereals, and in apple and grape juice (Speijers 2004), apricots, grapes, grape fruit, peaches, pears, apples, olives and cereals (Laidou et al. 2001; Kadakal and Nas 2002; Adegoke and Letuma 2013), dried fig (Senyuva and Gilbert 2008). PAT has been detected in apples and apple products, and occasionally in other fruits such as pears, apricots, peaches, and grapes. It has also become a quality indicator of fruit used for the production of apple juice concentrates. It is mainly produced in rotten parts of the fruits after infestation with PAT-producing fungus that can occur at 0  °C during storage or develops rapidly when fruits are returned to room temperature. PAT also appears to increase after storage when fruits remain at room temperature (20  °C) for short periods of time, a common procedure in fruit processing industries (Ismaiel and Papenbrock 2015). The contamination of PAT in fruit and fruit-derived products, especially in apple and derived products is very common worldwide (Alshannaq and Yu 2017). A. clavatus have been found to produce patulin in varieties of fruits, also A. sydowii, and A. oryzae in grapes (Erdoğan et al. 2014).

7.6  Gliotoxin 7.6.1  H  istorical Perspective and Producing Aspergillus Species Gliotoxin (GT) is a first epipolythiodioxopiperazine (ETP’s) reported and is the best characterized. Its name was derived from its identification as a metabolite of Gliocladium fimbriatum first isolated from cultures of the fungus Gliocladium fimbriatum (Nouri et al. 2015). GT is a sulfur-containing mycotoxin produced by several fungal species belonging to genera including Penicillium, Gliocladium, Thermoascus, and Aspergillus (Sugui et  al. 2007). Regarding Aspergillus, GT is produced by A. fumigatus and related species in section Fumigati including A. denticulatus, A. cejpii, and A. pseudofischeri. Even though pathogenic Aspergillus including A. niger, A. flavus, and A. terreus, and A. chevalieri (Varga et al. 2015), the most abundantly produced gliotoxins A. fumigatus, which exhibits a diverse array of biologic effects on the immune system (Lewis et al. 2005). A. fumigatus produces a variety of secondary metabolites, including gliotoxin, and this mycotoxin has received considerable attention for over two decades as a

226

F. A. Abo Nouh et al.

putative virulence factor based on the following observations: (1) up to 93% of A. fumigatus strains recovered from cancer patients with IA produced gliotoxin compared to less than 20% of the environmental isolates (2) A. fumigatus is the most prolific producer of gliotoxin among the pathogenic Aspergillus species tested (Sugui et  al. 2007). Production of gliotoxin from clinical isolates of various Aspergillus species indicated that most of the A. fumigatus isolates produced gliotoxin (95%) in comparison with other Aspergillus species (Kupfahl et al. 2008). The amount of toxin produced by A. fumigatus was substantially higher than the amount produced by other less frequent species of pathogenic Aspergillus including A. terreus and A. flavus. The most common species of Aspergillus that cause invasive aspergillosis world-­ wide are A. fumigatus, A. terreus, A. flavus, and A. niger. Although all the species produce gliotoxin, not every strain is a gliotoxin producer (Kwon-Chung and Sugui 2009). GT is an alkaloid with a low molecular size which has been known to possess a number of immunosuppressive activities, such as inhibition of superoxide release, migration, microbicidal activity cytokine release by leukoyctes, and T-lymphocyte-­ mediated cytotoxicity (Kamei and Watanabe 2005), also have genotoxic, cytotoxic, and apoptotic effects. A recent study demonstrated the presence of gliotoxin in cattle feedstuff. However, information is scarce about the presence of A. fumigatus and its mycotoxins in other feedstuffs (Pena et al. 2010). This mycotoxin has been suspected as one of the most likely virulence determinants among various secondary metabolites produced by the species (Nouri et al. 2015).

7.6.2  Occurrence and Common Food Products Involved There are reports of gliotoxin being confirmed in silage, hay, and straw and a number of studies of the metabolites formed by strains of A. fumigatus isolated from these feeding stuffs have been shown to produce gliotoxin in culture (Kurbatskaya and Trotstanetskii 1987). Previous studies claimed that environmental isolates of A. fumigatus rarely produce gliotoxin, in contrast to clinical isolates (Lewis et al. 2005). Kosalec et al. (2005) studied the in vitro production of gliotoxin in clinical strains of A. fumigatus and demonstrated that incubation at 37 °C resulted in higher gliotoxin production than at 25 °C. They found that gliotoxin was produced during mycelial growth (Keller et al. 2012). Other studies showed the isolation of A. fumigatus from cereal grains and other animal feed silages with ability to produce gliotoxin (Garon et al. 2006; Kupfahl et al. 2008; Richard et al. 2009). The A. fumigatus strains isolated from mixed cattle feed had higher gliotoxin levels than those isolated from corn silage (Pereyra et al. 2008). Keller et al. (2012) reported that high percentage of strains among A. fumigatus and related species isolated from pre- and post-fermented samples such as corn, sorghum, and wet brewer’s grains silage were able to produce gliotoxin. The A. fumigatus could be

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

227

grown on all culture media used to produce gliotoxin, but the substrates varied in their ability to induce gliotoxin production. Researchers recorded gliotoxin in agricultural substrates e.g. oats and hay (Scudamore and Livesey 1998) and corn (Alonso et al. 2013). Recently according to Nouri et al. (2015) in rice and barley media the growth of the isolate was better than in corn and wheat media. A rice medium is the best culture medium for gliotoxin production from A. fumigatus isolates. And also has the advantage of being quick, easy, cheap, and available.

7.7  Cyclopiazonic Acid 7.7.1  H  istorical Perspective and Producing Aspergillus Species Cyclopiazonic acid (CPA) is a mycotoxin that producing by strain of Aspergillus and Penicillium, which is an indole-derived compound and is a stable compound that tolerates a broad range of temperature, was first detected in 1968 as a metabolite of Penicillium cyclopium in groundnuts (Holzapfel 1968). The original isolate (P. cyclopium) was later referred to as P. griseofulvum and P. verrucosum var. cyclopium) Domer 2002). However, some strains of Aspergillus are also producers of CPA mycotoxin such as A. flavus (Luk et al. 1977; Trucksess et al. 1987). At the outbreak of Turkey X disease in Britain in the early 1960s may well have been a combination of aflatoxin and CPA, which are often produced concurrently (Trucksess et al. 1987; Gallagher et al. 1978). Further, empirical evidence indicates that commercial samples of CPA may be contaminated with, among other things, aflatoxin, yielding sometimes variable and confusing experimental data (Voss et al. 1990). Similarly to aflatoxins, CPA also been detected in both the mycelium and the sclerotia of A. flavus (Wicklow and Cole 1982: Barkai-Golan 2008). Other Aspergillus, including A. versicolor, A. oryzae, and A. tamarii have also been recorded as CPA producers (Dorner 1983; Dorner et al. 1984). CPA is consider as serious mycotoxins that cause degenerative disease and necrosis in the liver, spleen, pancreas, kidney, salivary glands, myocardium, heart, digestive tract, and skeletal muscles (Cole 1984; Barkai-Golan 2008). CPA was found to be sub-acutely toxic to rats, swine, guinea pigs, dogs, and poultry, involving several vital organs (Voss et al. 1990). Recently, the main producers of Claiming Aspergilli, several species in section Flavi including A. flavus, A. minisclerotigenes, A. oryzae, A. parvisclerotigenus, A. pseudocaelatus, A. pseudotamarii, A. tamarii, A. bertholletius, in section Versicolores including A. versicolor, and in section Fumigati including A. lentulus and A. fumisynnematus (Varga et al. 2015).

228

F. A. Abo Nouh et al.

7.7.2  Occurrence and Common Food Products Involved Molds may be divided into two main groups, namely the field fungi and the storage fungi. The former group CPA contains those species that proliferate in and under field conditions and that do not multiply once the grain is in storage. Thus, for instance, the CPA producing spp., commonly found on crops, is seldom found after about 6 weeks storage (Burdock and Flamm 2000). Natural occurrence of CPA has been reported in a variety of commodities including: millet (Lalitha Rao and Husain 1985; Amalaradjou 2008), Pinto beans (Trucksess et al. 1987), walnuts, Penguin, Brazil “Macuco” bird (Gallagher et al. 1978), rice, brown sausage (Norred et  al. 1987), corn (Urano et  al. 1992; Aresta et al. 2003; Amalaradjou 2008), peanuts (Urano et al. 1992), maize (Urano et al. 1992; Amalaradjou 2008), cheese (Le Bars 1990), sunflower (Ross et  al. 1991), tomato products (Motta and Soares 2001; Amalaradjou 2008). The toxin has also been accumulating in meat and eggs of chickens (Norred et al. 1988; Domer et al. 1994) and the milk of sheep (Domer et al. 1994) dosed with CPA)Domer 2002). Several A. flavus strains isolated from vine fruits produced cyclopiazonic acid, while all the A. tamarii strains isolated from fig orchards were cyclopiazonic acid producers (Barkai-Golan 2008).

7.8  Aspergillus Mycotoxins as Biocontrol Agents Mycotoxins are defined as the chemicals synthesized by fungi and released as toxic secondary metabolites. Mycotoxins might play a role in terms of economic and safe farming procedure (Yadav et al. 2019b, 2020c; Rastegari et al. 2020a). The effects of mycotoxins on insects have already been addressed by several research groups 50 years ago (Schrögel and Wätjen 2019). Insects encounter mycotoxins when they consume fungus-infected mummy fruits from their host plants. Mycotoxins can cause toxicity to insects, including insecticidal effects and developmental delay (Zeng et al. 2006). There are many reports concerning the toxicity of mycotoxins towards insects (Rastegari et  al. 2020b; Yadav et  al. 2020b). AFB1 proved to be harmful to Drosophila melanogaster, Aedes aegypti, Heterotermes indicola, Heliothis virescens, Corcyra cephalonica, mycophagous mites, Musca domestica, Locusta migratoria, Schistocerca gregoria, and Tenebrio molitor (Reiss 1975). There is variable sensitivity of insects to aflatoxin toxicity, initially examined in the fruit fly D. melanogaster (Alderman and Marth 1976), drosophila with larval growth in media contaminated with AFB1 leading to decreased viability, and small pupal case (Bettinger and Chinnici 1991). PAT had insecticidal activity towards D. melanogaster and Lucilia sericata. In concentrations of 20, 10, and 1 pg/cma PAT had strong insecticidal activities (Reiss 1975). D. melanogaster larvae, which feed naturally on fermenting fruits, exhibit significantly altered development on diets containing low AFB1 concentrations (i.e., less than 1 ppm); larvae feeding on

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

229

higher concentrations will die (Niu et al. 2009). Toll-deficient D. melanogaster was significantly less susceptible to GT of the A. fumigatus (Kwon-Chung and Sugui 2009) Zeng et  al. (2006) described toxicity of AFB1 to the corn earworm (CEW) (Helicoverpa zea) (Lepidoptera: Nuctuidae) larvae at different larval stages. For newly hatched first instar larvae 20 ng/g AFB1 caused 50% mortality while a higher concentration 200 ng/g AFB1 caused 100% mortality. Pupal weight of the larvae fed with 1 ng/g AFB1 in diet was significantly decreased compared with control insects. Low concentrations of AFB1 in the diet of first instars (less than 100 ng/g) can affect development, causing delayed pupation and reduced pupal weight; higher concentrations of AFB1 (200 ng/g) are lethal (Zeng et al. 2006). Spores of Aspergillus flavus have been observed to be highly pathogenic to freshly emerged house flies (Musca domestica (Diptera: Muscidae) by ingestion or even by contact (Amonkar and Nair 1965). A. flavus showed developmental toxicity also to rice moth larvae (Hedge et al. 1967). Feeding aflatoxin to larvae of mosquitos and house flies as well as to young Heliothis virescens (Lepidoptera: Nuctuidae) led to high mortality rates (Schrögel and Wätjen 2019). Abado-Becognee et  al. (1998) investigated the effect of fumonisin B1 on the growth and metabolism of yellow mealworm molitor. The presence of fumonisin B1 at a concentration of 450 μg/g diet reduced larval growth and metabolism for several weeks, but did not increase mortality (Broekhoven et al. 2014). Guo et al. (2014) observed the parameters of food choice, weight gain, and mortality for larvae T. molitor when reared on wheat grains colonized by various Fusarium species. Compared to the control grain several grains were avoided by the larvae while others were preferred by the larvae, which correlated with larval feeding behavior and weight gain. However, larvae were not always able to sense threats derived from infested grain, as among the preferred grains one grain which was colonized by Fusarium culmorum led to increased mortality (Schrögel and Wätjen 2019). The growth rate of yellow mealworm larvae is decreased also by AFB1 and OTA (Schrögel and Wätjen 2019). The A. flavus isolates were obtained from coconut insect pests naturally colonized cadavers of Stephanitis typica (lace bug) (nymphs and adults), Opisina arenosella (leaf-eating caterpillar) (larval stages), and Proutista moesta (plant hopper) (adults). The laboratory bioassay conducted with these fungi on the respective hosts yielded 80% mortality of S. typica nymphs within 3 days; 80–90% O. arenosella larvae were mycosed within 3–4 days (Gopal et al. 2000a) and 62.5% P. moesta insects died within 4 days (Ponnamma et al. 2000) under laboratory conditions. The mortality was 100% when the experiment was continued for 2–3 days more. The ideal spore concentration for achieving 100% mortality in short period (5–6 days) was 106 spores ml−1 (Gopal et al. 2000b). In response to A. flavus infection, within 24 h, the insects became lethargic, refused food indicating loss of appetite, and did not respond to external stimuli. After death due to fungal parasitism, their body became mummified and brittle (Gupta and Gopal 2002). In this background, the toxigenic nature of A. flavus isolates (AF1 and AF2) pathogenic to S. typica, O.

230

F. A. Abo Nouh et al.

arenosella, and P. moesta tested for their possible use as biological control agents against some of the insect pests of coconut(Gupta and Gopal 2002). The navel orange worm (NOW) (Amyelois transitella) (Lepidoptera: Pyralidae) is a serious crop pest that attacks almonds, pistachio, walnuts, and figs, causing millions of dollars of agricultural damage in the United States (Connell 2001; Campbell et al. 2003; Burks and Brandl 2004). Niu et al. (2009) demonstrated the extremely high tolerance of A. transitella to concentrations of AFB1 and OTA and showed that this tolerance exceeds that of other mycotoxin-associated species such as H. zea. The concentrations analyzed did not kill A. transitella when administered at early developmental stages and caused only marginal sub lethal effects. Comparisons of the toxicological effects in A. transitella and H. zea demonstrated that A. transitella larvae are 100 times more tolerant of AFB1 than H. zea and also are significantly more resistant to OTA. GT has been demonstrated to inhibit the growth of an array of different fungal species including A. nidulans, A. terreus, A. niger and has been utilized as an antifungal, antibiotic, most notably in the treatment of soilborne fungi (Howell & Stipanovic 1995; Aliaa 2008; Losada et al. 2009). Similarly, GT has been demonstrated to possess antibacterial properties inhibiting proteasomal activity in certain bacterial strains (Toxoplasma gondii and Plasmodium falciparum and ultimately growth (Paugam et al. 2002; Hatabu et al. 2006). Patulin has also been evaluated for control of several plant pathogens, including downy mildew of cucumbers, damping off of safflower, crown gall, and loose smut of wheat (Stott and Bullerman 1975). Strong fungistatic activity by PAT against Rhizopus nigricans, Monilia albicans, and Sporotrichum schenckii but no effect upon Aspergillus clavatus a PAT producer (Stott and Bullerman 1975). PAT was initially suggested for treatment of common cold, as it is anti-viral in addition to being antibacterial, but the trials on humans were quickly dropped because of the toxicity of PAT (Frisvad 2018).

References Abado-Becognee K, Fleurat-Lessard F, Creppy EE, Melcion D (1998) Effects of fumonisin B1 on growth and metabolism of larvae of the yellow mealworm Tenebrio molitor. Entomol Exp Appl 86:135–143 Abarca ML, Bragulat MR, Sastella G, Cabañas FJ (1994) Ochratoxin A production by strains of Aspergillus niger var. niger. Appl Environ Microbiol 60(7):2650–2652 Abarca ML, Accensi F, Bragulat MR, Cabañas FJ (2001) Current importance of ochratoxin A-producing Aspergillus spp. J Food Prot 64(6):903–906 Adegoke GO, Letuma P (2013) Mycotoxin and food safety in developing countries, strategies for the prevention and reduction of mycotoxin in developing countries. In: Makun HA (ed) Mycotoxin and food safety in developing countries. InTech, Rijeka, pp 123–136 Afolabi CG, Ojiambo PS, Ekpo EJA, Menkir A, Bandyopadhyay R (2007) Evaluation of maize inbred lines for resistance to Fusarium ear rot and fumonisin accumulation in grain in tropical Africa. Plant Dis 91:279–286

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

231

Aish JL, Rippon EH, Barlow T, Hattersley SJ (2004) Particular mycotoxins: Ochratoxin A.  In: Magan N, Olsen M (eds) Mycotoxins in food detection and control. Springer, New  York, pp 307–338 Alderman GG, Marth EH (1976) Inhibition of growth and aflatoxin production of Aspergillus Parasiticus by citrus oils Z. Lebensm Unters Forsch 160:353–358 Aliaa RES (2008) Control of root-rot diseases of Phaseolus vulgaris using gliotoxin. Malays J Microbiol 4(1):40–43 Alonso VA, Pereyra CM, Keller LAM, Dalcero AM, Rosa CAR, Chiacchiera SM, Cavaglieri LR (2013) Fungi and mycotoxins in silage: an overview. J Appl Microbiol 115:637–643 Alshannaq A, Yu JH (2017) Occurrence, toxicity, and analysis of major mycotoxins in food. Int J Environ Res 14:632 Amalaradjou MA (2008) Detection of Penicillium, Aspergillus and Alternaria Species in fruits and vegetables. In: Barkai-Golan R, Paster N (eds) Mycotoxins in fruits and vegetables. Academic, New York, pp 225–247 Amonkar SV, Nair KK (1965) Pathogenicity of Aspergillus flavus link to Musca domestica nebulo Fabricius. J Invertebr Pathol 7:513–514 Anjorin TS, Salako EA, Makun HA (2013) Mycotoxin and food safety in developing countries, control of toxigenic fungi and mycotoxins with phytochemicals. In: Makun HA (ed) Mycotoxin and food safety in developing countries. InTech, Rijeka, pp 181–202 Aresta A, Cioffi N, Palmisano F, Zambonin CG (2003) Simultaneous determination of ochratoxin A and cyclopiazonic, mycophenolic, and tenuazonic acids in cornflakes by solid phase microextraction coupled to high-performance liquid chromatography. J Agric Food Chem 51:5232–5237 Aziz NH, Youssef YA, El-Fouly MZ, Moussa LA (1998) Contamination of some common medicinal plant samples and spices by fungi and their mycotoxins. Bot Bull Acad Sin 39:279–285 Azziz-Baumgartner E, Lindblade K, Gieseker K et al (2005) Case-control study of an acute aflatoxicosis outbreak. Environ Health Perspect 113:1779–1783 Barkai-Golan R (2008) Aspergillus mycotoxins. In: Barkai-Golan R, Paster N (eds) Mycotoxins in fruits and vegetables. Academic, New York, pp 115–151 Battilani P, Pietri A (2002) Ochratoxin A in grapes and wine. Eur J Plant Pathol 108:639–643 Bayman P, Baker JL (2006) Ochratoxins: a global perspective. Mycopathologia 162:215–223 Bayman P, Baker JL, Doster MA, Michailides TJ, Mahoney NE (2002) Ochratoxin production by the Aspergillus ochraceus group and Aspergillus alliaceous. Appl Environ Microbiol 68(5):2326–2329 Bennett JW, Klich M (2003) Mycotoxin. Clin Microbiol Rev 16(3):497–516 Bettinger DA, Chinnici JP (1991) Utilization of response surface modeling to evaluate the interaction between aflatoxin B1 and caffeine on egg adult viability in Drosophila melanogaster. Va J Sci 42(3):311–320 Boonzaaijer G, Osenbruggen WAV, Kleinnijenhuis AJ, Dongen WDV (2008) An exploratory investigation of several mycotoxins and their natural occurrence in flavor ingredients and spices, using a multi-mycotoxin LC-MS/MS method. World Mycotoxin J 1:167–174 Broekhoven SV, Doan QHT, Huis AV, Loon JJAV (2014) Exposure of tenebrionid beetle larvae to mycotoxin-contaminated diets and methods to reduce toxin levels PROC. Neth Entomol Soc Meet 25:47–58 Brown RL, Cotty PJ, Cleveland TE (1991) Reduction in aflatoxin content of maize by atoxigenic strains of Aspergillus flavus. J Food Proc 54(8):623–626 Bryła M, Roszko M, Szymczyk K, Jędrzejczak R, Obiedziński MW, Sękul J (2013) Fumonisins in plant-origin food and fodder – a review. Food Addit Contam Pt A 30(9):1626–1640 Bucheli P, Kanchanomai C, Meyer I, Pittet A (2000) Development of ochratoxin A during robusta (Coffea canephora) coffee cherry drying. J Agric Food Chem 48:1358–1362 Burdock GA, Flamm WG (2000) Safety assessment of the mycotoxin cyclopiazonic acid. Int J Toxicol 19:195–218

232

F. A. Abo Nouh et al.

Burks CS, Brandl DG (2004) Seasonal abundance of the navel orange worm, Amyelois transitella, in figs and the effect of peripheral aerosol dispensers on sexual communication. J Insect Sci 4:40–47 Campbell BC, Molyneux RJ, Schatzki TF (2003) Current research on reducing pre- and post-­ harvest aflatoxin contamination of US almond, pistachio, and walnut. J Toxicol Toxin Rev 22:225–266 Ciconova P, Laciakova A, Mate D (2010) Prevention of Ochratoxin A contamination of food and Ochratoxin A detoxification by microorganisms – a review. Czech J Food Sci 28(6):465–474 Cole RJ (1984) Cyclopiazonic acid and related toxins. In: Betina V (ed) Mycotoxins: production, isolation, separation and purification. Elsevier, Amsterdam, pp 405–414 Connell JH (2001) Leading edge of plant protection for almond. Hort Technol 12:619–622 Dall’Asta C, Galaverna G, Mangia M, Sforza S, Dossena A, Marchelli R (2009) Free and bound fumonisins in gluten free food products. Mol Nutr Food Res 53:492–499 Detroy RW, Lillehoj EB, Ciegler A (1971) Aflatoxin and related compounds. In: Ciegler A, Kadis S, Ajl SJ (eds) Microbial toxins. Academic, New York, pp 3–178 Diener UL, Cole RJ, Sanders TH, Payne GA, Lee LS, Klich MA (1987) Epidemiology of aflatoxin formation by Aspergillus flavus. Annu Rev Phytopathol 25:249–270 Domer JW (2002) Recent advances in analytical methodology for cyclopiazonic acid. In: DeVries JW, Trucksess MW, Jackson LS (eds) Mycotoxin and food safety. Springer, New  York, pp 107–116 Domer JW, Cole RJ, Erlington DJ, Suksupath S, McDowell GH, Bryden WL (1994) Cyclopiazonic acid residues in milk and eggs. J Agric Food Chem 42:1516 Dorner JW (1983) Production of cyclopiazonic acid by Aspergillus tamarii Kita. Appl Environ Microbiol 46:1435–1437 Dorner JW, Cole RJ, Diener UL (1984) The relationship of Aspergillus flavus and Aspergillus parasiticus with reference to production of aflatoxins and cyclopiazonic acid. Mycopathologia 87:13–15 Erdoğan A, Ghimire D, Gürses M, Çetin B, Baran A (2014) Patulin contamination in fruit juices and its control measures. Eur J Sci Technol 14:39–48 Fente CA, Ordaz JJ, Vázquez BI, Franco CM, Cepeda A (2001) New additive for culture media for rapid identification of aflatoxin. Appl Environ Microbiol 67(10):4858–4862 Frisvad JC (2018) A critical review of producers of small lactone mycotoxins: patulin, penicillic acid and moniliformin. World Mycotoxin J 11(1):73–100 Frisvad JC, Frank JM, Houbraken J, Kuijpers AFA, Samson RA (2004) New ochratoxin A producing species of Aspergillus section Circumdati. Stud Mycol 50:23–43 Frisvad JC, Møller LLH, Larsen TO, Kumar R, Arnau J (2018) Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei. Appl Microbiol Biotechnol 102:9481–9515 Gallagher RT, Richard JL, Stahr HM, Cole RJ (1978) Cyclopiazonic acid production by aflatoxigenic and non aflatoxigenic strains of Aspergillus flavus. Mycopathologia 66:31–36 Garber RK, Cotty PJ (1997) Formation of sclerotia and aflatoxins in developing cotton bolls infected by the S Strain of Aspergillus flavus and potential for biocontrol with an atoxigenic strain. Phytopathology 87(9):940–945 Garon D, Richard E, Sage L, Bouchart V, Pottier D, Lebailly P (2006) Mycoflora and multimycotoxin detection in corn silage: experimental study. J Agric Food Chem 54:3479–3484 Gazzotti T, Lugoboni B, Zironi E, Barbarossa A, Serraino A, Pagliuca G (2009) Determination of fumonisin B1 in bovine milk by LC-MS/MS. Food Control 20:1171–1174 Gazzotti T, Zironi E, Lugoboni B, Barbarossa A, Piva A, Pagliuca G (2011) Analysis of fumonisins B1, B2 and their hydrolyzed metabolites in pig liver by LC–MS/MS.  Food Chem 125:1379–1384

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

233

Gelderblom WC, Jaskiewicz K, Marasas WF, Thiel PG, Horak RM, Vleggaar R, Kriek NP (1988) Fumonisins – novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl Environ Microbiol 54:1806–1811 Gopal M, Gupta A, Nair KRC, Sathiamma B, Nair CPR (2000a) Studies on cross-infectivity with entomofungal isolates of Aspergillus flavus Link. against Stephanitis typica D. and Opisina arenosella W., two pests of coconut. Indian Coconut J 31:12–15 Gopal M, Gupta A, Sathiamma B, Mohan C, Nair KRC, Soniya VP (2000b) A fungal pathogen of lace bug and leaf eating caterpillar, two insect pests of coconut palm. Coconut Res Dev 16:49–59 Gourama H, Bullerman LB (1995) Aspergillus flavus and Aspergillus parasiticus: Aflatoxigenic fungi of concern in foods and feeds: a review. J Food Prot 58(12):1395–1404 Guo Z, Doll K, Dastjerdi R, Karlovsky P, Dehne HW, Altincicek B (2014) Effect of fungal colonization of wheat grains with Fusarium spp. on food choice, weight gain and mortality of meal beetle larvae (Tenebrio molitor). PLoS One 9(6):e100112 Gupta A, Gopal M (2002) Aflatoxin production by Aspergillus flavus isolates pathogenic to coconut insect pests. World J Microbiol Biotechnol 18:325–331 Hatabu T, Hagiwara M, Taguchi N, Kiyozawa M, Suzuki M, Kano Sand Sato K (2006) Plasmodium falciparum: the fungal metabolite gliotoxin inhibits proteasome proteolytic activity and exerts a plasmodicidal effect on P. falciparum. Exp Parasitol 112:179–183 Heathcote JG, Hibbert JR (1978) Aflatoxins: chem biol aspect. Elsevier, New York, pp 173–186 Hedge UC, Chandra T, Shonmugasundaram ERB (1967) Toxicity of different diets contaminated with various fungi to rice moth larvae (Corcyra cephalonica St). Can J Comp Med Vet Sci 31:160–163 Hesseltine CW, Vandegraft EE, Fennell DI, Smith ML, Shotwell OL (1972) Aspergilli as ochratoxin producers. Mycologia 64:539–550 Holzapfel CW (1968) The isolation and structure of cyclopiazonic acid, a toxic metabolite of Penicillium cyclopium Westling. Tetrahedron 24(5):2101–2119 Howell CR, Stipanovic RD (1995) Mechanisms in the biocontrol of Rhizoctonia solani-Induced cotton seedling disease by Gliocladium virens: antibiosis. Phyopathology 85:469–472 Ismaiel AA, Papenbrock J (2015) Review mycotoxins: producing fungi and mechanisms of phytotoxicity. Agriculture 5:492–537 Jackson L, Jablonski J (2004) Particular mycotoxins: fumonisins. In: Magan N, Olsen M (eds) Mycotoxins in food detection and control. Woodhead Publishing Ltd., Cambridge, pp 367–405 Jiménez M, Mateo R, Querol A, Huerta T, Hernández (1991) Mycotoxins and mycotoxigenic moulds in nuts and sunflower seeds for human consumption. Mycopathologia 115:121–127 Kadakal C, Nas S (2002) Effect of activated charcoal on patulin levels in apple cider. Nahrung 46(1):31–33 Kamei K, Watanabe A (2005) Aspergillus mycotoxins and their effect on the host. Med Mycol 43:95–99 Keller LAM, Keller KM, Monge MP, Pereyra CM, Alonso VA, Cavaglieri LR, Chiacchiera SM, Rosa CAR (2012) Gliotoxin contamination in and pre- and post-fermented corn, sorghum and wet brewer’s grains silage in Sao Paulo and Rio de Janeiro State, Brazil. J Appl Microbiol 112:865–873 Kocsubé S, Varga J, Szigeti G, Baranyi N, Suri K, Tóth B, Toldi E, Bartók T, Mesterházy A (2013) Aspergillus species as mycotoxin producer in agriculture products in central. J Nat Sci 124:13–25 Kosalec I, Pepeljnjak S, Jandrlic M (2005) Influence of media and temperature on gliotoxin production in Aspergillus fumigatus strains. Arh Hig Rada Toksikol 56:269–273 Kupfahl C, Michalka A, Lass-Florl C, Fischer G, Haase G, Ruppert T, Geginat G, Hof H (2008) Gliotoxin production by clinical and environmental Aspergillus fumigatus strains. Int J Med Microbiol 298:319–327 Kurbatskaya ZA, Trotstanetskii AA (1987) Effect of temperature and humidity on the growth of Aspergillus fumigatus and formation of gliotoxin. Mikrobiol Zh 49:62–65

234

F. A. Abo Nouh et al.

Kwon-chung KJ, Sugui JA (2009) What do we know about the role of gliotoxin in the pathobiology of Aspergillus fumigatus? Med Mycol 47:97–103 Lai M, Semeniuk G, Hesseltine CW (1970) Conditions for production of ochratoxin A by Aspergillus species in synthetic medium. Appl Microbiol 19:542–544 Laidou IA, Thanassoupoulos CC, Kyriakides ML (2001) Diffusion of patulin in the flesh of pears inoculated with four post-harvest pathogens. J Phytopathol 149:457–461 Lalitha Rao B, Husain A (1985) (Paspalum scrobiculatum) causing ‘kodua poisoning’ in man and its production by associated fungi. Mycopathologia 89:177–180 Le Bars J (1990) Detection and occurrence of cyclopiazonic acid in cheeses. J Environ Pathol Toxicol Oncol 10(3):136–137 Lewis RE, Wiederhold NP, Lionakis MS, Prince RA, Kontoyiannis DP (2005) Frequency and species distribution of gliotoxin-producing Aspergillus isolates recovered from patients at a tertiary-care cancer center. J Clin Microbiol 43:6120–6122 Li P, Zhang Q, Zhang D, Guan D, Xiaoxia, Liu DX, Fang S, Wang X, Zhang W (2011) Aflatoxin measurement and analysis, aflatoxins – detection, measurement and control. Irineo TorresPacheco, IntechOpen. https://doi.org/10.5772/23954 Liu R, Qian Y, Thanaboripat D, Thansukon P (2004) Biocontrol of Aspergillus flavus and aflatoxin production. Kmit Sci J 4:1685–2044 Liu Q, Liu G, Liu H (2008) Investigation into status of contamination of strong carcinogen  – fumonisin in peanut, corn and their products and their rapid detection. Zhongguo Redai Yixue 8:1906–1908 Logrieco A, Ferracane R, Visconti A, Ritieni A (2010) Natural occurrence of fumonisin B2 in red wine from Italy. Food Addit Contam A 27:1136–1141 Losada L, Ajayi O, Frisvad JC, Yu J, Nierman WC (2009) Effect of competition on the production and activity of secondary metabolites in Aspergillus species. Med Mycol 47:88–96 Luk KC, Kobbe B, Townsend JM (1977) Production of cyclopiazonic acid by Aspergillus flavus Link. Appl Environ Microbiol 32:211–212 Majeed M, Asghar A, Randhawa MA, Shehzad A, Sohaib M, Abdullah (2013) Ochratoxin A in cereal products, potential hazards and prevention strategies: a review. Pak J Food Sci 23(1):52–56 Malir F, Ostry V, Leszkowicz AP, Malir J, Toman J (2016) Ochratoxin A: 50 years of research. Toxins 8(191):1–49 Marasas WFO (2001) Discovery and occurrence of the fumonisins: a historical perspective. Environ Health Perspect 109(2):239–243 Martins ML, Martins HM, Bernardo F (2001) Fumonisins B1 and B2 in black tea and medicinal plants. J Food Prot 64:1268–1270 Masoero F, Gallo A, Moschini M, Piva G, Diaz D (2007) Carryover of aflatoxin from feed to milk in dairy cows with low or high somatic cell counts. Animal 1:1344–1350 Missmer SA, Suarez L, Felkner M, Wang E, Merrill AH, Rothman KJ, Hendricks KA (2006) Exposure to fumonisins and the occurrence of neural tube defects along the Texas–Mexico border. Environ Health Perspect 114:237–241 Moake MM, Padilla-Zakour OI, Worobo RW (2005) Comprehensive review of patulin control methods in foods. Compr Rev Food Sci Food Saf 1:8–21 Motta SD, Soares LMV (2001) Survey of Brazilian tomato products for alternariol monomethyl ether, tenuazonic acid and cyclopiazonic acid. Food Addit Contam 18:630–634 Munkvold GP, Desjardins AE (1997) Fumonisins in maize: can we reduce their occurrence? Plant Dis 81:556–564 Murphy PA, Hendrich S, Landgren C, Bryant CM (2006) Food mycotoxins: an update. J Food Sci 71:51–65 Nakajima M, Tsubouchi H, Miyabe M, Ueno Y (1997) Survey of aflatoxin B1 and ochratoxin A in commercial green coffee beans by high-performance liquid chromatography linked with immunoaffinity chromatography. Food Agric Immunol 9:77–83

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

235

Niu G, Siegel J, Schuler MA, Berenbaum MR (2009) Comparative toxicity of mycotoxins to navel orange worm (Amyelois transitella) and corn earworm (Helicoverpa zea). J Chem Ecol 35:951–957 Njobeh PB, Dutton MF, Koch SH, Chuturgoon AA, Stoev SD, Mosonik JS (2010) Simultaneous occurrence of mycotoxins in human food commodities from Cameroon. Mycotoxin Res 26:47–57 Noonim P, Mahakarnchanakul W, Nielsen KF, Frisvad JC, Samson RA (2009) Fumonisin B2 production by Aspergillus niger in Thai coffee beans. Food Addit Contam A 26:94–100 Norred WP, Cole RJ, Dorner JW, Lansden JA (1987) Liquid chromatographic determination of cyclopiazonic acid in poultry meat. JAOAC 70:121–123 Norred WP, Porter JK, Domer JW, Cole RJ (1988) Occurrence of the mycotoxin cyc1opiazonic acid in meat after oral administration to chickens. J Agric Food Chern 36:113 Nouri MA, Ali AJA, Hashim AJ, Dheeb BI, Zaal AM (2015) Optimal conditions for gliotoxin production from Aspergillus fumigatus using solid state fermentation. Int J Sci Basic Appl Res 24(5):331–346 Obioha IW (1979) Distribution, production, analysis and effects of aflatoxin in animal tissues and effects of scirpene toxins on chicken embryos. Retrospective Theses and Dissertations Omurtag GZ, Yazicioglu D (2004) Determination of fumonisins B1 and B2 in herbal tea and medicinal plants in Turkey by high performance liquid chromatography. J Food Prot 67:1782–1786 Ostry V, Malir F, Toman J, Grosse Y (2017) Mycotoxins as human carcinogens-the IARC Monographs classification. Mycotoxin Res 33:65–73 Pagliuca G, Zironi E, Ceccolini A, Matera R, Serrazanetti GP, Pivac A (2005) Simple method for the simultaneous isolation and determination of fumonisin B1 and its metabolite aminopentol­1 in swine liver by liquid chromatography– fluorescence detection. J Chromatogr B 819:97–103 Paugam A, Creuzet C, Dupouy-Camet J, Roisín MP (2002) In vitro effects of gliotoxin, a natural proteasome inhibitor, on the infectivity and proteolytic activity of Toxoplasma gondii. Parisitol Res 88(8):785–787 Pena GA, Pereyra CM, Armando MR, Chiacchiera SM, Magnoli CE, Orlando JL, Dalcero AM, Rosa CAR, Cavaglieri LR (2010) Aspergillus fumigatus toxicity and gliotoxin levels in feedstuff for domestic animals and pets in Argentina. Lett Appl Microbiol 50:77–81 Pereyra CM, Alonso VA, Rosa CAR, Chiacchiera SM, Dalcero AM, Cavaglieri LR (2008) Gliotoxin natural incidence and toxigenicity of Aspergillus fumigatus isolated from corn silage and ready dairy cattle feed. World Mycotoxin J 1(4):457–462 Perrone G, Gallo A (2017) Aspergillus species and their associated mycotoxins. In: Moretti A, Susca A (eds) Mycotoxigenic fungi methods and protocols. Humana Press, New York, pp 33–49 Pitt JI (2000) Toxigenic fungi: which are important? Med Mycol 38(1):7–22 Ponnamma KN, Gopal M, Sharmila S (2000) Record of Aspergillus flavus (Link) on the plant hopper, Proutista moesta Westwood (Hemiptera: Derbidae). J Plant Crop 28:231–232 Puel O, Galtier P, Oswald IP (2010) Biosynthesis and toxicological effects of patulin. Toxins 2:613–631 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019a) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144 Rana KL, Kour D, Yadav AN (2019b) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge

236

F. A. Abo Nouh et al.

Razzaghi-Abyaneh M, Allameh A, Tiraihi T, Shams-Ghahfarokhi M, Ghorbanian M (2005) Morphological alterations in toxigenic Aspergillus parasiticus exposed to neem (Azadirachta indica) leaf and seed aqueous extracts. Mycopathologia 59(4):565–570 Reiss J (1975) Insecticidal and larvicidal activates of the mycotoxins aflatoxin B1, rubratoxin B, patulin and diacetoxyscir-penol toward Drosophila melanogaster. Chem Biol Interact 10:339–342 Richard JL, Bennett GA, Ross PF, Nelson PE (1993) Analysis of naturally occurring mycotoxins in feedstuffs and food. J Anim Sci 71:2563–2574 Richard E, Heutte N, Bouchart V, Garon D (2009) Evaluation of fungal contamination and mycotoxin production in maize silage. Anim Feed Sci Technol 148:309–320 Rizzi L, Simioli M, Roncada P, Zaghini A (2003) Aflatoxin B1 and clinoptilolite in feed for laying hens: effect on egg quality, mycotoxin residues in livers and hepatic mixed function oxidase activities. J Food Prot 66:860–865 Romero González R, Martínez Vidal JL, Aguilera Luiz MM, Garrido Frenich A (2009) Application of conventional solid-phase extraction for multimycotoxin analysis in beers by ultrahigh-performance liquid chromatography–tandem mass spectrometry. J Agric Food Chem 57:9385–9392 Ross PF, Rice LG, Casper R, Crenshaw JD, Richard JL (1991) Novel occurrence of cyclopiazonic acid in sunflower seeds. Vet Hum Toxieo 33:284 Saleemullah AI, Khalil IA, Shah H (2006) Aflatoxin contents of stored and artificially inoculated cereals and nuts. Food Chem 98:699–703 Samson RA, Houbraken JAMP, Kuijpers AFA, Frank JM, Frisvad JC (2004) New ochratoxin A or sclerotium producing species in Aspergillus section Nigri. Stud Mycol 50:45–61 Sangare-Tigori B, Moukha S, Kouadio HJ, Betbeder AM, Dano DS, Creppy EE (2006) Co-occurrence of aflatoxin B1, fumonisin B1, ochratoxin A and zearalenone in cereals and peanuts from CotedIvoire. Food Addit Contam 23:1000–1007 Santos L, Marın S, Sanchis V, Ramos AJ (2009) Screening of mycotoxin multicontamination in medicinal and aromatic herbs sampled in Spain. J Sci Food Agric 89:1802–1807 Schrögel P, Wätjen W (2019) Insects for food and feed-safety aspects related to mycotoxins and metals. Foods 8:288 Scott PM (2012) Recent research on fumonisins: a review. Food Addit Contam Pt A 29:2,242–2,248 Scudamore KA, Livesey CT (1998) Occurrence and significance of mycotoxins in forage crops and silage: a review. J Sci Food Agric 77:1–17 Seefelder W, Gossmann M, Humpf HU (2002) Analysis of fumonisin B1 in Fusarium proliferatum-­ infected asparagus spears and garlic bulbs from Germany by liquid chromatography-­ electrospray ionization mass spectrometry. J Agric Food Chem 50:2778–2281 Senyuva HZ, Gilbert J (2008) Identification of fumonisin B2, HT-2 toxin, patulin, and zearalenone in dried figs by liquid chromatography-time-of-flight mass spectrometry and liquid chromatography-­mass spectrometry. J Food Prot 71:1500–1504 Sewram V, Shephard GS, Merwe LVD, Jacobs TV (2006) Mycotoxin contamination of dietary and medicinal wild plants in the Eastern Cape Province of South Africa. J Agric Food Chem 54:5688–5693 Speijers GJA (2004) Particular mycotoxins: patulin. In: Magan N, Olsen M (eds) Mycotoxins in food detection and control. CRC Press, Boca Raton, pp 339–352 Stoev SD (2013) Food safety and increasing hazard of mycotoxin occurrence in foods and feeds. Crit Rev Food Sci 53(9):887–901 Stott WT, Bullerman LB (1975) Patulin: a mycotoxin of potential concern in foods. J Milk Food Technol 38(11):695–705 Strosnider H, Azziz-Baumgartner E, Banziger M, Bhat RV, Breiman R et al (2006) Public health strategies for reducing aflatoxin exposure in developing countries: a workgroup report. Environ Health Perspect 12:1898–1903 Sugui JA, Pardo J, Chang YC, Zarember KA, Nardone G, Galvez EM, Mullbacher A, Gallin JI, Simon MM, Kwon-Chung KJ (2007) Gliotoxin is a virulence factor of Aspergillus fumigatus: gliP deletion attenuates virulence in mice immunosuppressed with hydrocortisone. Eukaryot Cell 6(9):1562–1569

7  Aspergillus Mycotoxins: Potential as Biocontrol Agents

237

Teren J, Varga J, Hamari Z, Rinyu E, Kevei F (1996) Immunochemical detection of ochratoxin A in black Aspergillus strains. Mycopathologia 134:171–176 Trucksess MW, Mislivec PB, Young K et al (1987) Cyclopiazonic acid production by cultures of Aspergillus and Penicillium species isolated from dried beans, cornmeal macaroni and pecans. J Assoc Off Annal Chem 70:123–126 Tsubouchi H, Terada H, Yamamoto K, Hisada K, Sakabe Y (1995) Caffeine degradation and increased ochratoxin production by toxigenic strains of Aspergillus ochraceus isolated from green coffee beans. Mycopathologia 90:181–186 Urano T, Trucksess MW, Beaver RW et al (1992) Co-occurrence of cyclopiazonic acid and aflatoxins in corn and peanuts. J AOAC Int 75:838–841 Varga J, Due M, Frisvad JC, Samson RA (2007) Taxonomic revision of Aspergillus section Clavati based on molecular, morphological and physiological data. Stud Mycol 59:89–106 Varga J, Baranyi N, Chandrasekaran M, Vágvölgyi C, Kocsubé S (2015) Mycotoxin producers in the Aspergillus genus: an update. Acta Biol Szeged 9(2):151–167 Voss KA, Norred WP, Hinton DM et  al (1990) Subchronic oral toxicity of cyclopiazonic acid (CPA) in Sprague-Dawley rats. Mycopathologia 110:11–18 Wang Y, Wang L, Liu F, Wang Q, Selvaraj JN, Xing F, Zhao Y, Liu Y (2016) Ochratoxin A producing fungi, biosynthetic pathway and regulatory mechanisms. Toxins 8(3):83 Wicklow DT, Cole RJ (1982) Tremorgenic indole metabolites and aflatoxins in sclerotia of Aspergillus flavus: an evolutionary perspective. Can J Bot 60:525–528 Wild C, Gong Y (2010) Mycotoxins and human disease: a largely ignored global health issue. Carcinogenesis 31:71–82 Wilson DM, Mutabanhema W, Jurjevic Z (2002) Biology and ecology of mycotoxigenic Aspergillus species as related to economic and health concerns. In: DeVries JW, Trucksess MW, Jackson LS (eds) Mycotoxin and food safety. Springer, New York, pp 3–17 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan V, Dhaliwal HS, Saxena AK (2017) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Singh S, Mishra S, Gupta A (2019a) Recent advancement in white biotechnology through fungi. volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N (2020b) Microbiomes of extreme environments: biodiversity and biotechnological applications. CRC Press, Boca Raton Yadav AN, Singh J, Rastegari AA, Yadav N (2020c) Plant microbiomes for sustainable agriculture. Springer, Cham Zain ME (2011) Impact of mycotoxins on humans and animals. J Saudi Chem Soc 15(2):129–144 Zeng RS, Niu G, Wen Z, Schuler MA, Berenbaum MR (2006) Toxicity of aflatoxin B1 to Helicoverpa zea and bioactivation by cytochrome P450 monooxygenases. J Chem Ecol 32:1459–1471 Zinedine A (2010) Ochratoxin A in Moroccan foods: occurrence and legislation. Toxins 2:1121–1133

Chapter 8

Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health Hesham A. El Enshasy, Kugan Kumar Ambehabati, Ashraf F. El Baz, Santosh Ramchuran, R. Z. Sayyed, Divina Amalin, Daniel J. Dailin, and Siti Zulaiha Hanapi

Contents 8.1  I ntroduction 8.2  M  ethodology of Studying Trichoderma Biodiversity 8.3  Trichoderma Diversity in Different Habitats 8.3.1  Natural Soils, Decaying Wood and Plant Material 8.3.2  Endophytes 8.3.3  Air and Settled Dust 8.4  Agricultural Habitats 8.5  Trichoderma: Promoting Healthy Plant Growth 8.6  Trichoderma: Biological Control Agent 8.7  Biotechnological Applications 8.7.1  Production of Antibiotics and Other Secondary Metabolites 8.7.2  Production of Hydrolytic Enzymes 8.8  Conclusion and Future Prospect References

 240  240  242  242  244  245  245  247  248  250  250  252  253  254

H. A. El Enshasy (*) · K. K. Ambehabati · D. J. Dailin · S. Z. Hanapi Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), Johor Bahru, Malaysia e-mail: [email protected] A. F. El Baz Genetic Engineering and Biotechnology Research Institute, Sadat University, Sadat City, Egypt S. Ramchuran Bioprocess Development Department, CSIR Biosciences, Pretoria, South Africa R. Z. Sayyed Department of Microbiology, PSGVP Mandal’s, Arts, Science, and Commerce College, Shahada, Maharashtra, India D. Amalin Biological Control Research Unit, Center for Natural Sciences and Environmental Research, De La Salle University, Manila, Philippines © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_8

239

240

H. A. El Enshasy et al.

8.1  Introduction Trichoderma is a saprotrophic fungus which largely can be found in environments such as forest soil, roots and leaves. This fungus has been declared as soil fungi due to its significant for their fast growth. They exhibited high capacity to utilize different types of complex substrates and can act as a strong resistances towards different kind of toxic chemicals. Therefore, Trichoderma species is very abundance on decaying wood. This is mainly because of the heterotropic interactions such as decomposition and opportunistic endophytism. It can be found in all type of soils which includes from forest, salt marsh, agricultural even in desert soils. In addition to that, Trichoderma has been used as an efficient biocontrol agent against the phytopathogens (Sharma et al. 2019). The main mechanisms for the biocontrol process in this type of fungi have been assumed due to antibiosis, mycoparasitism and competition for space and resources (Bissett et al. 2015). This fungus evolved many mechanisms which contribute for the improvement of the plant resistance towards diseases, the plant’s growth as well as its productivity (Rastegari et al. 2020; Yadav et al. 2020d, 2019b). According to Bissett et al. (2015), out of 260 species, around 35 established species was mainly discovered for its economic importance mainly due to its capability of various enzyme productions or to be used as biocontrol agents. Global interest was given to researches related to Trichoderma fungus thanks to its applications in the field of agricultural and biotechnology (Verma et al. 2017a). Trichoderma has been thought to be associated with plants as epiphytes and endophytes. Epiphytes are beneficial microflora that can be found at the aerial parts of the plants that can be either harmful or beneficial towards the plant (Yadav et al. 2020b, c). The word endo derived from the Greek words which carry the meaning of within and “phyte” stands for plant. In another word, endophytes are the colonization which takes place inside the plants by any fungus or bacteria (Suman et al. 2016; Verma et al. 2017a; Yadav et al. 2020a). There are few reports supporting the fact that Trichoderma species found as endophytes of the plants. One of the well-­ known examples is the presence of Trichoderma in banana tissues (Wang et  al. 2000). According to the Pocasangre et al. (2000) study on the distribution of endophytic fungi from banana was conducted which is mainly about isolating the fungus from the central cylinder. Besides that, Sikora et al. (2008) did survey on isolating endorhiza of banana and use it for biocontrol of nematodes.

8.2  Methodology of Studying Trichoderma Biodiversity Most of the species identification for Trichoderma species has been performed according to their morphological characteristics. In order to carry out this, solid media with different components which are targeted for conidium production and its branching observation were used for the culture characteristics as well as for the

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

241

morphological studies (Hermosa et al. 2000). Most of the times, the morphological studies which aimed for conidiosphores structure identification can be done by referring to the taxonomic keys and the information provided by the literature studies. However, without having any professional expertise this practice may lead to incorrect conclusion. In order to overcome this issue for better species identification, biochemical and molecular methods are highly recommended (Photita et al. 2001). One of the useful tools which used for better species identification and give data for the ecological purpose of the species is metabolic profiling technique which also provides the possibilities of the quantitative measurement of the growth and consumption of different carbon and nitrogen sources. According to Kredics et  al. (2011), the cellulose-acetate electrophoresis based isoenyzme analysis with using glucose-6-phosphate dehydrogenase, glucose-6-phosphate isomerase, 6-phos-­ phogluconate dehydrogenase, peptidases A, B and D and phoshoglucomutase enzymes was used for isolation and identification of Trichoderma strains which derived from some clinical samples and wheat fields. On the other hand, another alternative for the biochemical technique was suggested by Neuhof et al. (2007), where the identification process was mainly based on intact-cell mass spectrometry. This method will help to identify hydrophobins in the mycelia as well as spores of the strains. The patterns of the hydrophobin reflect the characteristic of the species that being isolate and this method can also give a rapid and direct identification of class II hydrophobins (Hanada et al. 2008). When it comes to the molecular methods, methods like the DNA-fingerprinting, the sequence analysis of ribosomal internal transcribed spacer (ITS) region and the segments from genes encoding for the translation elongation factor 1-alpha (tef1), endochitinase (chi18-5, formerly known as ech42), RNA polymerase II subunit (rpb2) and calmodulin (cal1) is the suitable method for giving the accurate species identification for Trichoderma strains (Druzhinina et  al. 2008). The TrichOKEY which is also known as ITS-based online barcoding program becomes another useful tool for the species identification. For the analysis of tef1, ITS and rpb2 sequences the online programme known as TrichoBLAST and its updated version named TrichoMARK can be used. As an example, according to Nagy et al. (2007), by using the online barcoding programme name TrichoCHIT, any potential chitinase producing strain such as Trichoderma harzianum was used. Moreover, species-specific primers in polymerase chain reaction can be used for a quick and precise diagnosis. According to Kredics et al. (2011), this method allows for a fast and specific identification of Trichoderma pleurotum and Trichoderma pleuroticola. Both the strain is known as agent that causes the formation of green mould in the global production of Pleurotus ostreatus within the growing substrate and without any requirement of cultivation time (Xia et al. 2011a, b). The studies related to Trichoderma biodiversity mainly based on the standard culture approach which contains the collection of samples, the isolation of Trichoderma strains on selective media, however when this method is being applied, some strains can be easily identified and there are some which is even harder to do the isolation procedure. The diversity that had been detected by using this method

242

H. A. El Enshasy et al.

does not reflect the accurate diversity of the genus from the tested habitat. The metagenomic method provides the best solution to overcome this problem as it examining the habitat without doing any isolation or culturing of the strains. When the first attempt is done on biodiversity detection using this metagenomic approach by Hagn et al. (2007) the primers for Trichoderma specific were created for the ITSI fragment of the rRNA gene cluster. However, using this approach, only around 12 species have been identified as this ITSI alone is could not identify all the species because certain strains share the same allele (Samuels et al. 2006). To overcome these issues, Meincke et al. (2010) created the primer pair which is specific for Trichoderma for diversity analysis purpose. This specific primer help to amplify around 650 bp fragment of the ITS region which is suitable for identification by TrichOKEY and TrichoBLAST. The very first PCR-amplification was performed by having fungal specific forward primer and Trichoderma-specific reverse primer. For the second reaction, the Trichoderma-specific forward and reverse primers are used together. The ITS amplicons help to denature the gradient gel electrophoresis or help to clone to the pGEM-T easy vector. The currently developed primer system was applied on Trichoderma communities in the rhizosphere of potatoes. But this method could not detect the several species because reverse primer is located 30  bp upstream of the last genus-specific TrichOKEY hallmark (Nawaz et al. 2018). However, in a recent study conducted by Nawaz et al. (2018), six reverse primers were designed and their specificity and selectivity were tested. Along with the forward primer ITS5 this reverse primer can help to amplify the whole diagnostic region of ITS1. The six separated PCR amplifications from the tested soil that contain same forward and one reverse primers were combined, purified and subcloned to pGEM-T. The sequences of the individual clones were determined and analysed with TrichOKEY 2.0 and TrichoBLAST. Atanasova et al. (2010) applied this strategy to determine the diversity of the strain in samples.

8.3  Trichoderma Diversity in Different Habitats 8.3.1  Natural Soils, Decaying Wood and Plant Material Danielson and Davey (1973) found out that at the south part of the USA and at the state of Washington, Trichoderma can be found at variety of forest soil. Some of the strains like Trichoderma polysporum and Trichoderma viride were located near the strictly cool temperature regions. Trichoderma harzianum was isolated from warm climate area, while Trichoderma hamatum and Trichoderma pseudokoningii were dominantly growing at area with excessive moisture. Besides that, the isolation, morphological characterization as well as full identification of strains like Trichoderma aureoviride, T. harzianum, T. koningii, T. longibrachiatum and T. viride

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

243

from area like the wood of the oak, cork wood and dead wood of the apple twigs have been studied (Vasanthakumari and Shivanna 2011). The broad studies on the biodiversity of Trichoderma were conducted in North America and at some region in Europe. The isolated Trichoderma strains were analysed for their function to degrade the organochlorine xenobiotics but as mentioned earlier, the results from this method are difficult to be evaluated. This is mainly due to the fact that there is no available of molecular tools for the identification (Vasanthakumari and Shivanna 2011). According to Zhang et al. (2005), around 135 isolates of Trichoderma were obtained from four regions of China which are from Hebei, the northmost side, followed by Zheji-ang, the south-east side, Yunnan, west part and from the Himalayan part as well. The result from this study indicates from among the North to South part, the Northern China finalized as potential centre for origin of the haplotype of Trichoderma harzianum (Vasanthakumari and Shivanna 2011). One the other hand, Abd-Elsalam et al. (2010) isolated the fungi strain from the soil of protected area in Saudi Arabia and the identification process were carried out by suing M13-microsatelite PCR and ITS barcoding. Results from the investigation reveal that Trichoderma harzianum and Trichoderma longibrachiatum are present. The biodiversity study of Trichoderma from the European river floodplain habitat near the Danube national park, which was originally known for its riparian forest area in Vienna, Austria was carried out mainly based on the morphological examinations, sequence analysis of the ITS region and fragment of the tef1 gene as RAPD analysis (Zhang et al. 2005). Plant litter associated fungi was examined from the spring of the sheep herd in the western of Norway and isolated wide variety of fungi which includes two Trichoderma strains. However, the authors failed to determine the species by NCBI BLAST for its ITS sequences. But by using TrichOKEY the isolated named as Trichoderma hamatum while other were identified as Trichoderma koningiopsis (Sun et al. 2012). A wide-scale survey was done over 14 European countries which have temperate climate in order to learn about the biodiversity of Trichoderma by testing their morphology, ITS and tef1 sequences. Around 75 species were detected from European countries. By doing ITS barcoding-based study, some of the strains are found from soil and decaying wood. Then taxon-specific metagenomic method was used by Friedl and Druzhinina (2012), in order to determine the Trichoderma biodiversity in situ in soil samples from aspen and beech forests along the Danube floodplain. The obtained result shows that not only small number of Trichoderma species were capable of forming teleomorph but suggested that the biodiversity of the genus is higher on and above the small layer than inside the soil. Some of the strains associated with the host fungi or trees were found but the major of the species suggested to be necrotrophic on diverse fungi on wood and tree bark (Samuels et al. 2012b).

244

H. A. El Enshasy et al.

8.3.2  Endophytes Living plants or endophytes can be defined as organisms which live within the plant cells. They established a relationship with the plant that varies from symbiotic to pathogenic (Bailey et  al. 2006). There are certain types of Trichoderma strains which are capable of colonizing the root part of the plant and continue to have a symbiotic relationship with that particular plant. There has been a lot of investigation being carried out in order to prove that Trichoderma strains can develop endophytic relationship within the inner tissue part of the plant (Samuels et al. 2012a). Theobroma cacao which commonly known as cocoa plant was become the first target to carry out the study as this plant can grow easily at any country which have tropical climates. In South America the most common diseases that cause by this cocoa plant are black pod, witches broom and frosty pod rot. To overcome this major issue, extensive study was carried out on the endophytic microbial community of the cocoa plant (Samuels et al. 2012a). From this study, it was concluded that several fungus strains such as Trichoderma koningii, T. ovalisporum, and T. koningiopsis can play its role as endophytes in the cocoa plant (Degenkolb et al. 2008). According to the study done by Rubini et al. (2005), diversity study about endophytic fungi in the cocoa plant give rise for variety of fungal strains but low prevalence was given to the isolated strains. Posada et al. (2007) reported that there are few endophytic microbiota can be found in the coffee seedlings which contain some of the Trichoderma strains such as Trichoderma harzianum and Trichoderma hamatum. Besides the cocoa plant, similar studies were also conducted on other plants. One of the good example for this scenario is the Hevea spp. which also known as rubber tree. According to Chaverri et al. (2011), a new species named Trichoderma amazonicum was isolated from this rubber tree. In Mexico, two other Trichoderma fungus functioned as endophyte in two different plants. Zhang et al. (2007) Trichoderma strain was identified from Taxus mairei, while Samuels et  al. (2012b) identified Trichoderma solani from the tubers of Solanum hintonii. Six types of Trichoderma species were identified from the banana root where four of them were from the inside the root, while the rest two were isolated from the surface of the root. Among the species Trichoderma asperllum and Trichoderma virens showed the highest frequencies in the samples (Xia et al. 2011a, b). According to Dang et al. (2010), Trichoderma ovalisporum was isolated from the traditional Chinese medicinal plant where the strain shows effective antibacterial activity against several pathogenic microorganisms such as Staphylococcus aureus and Escherichia coli. Trichoderma strains were also isolated from other important medicinal plants such as Huperzia serrata and Salvia miltiorrhiza. Strains also were detected from some of the carnivorous plants. Some studies were done on Drosera rotundifolia which is also known as common sundew during the season of autumn and spring by Quilliam and Jones (2010). Trichoderma viride was isolated from all the samples. Other carnivorous plant which is Pinguicula vulgaris was also studied for the potential endophytic fungi. The root and seed from Dendrobium nobile and

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

245

Dendrobium chrysanthum also studied for the presence of endophytic and mycorrhizal fungi (Ming et al. 2012). Numerous studies and efforts were taken to overcome the growth of the harmful pathogenic fungi, Rhizoctonia solani. This fungus has the ability to cause serious quality as well as quantity damages on the potato tuber. However, the endophytic fungi that isolated from the potato plants were tested and based on the obtained result, isolates of Trichoderma atroviride show the highest inhibition against R. solani due to the mycoparasitic phenomena (Chen et al. 2011).

8.3.3  Air and Settled Dust Air plays pivotal role when it comes to the dispersal of spores and conidia of fungus. According to the study done by Madsen et al. (2007), Trichoderma species can be isolated from air of different environment which varies from outdoor to indoor air. Some good example of indoor air samples are those from heated wooden chips inside the buildings, from air filters that being used in hospitals, air ducts of the households, air conditioners, and achieve storage facilities. Trichoderma can be isolated from the outdoor air samples as well which normally from the rooftop of hospitals and houses. The air samples from agricultural area can be potential for this fungus isolation as well. According to Madsen et al. (2007) the dust blown from hay in England can be used for the isolation purpose. However, no species level identification was done for the samples that has been isolated from the air samples and settles dust. From the clinical wise, presence of conidia in the air plays a significant role for the occurrence of allergic diseases and can cause the infections like sinusitis or pneumonia. On the other hand, Hansen et al. (2010) concluded that Trichoderma harzianum which used as biocontrol agent can be detected in the air only during the treatment period.

8.4  Agricultural Habitats Abiotic and biotic stress plays a significant role towards the population and diversity of any microbial communities in the agricultural ecosystems (Rana et al. 2019a, b; Yadav et al. 2018a). This includes the species of the plant and its growth stage, soil physical and properties of the chemical that being used, usage of pesticides, the geographical region and most importantly the total microbial competition (Druzhinina et al. 2011). Trichoderma spp can be isolated from any type of agricultural fields as it exhinited significant positive impacts on plant cultivation. Those impacts include its role as efficient biocontrol agent, induction of systemic resistance, increase the uptake of nutrient, promote the plant growth and degradation of any pesticides that can bring negative impact to the soil. The rhizosphere attracts this fungus by having the presence of different soil borne fungi which function as its

246

H. A. El Enshasy et al.

prey and rich derived nutrient. The members of Trichoderma are preferred to be isolated from rhizosphere and non-rhizosphere soil rather than phyllosphere. Some of the species are ubiquitous where some are limited to certain geographical areas (Kour et al. 2019c). As mentioned earlier, the isolation of this fungus from various agricultural crop fields was carried out to conduct studies on its biological control ability against phytopathogens, so only limited number of studies that deal with the population, abundance and diversity of the genus of Trichoderma from specific crop fields were carried out. Trichoderma spp can be highly found in cereal crop fields and is one of the dominating fungi and prevalent taxa among other fungal communities. When it comes to the cereal crop field, the weather, the type of soil and farming management bring big influence to the distribution of the Trichoderma spp. Six different species of the fungus were discovered by the ITS barcoding and restriction fragment length polymorphism (RFLP) from the rhizosphere, rhizoplane and the soil bulk of potato (Liang et al. 2004). From the rhizosphere of coffee, Trichoderma isolates also have been discovered particularly from the soil of the coffee plants in the forest and semi-distributed forest area. The identification was done by ITS barcoding. Either its cultivated or uncultivated coffee regions, both of the different area show higher diversity of this isolates but the indices and the evenness for this isolates were the same at the both the habitats. Some chemical properties and the altitude of the samples concluded that the growth of the isolates was not preferred by the ecological perspective. It was also concluded that the host plant influence the genetic diversity of Trichoderma strains. Around 135 isolates of Trichoderma were collected from the rhizospheres of cocoa plant of different locations (Pavone and Domenico 2012). From the rhizosphere of sugar beet, sixteen isolates were collected and the identification process was done based on the morphology, ITS and tef1 analysis. When it comes to the oilseed rape rhizosphere, Trichoderma spp. were the most prevalent fungi and most importantly it showed high biodiversity and specificity in the bulk soil of oilseed rape. Another most important plant that acts as a rhizosphere for Trichoderma isolates is the oil palm. Among the isolates strains, Trichoderma harzianum and Trichoderma virens were the most prevalent species that had been recovered from the soils of oil palm in Malaysia. Population wise, it shows the high in both the cultivated and semi-cultivated oil palm ecosystems. However, the population increased when empty fruit bunches were added to the fields and the moisture content and the pH of the soil did not bring any effect towards the distribution of the strains. In conclusion the diversity and the abundance of the Trichoderma were higher in bulk soil than in rhizosphere soil (Naeimi et al. 2011).

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

247

8.5  Trichoderma: Promoting Healthy Plant Growth In the recent time, Trichoderma spp. has been widely suggested to be used for efficient plant growth as a good plant growth promoting fungi (PGPF). These have capability of producing some of the secondary metabolites in particularly siderophores, phosphate-solubilizing enzymes and phytohormones for plant growth and soil health (Doni et  al. 2013; Kour et  al. 2019b; Yadav 2019). This plant growth promoting traits is considered one of their beneficial trait and this traits can be seen through different type of mechanisms such as antibiosis, degradation of toxins, mycoparasitism, inactivation of pathogenic enzymatic pathway and also but not least the enhanced nutrient uptake which leads to the overall development (Lorito et al. 2010; Kaur et al. 2020; Kumar et al. 2019; Singh et al. 2020). This fungus is known as hemibiotrophic fungus which is effective towards reducing the severity of the plant diseases by several mechanisms which have been mentioned above (Fontanelle et al. 2011). Most of the secondary metabolites produced by Trichoderma are strain dependent, can contain both volatile and nonvolatile antifungal substances and it is rhizosphere-competent strains which mainly involve in colonizing the surface root which have been shown for causing direct impact on the plants. It helps to increase the nutrient uptakes which eventually leads to better physical growth of the plant (Gal-Hemed et al. 2011). According to Doni et al. (2014), the usage of Trichoderma as plant growth promoter shows significant positive impact towards the height of the plant, number of leaf and the length of the root. The possibilities for this to occur are mainly because of mechanisms which involve nutrient usage and the tolerance to abiotic and biotic stress. In addition to that, phytohormones produced by this fungus play a pivotal role for the enhanced growth of the plant. Some of the reports include phytohormones such as cytokinin like molecules and gibberellins related molecules can make biological enhancement on the crop fertility. On the other hand, Kashyap et al. (2017) also mentioned that the rice which inoculated with the Trichoderma shows higher photosynthetic rate. Other good impact shown by rice with the presence of Trichoderma is better uptake of the nutrients and increased resistance towards drought. On the other hand, maize plant, this fungus increased the plant’s biomass production as well as developed better root hair. Trichoderma also helped to increase the seed germination process, increase the osmotic, salinity and chilling by initiate the physiological protection against any form of cellular damage (Mastouri et al. 2010). The interaction in between Trichoderma harzianum strain and tomato-root system was also studied at the beginning stage of the root colonization. The presences of the fungus inoculation in the production medium cause the profuse adhesion of the hyphae to the roots and the colonization of the root epidermis and cortex. The green fluorescent protein (GFP) shows the hyphal growth and the formation of the papilla like hyphal tips which induced by the plant. Trichoderma harzianum in particular is able to control and inhibit the growth of B. cinerea on grapes by colonize the blossom tissue and exclude the pathogen from

248

H. A. El Enshasy et al.

the infected side. According to Kashyap et al. (2017), Trichoderma species used the competition for nutrient as their major mechanisms to inhibit the soil microorganisms. In addition to that, Trichoderma has the advantage of mobilizing and take up all the nutrients which makes much more efficient and more competitive than many other soil microbes. However, the biotic components of the soil have several impacts on the bio control activity of Trichoderma against other plant pathogens. According to Kashyap et al. (2017), when the Gfp contained mutant strain used, it shows higher level of microbial soil biomass that induce the shift from the hyphal growth to sporulate in Trichoderma (Table 8.1).

8.6  Trichoderma: Biological Control Agent Fungi have been used for biocontrol purpose in much modern agricultural system. This is mainly because most of the fungi have the ability to reduce the negative impact of plant pathogen (Rana et al. 2020; Yadav et al. 2018b). Trichoderma sp. have gained much more interest than any other fungi due to their surviving ability under any form of unfavourable condition, high capacity for reproductive purpose, Table 8.1  The effect of Trichoderma inoculum on the agronomical and physiological aspects of the crops Trichoderma strain Trichoderma sp.

Trichoderma harzianum

Trichoderma harzianum

Trichoderma asperelloides T203 Trichoderma hamatum Trichoderma atroviride

Crop Chickpea

Application mode Agar plates were inoculated with a fungal mycelial disc of 5 mm diameter Cucumber 5 × 106 conidia per g of soil or sprayed on roots at a concentration of 1 × 108 conidia/ml Chrysanthemum 5 × 106 conidia per g of soil or sprayed on roots at a concentration of 1 × 108 conidia/ml Arabidopsis Root system was inoculated with a solution containing 1 × 105 spores/ml Arabidopsis Trichoderma bran inoculum added to soil before sowing Lettuce The substrate was supplied with prepared tablets containing 4.5 × 105 conidia

Effects References Rawat et al. Increased (2011) solubilization of inorganic phosphate Chang et al. (1986)

Promoted seed germination, vegetative growth, and flowering Promoted seed germination, vegetative growth and flowering Improved seed germination

Brotman et al. (2013)

Promoted root and shoot growth

Studholme et al. (2013)

Chang et al. (1986)

Enhanced shoot and Colla et al. root dry weight, and 2015 chlorophyll content

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

249

capability to resist against other plant pathogenic fungi and can able to produce secondary metabolites (Contreras-Comejo et al. 2016; Benítez et al. 2004). Besides that, this fungus has been also used in various biotechnological applications and used in agriculture field mainly to enhance the growth and the yield of the plants (Lorito et al. 2010; Hermosa et al. 2012). Any form of penetration or interaction in plant roots normally will activate its immune system but in case of Trichoderma sp. it will remodel the immune system of the plant and help it to be recognized as non-pathogenic plant. The strains of the fungus can able to eliminate the synthesis of JA and ET which mainly involved in inducing systematic resistance (Hermosa et  al. 2012). The systematic resistance induced by T. asperellum or T. harzianum T39 against B. cinerea in A. thaliana was determined as well. Trichoderma sp. plays an important role when it comes to suppressing the formation of any plant disease and plant pathogen in both the field condition and greenhouse condition. The fungus can produce wide range of elicitors which will interact with the receptors and recognition of Trichoderma and this will lead to the induction of resistance in the plant (Salas-Marina et al. 2011). In addition, different types of Trichoderma strains are able to produce little amount of secondary metabolites and these metabolites seem to induce the pathogenesis-­ related protein and eventually reduce the symptoms of any disease (Vinale et  al. 2006). Through the mycoparasistm process, Trichoderma can parasitize the plant pathogen during different stages of development. This is done by producing several enzymes such as chitinase, proteases and glucanases which will help to flow the nutrient into the mycoparasite and finally degrade the host of the pathogen (Inch and Gilbert 2011). Table 8.2 shows the different Trichoderma strains against different bacterial pathogens. Both the mono and dicotyledonous species show strong resistance towards attack of various pathogens when the plant is well pre-treated with Trichoderma. The plant colonization caused by this fungus inhibits the growth of different pathogens at the side of inoculation and also when the biocontrol fungus inoculated at different times or sites than that of the pathogen. In addition to that, the resistance of the plant shown by the colonization of some of the Trichoderma sp. is pretty much similar to that elicited by the rhizobacteria where it enhance the defense system of the plant but do not directly involve with the production of the pathogenesis-related proteins known as PR proteins. Recent studies have been done at the molecular level by using the high-density oligonucleotide microarray approach and it was found out that the gene induced by Trichoderma was associated with the biotic and abiotic stresses and also RNA, DNA and protein metabolism. The genes that codify for the extensin and also extensin look like proteins were mainly induced by the biological agents. The plant starts to interact with Trichoderma, different types of metabolites which belong to different classes will start to be produced as elicitors or as resistance inducers (Woo and Lorito 2007). Proteins with enzymatic activity such as xylanase, avirulence are able to induce the plant defence mechanisms and induce the production of low molecular weight compound as a result of fungus–plant interaction. Some of these low molecular weight compounds which have the ability to

250

H. A. El Enshasy et al.

Table 8.2 Different Trichoderma strains against different bacterial pathogens Trichoderma Strains Trichoderma harzianum

Plant Tomato

Trichoderma spp.

Rice

Trichoderma asperellum

Tomato

Trichoderma harzianum T23

Activity in vitro

Trichoderma reesei

Arabidopsis and tomato

Trichoderma asperelloides T203 Trichoderma atroviride

Tomato

Tomato

Pathogen Clavibacter michiganensis subsp. michiganensis Xanthomonas oryzae pv. Oryzae Xanthomonas campestris pv. vesicatoria Clavibacter michiganensis and Erwinia Amylovora Clavibacter michiganensis

Mechanisms/ activity Lysosime and prevent activity Biocontrol activity

Biocontrol activity, antagonism dosage

Production of viridiofungin A (VFA) Production of extracellular enzyme, swollenin Pseudomonas syringe Increase level of pv. WRKY 40 transcription factor Alternaria solani Secrete Sm1 and Ep11 protein

References Utkhede and Koch (2004) Gokil-Prasad and Sinha (2012) Suárez-Estrella et al. (2014) El-Hasan et al. (2009) Saloheimo et al. (2002) Brotman et al. (2012) Salas-Marina et al. (2011)

degrade fungal cell wall have been purified and further characterized. These compounds have been mainly composed of oligosaccharides with or without amino acids moiety. In these interaction mechanisms Trichoderma activates the mycoparasitic gene expression cascade. Besides the activated antimicrobial effect, their action might stimulate the biological activity of the resident antagonistic microbial populations or the introduced Trichoderma strains and this will induce the effect of induced systematic resistance on the plant.

8.7  Biotechnological Applications 8.7.1  P  roduction of Antibiotics and Other Secondary Metabolites There are several compounds which are not involved for the normal growth and the reproduction of any organisms. These compounds are called as secondary metabolites. However, they play pivotal role when it comes to the development, signaling and the interaction between one organism and other (Rastegari et al. 2019; Yadav et al. 2019a; Saxena et al. 2016). The absence of these metabolites will result in the long term impairment on the survival of the organism rather than causing a direct and immediate death. According to Mukherjee et al. (2012), certain environmental

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

251

factors will cause the organism to be dependent on the secondary metabolites such as in case of iron deficiency as siderophores act as replacement to support growth. Plants use these secondary metabolites as a defence system against herbivores and other inters species. According to Vipul et al. (2014), humans use it for medicine, flavourings and drug creation purposes. On the other hand, it also can be used as efficient weapon against other pathogenic bacteria, amoeba, fungi, insects and even large animals. Secondary metabolites can be used as agent for symbiosis purpose between plants and other organisms (Kour et al. 2019a). Commonly known as filamentous fungi, Trichoderma spp., can be found nearly in most of the soils and other habitats. They have the capability of adapting to different ecological conditions and lifestyles. Trichoderma fungus has economical important mainly due to the fact that it can be used as a good biocontrol agent which help to inhibit the growth of phytopathogenic fungi. It can be functioned as biocontrol agent because of the presence of extracellular enzymes and secondary metabolites. Particularly the secondary metabolites produced by the fungus can be used in biotechnological and pharmaceutical purposes. This includes secondary metabolites such as peptaibols, non-ribosomal peptides, terpenes, steroid and many more. Although there have been 373 different molecules that have been identified so far, their specific activity is still cannot be determined. According to Verma et  al. (2017b), these fungal biocontrol agents have been mainly used against any soil related diseases. In order for them to perform as an efficient biocontrol agent they must show different mechanisms of action when it comes to their antagonistic interaction with any fungal pathogens. Some good examples are the mycoparasitism, antibiotic activity, basic competitions for nutrients, induction of systematic resistance and cell wall lytic enzyme activity. Trichodermin, gliovirin and harzianic acid are the best known metabolites that being produced by Trichoderma species (Singh 2010). Strains such as T. viride, T. harzianum and T. atroviride are capable of producing pyrone (6-pentyl-2H-­ pyran-2-one). These metabolites are the main reason behind the release of coconut aroma. Pyrone is also known for its antifungal activity against plant pathogenic fungi. The fungus also produces cytosporone which show strong in vitro antibiotic activity against some pathogenic bacteria and fungi. Koninginis metabolites are also capable of inhibiting the growth of fungus such as Gaeumannomyces graminis var. It also can kill some of the soil-borne plant pathogens such as Fusarium oxysporum, Pythium middletonii, Rhizoctonia solani and many more (Vinale et al. 2006). These secondary metabolites in particular can prevent the spore germination by the fungal pathogens. According to Vinale et al. (2006), a secondary metabolite called T22 azaphilone from the liquid culture of T. harzianum was isolated. These metabolites inhibit several plant pathogens such as R. solani and G. graminis var. Trichoderma hamatum produces viridiol which reduces and at certain circumstances inhibits mycotoxin like aflatoxin which produced during the fungal interaction. So the usage of this secondary metabolites produced by Trichoderma strains can induce the resistance level of the host and also promote the yield of the crop which can be the most suitable replacement for the chemical usages. Due to the presence of the secondary metabolites, Trichoderma

252

H. A. El Enshasy et al.

strains can also be used as biofertilizers where there are two strains, namely Trichoderma harzianum T22 and T39 used as active agents for various commercial biopesticides and biofertilizers. Most of the fungus around the world has the ability to produce potential toxins in the form of antibiotics which can kill other pathogenic microbes regardless its concentration level. The differences in between these antibiotics somehow show different activities against both prokaryotes and eukaryotes. Paracelsin is the first antibiotic discovered that produced by the species Trichoderma. Most of the time it produces large compounds that have the antibiotic activity and this production is mainly dependent on the factors such as pH, temperature and quantity of microorganisms. A single Trichoderma species can produce different type of antibiotic compounds and likewise the given antibiotic has the potential of being produced by different strains. However, according to the study done by Sivasithamparam and Ghisalberti (2014), it revealed that different isolates of same species can produce different compounds as well. Trichoderma harzianum often leads to the production of antibiotic where the methanolic extract from the dual culture of this fungus showed strong antimicrobial activity against Staphylococcus aureus. Moreover, general Trichoderma species that can be found in marine habitat also known to produce bioactive metabolites such as antimycobacterial. According to the study conducted by Wu et al. (2014), from the culture of marine Trichoderma strain tentatively named as MF106, the particular strain shows antimicrobial effects towards human pathogenic strains such as Staphylococcus aureus. The strains also known to be used for the protection purpose of grapevine wounds from the infected trunk pathogens. In a nutshell, Trichoderma spp. can be used on a wide spectrum for both in  vitro and in  vivo (Kotze et al. 2011).

8.7.2  Production of Hydrolytic Enzymes Currently, most of important crops which have economic purposes largely are being destroyed by the pathogens fungi in particular which the most aggressive is soil-­ borne pathogen. There is some investigation being carried out in order to overcome this problem. One of the well-known steps is the usage of chemical pesticides to control the growth of these pathogenic microorganisms (Yadav et  al. 2018a, b). However, using chemical pesticides can cause long term effect towards the human health as well as the environment. Thus, eco-friendly alternatives have been approached to replace the usage of the chemical pesticides. Trichoderma fungus can be an eco-friendly replacement for the chemical pesticides due to its ability of producing hydrolytic enzymes. The cell wall of the fungus can able to produce hydrolytic enzymes such as cellulase, chitinase and more. This enzyme plays a pivotal role when it comes to the degradation of biomass (Schuster and Schmoll 2010). The cell wall of Trichoderma is mainly made up of β-1,3glucans and chitin and sometimes cellulose in some of the oomycetes. There are

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

253

some demonstrations that have been done to give a clear picture on how some of the Trichoderma strains produce hydrolytic enzymes to inhibit the growth of pathogenic microorganisms such as in case of Trichoderm harzianum. In most cases, the production of this enzymes mainly depends on factors such as availability of type of carbon source, presence of light, growth rate and secretion stress (Tisch and Schmoll 2013). Besides than the strain that have been mentioned above, Trichoderma reesei is another widely used strain which produces cellulose and the hemicellulose degrading enzyme. Both of these enzymes are highly used for industrial purposes. Häkkinen et al. (2012) mentioned that a complex system will be formed by the large number of carbohydrate active enzymes that being produced by the fungus which will be regulated by the series of environmental and physical factors. Trichoderma hamatum on the other hand possesses high antimicrobial activity mainly because it consists of specific β-glucanase and chitinase. Both of these enzymes play significant role when it comes to the cell wall degradation. According to Ahmed et al. (2009) three type of glucanases: exoglucanase (EXG), endoglucanase (EG), and β-glucosidase (BGL) have been isolated from Trichoderma harzianum. These enzymes also being used for malting, baking, alcohol production, paper and textile industries (Galante et al. 2014).

8.8  Conclusion and Future Prospect For many years, based on its GRAS status according to FDA, Trichoderma has been applied in agriculture to promote cell growth and control of plant diseases without any potential risk to the environment. However, the non-agriculture applications of this microbe are still very limited even it consider as one of the safest microbes without any potential pathogenicity to human and animal. Based on the high capacity of Trichoderma for the production of hydrolysis enzymes, primary and secondary metabolites, it is strongly believed that this microbe has very high potential in biotechnology industries. In addition, this microbe has high capacity to grow on wide range of cheap substrates as a result of the high capacity to produce wide range of hydrolases enzymes to breakdown the complex carbon and nitrogen sources. The high capacity for enzyme excretion makes it also a very attractive biofactory for native and recombinant enzyme production. These all together giving us the strong confident of the high potential future application of Trichoderma not only in green biotechnology (agriculture) but also in white biotechnology (industry) for the production of their own native and recombinant products. Acknowledgement  The authors are grateful for the support of the Ministry of Higher Education and HICoE program, Malaysia; CSIR, South Africa, College of Art, Science, and Commerce, Shahada Maharashtra, India; and De La Salle University, Philippines for providing the facility and supporting the network for this cooperative work.

254

H. A. El Enshasy et al.

References Abd-Elsalam KA, Almohimeed I, Moslem MA, Bahkali AH (2010) M13-microsatellite PCR and rDNA sequence markers for identification of Trichoderma (Hypocreaceae) species in Saudi Arabian soil. Genet Mol Res 9:2016–2024 Ahmed S, Bashir A, Saleem H, Saadia M, Jamil A (2009) Production and purification of cellulose-­degrading enzymes from a filamentous fungus Trichoderma harzianum. Pak J Bot 41:1411–1419 Atanasova L, Friedl MA, Bauer H, Puxbaum H, Kubicek CP, Druzhinina IS (2010) Metagenomic study of air borne diversity of mycoparasitic fungus Trichoderma (anamorph Hypocrea). In: Abstracts of the third joint conference of German society for hygiene and microbiology. P no. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, Samuels GJ, Choi IY, Holmes KA (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464 Benítez T, Rincón AM, Limón MC, Codón AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260 Bissett J, Gams W, Samuels GJ (2015) Accepted Trichoderma names in the year 2015. IMA Fungus 6:263–295 Brotman Y, Lisec J, Méret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma- induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158:139–146 Brotman B, Landau A, Cuadros-Inostroza A, Takayuki T, Fernie A, Chet I, Viterbo A, Willmitzer L (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9:e1003221 Chang YC, Baker R, Klefield O, Chet I (1986) Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. Plant Dis 70:145–148 Chaverri P, Gazis RO, Samuels GJ (2011) Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and H. guianensis from the Amazon basin. Mycologia 103:139–151 Chen XY, Qi YD, Wei JH, Zhang Z, Wang DL, Feng JD, Gan BC (2011) Molecular identification of endophytic fungi from medicinal plant Huperzia serrata based on rDNA ITS analysis. World J Microbiol Biotechnol 27:495–503 Colla G, Rouphael Y, Di ME, El-Nakhel C, Cardarelli M (2015) Co-inoculation of Glomus intraradices and Trichoderma atroviride acts as a sbiostimulant to promote growth, yield and nutrient uptake of vegetable crops. J Sci Food Agric 95:1706–1715 Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J, Muyzer G (2016) Ecological functions of spp. and their secondary metabolites in the rhizosphere: interactions with plants . FEMS Microbiol Ecol 92(4):fiw036 Dang L, Li G, Yang Z, Luo S, Zheng X, Zhang K (2010) Chemical constituents from the endophytic fungus Trichoderma ovalisporum isolated from Panax notoginseng. Ann Microbiol 60:317–320 Danielson RM, Davey CB (1973) The abundance of Trichoderma propagules and the distribution of species in forest soils. Soil Biol Biochem 5:485–494 Degenkolb T, Dieckmann R, Nielsen KF, Gräfenhan T, Theis C, Zafari D, Chaverri P, Ismaiel A, Brückner H, Von DH, Thrane U, Petrini O, Samuels GJ (2008) The Trichoderma brevi-­ compactum clade: a separate lineage with new species, new pep-taibiotics, and mycotoxins. Mycol Prog 7:177–219 Doni F, Al-Shorgani NKN, Tibin EMM, Abuelhassan NN, Anizan I, Che-Radziah CMZ (2013) Microbial involvement in growth of paddy. Curr Res J Biol Sci 5:285–290 Doni F, Isahak A, Zain CRCM, Ariffin SM, Mohamad WNW, Yusoff WMW (2014) Formulation of Trichoderma sp. SL2 inoculants using different carriers for soil treatment in rice seedling growth. Springerplus 3:532 Druzhinina IS, Komoń M, Kredics L, Hatvani L, Antal Z, Belayneh T, Kubicek CP (2008) Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

255

Trichoderma longibrachiatum, both capable to cause invasive mycoses of humans. Microbiol SGM 154:3447–3459 Druzhinina IS, Seidl SV, Herrera EA, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759 El-Hasan A, Walker F, Schöne J, Buchenauer H (2009) Detection of viridiofungin A and another antifungal metabolites excreted by Trichoderma harzianum active against different plant pathogens. Eur J Plant Pathol 124:457–470 Fontanelle ADB, Guzzo SD, Lucon CMM, Harakava R (2011) Growth promotion and induction of resistance in tomato plant against Pseudomonas euvesicatoria and Alternaria solani by Trichoderma spp. Crop Prot 30:1492–1500 Friedl MA, Druzhinina IS (2012) Taxon-specific metagenomics of Trichoderma reveals a narrow community of opportunistic species that regulate each other’s development. Microbiology 158(1):69–83 Galante Y, De Conti A, Monteverdi R (2014) Application of Trichoderma enzymes in the textile industry. Trichod Glioclad 2:311–325 Gal-Hemed I, Atanasova L, Komo-Zelazowsla M, Druzhinina IS, Viterbo A, Yarden O (2011) Marine isolates of Trichoderma spp. as potential halotolerant agents of biological control for arid-zone agriculture. Appl Environ Microbiol 77(15):5100–5109 Gokil-Prasad G, Sinha AP (2012) Comparative antagonistic potential of fungal and bacterial bioagents against isolates of Xanthomonas oryzae pv oryzae. Ann Plant Prot Sci 20(1):154–159 Hagn A, Wallisch S, Radl V, Charles MJ, Schloter M (2007) A new cultivation independent approach to detect and monitor common Trichoderma species in soils. J Microbiol Methods 69:86–92 Häkkinen M, Arvas M, Oja M, Aro N, Penttilä M, Saloheimo M, Pakula TM (2012) Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb Cell Factories 11:134 Hanada RE, De JS, Pomella AW, Hebbar KP, Pereira JO, Ismaiel A, Samuels GJ (2008) Trichoderma martiale sp. nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycol Res 112:1335–1343 Hansen VM, Winding A, Madsen AM (2010) Exposure to bioaerosols during the growth season of tomatoes in an organic greenhouse using Supresivit (Trichoderma harzianum) and Mycostop (Streptomyces griseoviridis). Appl Environ Microbiol 76:5874–5881 Hermosa M, Grondona I, Et I, Diaz-Minguez J, Castro C, Monte E, Garcia-Acha I (2000) Molecular characterization and identification of biocontrol isolates of Trichoderma spp. Appl Environ Microbiol 66:1890–1898 Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25 Inch S, Gilbert J (2011) Scanning electron microscopy observations of the interaction between Trichoderma harzianum and perithecia of Gibberella zeae. Mycologia 103:1–9 Kashyap PL, Kumar S, Srivastava AK (2017) Nanodiagnostics for plant pathogens. Environ Chem Lett 15:7–13 Kaur T, Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Dhaliwal HS, Saxena AK (2020) Microbe-mediated biofortification for micronutrients: Present status and future challenges. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 1–17. https://doi.org/10.1016/B978-0-12-820528-0.00002-8 Kotze C, Van Niekerk J, Halleen F, Mostert L, Fourie P (2011) Evaluation of biocontrol agents for grapevine pruning wound protection against trunk pathogen infection. Phytopathol Mediterr 50:247–263 Kour D, Rana KL, Kaur T, Singh B, Chauhan VS, Kumar A, Rastegari AA, Yadav N, Yadav AN, Gupta VK (2019a) Extremophiles for hydrolytic enzymes productions: biodiversity and potential biotechnological applications. In: Molina G, Gupta VK, Singh B, Gathergood N (eds)

256

H. A. El Enshasy et al.

Bioprocessing for biomolecules production. Springer, New  York, pp  321–372. https://doi. org/10.1002/9781119434436.ch16 Kour D, Rana KL, Yadav N, Yadav AN, Kumar A, Meena VS, Singh B, Chauhan VS, Dhaliwal HS, Saxena AK (2019b) Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: Kumar A, Meena VS (eds) Plant growth promoting rhizobacteria for agricultural sustainability: from theory to practices. Springer, Singapore, pp 19–65. https://doi.org/10.1007/978-981-13-7553-8_2 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019c) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, volume 2: perspective for value-added products and environments. Springer, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kredics L, Láday M, Körmöczi P, Manczinger L, Rákhely G, Vágvölgyi C, Szekeres A (2011) Trichoderma communities of the winter wheat rhizosphere. Agrár-és Vidékfejlesztési Szemle 6:413–418 Kumar V, Joshi S, Pant NC, Sangwan P, Yadav AN, Saxena A, Singh D (2019) Molecular approaches for combating multiple abiotic stresses in crops of arid and semi-arid region. In: Singh SP, Upadhyay SK, Pandey A, Kumar S (eds) Molecular approaches in plant biology and environmental challenges. Springer, Singapore, pp  149–170. https://doi. org/10.1007/978-981-15-0690-1_8 Liang C, Li B, Lu G (2004) Gliocladium and Trichoderma in agricultural soil. J Zhejiang Univ Agric Life Sci 30:415–424 Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417 Madsen AM, Hansen VM, Meyling NV, Eilenberg J (2007) Human exposure to airborne fungi from genera used as biocontrol agents in plant production. Ann Agric Environ Med 14:5–24 Mastouri F, Bjorkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221 Meincke R, Weinert N, Radl V, Schloter M, Smalla K, Berg G (2010) Development of a molecular approach to describe the composition of Trichoderma communities. J Microbiol Methods 80:63–69 Ming Q, Han T, Li W, Zhang Q, Zhang H, Zheng C, Huang F, Rahman K, Qin L (2012) Tanshinone IIA and tanshinone I production by Trichoderma atroviride D16, an endophytic fungus in Salvia miltiorrhiza. Phytomedicine 19:330–333 Mukherjee PK, Horwitz BA, Kenerley CM (2012) Secondary metabolism in Trichoderma–a genomic perspective. Microbiology 158:35–45 Nagy V, Seidl V, Szakacs G, Komoń-Zelazowska M, Kubicek CP, Druzhinina IS (2007) Application of DNA bar codes for screening of industrially important fungi: the Haplotype of Trichoderma harzianum sensu stricto indicates superior chitinase formation. Appl Environ Microbiol 73(21):7048–7058 Naeimi S, Khodaparast SA, Javan NM, Vágvölgyi CS, Kredics L (2011) Species patterns and phylogenetic relationships of Trichoderma strains in rice fields of southern Caspian Sea, Iran. Cereal Res Commun 39:560–568 Nawaz K, Shahid AA, Bengyella L, Subhani MN, Ali M, Anwar W, Iftikhar S, Ali SW (2018) Diversity of Trichoderma species in chili rhizosphere that promote vigor and antagonism against virulent Phytophthora capsici. Sci Hortic 239:242–252 Neuhof T, Dieckmann R, Druzhinina IS, Kubicek CP, Nakari ST, Penttilä M, Von DH (2007) Direct identification of hydrophobins and their processing in Trichoderma using intact-cell MALDI-TOF MS. FEBS J 274:841–852 Pavone M, Domenico F (2012) Biocontrol de Rhizoctonia solani Kühn por Trichoderma spp (Ph.D. thesis). Universidad Central de Venezuela

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

257

Photita W, Lumyong S, Lumyong P (2001) Endophytic fungi of wild banana (Musa acuminata) at doi Suthep Pui National Park, Thailand. Mycol Res 105:1508–1513 Pocasangre L, Sikora R, Vilich V, Schuster R (2000) Survey of banana endophytic fungi from central America and screening for biological control of the burrowing nematode (Radopholus similis). Info Musa 9:3–5 Posada F, Aime MC, Peterson SW, Rehner SA, Vega FE (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol Res 111:748–757 Quilliam RS, Jones DL (2010) Fungal root endophytes of the carnivorous plant Drosera rotundifolia. Mycorrhiza 20:341–348 Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Springer, Cham, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rana KL, Kour D, Yadav N, Yadav AN (2020) Endophytic microbes in nanotechnology: current development, and potential biotechnology applications. In: Kumar A, Singh VK (eds) Microbial endophytes. Woodhead Publishing, Cambridge, pp 231–262. https://doi.org/10.1016/ B978-0-12-818734-0.00010-3 Rastegari AA, Yadav AN, Yadav N, Tataei Sarshari N (2019) Bioengineering of secondary metabolites. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  55–68. https://doi.org/10.1016/ B978-0-444-63504-4.00004-9 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge Rawat L, Singh Y, Shukla N, Kumar J (2011) Alleviation of the adverse effects of salinity stress in wheat (Triticum aestivum L.) by seed biopriming with salinity tolerant isolates of Trichoderma harzianum. Plant Soil 347:387–400 Rubini MR, Silva RT, Pomella AW, Maki CS, Araújo WL, Dos S, Azevedo JL (2005) Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. Int J Biol Sci 1:24 Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Herrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol 131:15–26 Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssöne E, Bathia A, Ward M, Pentilla M (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269:4202–4211 Samuels GJ, Dodd SL, Lu BS, Petrini O, Schroers HJ, Druzhinina IS (2006) The Trichoderma koningii aggregate species. Stud Mycol 56:67–133 Samuels GJ, Ismaiel A, Mulaw TB, Szakacs G, Druzhinina IS, Kubicek CP, Jaklitsch WM (2012a) The Longibrachiatum clade of Trichoderma: a revision with new species. Fungal Divers 55:77–108 Samuels GJ, Ismaiel A, De SJ, Chaverri P (2012b) Trichoderma stromaticum and its overseas relatives. Mycol Prog 11:215–254 Saxena AK, Yadav AN, Rajawat M, Kaushik R, Kumar R, Kumar M, Prasanna R, Shukla L (2016) Microbial diversity of extreme regions: an unseen heritage and wealth. Indian J Plant Genet Resour 29:246–248

258

H. A. El Enshasy et al.

Schuster A, Schmoll M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87:787–799 Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P, Thakur S, Thakur N, Sudheer S, Yadav N, Yadav AN, Rastegari AA, Singh K (2019) Trichoderma: biodiversity, ecological significances, and industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Springer, Cham, pp 85–120. https://doi.org/10.1007/978-3-030-10480-1_3 Sikora RA, Pocasangre L, Felde A, Niere B, Vu TT, Dababat A (2008) Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes. Biol Control 46:15–23 Singh RK (2010) Trichoderma: a bio-control agent for management of soil borne diseases Singh A, Kumari R, Yadav AN, Mishra S, Sachan A, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Awasthi AK, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–16. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Sivasithamparam K, Ghisalberti E (2014) Secondary metabolism in Trichoderma. Trichoderma and Gliocladium volume 1: basic biology, taxonomy. Genetics 1:139 Studholme DJ, Harris B, LeCocq K, Winsbury R, Perer AV, Ryder L, Ward JL, Beale MH, Thornton CR, Grant M (2013) Investigating the beneficial traits of Trichoderma hamatum GD 12 for sustainable agriculture-insights from genomics. Front Plant Sci 4:258 Suárez-Estrella F, Ros M, Vargas-García MC, López MJ, Moreno J (2014) Control of Xanthomonas campestris pv. vesicatoria using agroindustrial wasted-based compost. J Plant Pathol 96(2):243–248 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh D, Abhilash P, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, research perspectives. Springer, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7 Sun R, Liu Z, Fu K, Fan L, Chen J (2012) Trichoderma biodiversity in China. J Appl Genet 53:343–354 Tisch D, Schmoll M (2013) Targets of light signalling in Trichoderma reesei. BMC Genomics 14:657 Utkhede R, Koch C (2004) Biological treatments to control bacterial canker of greenhouse tomatoes. Biocontrol 49:305–313 Vasanthakumari MM, Shivanna MB (2011) Fungal assemblages in the rhizosphere and rhizoplane of grasses of the subfamily Panicoideae in the Lakkavalli region of Karnataka, India. Microbes Environ 26:228–236 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017a) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-­ ecological perspectives: volume 2: microbial interactions and agro-ecological impacts. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017b) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crops improvement. Plant-microbe interactions in agro-ecological perspectives. Springer, New York, pp 543–580 Vinale F, Marra R, Scala F, Ghisalberti E, Lorito M, Sivasithamparam K (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148 Vipul K, Mohammad S, Muksesh S, Sonika P, Anuradha S (2014) Role of secondary metabolites produced by commercial Trichoderma species and their effect against soil borne pathogens. Biosens J 3:2 Wang C, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-­ carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gac A derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46:898–907

8  Trichoderma: Biocontrol Agents for Promoting Plant Growth and Soil Health

259

Woo SL, Lorito M (2007) Exploiting the interactions between fungal antagonists, pathogens and the plant for biocontrol. Novel biotechnologies for biocontrol agent enhancement and management. Springer, Amsterdam, pp 107–130 Wu B, Oesker V, Wiese J, Schmaljohann R, Imhoff JF (2014) Two new antibiotic pyridones produced by a marine fungus, Trichoderma sp. strain MF106. Mar Drugs 12:1208–1219 Xia X, Lie TK, Qian X, Zheng Z, Huang Y, Shen Y (2011a) Species diversity, distribution, and genetic structure of endophytic and epiphytic Trichoderma associated with banana roots. Microb Ecol 61:619–625 Xia X, Lie TK, Qian X, Zheng Z, Huang Y, Shen Y (2011b) Species diversity, distribution, and genetic structure of endophytic and epiphytic Trichoderma associated with banana roots. Microb Ecol 61:619–625 Yadav AN (2019) Fungal white biotechnology: conclusion and future prospects. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 3: perspective for sustainable environments. Springer, Cham, pp 491–498. https://doi. org/10.1007/978-3-030-25506-0_20 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018a) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, Cambridge, pp 305–332 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018b) Biodiversity of the Genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering, Penicillium system properties and applications. Elsevier, Amsterdam, pp  3–18. https://doi.org/10.1016/ B978-0-444-63501-3.00001-6 Yadav AN, Kour D, Rana KL, Yadav N, Singh B, Chauhan VS, Rastegari AA, Hesham AE-L, Gupta VK (2019a) Metabolic engineering to synthetic biology of secondary metabolites production. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp  279–320. https://doi.org/10.1016/ B978-0-444-63504-4.00020-7 Yadav AN, Singh S, Mishra S, Gupta A (2019b) Recent advancement in white biotechnology through fungi, volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N, Kour D (2020b) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020d) Plant microbiomes for sustainable agriculture. Springer, Cham Zhang C, Druzhinina I, Kubicek CP, Xu T (2005) Trichoderma bio-diversity in China: evidence for a North to South distribution of species in East Asia. FEMS Microbiol Lett 251:251–257 Zhang CL, Liu SP, Lin FC, Kubicek CP, Druzhinina IS (2007) Trichoderma taxi sp. nov., an endophytic fungus from Chinese yew Taxus mairei. FEMS Microbiol Lett 270:90–96

Chapter 9

Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance and Disease Resistance Fatma A. Abo Nouh, Hebatallah H. Abo Nahas, and Ahmed M. Abdel-Azeem

Contents 9.1  9.2  9.3  9.4 

Introduction History of P. indica and Systemic Position The Diversity of P. indica and Plant Habitat P. indica Strategies for Root Colonization and Interaction Structures 9.4.1  Endophytic and Necrotrophic Mode of Life 9.4.2  Biotrophic Interaction with Living Plant Cells 9.5  Effects of Biotic and Abiotic Stresses on Plants 9.6  P. indica Fungal Endophytes for Conferring Salt Stress Tolerance 9.7  P. indica Fungal Endophytes for Conferring Disease Resistance 9.8  Applications and Recent Researches in P. indica 9.9  Conclusion and Future Prospects References

 261  262  263  264  266  266  266  271  273  274  276  277

9.1  Introduction Increased incidences of abiotic and biotic stresses impacting productivity in important crops are being witnessed all over the world. The problem of soil drought and salinity presents one of the greatest problems in agriculture. Many keys to agricultural success in arid and semiarid areas are to use adequate plant species and to use the soil biology potential to maintain soil fertility, to guard against abiotic stress (Kour et al. 2020a; Zarea et al. 2013) and biotic stress (Dresselhaus and Hückelhoven 2018). The fungal endophytes provide immune system to host plant to defend F. A. Abo Nouh · A. M. Abdel-Azeem (*) Systematic Mycology Laboratory, Botany Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt H. H. Abo Nahas Zoology Department, Faculty of Science, Suez Canal University, Ismailia, Egypt © Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_9

261

262

F. A. Abo Nouh et al.

against phytopathogenic organisms (Jain and Pundir 2017; Rana et al. 2019a) and help plants to adapt to new habitats and against abiotic stress by making genetical, physiological, and ecological modification to its host plants (Lugtenberg et al. 2016; Ali et  al. 2018; Yadav et  al. 2019c). Focusing on fungal microbe’s endophytes P. indica were defined as organisms that colonize in living plant tissue during their entire life cycle (Kusari and Spiteller 2012; Anitha et al. 2013; Lugtenberg et al. 2016; Arora and Ramawat 2017; Jain and Pundir 2017; Khare et al. 2018; Lata et al. 2018; Abo Nouh 2019; Chhipa and Deshmukh 2019); and live in a broad variety of host plant species (e.g., barley, maize, parsley, poplar, tobacco, and wheat) without causing disease symptoms (Desisa 2017). The symbiotic fungus P. indica displays an endophytic lifestyle and has the ability to colonize the root cortex cells of a wide range of mono- and dicotyledonous plants, displaying a broad range of beneficial effects to the host (Baltruschat et al. 2008; Sherameti et al. 2005, 2008; Waller et al. 2005; Yadav et al. 2010; Lahrmann and Zuccaro 2012). The root endophyte fungus P. indica enhances the tolerance of colonized plants against drought, acidity, heavy metals, and various other abiotic stresses as well as biotic stresses (microbial pathogens/insects), promotes nutrient uptake, and stimulates growth and seed production (Verma et al. 1998; Varma et al. 1999; Sahay and Varma. 1999; Peškan-Berghöfer et al. 2004; Waller et al. 2005, 2008; Oelmüller et al. 2009; Krishnaveni et al. 2014; Basu et al. 2016; Justice et al. 2018; Xu et al. 2018).

9.2  History of P. indica and Systemic Position During a routine isolation of AM fungi in the desert Thar (Rajasthan, India), Verma and his collaborators were isolated P. indica for the first time from the soil of two xerophytic plants, namely Prosopis juliflora and Ziziphus nummularia as a contaminant (Verma et al. 1998; Varma et al. 2013). At the first superficial view it seems that the isolated spore is a vesicle of an AM fungus and belongs to a fungus of the Glomeromycota. But this spore was well growing on artificial complex media (P. indica can be easily cultivated in axenic culture). Therefore, this species could not be a member of the Glomeromycota because Glomeromycota are growing in biotrophic interaction with plants only (Verma et al. 1998). The isolated fungus was described as a new species of family Sebacinaceae, order Sebacinales, phylum Hymenomycetes, Basidiomycota. The fungus was named P. indica based on its characteristic pear-shaped chlamydospores (Verma et al. 1998; Varma et al. 1999; Kost and Rexer 2013; Varma et al. 2013; Krishnaveni et al. 2014; Pan et al. 2017). P. indica, an axenically cultivable phytopromotional, is a biotrophic mutualistic root endosymbiont and has been reported to mimic capabilities of typical arbuscular mycorrhizal (AM) fungi (Gill et al. 2016). They also lack cystidia and structures formed during cytokinesis on some basidiomycetous hyphae, the so-called clamp connections. Like other cultivable species of the Sebacinales, P. indica forms moniliod hyphae, which look like pearls in a chain (Selosse et al. 2007). The first

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

263

experiments with P. indica revealed that the co-cultivation of the fungus together with young maize seedlings causes a strong support for the growth of their shoots (Kost and Rexer 2013).

9.3  The Diversity of P. indica and Plant Habitat P. indica is a cultivable fungus and can grow on synthetic media without a host (Verma et al. 1998; Peškan-Berghöfer et al. 2004). The host range includes trees, agricultural, horticultural, monocots, dicots, and mosses (Glen et al. 2002; Peškan-­ Berghöfer et  al. 2004; Barazani et  al. 2005; Sherameti et  al. 2005; Waller et  al. 2005), suggesting that the interaction is based on general recognition and signaling processes (Camehl et al. 2013). Inoculation of a broad variety of plants with P. indica had a positive effect on their general biomass production (Varma et al. 1999), and subsequent analyses showed that P. indica exerts a variety of physiological effects. It promotes the establishment of micro-propagated plants (Sahay and Varma 1999), adventitious root formation in cuttings, and lignan production of hairy root cultures; enhances flowering; increases yield; and induces higher tolerance of and resistance to abiotic and biotic stresses (Waller et al. 2005). P. indica has been termed as plant probiotic because of its plant growth-­promoting activity and its role in enhancement of the tolerance of the host plants against abiotic and biotic stresses (Basu et al. 2016). The fungus possesses unique properties to act as biofertilizer, bioprotector, and immunoregulator. It also plays a key role in protecting roots from insects by increasing the tolerance of the host roots (Varma et al. 1999; Waller et al. 2005; Serfling et al. 2007; Prasad et al. 2008; Bagde et al. 2010). The underlying mechanism of the fungus beneficial activity is not yet understood, but it is observed that the plant antioxidant system is activated and thus implicated in the improvement of abiotic and biotic stress tolerance (Waller et al. 2005; Varma et al. 2013). P. indica is capable to colonize with the root of both gymnosperm and angiosperm and the colonization is restricted to the rhizodermis (Deshmukh et al. 2006). P. indica tremendously improves the growth and overall biomass of diverse hosts including legumes (Verma et  al. 1998; Varma et  al. 1999); industrial crops (Singh et al. 2011); important plants such as Oryza sativa, Zea mays, Tridax procumbens, Nicotiana tabacum, Arabidopsis thaliana, and Brassica oleracea var. capitata (Varma et al. 2012a); tobacco (Tanha et al. 2014); the agriculturally important barley, the model plants (Lugtenberg et al. 2016); and medicinal plants such as Artemisia annua, Abrus precatorius, Azadirachta indica, Bacopa monnieri, Curcuma longa, Linum album, Stevia rebaudiana, Trigonella foenum-graecum (Oelmüller et al. 2009, Kumar et al. 2017). It colonizes the root cortex, grows interand intracellularly, forms pear-shaped spores within the cortex and extramatrically, and does not invade the endodermis and the aerial parts of the plants (Oelmüller et al. 2009; Abo Nouh 2019). This fungus can colonize roots of a wide range of higher plants and provide plants with multifaceted amenities such as nutrient uptake, disease resistance, stress

264

F. A. Abo Nouh et al.

tolerance, and growth promotion involving value addition (Unnikumar et al. 2013). Interaction between P. indica and Chinese cabbage (Brassica campestris cv. Chinensis) results in growth and biomass promotion of the host plant and in particular in root hair development (Dong et al. 2013). P. indica can be cultivated easily on synthetic media and colonized with cabbage and spinach of Brassicaceae family, in contrast to Arbuscular mycorrhizal fungi (AMF) (Bagheri et al. 2014). Unlike AM fungi, P. indica can grow without a plant host. This characteristic is advantageous for mass production and potential commercialization because production does not require the additional complexity of growing plants to rear the fungus. P. indica also colonizes plants that AM fungi cannot, such as members of the Brassicaceae family (Deshmukh et al. 2006) and members of Cruciferae family (Gosal et al. 2013). P. indica has been reported to perform multifarious functions e.g. biological hardening during transplantation of micro-propagated plantlets (Singh et al. 2003), and increased endogenous content of spilanthol after realization of its mutual interaction with medicinal plants such as Spilanthes calva (Rai et al. 2004). P. indica colonizes the epidermal and rhizodermal parts of the Arabidopsis roots and root hairs, and forms pear-shaped spores. The hyphae never invade the endodermis or central meristematic tissue of the root and never proceed to aerial systems, stem, or foliage. Propagation of the fungus does not only exclusively occur within the cells, but also at the root surface and in its environment (soil system). Interaction between the two partners leads to growth promotion of the seedlings (Oelmüller et al. 2009). P. indica infestation in Helianthus annuus and Aristolochia elegans has resulted into the stimulated synthesis of valuable compounds (Bagde et al. 2010; Gill et al. 2016). Mutualistic fungi P. indica, added to propagation media, have been shown to increase root weight and root initiation in a range of plant species, including dwarf umbrella tree (Schefflera arboricola), anglojap yew (Taxus media), bearberry (Arctostaphylos uva-ursi), geranium (Pelargonium sp.), rose (Rosa ‘Scarlet Cupido’), malabar nut (Adhatoda vasica), and poinsettia (Justice et al. 2018).

9.4  P  . indica Strategies for Root Colonization and Interaction Structures One of the specific features of P. indica is the ability to interact with the roots of many plant species of different taxa. The morphology of the interacting structures depends on the involved partners. These interacting partners could be mosses, ferns, gymnosperms, and angiosperms (Kost and Rexer 2013). Some facts related with the lifestyle and the mechanisms underlying root colonization of P. indica from its interaction with many plants (such as Hordeum vulgare and Arabidopsis thaliana) have been unraveled (Deshmukh et al. 2006; Schäfer and Kogel 2009). Within the host plant root tissues, structures similar to arbuscules and vesicles occur in the intercellular spaces as well as may be packed intracellularly which enhances the interaction interface among the microsymbiont and the host plant tissues or may act

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

265

as storage organ of the microsymbiont (Gosal et al. 2013). All plant species, which are able to form one of the different mycorrhizal types, can be used by Piriformospora as a host (Kost and Rexer 2013). Generally, symbionts colonize rhizodermal and cortical cell layers of roots. The sites of P. indica infection include the root tip, root hairs, and the root differentiation zone from where the fungus reaches the cortical tissue and starts producing spores in epidermis and cortex within a week. The intracellular existence of this fungus indicates its potential to exist inside root cells as hyphae and spores, without provoking tissue necrotization (Deshmukh et al. 2006; Gosal et al. 2013). Root colonization by P. indica is also known to start within interacellular chlamydospore germination and forming extracellular hyphal mats, and simultaneously penetrating rhizodermal and cortical cells (Deshmukh et al. 2006; Jacobs et al. 2011). The fungus either colonizes roots intracellularly via rhizodermal cells or penetrates cortical cells after an initial intercellular growth phase. Root colonization gradiently increases with tissue age as the maturation zone is predominantly colonized, while the fungus is almost absent at the meristematic zone. Accordingly, sporulation is mainly found at extracellular regions of the maturation zone in addition to intracellular sporulation at rhizodermal and cortical cells of the same tissue (Jacobs et al. 2013). P. indica forms typical pyriform chlamydospores which act as perennation bodies similar to the AM spores and forms extended hyphal structures that ramify the soil in vicinity of the host roots hunting and accumulating nutrients like phosphorus, iron, manganese, zinc, and many more from a diameter of several square meters of the soil (Gosal et al. 2013). The colonization patterns of the various root regions harbor some quantitative as well as qualitative differences, which distinguish P. indica on H. vulgare and A. thaliana from endomycorrhizal fungi. The fungal root colonization increases with root maturation and the highest fungal biomass has been found in the differentiation, particularly in the root hair zones (Deshmukh et al. 2006). Importantly, the physiological activity of host cells has been considered as a prerequisite for efficient nutrient exchange between the symbiotic partners (Schäfer and Kogel 2009). Thus, root colonization pattern of P. indica differs from than that of AM fungi, which are known to prefer entially colonize younger root parts (Gill et al. 2016). P. indica with plants, especially emphasizing its life strategies in host plants, has shown that root colonization by P. indica and its lifestyle in plant may vary depending on the environmental factors, the genetic predisposition, and the developmental stage of host plants and plant organs, respectively (Desisa 2017). Interaction structures occur in P. indica by two ways according to Kost and Rexer (2013): Endophytic and Necrotrophic Mode of Life and Biotrophic Interaction with Living Plant Cells.

266

F. A. Abo Nouh et al.

9.4.1  Endophytic and Necrotrophic Mode of Life The fungal colonization of roots begins with a biotrophic growth phase, in which living cells are colonized, and followed by a cell death dependent phase, in which root cells are actively killed by the fungus (Qiang et al. 2011; Yadav et al. 2020c, d). P. indica is able to destroy the cells at the beginning of the interaction and behaves itself like a necrotrophic parasite in some cases (Deshmukh et al. 2006; Kogel et al. 2006; Schäfer et al. 2007). If hyphae of P. indica invade into a plant cell, the hyphal tip forms a small inconspicuous appressorium on the surface of the outer wall of the rhizoids or root cells. After the plant cell wall is locally dissoluted by fungal enzymes, the hyphal tip intrudes into the plant cell. Mostly the invaded root cells of plant species are killed before infection, or they die off during the contact phase of the hyphae. The fungal hyphae cross the cell wall with thin penetration peg. The cell content will be saprophytically decomposed by the fungus. Very often P. indica develops its chlamydospores inside these dead root cells (Kost and Rexer 2013). The established fungus is located within the root’s cortical cells but does not colonize or damage meristematic cells (Harman and Uphoff 2019).

9.4.2  Biotrophic Interaction with Living Plant Cells It possesses genes for a biotrophic lifestyle, and lacks genes for nitrogen metabolism, but also shares characteristics with symbiotic fungi and obligates biotrophic pathogens (Zuccaro et al. 2011). In contrast to the widely distributed necrotrophic type of interaction between the hyphae of P. indica and the root cells of plants, a small group of plants have developed an equilibrated biotrophic interaction between the hyphae of P. indica and the living cells of the plant. In case of this interaction, the invading hyphae of P. indica do not destroy the invaded cells of host plant. This interaction could be interpreted as biotrophic and mutualistic (Kost and Rexer 2013).

9.5  Effects of Biotic and Abiotic Stresses on Plants Due to global warming, and potential climate abnormalities associated with it, plants have evolved to live in environments where they are often exposed to number of abiotic and biotic stress combinations (Rastegari et  al. 2020a, b; Yadav et  al. 2020e). Being sessile, they have developed specific mechanisms that allow them to detect precise environmental changes and respond to complex stress conditions, minimizing damage while conserving valuable resources for growth and reproduction (Fig. 9.1). Plants activate a specific and unique stress response when subjected to a combination of multiple stresses (Atkinson and Urwin 2012). Based on the number of interacting factors, stresses can be grouped into three categories: single,

267

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

Insects

Mites

Fungi

Light

Bacteria

Drought Heat

Viruses

Heat

Viruses

Drought

Bacteria

Salt

Fungi

Nutrient

Insects Nematodes

Mites

Fig. 9.1  Abiotic and biotic stress factors on plant

multiple individual, and combined stresses. A single stress represents only one stress factor affecting plant growth and development, whereas multiple stresses represent the impact of two or more stresses occurring at different time periods without any overlap (multiple individual) or occurring concurrently with at least some degree of overlap between them (combined) (Singh and Yadav 2020; Yadav et al. 2020a, b). The co-occurrence of drought and heat stresses during summer is an example of a combined abiotic stress, whereas a bacterial and fungal pathogen attacking a plant at the same time represents a case of combined biotic stress (Kour et al. 2020a, b; Pandey et al. 2017). Plants are faced with numerous biotic stresses and adverse environmental conditions. They respond to these stresses through several morphological, biochemical, and molecular mechanisms and evidence suggests that there are interactions among their respective signaling pathways (Gimenez et al. 2018; Kour et al. 2020c; Yadav et al. 2017). Abiotic stress factors such as heat, cold, drought, salinity, and nutrient stress have a huge impact on world agriculture, and it has been suggested that they reduce average yields by >50% for most major crop plants (Yadav and Yadav 2018; Wang et al. 2003; Atkinson and Urwin 2012). Abiotic stresses have become an integral part of crop production. In general, plants suffer from dehydration or osmotic stress under drought, salinity, and low temperature condition which causes reduced availability of water (dehydration) for cellular function and maintenance of cellular turgor pressure (Kumar et al. 2019a; Varma et al. 2013; Yadav et al. 2019e). Plants become nutrient deficient and lose their normal physiological pattern of growth and

268

F. A. Abo Nouh et al.

development due to varying levels of acidic conditions; early exposure to salinity results in ion toxicity; drought decreases germination rates, causes inhibition of photosynthesis, loss of membrane integrity, and increased generation of reactive oxygen species (Lata et al. 2018; Yadav et al. 2019a). Drought, heat, and salt stress affect plant–water relations triggering complex plant responses, which include increased production of osmolytes (Bohnert et al. 1995; Wang et al. 2003; Verma et al. 2017). Osmotic potential is determined primarily by two components: solute potential and matrix potential, and it is likely that symbiotic fungi contribute to the matrix potential, which is particularly important in helping plants retain water and thereby enhance plant drought tolerance (Rodriguez et al. 2008). Plant growth is greatly affected by drought stress and plants must adapt to this stress to survive (Xiong et al. 2002; Bartels and Sunkar 2005; Yamaguchi-­ Shinozaki and Shinozaki 2006, Shinozaki and Yamaguchi-Shinozaki 2007). Drought and salinity are two major environmental factors determining plant productivity and plant distribution (Rana et al. 2019b; Yadav et al. 2018a, b). Drought and salinity affect more than 10% of arable land, and desertification and salinization are rapidly increasing on a global scale declining average yields for most major crop plants by more than 50% (Bartels and Sunkar 2005; Kour et al. 2019a, c). Salt stress affects plants in numerous ways such as ion toxicity, nutritional disorders, physiological drought, oxidative stress, modification of metabolic processes, membrane incompetence, and reduction of cell division. When plant is exposed to high salt at germination it causes physiological drought and reduction in leaf expansion (Kumar et al. 2019b, c). The osmotic effects of salinity stress can be observed immediately after salt application and are believed to continue for the duration of exposure, resulting in inhibited cell expansion and cell division, as well as stomatal closure (Munns 2002). Exposure to drought or salt stress triggers many common reactions in plants. Both stresses lead to cellular dehydration, which causes osmotic stress and removal of water from the cytoplasm into the extracellular space resulting in a reduction of the cytosolic and vacuolar volumes. Another consequence is the production of reactive oxygen species which then in turn affects cellular structures and metabolism negatively (Bartels and Sunkar 2005). One of the severe factors is salt accumulation in soil, limiting the productivity of plants, that causes adverse effects on germination, plant growth, and crop yield (Munns and Tester 2008). Salt stress causes loss of water use efficacy, increases ions, induces heat stress, and reduces stem extension. Biological macromolecules are damaged due to production of free ions. It was found that salinity stress resulted in decrease of water content, accumulation of hydrogen peroxide, and electrolyte release in plants (Batool et al. 2014). High salt concentration in soil is a main factor that limits the yield of agricultural crops (Munns and Tester 2008). High salinity affects plants in two main ways: high concentrations of salts in the soil disturb the capacity of roots to extract water and high concentrations of salts within the plant itself can be toxic, resulting in an inhibition of many physiological and biochemical processes such as nutrient uptake and assimilation (Carillo et al. 2011). At low salt concentrations, yields are mildly affected or not affected at all. As the concentrations increase, the yields move towards zero, since most plants,

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

269

glycophytes, including most crop plants, will not grow in high concentrations of salt and are severely inhibited or even killed by 100–200 mM NaCl. The reason is that they have evolved under conditions of low soil salinity and do not display salt tolerance (Carillo et al. 2011). Salt stress has been shown to affect carbohydrate partitioning and metabolism, leading to the synthesis of new compounds. In plants exposed to salinity, the total nonstructural carbohydrate content in the leaves was reduced significantly compared with plants that are not exposed to salinity. The decrease in total soluble carbohydrates due to salinity could also be related to limited carbohydrate availability as a consequence of a decline in photosynthesis (Zarea et al. 2013). Drought stress induces a range of physiological and biochemical responses in plants such as stomatal closure, repression of growth and photosynthesis, and activation of respiration (Kour et al. 2019b; Yadav et al. 2019b; Singh et al. 2011). Heat and drought stress in particular can cause disproportionate damage to crops compared with either stress individually. However, when examining the effects of an abiotic stress with simultaneous impact of a pathogen or herbivore, both positive and negative interactions have been observed depending on the timing, nature, and severity of each stress. An increase in temperature can create a negative interactive effect by lowering resistance to bacterial, viral, fungal, and nematode pathogens: in wheat (Atkinson and Urwin 2012; Verma et  al. 2016, 2019). Drought stress can cause detrimental effects to plant pathogen resistance. In both sorghum and the common bean, drought-treated plants had a higher susceptibility to the charcoal rot fungus Macrophomina phaseolina. Similarly, drought stress increased the spread of fungal and bacterial leaf scorch symptoms on date. Exposure of Arabidopsis to drought stress allowed greater infection levels of an avirulent isolate of P. syringae (Atkinson and Urwin 2012). Drought is one of the major abiotic stress limiting plants growth and productivity in many areas of the world. Expansion of drought leads to osmotic stress, specific ions toxicity, and ionic imbalances (Tanha et  al. 2014). Drought stress induces a range of physiological and biochemical responses in plants such as stomatal closure (Schroeder et al. 2001). Prolonged water stress causes decline in leaf water potential and stomatal opening, reduces leaf size, suppresses root growth, reduces seed number, size, and viability, delays flowering and fruiting, and limits plant growth and productivity, while high salinity and drought have been the major causes of osmotic stress to plants (Lata et al. 2018). Upon exposure to heat stress, non-symbiotic panic grass and tomato plants significantly increased osmolyte concentrations as predicted. Increased osmolyte concentrations correlated with the development of subsequent wilting and desiccation symptoms prior to plant death (Rodriguez et al. 2008). Higher temperature results in extensive denaturation and aggregation of cellular proteins, which, if unchecked, lead to cell death. Low temperature impairs metabolic processes, through alterations in membrane properties, changes in structure of proteins and interactions between macromolecules as well as inhibition of enzymatic reactions (Lata et al. 2018). Heavy metals interfere with numerous biochemical and physiological

270

F. A. Abo Nouh et al.

processes including photosynthesis, respiration, nitrogen and protein metabolism, and nutrient uptake (Lata et al. 2018). The plant has to bear several biotic stresses like the infection by a variety of phytopathogens belonging to diverse groups of viruses, bacteria, fungi, nematodes, insects, and higher animals particular concern for the herbivores (Gosal et al. 2013). Biotic stresses mainly result in disease in plants. Microorganisms can cause plant wilt, leaf spots, root rot, seed damage, and many more problems. Insects can cause severe physical damage to plants, including to the leaves, stem, bark, and flowers. Insects’ canals act as a vector of viruses and bacteria from infected plants to healthy plants. Invasive plants through allelopathy cause severe damage to native plants (Lata et al. 2018). There are two types of fungi parasites: nectrotrophs, which kill host cells using toxins, and biotrophs. Together with bacteria, they cause vascular wilts, leaf spots, and cankers among other symptoms, and can infect different parts of the plant. Nematodes withdraw the contents of plant cells and can feed on all parts of the plant, but plant parasitic nematodes primarily cause soil-borne diseases and attack plants’ root system. They produce symptoms related to nutrient deficiency, such as wilting or stunting. Viruses produce not only local lesions but also systemic damage that causes stunting, chlorosis, and malformations affecting different parts of the plant, although they rarely kill their hosts. On the other hand, insects and mites are the pest to be highlighted. They damage plants through feeding or egg laying (Gimenez et al. 2018). In contrast, abiotic stress may also interact positively with pathogen stress. In barley, increase in salt-induced osmotic stress was directly correlated with resistance to powdery mildew, while drought stress can enhance resistance to the fungus Botrytis cinerea in tomato. Pathogens may also actively interfere with plant–water relations in order to increase pathogenesis. For example, they may cause stomatal closure to reduce water loss from infected tissues, thus having a positive effect on plant tolerance against abiotic stress (Atkinson and Urwin 2012). Infection with viruses can actually provide protection from drought stress. In virus-infected tobacco, beet, and rice drought symptoms appeared later and leaves maintained water longer than their uninfected counterparts (Atkinson and Urwin 2012). Abiotic stress conditions also directly affect plant–pest interactions by altering plant physiology and defense responses. Additionally, abiotic stress conditions such as drought enhance competitive interactions of weeds on crops as several weeds exhibit enhanced water use efficiency than crops, and also known to influence the occurrence and spread of pathogens, insects, and weeds (Pandey et al. 2017). On the other hand, drought stress is reported to provide endurance to tomato, Medicago sativa, and Arabidopsis thaliana against Botrytis cinerea (causal agent of gray mold), Oidium neolycopersici (causal agent of powdery mildew), Verticillium albo-atrum (causal agent of verticillium wilt), and Pseudomonas syringae (causal agent of bacterial speck disease), respectively (Pandey et al. 2017).

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

271

9.6  P  . indica Fungal Endophytes for Conferring Salt Stress Tolerance Salinity is the concentration of dissolved mineral salts present in the soils (soil solution) and waters. The dissolved mineral salts consist of the electrolytes of cations and anions. The major cations in saline soil solutions consist of Na+, Ca2+, Mg2+, and K+, and the major anions are Cl−, SO42−, HCO3−, CO32−, and NO3− (Zarea et  al. 2013). The composition and concentration of soluble salts in root zone medium solution are known to influence plant growth, both by creating osmotic imbalance and via specific physiological toxicity of ions. Osmotic stress lowers the potential energy of the solution and causes reduced growth, due to the additional energy required by plants to take up water (Zarea et al. 2013). P. indica is known to impart tolerance towards many abiotic stress factors like extreme cold temperature, drought, and saline soil conditions (Gosal et al. 2013). The main mechanisms thought to be involved in salt stress alleviation by P. indica fungus may be summarized as follows: (1) improvement of mineral nutrition leading to plant growth promotion and (2) modification of some physiological processes and enzymatic activities involved in plant antioxidative reactions (Zarea et al. 2013). During salt and drought stress, P. indica maintains a high antioxidative environment by primarily inducing the defense system. Also, it has shown to induce several antioxidative enzymes during salt and drought stress that are involved in detoxification of reactive oxygen species such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), peroxidase (POD), monodehydroascorbate reductase (MDHAR), and dehydroascorbate reductase (DHAR). P. indica also increased the level of osmolytes (polyamines, proline, etc.), in response to salinity and drought stress (Varma et al. 2013). Salinity affects all important processes, such as growth, photosynthesis, protein synthesis, and lipid and energy metabolism, resulting in all phases of plant life from germination to seed production (Bagheri et al. 2014). P. indica has been shown to increase resistance against tolerance to abiotic stress in plants. Fungal colonization has shown to promote plant growth which is a characteristic effect and can also be observed under stress conditions. P. indica modulates the defense system and alters the metabolism to compensate the loss in photosynthesis and prevent oxidative damage caused by stress (Varma et al. 2013). Waller et al. (2005) investigated salt stress tolerance in barley leaves which were exposed to moderate and high salt concentrations in hydroponic culture. The plants show leaf chlorosis and reduced growth. The detrimental effect of moderate salt stress is completely abolished by P. indica, as shown by the fact that infested plants produce higher biomass than non-stressed control plants under these conditions. P. indica can with stand alkaline pH up to 11.0. The fungus found to have optimum growth at pH 6.0–10.0. Increase in cell dry biomass and radial growth along with presence of significant amount of chlamydospores at a wide range of pH 4.0–11.0 has been recorded for P. indica. The fungus can tolerate and shows prominent growth and metabolism at low acidic pH 4.0 to high alkaline pH 11.0 (Basu

272

F. A. Abo Nouh et al.

et  al. 2016). P. indica a root endophytic fungus has already been proved to have beneficial influence on plant growth especially under water scarcity and salt stress (Basu et al. 2016). P. indica also increased plant tolerance to abiotic stresses including salt stress in barley (Baltruschat et al. 2008; Alikhani et al. 2013), tomato (Cruz et al. 2010), and wheat (Rabiey et al. 2015). The fungus conferred drought tolerance in Chinese cabbage and enhanced seed production and grain yield (Sun et al. 2010). Interaction between barley and P. indica has been studied with respect to salt tolerance, and findings have suggested that barley was able to tolerate moderate salt stress (100 mM) in hydroponic culture (Waller et al. 2005). They investigated salt stress tolerance in barley leaves which were exposed to moderate (100 mM NaCl) and high (300 mM NaCl) salt concentrations in hydroponic culture. They found that detrimental effect of moderate salt stress was completely abolished by P. indica, with a higher biomass gain. However, under high salt stress conditions, both noninfested and infested plants exhibited a severe biomass reduction. Also, P. indica has shown to induce elevated amount of ascorbic acid and increase activities of antioxidant enzymes in barley roots during its symbiotic association under salt stress conditions suggesting that antioxidants might play a role in both inherited and endophyte-mediated plant tolerance to salinity (Baltruschat et al. 2008; Varma et al. 2013). Waller et al. (2005) observed that the root endophytic fungus P. indica had increased Hordeum vulgare L. tolerance to salt stress. Similarly, they showed that P. indica protects H. vulgare from high salt stress (300  mM NaCl) (Terhonen et al. 2019). Tolerance of plants to salt stress is associated with the alleviation of antioxidant enzymes as suggested by earlier studies (Rodriguez et  al. 2008). Considerable research has been carried out on the mechanism of salt stress tolerance conferred to plants colonized with P. indica and this trait has been demonstrated for barley as well as wheat, rice, and tobacco and involves the induction of a high antioxidant environment for the detoxification of reactive oxygen species and an enhanced photosynthetic efficiency (Johnson et al. 2014). According to Basu et al. (2016) P. indica showed a tendency to grow under calcareous condition with at high alkaline pH in vitro. The study explores the possibilities of P. indica as an excellent bio-inoculant for nutrient management in calcareous soil. Present study was conducted to understand P. indica capacity to withstand high alkaline pH. P indica was also subjected to stress of different concentration of calcium carbonate with respect to calcareous soil. This study has great significance as the fungus is being exploited and tested for bioremediation of calcareous soil. The pre-colonization of roots with P. indica resulted in decreased disease severity in tomato caused by early blight. They concluded that P. indica treatments led to priming of defense-related gene expression in tomato. Recent studies have shown that root fungal endophytes of agricultural crops can help host plants to live in harsh environments, thereby increasing their stress tolerance against abiotic factors (Terhonen et al. 2019).

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

273

9.7  P  . indica Fungal Endophytes for Conferring Disease Resistance Biotic stress results due to damage done to plants by other living microorganisms, such as bacteria, viruses, fungi, parasites, and organisms such as beneficial and harmful insects, weeds, and cultivated or native plants (Lata et  al. 2018; Yadav 2017a, b). Fungal endophytes are capable of protecting the plant against pathogens through various strategies, such as competition with pathogens for colonization and nutrients, the production of antibiotics, and the induction of resistance in the host plant (Kumar et al. 2019; Suman et al. 2016; Yadav et al. 2018c, 2019d). P. indica is an interesting endophytic fungus capable of colonizing roots and forming symbiotic relationship with every possible plant on earth (Desisa 2017). Biotic stress protection by P. indica was first shown in barley roots. P. indica enhanced barley grain yield, tolerance to mild salt stress, and resistance against root and leaf pathogens, including the necrotrophic fungus F. culmorum (root rot) and the biotrophic fungus Blumeria graminis. Beneficial effects are also observed for the crops like wheat, maize, and rice (Waller et al. 2005; Oelmüller et al. 2009). P. indica colonizes the cortex of roots of a wide variety of plant species, promotes their growth, and induces resistance against soil-borne fungal pathogens in a manner similar to arbuscular mycorrhizal fungi. The inoculation of P. indica followed by colonization of the internal tissues of the plant may impart systemic resistance to various fungal and bacterial pathogens (Gosal et al. 2013). On inoculation, P. indica vigorously infects host root tissue and blocks the receptors for the attachment and adsorption of the phytopathogens which could be considered as the nonspecific physical way of this beneficial fungus to safeguard the inoculated plant (Gosal et al. 2013). P. indica-infested plants are more resistant to biotic stress. When barley plants are exposed to the necrotrophic fungal pathogen F. culmorum, P. indica-infested plants are more resistant to root diseases. Root infection of wild-type plants causes a severe reduction in the root fresh weight and this devastating effect is strongly diminished in the presence of P. indica (Waller et al. 2005; Oelmüller et al. 2009). In barley, the root endophyte P. indica confers disease resistance by a different mechanism. Symbiotic plants are thought to resist necrotrophic root pathogens due to increased activity of glutathione–ascorbate antioxidant systems (Waller et  al. 2005; Rodriguez and Redman 2008). P. indica has been shown to increase resistance to biotic stresses including a wheat leaf disease (caused by B. graminis), a wheat stem base disease (caused by Oculimacula spp.), wheat and barley root rot diseases (caused by F. culmorum, Gaeumannomyces graminis) (Serfling et al. 2007; Harrach et al. 2013), a maize root disease (caused by F. verticillioides) (Kumar et al. 2009), a lentil vascular wilt disease (caused by F. oxysporum) (Dolatabadi et  al. 2012), crown rot disease (caused by F. culmorum and F. graminearum) (Rabiey et al. 2015). In tomato infected with Verticillium dahliae, P. indica increased leaf and fruit biomass and decreased disease severity. Also in tomato, P. indica reduced the concentration of Pepino mosaic virus in shoots (Fakhro et al. 2010).

274

F. A. Abo Nouh et al.

The inoculated wheat with P. indica may subsequently reduce the symptoms caused by several fungal pathogens on leaves, stems, and roots that were addressed under greenhouse and field conditions and also indicated by increased hydrogen peroxide formation in leaves challenged with powdery mildew (Desisa 2017). Root colonization by P. indica protects plants against various diseases. These include the root rot pathogens Verticillium, Fusarium foot rot, Rhizoctonia and Thielavopsis, and several fungal diseases of roots and stems, including Alternaria brassicae, Botrytis cinerea, and powdery mildew (Harman and Uphoff 2019). Colonization of P. indica controlled various plant diseases such as powdery mildew, eyespot, Rhizoctonia root rot, Fusarium wilt, black root rot, yellow leaf mosaic, Verticillium wilt, cyst nematode, and leaf blight in barley, wheat, maize, tomato, and Arabidopsis plants. Reduced severity of Verticillium wilt by 30% in tomato caused by Verticillium dahlia, and increased leaf biomass by 20% (Chhipa and Deshmukh 2019). P. indica has bio protection performance against the root parasite F. verticillioides in maize and observed stimulated increase in biomass, root length, and root number compared to the plants grown with F. verticillioides alone. The decrease of antioxidant enzyme activities due to the presence of P. indica helped the plant to overcome the disease load of F. verticillioides (Kumar et  al. 2009; Varma et  al. 2013). The effect of P. indica as bio protector on barley was assessed under semi-­ natural conditions using Mitscherlich pots (Waller et al. 2005), under these conditions P. indica acted as both a biofertilizer and a biocontrol agent (Waller et  al. 2005; Varma et al. 2013). P. indica exerts beneficial activity against two major cereal pathogens (F. culmorum and Cochliobolus sativus) that cause enormous worldwide economic losses (Waller et  al. 2005). The effect of P. indica against pathogen is based on inhibitory activity by dual bixenic culture technique, volatile metabolites against pathogen, P. indica culture filtrate, and role of lytic enzymes in pathogen inhibition (Varma et al. 2013). Major mechanisms of biological plant disease protection by P. indica are: Competition for occupying niches or nutrients, Production of antibiotics, Induced resistance and mycoparasitism (Desisa 2017). P. indica has also been shown to increase both crop yield and plant defense of a variety of crops (barley, tomato, maize) against root pathogens (Desisa 2017).

9.8  Applications and Recent Researches in P. indica Notably, compared to many other endophytes, P. indica can be cultured very easily in a bioreactor in order to prepare effective biofertilizer formulations (Singh et al. 2003; Oelmüller et al. 2009; Bagde et al. 2010; Qiang et al. 2011). P. indica reduces the harmful impact of stress on photosynthetic concert of the host plants and stabilizes growth and nutrition under salinity, drought, and heat (Baltruschat et al. 2008; Sherameti et al. 2008; Varma et al. 2012b). P. indica induces antioxidant system, the expression of abiotic stress-responsive genes, and protein to confer tolerance in different plant species such as Chinese cabbage (Sun et al. 2010), Arabidopsis thaliana (Sherameti et al. 2008), and Hordeum vulgare (Baltruschat et al. 2008; Ansari et al.

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

275

2014). However, despite all of these described benefits, Franken (2012) states that it may be difficult to place P. indica on the market because (1) the fungus was first isolated in India and is protected by patent in many countries (international publication number—WO 99/29177) making any commercial prospect reliant on the patent owner to manufacturing it or licensing it for manufacture and (2) it sometimes has unexplained negative effects on plant growth. The fungus possesses positive phytopromotional effects due to production/modulation of phytohormone levels (plant bioregulation ability), apart from its role in mobilization and transportation of the plant unavailable phosphorous reserves in soil beyond the depletion zone (P-mobilizer ability) (Gosal et al. 2013). Endophyte-­ enhanced plant growth promotion is another conferred beneficial trait that, at least for the root-colonizing endophyte P. indica, is likely achieved through enhanced nutrient uptake and translocation, and by the modulation of phytohormones involved in growth and development (Johnson et al. 2014; Lugtenberg et al. 2016). P. indica is already reported to be involved in high salt tolerance, disease resistance, and strong growth-promoting activities leading to enhancement of host plant yield (Basu et al. 2016). P. indica inocula are very effective for their commercial applications to various crops within the defined parameters, viz. inocula quantity, inoculation time point, as well as soils election for plant cultivation. Moreover, P. indica root endophyte has been credibly evidenced to minimize the use of chemical fertilizers, control crop yield, and also to provide increased resistance and tolerance in plants against biotic and abiotic stresses (Unnikumar et  al. 2013; Gill et  al. 2016). The axenic cultivability of P. indica on economically viable synthetic media makes it suitable for mass scale inoculum production for application in agro-forestry and horticulture (Desisa 2017). P. indica confers drought stress tolerance to Arabidopsis, and this is associated with the priming of the expression of a quite diverse set of stress-related genes in the leaves. When seedlings are first exposed to drought stress and then transferred to soil, many colonized seedlings reach the flowering stage and produce seeds, while the percentage for uncolonized seedlings is much lower (Desisa 2017). P. indica’s wide host benefits as well as its amenability for fundamental biological studies are attractive properties for research and its potential to transform the productivity of agricultural crops sustainably is exciting. With respect to barley, P. indica interactions have shown enhanced grain yield (Murphy et al. 2014) and at low temperatures with higher nutrient input, P. indica also appeared to trigger flowering earlier and still increase grain yield. These results indicate that P. indica could be developed as an effective crop treatment in low temperature-stressed barley and may have the potential to increase crop yield under colder growing environments on the proviso that adequate nutrients are supplied (Lugtenberg et al. 2016). P. indica as a mycofertilizer has produced a greater keenness among mycorrhizologists, due to being easily culturable, plant growth enhancer and inducer. In the present work, the recently discovered root endophytic-fungi P. indica has been optimized and tested for its growth enhancement (Krishnaveni et al. 2014). Considering the recent researches, P. indica is a promising agent for use in organic agriculture to manage nutrient deficiency in calcareous soil (Basu et al. 2016). P. indica is one of

276

F. A. Abo Nouh et al.

the most studied fungi for its plant growth promotion activity and stress resistance (Varma et al. 1999; Franken 2012; Kumar et al. 2017). P. indica, a wide host root-­ colonizing, has been used as a model to study the mechanisms and evolution of mutualistic symbiosis (Dong et  al. 2013). Nonetheless, a powder formulation of P. indica has been developed under the trade name “ROOTONIC” and is currently deployed in field trials in India (Shrivastava and Varma 2014; Lugtenberg et  al. 2016). Presently, these fungi can be grown with host plants in pot culture containing soil, sand, or expanded clay. They have also been grown by using hydroponics, aeroponics, and root organ culture; all of which are not a cost-effective proposition. P. indica can be propagated on several economically viable synthetic media, potato dextrose media. Fermentation technique should be optimized to device a simple, cheap, and commercially viable technique for the mass scale inoculums production for application in agro-forestry and horticulture (Desisa 2017). General characteristics of P. indica according to Krishnaveni et al. (2014); Gill et al. (2016); Desisa (2017). • Increase the potential of plants and their essential ingredients. • Applicable in agriculture, floriculture, viticulture, and reclamation of degraded and heavily mined soils. • Used in form of culture filtrate for development and formulation into biofertilizer. • Acts as biofertilizer, bioprotector, immune regulator, and agent for biological hardening of tissue cultured plants. • Mediates nutrient uptake, pathogenic inhibitor, stimulates growth and seed production. • Confers resistance to toxins, resistance to heavy metal ions, promotes salt stress and other abiotic stress.

9.9  Conclusion and Future Prospects Many plant growth-promoting fungi and bacteria have been identified in the last decades and the basis for their molecular interaction with plants has been studied. It is conceivable that the primary interest of the heterotrophic fungus is to gain access to photoassimilates. This is also obvious for P. indica, which was originally identified in a desert, where survival is dependent on an efficient association with roots due to the limitations of C compounds in the soil. The beneficial effects for the plant are at least in part caused by a better nutrient supply by the fungal hyphae. Many studies show that symbiosis of plants with endophytic-fungi could be a good solution for reducing the effects of salinity. P. indica possesses the phytopromotional to biocontrol properties, imparts stress tolerance to abiotic as well as biotic factors, and also exhibits enhanced nutritional availability to the inoculated plant. It has enormous application potentials for the biotization of the micro-propagated plants

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

277

and thus has a pivotal role to play in the new age phenomena of sustainable agriculture for enhanced productivity. Finally, several studies have demonstrated that P. indica may be used for phytoremediation, because it accumulates heavy metals and prevents their uptake into the plants. Taken together, the increasing interest in this fungus worldwide will lead to novel information that will disclose potential agronomical and biotechnological applications.

References Abo Nouh FA (2019) Endophytic fungi for sustainable agriculture. Microbial Biosyst 4(1):31–44 Ali AH, Radwan U, El-Zayat S, El-Sayed MA (2018) Desert plant-fungal endophytic association: the beneficial aspects to their hosts. Biol Forum Int J 10(1):138–145 Alikhani M, Khatabi B, Sepehri M, Nekouei MK, Mardi M, Salekdeh GH (2013) A proteomics approach to study the molecular basis of enhanced salt tolerance in barley (Hordeum vulgare L.) conferred by the root mutualistic fungus Piriformospora indica. Mol BioSyst 9:1498–1510 Anitha D, Vijaya T, Pragathi D, Reddy NV, Mouli KC, Venkateswarulu N, Bhargav DS (2013) Isolation and characterization of endophytic fungi from endemic medicinal plants of Tirumala Hills. Int J Life Sci Biotechnol Pharm Res 2(3):367–373 Ansari MW, Gill SS, Tuteja N (2014) Piriformospora indica a powerful tool for crop improvement. Proc Indian Natl Sci Acad 80(2):317–324 Arora J, Ramawat KG (2017) An introduction to endophytes. In: Maheshwari DK (ed) Endophytes: biology and biotechnology, sustainable development and biodiversity 15. Springer, Cham, pp 1–16 Atkinson JN, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3544 Bagde US, Prasad R, Varma A (2010) Interaction of Mycobiont: Piriformospora Indica with medicinal plants and plants of economic importance. Afr J Biotechnol 9(54):9214–9226 Bagheri AA, Saadatmand S, Niknam V, Nejadsatari T, Babaeizad V (2014) Effects of Piriformospora indica on biochemical parameters of Oryza sativa under salt stress. Int J Biosci 4(4):24–32 Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510 Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146:234–243 Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58 Basu K, Kumari TGV, Kharkwal AC, Abdin MZ, Kumar V, Varma A (2016) Study of Piriformospora indica as bioinoculant for nutrient management in Calcareous soil. Int J ChemTech Res 9(1):73–81 Batool N, Shahzad A, Ilyas N (2014) Plants and salt stress. Int J Agric Crop Sci 7(14):1439–14461 Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111 Camehl I, Sherameti I, Seebald E, Johnson JM, Oelmueller R (2013) Role of defense compounds in the beneficial interaction between Arabidopsis thaliana and Piriformospora indica. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Berlin, pp 239–250

278

F. A. Abo Nouh et al.

Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In: Shanker A (ed) Abiotic stress in plants - mechanisms and adaptations. InTech, Rijeka, pp 21–38 Chhipa H, Deshmukh SK (2019) Fungal endophytes: rising tools in sustainable agriculture production. In: Jha S (ed) Endophytes and secondary metabolites. Springer, Cham, pp 1–24 Cruz C, Martins-Loução MA, Varma A (2010) The influence of plant co-culture of tomato plants with Piriformospora indica on biomass accumulation and stress tolerance. Acta Hortic 868:123–128 Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiß M, Waller F, Kogel K-H (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Natl Acad Sci USA 103(49):18450–18457 Desisa B (2017) Endophytics fungus Piriformospora indica and its mechanism of plant growth promotion. World Sci News 87:99–113 Dolatabadi HK, Goltapeh EM, Mohammadi N, Rabiey M, Rohani N, Varma A (2012) Biocontrol potential of root endophytic fungi and Trichoderma species against Fusarium wilt of lentil under in vitro and greenhouse conditions. J Agric Sci Technol 14:407–420 Dong S, Tian Z, Chen PJ, Kumar RS, Shen CH, Cai D, Oelmüller R, Yeh KW (2013) The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots. J Exp Bot 64(14):4529–4540 Dresselhaus T, Hückelhoven R (2018) Biotic and abiotic stress responses in crop plants. Agronomy 8:267–273 Fakhro A, Andrade-Linares DR, Bargen SV, Bandte M, Büttner C, Grosch R, Schwarz D, Franken P (2010) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200 Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and biology behind. Appl Microbiol Biotechnol 96:1455–1464 Gill SS, Gill R, Trivedi DK, Anjum NA, Sharma KK, Ansari MW, Ansari AA, Johri AK, Prasad R, Pereira E, Varma A, Tuteja N (2016) Piriformospora indica: potential and significance in plant stress tolerance. Front Microbiol 7:332 Gimenez E, Salina M, Manzano-Agugliaro F (2018) Worldwide research on plant defense against biotic stresses as improvement for sustainable agriculture. Sustainability 10:391–410 Glen M, Tommerup IC, Bougher NL, O’Brien PA (2002) Are Sebacinaceae common and widespread ectomycorrhizal associates of Eucalyptus species in Australian forests. Mycorrhiza 12:243–247 Gosal SK, Kalia A, Varma A (2013) Piriformospora indica: perspectives and retrospectives. In: Varma A, Kost G, Oelmueller R (eds) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Berlin, pp 53–77 Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Hindawi Sci 2:9106395 Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel K-H (2013) The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol Plant-Microbe Interact 26(5):599–605 Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schäfer P (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156:726–740 Jacobs A, Kogel KH, Schäfer  P (2013) Root-based innate immunity and its suppression by the mutualistic fungus Piriformospora indica. In: Varma A, Kost G, Oelmueller R (eds) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Berlin, pp 223–237 Jain P, Pundir RK (2017) Potential role of endophytes in sustainable agriculture-recent developments and future prospects. In: Maheshwari DK (ed) Endophytes: biology and biotechnology, sustainable development and biodiversity 15. Springer, Cham, pp 145–160

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

279

Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agric 52:103–122 Justice AH, Faust JE, Kerrigan JL (2018) Evaluating a novel method to introduce a mycorrhizal-­ like fungus, Piriformospora indica, via an inoculated rooting substrate to improve adventitious root formation. Am Soc Hortic Sci 28(2):149–153 Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol 9(2732):1–12 Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite- what decide? Curr Opin in Plant Biol 9:358–363 Kost G, Rexer K-H (2013) Morphology and ultrastructure of Piriformospora indica. In: Varma A, Kost G, Oelmueller R (eds) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Berlin, pp 25–36 Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A, Sayyed RZ, Hesham AE-L, Dhaliwal HS, Saxena AK (2019a) Drought-tolerant phosphorus-solubilizing microbes: biodiversity and biotechnological applications for alleviation of drought stress in plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting rhizobacteria for sustainable stress management: volume 1: rhizobacteria in abiotic stress management. Springer, Singapore, pp 255–308. https://doi.org/10.1007/978-981-13-6536-2_13 Kour D, Rana KL, Yadav N, Yadav AN, Kumar A, Meena VS, Singh B, Chauhan VS, Dhaliwal HS, Saxena AK (2019b) Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: Kumar A, Meena VS (eds) Plant growth promoting rhizobacteria for agricultural sustainability: from theory to practices. Springer, Singapore, pp 19–65. https://doi.org/10.1007/978-981-13-7553-8_2 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019c) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, volume 2: perspective for value-added products and environments. Springer, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V, Dhaliwal HS, Saxena AK (2020a) Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolour L.) by drought-adaptive and phosphorus-solubilizing microbes. Biocatal Agric Biotechnol 23:101501. https://doi.org/10.1016/j.bcab.2020.101501 Kour D, Rana KL, Yadav AN, Sheikh I, Kumar V, Dhaliwal HS, Saxena AK (2020b) Amelioration of drought stress in Foxtail millet (Setaria italica L.) by P-solubilizing drought-tolerant microbes with multifarious plant growth promoting attributes. Environ Sustain 3:23–34. https://doi.org/10.1007/s42398-020-00094-1 Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal HS, Saxena AK (2020c) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi. org/10.1016/j.bcab.2019.101487 Krishnaveni N, Dipika B, Ramani DG, Chakravarthy C (2014) Cultivable endophytic mycobiont Piriformospora indica in millet growth promotion. Int J Sci Eng Technol Res 3(7):2033–2047 Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790 Kumar P, Pagano M, O’Donovan A (2017) Mycosphere essay 18: biotechnological advances of beneficial fungi for plants. Mycosphere 8(3):445–455 Kumar V, Soni R, Jain L, Dash B, Goel R (2019) Endophytic fungi: recent advances in identification and explorations. In: Singh BP (ed) Advances in endophytic fungal research, fungal biology. Springer, Cham, pp 267–281 Kumar M, Kour D, Yadav AN, Saxena R, Rai PK, Jyoti A, Tomar RS (2019a) Biodiversity of methylotrophic microbial communities and their potential role in mitigation of abiotic stresses in plants. Biologia 74:287–308. https://doi.org/10.2478/s11756-019-00190-6

280

F. A. Abo Nouh et al.

Kumar M, Saxena R, Rai PK, Tomar RS, Yadav N, Rana KL, Kour D, Yadav AN (2019b) Genetic diversity of methylotrophic yeast and their impact on environments. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 3: perspective for sustainable environments. Springer, Cham, pp  53–71. https://doi. org/10.1007/978-3-030-25506-0_3 Kumar V, Joshi S, Pant NC, Sangwan P, Yadav AN, Saxena A, Singh D (2019c) Molecular approaches for combating multiple abiotic stresses in crops of arid and semi-arid region. In: Singh SP, Upadhyay SK, Pandey A, Kumar S (eds) Molecular approaches in plant biology and environmental challenges. Springer, Singapore, pp  149–170. https://doi. org/10.1007/978-981-15-0690-1_8 Kusari S, Spiteller M (2012) Metabolomics of endophytic fungi producing associated plant secondary metabolites: progress, challenges and opportunities. In: Roessner U (ed) Metabolomics. InTech, Rijeka, pp 241–266 Lahrmann U, Zuccaro A (2012) Opprimo ergo sum—evasion and suppression in the root endophytic fungus Piriformospora indica. Mol Plant-Microbe Interact 25(6):727–737 Lata R, Chowdhury S, Gond SK, White JF (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Appl Microbiol 66(4):268–276 Lugtenberg BJJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92(12):1–17 Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250 Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681 Murphy PR, Doohan FM, Hodkinson TR (2014) Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis 62:29–39 Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17 Pan R, Xu L, Wei Q, Wu C, Tang W, Oelmüller R, Zhang W (2017) Piriformospora indica promotes early flowering in Arabidopsis through regulation of the photo period and gibberellins pathways. PLoS One 12(12):e0189791 Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-­ morphological traits. Front Plant Sci 8(537):1–15 Peškan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma AK, Oelmüller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122:465–477 Prasad R, Sharma M, Chatterjee S, Chauhan G, Tripathi S, Das A, Kamal S, Rawat AKS, Bhutani KK, Rai MK, Pushpangdan P, Varma A (2008) Interactions of Piriformospora indica with medicinal plants. In: Varma A (ed) Mycorrhiza. Springer, Berlin, pp 655–678 Qiang X, Weiss M, Kogel KH, Schäfer P (2011) Piriformospora indica—a mutualistic basidiomycete with an exceptionally large plant host ranges. Mol Plant Pathol 13(5):508–518 Rabiey M, Ullah I, Shaw MW (2015) The endophytic fungus Piriformospora indica protects wheat from fusarium crown rot disease in simulated UK autumn conditions. Plant Pathol 64:1029–1040 Rai MK, Varma A, Pandey AK (2004) Antifungal potential of Spilanthes calva after inoculation of Piriformospora indica. Mycoses 47:479–481 Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi: volume 1: diversity and enzymes perspectives. Springer, Cham, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological appli-

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

281

cations. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge, MA Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge, MA Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59(5):1109–1114 Rodriguez RJ, Henson J, Volkenburgh EV, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. Int Soc Microbial Ecol J 2:404–416 Sahay NS, Varma A (1999) Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiol Lett 181:297–302 Schäfer P, Kogel KH (2009) The Sebacinoid fungus Piriformospora indica: an orchid mycorrhiza which may increase host plant reproduction and fitness. In: Deising VH (ed) Plant relationships, The mycota, 2nd edn. Springer, Berlin, pp 99–112 Schäfer P, Khatabi B, Kogel KH (2007) Root cell death and systemic effects of Piriformospora indica:a study on mutualism. FEMS Microbiol Lett 275:1–7 Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plant. Nature 410: 327–330 Selosse MA, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878 Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531 Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-­ degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247 Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant-Microbe Interact 21(6):799–807 Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227 Shrivastava S, Varma A (2014) From Piriformospora indica to rootonic: a review. Afr J Microbiol Res 8(32):2984–2992 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Singh A, Singh A, Kumari M, Rai MK, Varma A (2003) Biotechnological importance of Piriformospora indica Verma et  al-a novel symbiotic Mycorrhiza-like fungus: an overview. Indian J Biotechnol 2:65–75 Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6(2):175–191 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh D, Abhilash P, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, research perspectives. Springer, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7 Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of droughtrelated genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017

282

F. A. Abo Nouh et al.

Tanha SR, Ghasemnezhad A, Babaeizad V (2014) A study on the effect of endophyte fungus, Piriformospora indica, on the yield and phytochemical changes of globe artichoke (Cynara scolymus L.) leaves under water stress. Int J Adv Biol Biomed Res 2(6):1907–1921 Terhonen E, Blumenstein K, Kovalchuk A, Asiegbu FO (2019) Forest tree microbiomes and associated fungal endophytes: functional roles and impact on forest health. Forests 10(42):1–33 Unnikumar KR, Sree KS, Varma A (2013) Piriformospora indica: a versatile root endophytic symbiont. Symbiosis 60:107–113 Varma A, Verma S, Sahay N, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant growth promoting root endophyte. Appl Environ Microbiol 65:2741–2744 Varma A, Bakshi M, Lou B, Hartmann A, Oelmüller R (2012a) Piriformospora indica: a novel plant growth promoting mycorrhizal fungus. Agric Res 1(2):117–131 Varma A, Sherameti I, Tripathi S, Prasad R, Das A, Sharma M, Bakshi M, Johnson JM, Bhardwa S, Arora M, Rastogi K, Grawal AA, Kharkwal AC, Talukdar S, Bagde US, Bisaria VS, Upadhyaya CP, Won PS, Chen Y, Ma J, Lou B, Adya A, Zhang L, Meghvansi MK, Sree KS, Gosal SK, Srivastava RB, Johri AK, Kumar M, Dua M, Cruz C, Oelmüller R (2012b) In: Hock B (ed) The symbiotic fungus Piriformospora indica: review. Fungal associations, The Mycota. IX, 2nd edn. Springer, Berlin, pp 231–254 Varma A, Chordia P, Bakshi M, Oelmüller R (2013) Introduction to sebacinales. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Berlin, pp 3–24 Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarabhoy A, Bisen P, Bütenhorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–903 Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016) Molecular diversity and multifarious plant growth promoting attributes of bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58 Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-­ ecological perspectives: volume 2: microbial interactions and agro-ecological impacts. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22 Verma P, Yadav AN, Khannam KS, Mishra S, Kumar S, Saxena AK, Suman A (2019) Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of India. Saudi J Biol Sci 26:1882–1895. https://doi.org/10.1016/j.sjbs.2016.01.042 Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven P, Neumann C, Wettstein DV, Franken P, Kogel K-H (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391 Waller DM, Dole J, Bersch AJ (2008) Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa. Evolution 62(4):917–931 Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14 Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:65–83 Xu L, Wu C, Oelmüller R, Zhang W (2018) Role of phytohormones in Piriformospora indica-­ induced growth promotion and stress tolerance in plants: more questions than answers. Front Microbiol 9(1646):1–13 Yadav AN (2017a) Agriculturally important microbiomes: biodiversity and multifarious PGP attributes for amelioration of diverse abiotic stresses in crops for sustainable agriculture. Biomed J Sci Tech Res 1:1–4 Yadav AN (2017b) Beneficial role of extremophilic microbes for plant health and soil fertility. J Agric Sci 1:1–4

9  Piriformospora indica: Endophytic Fungus for Salt Stress Tolerance…

283

Yadav AN, Yadav N (2018) Stress-adaptive microbes for plant growth promotion and alleviation of drought stress in plants. Acta Sci Agric 2:85–88 Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285(34):26532–26544 Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan V, Dhaliwal HS, Saxena AK (2017) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:45–57 Yadav AN, Kumar V, Prasad R, Saxena AK, Dhaliwal HS (2018a) Microbiome in crops: diversity, distribution and potential role in crops improvements. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology. Elsevier, New York, pp 305–332 Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP, Saxena AK, Dhaliwal HS (2018b) Actinobacteria from rhizosphere: molecular diversity, distributions and potential biotechnological applications. In: Singh B, Gupta V, Passari A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, New York, pp 13–41. https://doi.org/10.1016/ B978-0-444-63994-3.00002-3 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018c) Biodiversity of the genus Penicillium in different habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and future developments in microbial biotechnology and bioengineering, Penicillium system properties and applications. Elsevier, Amsterdam, pp  3–18. https://doi.org/10.1016/ B978-0-444-63501-3.00001-6 Yadav AN, Gulati S, Sharma D, Singh RN, Rajawat MVS, Kumar R, Dey R, Pal KK, Kaushik R, Saxena AK (2019a) Seasonal variations in culturable archaea and their plant growth promoting attributes to predict their role in establishment of vegetation in Rann of Kutch. Biologia 74:1031–1043. https://doi.org/10.2478/s11756-019-00259-2 Yadav AN, Mishra S, Singh S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. Volume 1: diversity and enzymes perspectives. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi. Volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019d) Recent advancement in white biotechnology through fungi. Volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Yadav N, Sachan SG, Saxena AK (2019e) Biodiversity of psychrotrophic microbes and their biotechnological applications. J Appl Biol Biotechnol 7:99–108 Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer, Cham Yadav AN, Rastegari AA, Yadav N (2020b) Microbiomes of extreme environments: biodiversity and biotechnological applications. CRC Press, Taylor & Francis, Boca Raton Yadav AN, Rastegari AA, Yadav N, Kour D (2020c) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020d) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020e) Plant microbiomes for sustainable agriculture. Springer, Cham Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803 Zarea J, Chordia P, Varma A (2013) Piriformospora indica versus salt stress. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica—sebacinales and their biotechnological applications. Springer, Berlin, pp 263–281 Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel KH (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7(10):e1002290

Chapter 10

Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes K. Kiran Kumar

Contents 10.1  I ntroduction 10.2  N  ematophagous Fungi 10.2.1  Nematode Trapping Fungi 10.2.2  Endoparasitic Fungi 10.2.3  Egg and Female Parasitic Fungi 10.2.4  Toxin Producing Fungi 10.2.5  Endophytic Fungi 10.3  Nematode-Fungal Interaction 10.3.1  Recognition 10.3.2  Attraction 10.3.3  Adhesion 10.3.4  Penetration and Digestion 10.4  Extracellular Enzymes 10.5  Commercialization 10.6  Conclusion and Future Prospects References

 285  287  287  291  292  294  294  296  296  296  297  297  297  300  304  304

10.1  Introduction Plant parasitic nematodes are considered to be the major constraint on plant productivity, and they have been found to attack almost every part of the plant including roots, stems, leaves, fruits, and seeds. They are also responsible for invasion of secondary pests and pathogens by causing wounds in the host roots (Caboni et al. 2016). Global annual yield losses from plant parasitic nematodes have been estimated at 12.6% ($215.77 billion) for top 20 life sustaining crops (Abd-Elgawad and Askary 2015). Among different groups of plant parasitic nematodes, root knot (Meloidogyne spp.) and cyst nematodes (Heterodera and Globodera spp.) are economically important by forming complex feeding structures like giant cells and K. K. Kumar (*) Department of Nematology, ICAR-Central Citrus Research Institute, Nagpur, Maharashtra, India

© Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_10

285

286

K. K. Kumar

syncytia in the roots of their hosts which act as a nutrient sink to the nematode. Apart from these, root-lesion nematodes (Pratylenchus spp.), burrowing nematode (Radopholus similis), stem nematode (Ditylenchus dipsaci), reniform nematode (Rotylenchulus reniformis), and several other plant parasitic nematodes causing economic damage to the crops (Jones et al. 2013). Many traditional chemical pesticides such as fumigants, organophosphates, and carbamates have been used for the management of plant parasitic nematodes (Kour et al. 2020). However, the usage of harmful chemical pesticides cause environmental toxicity, health effects and further withdrawal of some pesticides has led to the development and adoption of non-chemical alternatives for the management of plant parasitic nematodes (Davies and Curtis 2011; Kumar et al. 2018). In addition, these chemicals do not affect the development of nematode eggs in soil, since the egg shell of nematode acts as a barrier which makes them resistant to chemical pesticides (Baron et al. 2019). Crop rotation and use of resistant cultivars have been used as the management strategies for plant parasitic nematodes. However, these practices are limited by the size of growing area, wide host range of nematode species, and high genetic diversity among or within nematode populations (Berlitz et al. 2014; Li et al. 2015). Biological control, an alternative for the management of plant parasitic nematodes. The usage of biocontrol agents is increasing these days, due to their reduced environmental toxicity, target specificity, and safety to non-target organisms (Kumar and Singh 2015; Jiang et al. 2017). These biocontrol agents include fungi, bacteria, viruses, nematodes, and other invertebrates which have an antagonistic activity against plant parasitic nematodes. The market for biological nematicides has risen by nearly 20% from 2009 to the present, according to the Markets and Markets report, with most of the development in field crops. Nematicide sales amounted to just over $1 billion in 2014 and are anticipated to expand at a compound annual growth rate (CAGR) of 2.7% over the next 10 years to $1.3 billion over 20 years (Jiang et al. 2017). Currently several biocontrol agents such as fungi and bacteria have been widely used as commercial products for the management of plant parasitic nematodes. Fungal antagonists have been considered as the most promising biocontrol agents and attention is being paid to the exploitation of fungi to control plant parasitic nematodes (Stirling 2011; Moosavi and Zare 2012; Lamovsek et al. 2013). Among different fungal biocontrol agents, the most widely studied species for nematode management include Pochonia chlamydosporia, Purpureocillium lilacinum, Arthrobotrys oligospora, Trichoderma spp. and Verticillium spp. (Rastegari et al. 2020a, b; Yadav et al. 2020a, b). This chapter reviews different categories of nematophagous fungi, mode of action, and knowledge of the interactions between nematodes and nematode trapping fungi and commercialization of different fungal products for the management of plant parasitic nematodes.

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

287

10.2  Nematophagous Fungi This group of fungi has been widely used as biocontrol agents of plant parasitic nematodes due to their antagonistic, parasitic, and predatory action against different species. There are approximately 700 fungal species reported to be able to attack different life stages of nematodes (juveniles, adults, and eggs) (Li et al. 2015; Jiang et  al. 2017). Over the decades, several researchers have worked on fundamental studies and their potential as biocontrol agents against different plant parasitic nematodes. Based on their infection mechanism, they are subdivided into four categories viz., nematode trapping fungi, endoparasitic fungi, egg and female parasitic fungi, and toxin producing fungi (Dackman et  al. 1992; Nordbring-Hertz et  al. 2006) (Table 10.1).

10.2.1  Nematode Trapping Fungi These are soil borne fungi that have the ability to capture and kill nematodes by using trapping structures, including adhesive hyphae, adhesive knobs, constricting rings and non-constricting rings, and adhesive networks (Nordbring-Hertz et  al. 2011; Jiang et al. 2017). The type of trapping structure formed mainly depends on the fungal species or strains of fungal species and both biotic and abiotic environmental factors (Nordbring-Hertz et al. 2006). Based on phylogenetic analysis results using ribosomal RNAs (rRNAs) and protein coding genes, these trapping devices could serve as indicators for generic delimitation among these fungi (Ahren et al. 1998; Scholler et al. 1999; Li et al. 2005). There are about 380 species of nematode trapping fungi have been reported from different regions of the world (Zhang et al. 2011). They are usually non-host specific and can infect all soil dwelling nematodes. All the known nematode trapping fungi belong to the order Orbiliales of the phylum Ascomycota (Zhang and Hyde 2014). These fungi can live both saprophytically on organic matter and as predatory by capturing tiny animals. However, they can shift from saprophytic to predatory lifestyle in the presence of nematode prey by the production of trapping structures (Li et al. 2011; Yang et al. 2012; Zhang and Hyde 2014). The application of these fungi for nematode suppression was accompanied by addition of large amounts of organic matter and in most cases the levels of nematode control were unpredictable (Stirling 1991). 10.2.1.1  Adhesive Hyphae These are mostly produced by lower fungi belongs to the genera Stylopage and Cystopage under phylum Zygomycota (Table 10.1). They cannot produce complex devices for capturing nematodes due to the absence of septa (Barron 1977). However, septate fungi such as Arthrobotrys botryospora, Dactylaria psychrophila,

288

K. K. Kumar

Table 10.1  Different categories of nematophagous fungi Category Nematode trapping fungi

Nematode trapping structure Adhesive hyphae

Name of fungi Stylopage hadra Cystopage cladospora Adhesive knobs Dactylellina ellipsospora Dactylellina drechsleri Dactylaria candida Monacrosporium haptotylum Gamsylella querci Gamsylella robusta Gamsylella parvicollis Nematoctonus sp. Non-constricting rings Dactylaria candida Dactylaria lysipaga Adhesive knobs + non-­ Dactylellina constricting rings appendiculata Dactylellina haptotyla Constricting rings A. dactyloides A. brochopaga Drechslerella stenobrocha Drechslerella brochopaga Drechslerella dactyloides Adhesive knobs + adhesive Nematoctonus spores concurrens Adhesive networks Arthrobotrys oligospora Arthrobotrys musiformis Arthrobotrys conoides Arthrobotrys vermicola Arthrobotrys superba Dactylaria scaphoides

Phylum Zygomycota Zygomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Basidiomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Basidiomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota Ascomycota (continued)

Table 10.1 (continued) Category Endoparasitic fungi

Nematode trapping structure Adhesive conidia

Adhesive spores

Ingested conidia

Zoospores

Egg parasitic fungi

Appresoria

Zoospores Toxin producing fungi Endophytic fungi

Toxic droplets Toxin, spiny structures

Name of fungi Drechmeria coniospora Hirsutella rhossiliensis Hirsutella minnesotensis Cephalosporium balanoides Nematoctonus concurrens Nematoctonus haptocladus Nematoctonus leiosporus Harposporium anguillulae Harosporium cerbri Catenaria auxillaris Catenaria anguillulae Myzocytiopsis glutinospora Myzocytiopsis vermicola Myzocytiopsis enticularis Myzocytiopsis humicola Pochonia chlamydosporia Purpureocillium lilacinum (=Paecilomyces lilacinus) Acremonium (=Cephalosporium) sp. Dactylella oviparasitica Dactylella lysipaga Lecanicillium psalliotae Lecanicillium lecanii Nematophthora gynophila Pleurotus ostreatus Coprinus comatus Fusarium oxysporum Neotyphodium spp. Acremonium Penicillium oxalicum

Phylum Ascomycota Ascomycota Ascomycota Ascomycota Basidiomycota Basidiomycota Basidiomycota Ascomycota Ascomycota Blastocladiomycota Blastocladiomycota Oomycota Oomycota Oomycota Oomycota Ascomycota Ascomycota

Ascomycota

Ascomycota Ascomycota Ascomycota Ascomycota Oomycota Basidiomycota Basidiomycota Ascomycota Ascomycota Ascomycota Ascomycota

290

K. K. Kumar

and A. superba can capture nematodes with adhesive hyphae under certain conditions (Chen and Dickson 2004). The infection begins with the capture organ being adhered by nematode. Within few minutes, the nematodes added to a fungal colony were captured and penetrated within 1 h by the trap forming cell hyphae. After 6 h, the whole nematode body was filled with hyphae. The dead nematode did not induce traps but developed a large number of thin hyphae around the nematode. 10.2.1.2  Adhesive Knobs These are very effective trapping structures and nematodes are often attacked at more than one infection site (Barron 1977). These knobs are covered by a thin layer of adhesive materials and the infection process involves one knob and several associated hyphal elements. These adhesive knobs produce an infection peg and infection bulb. From this bulb, the infection hyphae proliferate within the nematode and digest the inner contents. The adhesive knobs are found in Ascomycota and Basidiomycota (Table 10.1). This group of fungi is unique in forming clamp connections on the secondary hyphae (Chen and Dickson 2004). The genomic studies of adhesive knob forming species, Monacrosporium haptotylum indicated the enrichment of small secreted proteins (SSPs) that were highly and differentially expressed during the interaction with nematode hosts (Meerupati et al. 2013). 10.2.1.3  Adhesive Networks This is the most common type of nematode trapping structure observed in Arthrobotrys spp. (Table  10.1). The trap may consist of a single ring or a three-­ dimensional network. A. oligospora, a model organism for understanding the interaction between fungi and nematodes, forms a three-dimensional adhesive network during infection process. The genomic and proteomic analyses of this fungus provide insights into nematode trap formation including G-protein coupled receptors, adhesive proteins, cell division cycle, peroxisome related proteins, and proteins involved in energy supplementation (Yang et al. 2011). 10.2.1.4  Constricting Rings Among different trapping structures, constricting rings are probably the only ones that actually capture the nematodes and considered to be the lineal strategy after which other trapping structures evolved (Yang et al. 2007a; Liu et al. 2012). In general, trapping fungi that form constricting rings are more abundant in soils rich in organic matter and influenced by the population density of nematodes (Linford 1937; Gray 1985). However, the trapping mechanism is completely different in contrast to others. When a nematode passing into the ring, it stimulates the inner face of the ring such that the three cells comprising the ring inflate centripetally to about

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

291

three times and get trapped within 0.1 s. The pressure exerted by nematode on the ring during this process causes the activation of G-protein coupled receptors which leads to an increase in cytoplasmic Ca2+, and activation of calmodulin that opens the water channels, and thereby inflates the ring trapping the nematode (Chen et  al. 2001). The genome sequence of Drechslerella stenobrocha constricting ring forming fungus revealed that the downregulation of saprophytic enzyme genes and the upregulation of infection related genes during the capture of nematodes indicated a transition between saprophagous and predatory life strategies. This study also indicated that protein kinase C (PKC) signal pathway and Zn (2)-C6 type transcription factors were responsible for trap formation in D. stenobrocha (Liu et  al. 2014). Following the capture an infection peg is produced by one of the three ring cells and a small globose infection bulb develops after the penetration of infection peg into the body cavity of the nematodes. Trophic hyphae quickly digest and absorb the internal contents of nematode leaving only the cuticle structures. 10.2.1.5  Non-constricting Rings Non-constricting rings are generally produced by erect lateral branches produced from septate hyphae. When a nematode thrusts its head inside the non-constricting ring, it gets wedged and held by friction. During this, the ring often breaks at the point of weakness near the stalk apex and this process may be repeated until several rings are wedged around the host. Following capture, the fungi penetrate and consume the inner contents of the host (Zaki 1994). Dactylaria candida and D. lysipaga usually generally form non-constricting rings during infection process (Table 10.1).

10.2.2  Endoparasitic Fungi These are a group of fungi that infect nematodes mainly by conidia (Drechmeria coniospora), ingestive spores (Harposporium spp.), adhesive spores (Nematoctonus concurrens) or zoospores (Catenaria anguillulae) (Table 10.1). Their spores either adhere to the nematode cuticle or swallowed by the host and then germinate inside the nematode body which finally result in the death of nematode. In D. coniospora surface proteins and chymotrypsin-like proteases were involved in the infection process (Lopez-Llorca et al. 2008; Jansson and Friman 1999). Although some of these like Nematophthora gynophila could parasitize a large number of nematodes viz., Heterodera avenae, H. trifolii, H. schachtii, H. goettengiana, H. cruciferae, etc., and their bioefficacy was dependent on adequate soil moisture and on the relative number of nematodes and endozoic units present in the soil. Besides, their obligate nature posed a problem for mass production (Kerry 1987).

292

K. K. Kumar

10.2.3  Egg and Female Parasitic Fungi The research on egg and female parasitic fungi has been initiated in the 1990s. These fungi use either appressoria (Purpureocillium spp., Pochonia spp.,) or zoospores (Nematophthora gynophila) to kill different life stages (Lopez-Llorca et al. 2008) (Table 10.1). The relationship between nematodes and these fungi was variable, but as some of the isolates were highly virulent, they were extensively used and are still available as formulations in the market, especially for sedentary endoparasites. However, it is important to ascertain the quality parameters, namely colony forming units (CFU), presence of contaminants of these formulations before application in the field for control of nematode population. Among different egg parasitic fungi, P. chlamydosporia and P. lilacinum are widely used as biocontrol agents. 10.2.3.1    Pochonia chlamydosporia P. chlamydosporia is considered as potential biocontrol agent of endoparasitic nematodes due to their ability to colonize the rhizosphere of plants and cultivars, to produce chlamydospores in  vitro and to infect eggs of endoparasitic nematodes such as root knot (Meloidogyne spp.) and cyst nematodes (Heterodera avenae, H. glycines, H. schachtii) (Manzanilla-Lopez et al. 2013; Dallemole-Giaretta et al. 2015). In addition, this fungus has shown activity against false root-knot nematode, Nacobbus aberrans, burrowing nematode, Radopholus similis, citrus nematode, Tylenchulus semipenetrans, and reniform nematode, Rotylenchulus spp. (Manzanilla-­ Lopez et al. 2013; Abd-Elgawad and Askary 2018). The specificity of this fungus towards sedentary endoparasitic nematodes is associated with the recognition of both quantitative and qualitative changes in root exudates patterns during nematode infection (Wang and Bergeson 1974). Crops such as beans, cabbage, crotalaria, kale, pigeon pea, potato, pumpkin, and tomato are considered as good hosts (200 CFU/cm2 of root) for colonization of this fungus in the rhizosphere. Whereas, chilli, sweet potato, cowpea, rye, tobacco, and cotton are considered as moderate hosts (100–200 CFU/cm2 of root) and poor hosts (60% of nematodes were killed and degraded after being treated with crude extract or the purified enzyme for 12 h 100% mortality of H. Panagrellus redivivus, Heterodera glycines J2 was observed in 100 μl glycines crude enzyme solution after incubation for 12 h

Yang et al. (2005)

Li et al. (2006)

Wang et al. (2006a)

Wang et al. (2006b)

Wang et al. (2007)

(continued)

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

299

Table 10.3 (continued) Fungi Arthrobotrys conoides

Protease Ac1

Dactylella varietas

Dv1

Monacrosporium cystosporium

Mc1

Cordyceps sinensis

Csp1

Cordyceps sinensis

Csp2

Hirsutella rhossiliensis

Hasp

Monacrosporium thaumasium

Mt1

Duddingtonia flagrans

Df1

Esteya vermicola

Evsp

Fungal activity against nematode Immobilization of 60–80% P. redivivus population after treated with crude enzyme for 24 h. Whereas, 40–50% of B. xylophilus nematode population was immobilized after 24 h of treatment Panagrellus redivivus 50–100% tested and Caenorhabditis nematodes were killed and degraded after elegans being treated with either the crude extract or the purified enzyme for 12 h 70–80% of P. redivivus Panagrellus were immobilized after redivivus, being treated with the Bursaphelenchus crude and the purified xylophilus proteases for 24 h, but only 50–60% of B. xylophilus were immobilized Hepialus spp. Loosening and degradation of cuticle in larvae Hepialus spp. Loosening and degradation of cuticle in larvae Heterodera glycines The mortality of J2 was significantly higher in purified hasp solutions (43 ± 5% mortality at 4 U/ml and 53 ± 4% mortality at 8 U/ml) than in the buffer control (22 ± 2%) Angiostrongylus 23.9% reduction in the vasorum number of L1 larvae, compared with control Cyathostomin 58% reduction of L3 larvae, after 24 h of treatment compared with control Bursaphelenchus xylophilus Testing nematode Panagrellus redivivus, Bursaphelenchus xylophilus

Reference Yang et al. (2007b)

Yang et al. (2007c)

Yang et al. (2008)

Zhang et al. (2008) Zhang et al. (2008) Wang et al. (2009)

Soares et al. (2012) Braga et al. (2012)

Wang et al. (2015)

300

K. K. Kumar

Table 10.4  Chitinases purified/cloned in nematophagous fungi Nematophagous fungi Pochonia chlamydosporia (=Verticillium chlamydosporium) P. suchlasporia (V. suchlasporium) Paecilomyces lilacinus (strain 251) Lecanicillium lecanii (Verticillium lecanii) Lecanicillium psalliotae

Chitinase Chi43

Clonostachys rosea (=Gliocladium roseum) Paecilomyces variotii

CrChi1 Chi 32

Paecilomyces variotii

Chi 46

Pochonia chlamydosporia

PcChi44

Testing nematode Globodera pallida

Fungal activity against nematode Reference Treated eggs showed Tikhonov surface damage et al. (2002)

Plc Chi2 LpChi1

Meloidogyne incognita

Meloidogyne incognita Meloidogyne incognita Meloidogyne incognita

Inhibition of egg hatching by 38.2% after 3 days of treatment

Scars on the surface and peeling of eggshells was observed for about 24 h after treatment

Khan et al. (2003) Lu et al. (2005) Gan et al. (2007a)

Gan et al. (2007b) Nguyen et al. (2009) Nguyen et al. (2009) Mi et al. (2010)

various nematophagous fungi (Li et al. 2015). Table 10.4 showed a list of chitinases either purified or cloned from different nematophagous fungi and their activity on different species of nematode eggs under in vitro conditions. Collagenases are another group of enzymes which are suspected to play a role in nematode infection. Initially Schenck et al. (1980) reported that eight nematophagous fungi could secrete collagenases. Later Tosi et  al. (2002) reported that Arthrobotrys genus could produce collagenases.

10.5  Commercialization The development of a biocontrol agent needs several steps aimed at isolation in pure culture and screening by different bioassay tests under in vitro, in vivo, and ex vivo conditions (Montesinos 2003). For commercialization of any product, the bioagent must be produced in a large scale, formulated by means of biocompatible additives to improve the storage capacity of the product. Further, quality control, registration of the particular formulated product and implementation are required (Ravensberg 2011).

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

301

In case of nematophagous fungi, various species have been tested for their efficacy in control of plant parasitic nematodes. However, only a few species have been commercialized for large scale multiplication and field application. Table 10.5 demonstrates a list of commercial products of nematophagous fungi produced by various companies under different trade names. Among these, the formulations of Table 10.5  Commercial products of fungal biocontrol agents developed against plant parasitic nematodes

Biocon

Formulation type Water dispersible granule, water dispersible powder Granulate, WP Water dispersible granule WP

Shakti Paecil Yorker

WP WP

Pl plus

Wettable powder Talc

Fungal species Trade name Bioact Purpureocillium lilacinum (=Paecilomyces lilacinus)

PL Gold PL 251

Miexianning

Melocon

Nematofree

Water dispersible granule WP

Paecilo WP Gmax bioguard Talc Green Nemagon Bio-Nematon

Biostat

Target nematode Root-knot nematodes, cyst nematodes, reniform nematode, burrowing nematode, citrus nematode, golden cyst nematode and lesion nematode

Producer/country Bayer Crop Science/ USA

BASF Worldwide/ Germany Biological Control Products/South Africa Asiatic Technologies, Inc./Philippines Shakti Biotech/India Agriland Biotech Limited/India Biological Control Products/South Africa Agricultural Institute, Yunnan Academy of Tobacco Science/ China Prophyta GmbH/ Germany; Certis/ USA International Panaacea Ltd./India Agri life/India GreenMax AgroTech/ India

Liquid Liquid/ powder

Imported from T. Stanes and company limited, India by Gaara company, Egypt LAM International/ USA (continued)

302

K. K. Kumar

Table 10.5 (continued) Formulation Fungal species Trade name type Pochonia chlamydosporia Xianchongbike Liquid

Pochonia chlamydosporia KlamiC® (IMI SD 187) P. chlamydosporia Rizotec® (Pc-10) PcMR-1 strain

Arthrobotrys robusta Arthrobotrys irregularis

Royal 300 Royal 350

Myrothecium verrucaria

DiTera®

Trichoderma harzianum

Romulus

Liquid

Commander

Unspecified Root-knot nematodes Dry flowable Root-knot nematode, cyst nematode, root-lesion nematode, stubby-root nematode, citrus nematode, burrowing nematode, sting nematode WP Root-knot nematodes, cyst Wettable nematodes powder, liquid, lyophilized Unknown

Trichobiol

WP

Trifesol

WP

Ecosom-TH

Trichoderma viride (strain 2684)

Granulate

Target nematode Root-knot nematodes, cyst nematodes, false root-knot nematode, reniform nematode

Producer/country Laboratory for Conservation and Utilization of Bio-resources, Yunnan University/ China CENSA/Cuba Rhizoflora, Viçosa (Brazil) Clamitec, Myco solutions, lda/ Portugal France France Valent Biosciences Corp/USA

Dagutat Biolab/South Africa Agri Life SOM Phytopharma Limited/India HTC Impex Private Limited/India Control Biológico Integrado; Mora Jaramillo Arturo Orlando—Biocontrol/ Colombia BioCultivos S.A., Bogotá, Colômbia (continued)

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

303

Table 10.5 (continued) Fungal species Trichoderma lignorum

Trade name Mycobac

Beauveria bassiana strain Botanigard GHA B. bassiana strain GHA Mycotrol Verticillium lecanii

Mycotal

Nemaxxion Consortium (Bacillus Biol subtilis, Trichoderma spp., Paecilomyces spp. and extracts of Tagetes sp.) Consortium (Arthrobotrys Rem G spp., Dactylella spp., Paecilomyces spp., Mycorrhiza (Glomus spp.), and bacteria (Bacillus spp. and Pseudomonas spp.))

Formulation type Unknown

Target nematode

ES/WP

Root-knot nematodes Root-knot nematodes Root-knot nematode (Meloidogyne incognita) Root-knot GreenCorp/Mexico. nematodes

ES WP

Liquid

Producer/country Laboratórios Laverlam/Colombia

Green Solutions/Italy

P. chlamydosporia, P. lilacinum, and A. robusta, A. irregularis have been widely used for nematode management in vegetables and fruit crops. Although, nematophagous fungi provides several advantages over traditional products, the Commercialization of these bioproducts lags far behind due to inconsistent performance, quality control issues, limited shelf life of product, slow rate of kill, lack of field persistence of some formulations, difficulties in scale-up production, expensive and time consuming registration process and marketable issues, etc. (Moosavi and Askary 2015; Venkatesan and Pattar 2017). There is a need to focus on improving the formulation and manufacturing technologies that reduce costs and enhance shelf life of the commercial product. The development and success of a biocontrol agent for plant parasitic nematodes require a better knowledge on the biology and ecology of the nematophagous fungi and the nematode, its host cultivar, method and time of application, and the various biotic and abiotic factors regulating the efficacy of biocontrol agent, the root diffusates differ markedly between plant species and cultivar which influences the proliferation of fungi (Tunlid and Ahrén 2001; Morton et  al. 2004; Davies 2005). In addition, several soil microbes or their metabolites compete with the introduced bioagents for scarce energy sources. These can significantly affect the efficacy of

304

K. K. Kumar

the agent even when added to soil in a pre-colonized substrate. For example, egg masses of Meloidogyne spp. harbored 122 bacteria and 19 fungi, 23% and 74% of which, respectively, were antagonistic to P. chlamydosporium (Kok and Papert 2001). Bacillus sp. strain H6 isolated from a fungistatic soil produced iturin like compounds from that caused swelling in the conidia and germ tube of nematophagous fungi (Li et al. 2007a). Such sensitivity of a biocontrol agent to antagonism by an isolate of another microbe varies with the isolate (Montfort et al. 2006).

10.6  Conclusion and Future Prospects Over the past 50 years, the number of scientists involved in research on the biocontrol of nematodes has increased significantly. Although several biocontrol agents for nematodes have been reported, only few organisms were developed as commercial bioagents. Surveys and empirical tests are being replaced by quantitative experimentation and basic research at genomic levels is being undertaken. Such information is essential for a realistic appraisal of the impact of microbial agents on nematode pests and for monitoring the spread and survival of the releases organisms. Our research efforts need to be directed towards identifying the factors governing their proliferation in soil and to remove the constraints wherever feasible. With the application of molecular biology, the molecular mechanisms of the interaction between nematode and fungal species can be understood, which further helps to develop new screening procedures of nematophagous fungi to control plant parasitic nematodes.

References Abd-Elgawad MMM, Askary TH (2015) Impact of phytonematodes on agriculture economy. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CAB International, Wallingford, pp 3–49 Abd-Elgawad MMM, Askary TH (2018) Fungal and bacterial nematicides in integrated nematode management strategies. Egypt J Biol Pest Co 28:74 Åhman J, Johanson T, Olsson M, Punt PJ, van den Hondel CAMJJ, Tunlid AS (2002) Improving the pathogenicity of a nematodetrapping fungus by genetic engineering of a subtilisin with nematotoxic activity. Appl Environ Microbiol 689:3408–3415 Ahren D, Ursing BM, Tunlid A (1998) Phylogeny of nematode-trapping fungi based on 18S rDNA sequences. FEMS Microbiol Lett 158:179–184 Athman SY, Dubois T, Coyne D, Gold CS, Labuschagne N, Viljoen A (2007) Effect of endophytic Fusarium oxysporum on root penetration and reproduction of Radopholus similis in tissue culture derived banana (Musa sp.) plants. Nematol 9:599–607 Atkins SD, Hidalgo-Diaz L, Kalisz H, Mauchline TH, Hirsch PR, Kerry BR (2003) Development of a new management strategy for the control of root-knot nematodes (Meloidogyne spp.) in organic vegetable production. Pest Manag Sci 59:183–189 Baron NC, Rigobelo EC, Zied DC (2019) Filamentous fungi in biological control: current status and future perspectives. Chil J Agr Res 79(2):307–315

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

305

Barron GL (1977) The nematode-destroying fungi. Lancaster Press, Lancaster, PA Berlitz DL, Knaak N, Cassal MC, Fiuza LM (2014) Bacillus and biopesticides in control of phytonematodes. In: Sahayaraj K (ed) Basic and applied aspects of biopesticides. Springer, New Delhi, pp 3–16 Bonants PJM, Fitters PFL, Thijs H, den Belder E, Waalwijk C, Henfling JWDM (1995) A basic serine protease from Paecilomyces lilacinus with biological activity against Meloidogyne hapla eggs. Microbiol 141:775–784 Borrebaeck CA, Mattiasson B, Nordbring-Hertz B (1984) Isolation and partial characterization of a carbohydrate-binding protein from a nematode-trapping fungus. J Bacteriol 159:53–56 Bourne JM, Kerry BR (2000) Observations on the survival and competitive ability of the nematophagous fungus Verticillium chlamydosporium in soil. Int J Nematol 10:9–18 Bourne JM, Kerry BR, de Leij FAAM (1996) The importance of the host plant on the interaction between root-knot nematodes (Meloidogyne spp.) and the nematophagous fungus Verticillium chlamydosporium Goddard. Biocontr Sci Technol 6:539–548 Braga FR, Araújo JV, Soares FEF, Geniêr HLA, Queiroz JH (2012) An extracellular serine protease of an isolate of Duddingtonia flagrans nematophagous fungus. Biocontrol Sci Tech 22:1131–1142 Brand D, Soccol CR, Sabu A, Roussos S (2010) Production of fungal biological control agents through solid state fermentation: a case study on Paecilomyces lilacinus against root-knot nematodes. Micol Aplicada Int 22:31–48 Caboni P, Aissani N, Demurtas M, Ntalli N, Onnis V (2016) Nematicidal activity of acetophenones and chalcones against Meloidogyne incognita, and structure–activity considerations. Pest Manag Sci 72:125–130 Chen SY, Dickson DW (2004) Biological control of nematodes by fungal antagonists. In: Chen ZX, Chen SY, Dickson DW (eds) Nematology advances and perspectives, Vol-II Nematode management and utilization. CAB International, Wallingford, pp 979–1025 Chen TH, Hsu CS, Tsai PJ, Ho YF, Lin NS (2001) Heterotrimeric G-protein and signal transduction in the nematode-trapping fungus Arthrobotrys dactyloides. Planta 212:858–863 Chen LL, Liu LJ, Shi M, Song XY, Zheng CY, Chen XL, Zhang YZ (2009) Characterization and gene cloning of a novel serine protease with nematicidal activity from Trichoderma pseudokoningii SMF2. FEMS Microbiol Lett 299(2):135–142 Ciancio A (1995) Observations on the nematicidal properties of some mycotoxins. Fundam Appl Nematol 18(5):451–454 Dababat AEA, Sikora RA (2007) Induced resistance by the mutualistic endophyte, Fusarium oxysporum strain 162, toward Meloidogyne incognita on tomato. Biocontrol Sci Tech 17(9):969–975 Dackman C, Jansson HB, Nordbring-Hertz B (1992) Nematophagous fungi and their activities in soil. In: Stotzky G, Bollag JM (eds) Soil biochemistry. Marcel Dekker, New York, pp 95–103 Dallemole-Giaretta R, Grassi de Freitas L, Lopes EA, da Silva MCS, Kasuya MCM, Ferraz S (2015) Pochonia chlamydosporia promotes the growth of tomato and lettuce plants. Acta Scientiarum 37(4):417–423 Dandurand LM, Knudsen GR (2016) Effect of the trap crop Solanum sisymbriifolium and two biocontrol fungi on reproduction of the potato cyst nematode, Globodera pallida. Ann Appl Biol 169(2):180–189 Davies KG (2005) Interactions between nematodes and microorganisms: bridging ecological and molecular approaches. Adv Appl Microbiol 57:53–78 Davies KG, Curtis RH (2011) Cuticle surface coat of plant-parasitic nematodes. Annu Rev Phytopathol 49:135–156 de Freitas Soares FE, Sufiate BL, de Queiroz JH (2018) Nematophagous fungi: far beyond the endoparasite, predator and ovicidal groups. Agric Natu Resour 52(1):1–8 de Leij FAAM (1992) Significance of ecology in the development of Verticillium chlamydosporium as a biological control agent against root-knot nematodes (Meloidogyne spp.). Ph.D. thesis, University of Wageningen, The Netherlands de Leij FAAM, Davies KG, Kerry BR (1992) The use of Verticillium chlamydosporium and Pasteuria penetrans alone and in combination to control Meloidogyne incognita on tomato plants. Fund Appl Nematol 15:235–242

306

K. K. Kumar

Dijksterhuis J, Veenhuis M, Harder W, Nordbring-Hertz B (1994) Nematophagous fungi: physiological aspects and structure—function relationships. Adv Microb Physiol 36:111–143 DiLegge MJ, Manter DK, Vivanco JM (2019) A novel approach to determine generalist nematophagous microbes reveals Mortierella globalpina as a new biocontrol agent against Meloidogyne spp. nematodes. Sci Rep 9(1):7521 Du B, Xu Y, Dong H, Yan L (2019) Phanerochaete chrysosporium strain B-22, a parasitic fungus infecting Meloidogyne incognita. PLoS One 15(1):e0216688 Eapen SJ, Beena B, Ramana KV (2005) Tropical soil microflora of spice-based cropping systems as potential antagonists of root-knot nematodes. J Invertebr Pathol 88:218–225 Escudero N, Ferreira SR, Lopez-Moya F, Naranjo-Ortiz MA, MarinOrtiz AI, Thornton CR, Lopez-­ Llorca LV (2016) Chitosan enhances parasitism of Meloidogyne javanica eggs by the nematophagous fungus Pochonia chlamydosporia. Fungal Biol 120:572–585 Ferreira PA, Ferraz S, Lopes EA, Freitas LG (2008) Parasitismo de ovos de Meloidogyne exigua por fungos nematófagos e estudo da compatibilidade entre os isolados fúngicos. Revista Trópica: Ciências Agrárias e Biológicas 2:15–21. [in Portuguese] Gan Z, Yang J, Tao N, Liang L, Mi Q, Li J, Zhang K-Q (2007a) Cloning of the gene Lecanicillium psalliotae chitinase Lpchi1 and identification of its potential role in the biocontrol of root-knot nematode Meloidogyne incognita. Appl Microbiol Biotechnol 76(6):1309–1317. https://doi. org/10.1007/s00253-007-1111-9 Gan Z, Yang J, Tao N, Yu Z, Zhang K-Q (2007b) Cloning and expression analysis of a chitinase gene Crchi1 from the mycoparasitic fungus Clonostachys rosea (syn. Gliocladium roseum). J Microbiol 45(5):422–430 Gortari MC, Hours RA (2008) Fungal chitinases and their biological role in the antagonism onto nematode eggs. A review. Mycol Progress 7:221–238. https://doi.org/10.1007/ s11557-008-0571-3 Gray N (1985) Ecology of nematophagous fungi: effect of soil moisture, organic matter, pH and nematode density on distribution. Soil Bio Biochem 17:499–507 Guo J, Zhu C, Zhang C, Chu Y, Wang Y et al (2012) Thermolides, potent nematocidal PKS-NRPS hybrid metabolites from thermophilic fungus Talaromyces thermophilus. J Am Chem Soc 134:20306–20309 Hallmann J, Sikora RA (1994) Influence of Fusarium oxysporum, a mutualistic fungal endophyte, on Meloidogyne incognita infection of tomato. J Plant Dis Prot 101(5):475–481 Hsueh YP, Mahanti P, Schroeder FC, Sternberg PW (2013) Nematode trapping fungi eavesdrop on nematode pheromones. Curr Biol 23:83–86. https://doi.org/10.1016/j.cub.2012.11.035 Huang XW, Zhao NH, Zhang KQ (2004) Extracellular enzymes serving as virulence factors in nematophagous fungi involved in infection of the host. Res Microbiol 115:811–816 Jansson HB, Friman E (1999) Infection-related surface proteins on conidia of the nematophagous fungus Drechmeria coniospora. Mycol Res 103(2):249–256 Jiang X, Xiang M, Liu X (2017) Nematode-trapping fungi. Microbiol Spectr 5(1):28128072. https://doi.org/10.1128/microbiolspec.FUNK-0022-2016 Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WM, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14(9):946–961 Kerry BR (1987) Biological control. In: Brown RH, Kerry BR (eds) Principles and practice of nematode control in crops. Academic Press, Sydney, pp 233–263 Kerry BR, Hidalgo-Diaz L (2004) Application of Pochonia chlamydosporia in the integrated control of root-knot nematodes on organically grown vegetable crops in Cuba. Multitr Inter Integ Contr 27:123–126 Kerry BR, Hirsch PR (2011) Ecology of Pochonia chlamydosporia in the rhizosphere at the population, whole organisms and molecular scale. In: Davies KG, Spiegel Y (eds) Biological control of plant-parasitic nematodes: building coherence between microbial ecology and molecular mechanisms. Progress in biological control. Springer, Dordrecht, pp 71–182

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

307

Khan A, Williams K, Molloy MP, Nevalainen H (2003) Purification and characterization of a serine protease and chitinases from Paecilomyces lilacinus and detection of chitinase activity on 2D gels. Prot Expres Purif 32:210–220 Khan A, Williams KL, Nevalainen HK (2004) Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biol Control 31(3):346–352 Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH et al (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:14 Kok CH, Papert A (2001) Microflora of Meloidogyne egg masses: species composition, population density and effect on the biocontrol agent Verticillium chlamydosporium (Goddard). Nematol 3(8):729–734 Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V, Vyas P, Dhaliwal HS, Saxena AK (2020) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi.org/10.1016/j. bcab.2019.101487 Kumar S, Singh A (2015) Biopesticides: present status and the future prospects. J Fertil Pestic 6:e129 Kumar KK, Sridhar J, Murali-Baskaran RK, Senthil-Nathan S, Kaushal P, Dara SK, Arthurs S (2018) Microbial biopesticides for insect pest management in India: current status and future prospects. J Invertebr Pathol 165:74–81 Kwok OCH, Plattner R, Weisleder D et al (1992) A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J Chem Ecol 18:127 Lamovsek J, Urek G, Trdan S (2013) Biological control of rootknot nematodes (Meloidogyne spp.): microbes against pests. Acta Agric Slov 101(2):263–275 Li G, Zhang K-Q (2014) Nematode-toxic fungi and their nematicidal metabolites. In: Zhang K-Q, Hyde KD (eds) Nematode-trapping fungi. Springer, Dordrecht, pp 313–375 Li Y, Hyde K, Jeewon R, Cai L, Vijaykrishna D, Zhang K (2005) Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Mycologia 97:1034–1046 Li J, Yang JK, Huang XW, Zhang KQ (2006) Purification and characterization of an extracellular serine protease from Clonostachys rosea and its potential as a pathogenic factor. Process Biochem 41:925–929 Li G, Zhang K, Xu J, Dong J, Liu Y (2007a) Nematicidal substances from fungi. Recent Pat Biotechnol 1:212–233 Li G, Wang X, Zheng L, Li L, Huang R, Zhang K (2007b) Nematicidal metabolites from the fungus Pleurotus ferulae Lenzi. Ann Microbiol 57:527–529 Li L, Ma M, Liu Y, Zhou J, Qu Q, Lu K, Fu D, Zhang K (2011) Induction of trap formation in nematode-trapping fungi by a bacterium. FEMS Microbiol Lett 322:157–165 Li J, Zou C, Xu J, Ji X, Niu X, Yang J, Huang X, Zhang K-Q (2015) Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annu Rev Phytopathol 53:67–95 Lima-Rivera DL, Lopez-Lima D, Desgarennes D, Velazquez-Rodriguez AS, Carrion G (2016) Phosphate solubilization by fungi with nematicidal potential. J Soil Sci Plant Nutr 16:507–524 Linford MB (1937) Stimulated activity of natural enemies of nematodes. Science 85:123–124 Liu K, Tian J, Xiang M, Liu X (2012) How carnivorous fungi use three-celled constricting rings to trap nematodes. Prot Cell 3(5):325–328 Liu K, Zhang W, Lai Y, Xiang M, Wang X, Zhang X, Liu X (2014) Drechslerella stenobrocha genome illustrates the mechanism of constricting rings and the origin of nematode predation in fungi. BMC Genom 15:114 Lopez-Llorca LV (1990) Purification and properties of extracellular proteases produced by the nematophagous fungus Verticillium suchlasporium. Can J Microbiol 36:530–537

308

K. K. Kumar

Lopez-Llorca LV, Olivares-Bernabeu C, Salinas J, Jansson HB, Kolattukudy PE (2002) Pre-­ penetration events in fungal parasitism of nematodes eggs. Mycol Res 106:499–506 Lopez-Llorca LV, Maciá-Vicente JG, Jansson HB (2008) Mode of action and interactions of nematophagous fungi. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Integrated management of plant pests and diseases, vol 2. Springer, Dordrecht, pp 51–76 Lu Z-X, Laroche A, Huang HC (2005) Isolation and characterization of chitinases from Verticillium lecanii. Can J Microbiol 51:1045–1055 Luo H, Liu Y, Fang L, Li X, Tang N, Zhang K (2007) Coprinus comatus damages nematode cuticles mechanically with spiny balls and produces potent toxins to immobilize nematodes. Appl Environ Microbiol 73:3916–3923 Manzanilla-Lopez RH, Esteves I, Finetti-Sialer MM, Hirsch PR, Ward E, Devonshire J, Hidalgo-­ Diaz L (2013) Pochonia chlamydosporia: advances and challenges to improve its performance as a biological control agent of sedentary endo-parasitic nematodes. J Nematol 45(1):1–7 Meerupati T, Andersson K-M, Friman E, Kumar D, Tunlid A et  al (2013) Genomic mechanisms accounting for the adaptation to parasitism in nematode trapping fungi. PLoS Genet 9(11):e1003909 Mi Q, Yang J, Ye F, Gan Z, Wu C, Niu X, Zou C, Zhang KQ (2010) Cloning and overexpression of Pochonia chlamydosporia chitinase gene pcchi44, a potential virulence factor in infection against nematodes. Process Biochem 45(5):810–814 Migunova V, Sasanelli N, Kurakov A (2018) Effect of microscopic fungi on larval mortality of the root-knot nematodes Meloidogyne incognita and Meloidogyne javanica. Biol Integr Contr Plant Pathog 133:27–31 Montesinos E (2003) Development, registration and commercialization of microbial pesticides for plant protection. Int Microbiol 6(4):245–252 Montfort WS, Kirkpatrick TL, Long DL, Rideout S (2006) Efficacy of a novel nematicidal seed treatment against Meloidogyne incognita on cotton. J Nematol 38:245–249 Moosavi MR, Askary TH (2015) Nematophagous Fungi: commercialization. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CAB International, Wallingford, pp 187–202 Moosavi MR, Zare R (2012) Fungi as biological control agents of plant-parasitic nematodes. In: Mérillon J, Ramawat K (eds) Plant defence: biological control. Progress in biological control, vol 12. Springer, Dordrecht, pp 67–107 Morton O, Hirsch P, Kerry B (2004) Infection of plant-parasitic nematodes by nematophagous fungi–a review of the application of molecular biology to understand infection processes and to improve biological control. Nematol 6(2):161–170 Murray DS, Wharton DA (1990) Capture and penetration processes of the free-living juveniles of (Nematoda) by the nematophagous fungus, Arthrobotrys oligospora. Parasitol 101(1):93–100 Nguyen V-N, Oh I-J, Kim Y-J, Kim K-Y, Kim Y-C, Park R-D (2009) Purification and characterization of chitinases from Paecilomyces variotii DG-3 parasitizing on Meloidogyne incognita eggs. J Ind Microbiol Biotechnol 36:195–203 Niu XM (2017) Secondary metabolites from Pochonia chlamydosporia and other species of Pochonia. In: Manzanilla-López R, Lopez-Llorca L (eds) Perspectives in sustainable nematode management through Pochonia chlamydosporia applications for root and rhizosphere health. Springer, Cham, pp 131–168 Nordbring-Hertz B, Chet I (1986) Fungal lectins and agglutinins. In: Mirelman D (ed) Microbial lectins and agglutinins: properties and biological activity. Wiley, New York, pp 393–408 Nordbring-Hertz B, Mattiasson B (1979) Action of a nematode trapping fungus shows lectin-­ mediated host–microorganism interaction. Nature 281:477–479 Nordbring-Hertz B, Jansson HB, Tunlid A (2006) Nematophagous fungi. Wiley, Hoboken, NJ Nordbring-Hertz B, Jansson H-B, Tunlid A (2011) Nematophagous fungi. Wiley, Chichester, pp 1–13

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

309

Park JO, Hargreaves JR, McConville EJ, Stirling GR, Ghisalberti EL (2004) Production of leucinostatins and nematicidal activity of Australian isolates of Paecilomyces lilacinus (Thom) Samson. Lett Appl Microbiol 38:271–276 Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020a) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Cambridge Rastegari AA, Yadav AN, Awasthi AA, Yadav N (2020b) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Cambridge Ravensberg WJ (2011) A roadmap to the successful development and commercialization of microbial pest control products for control of arthropods, vol 10. Springer, New York Rinu K, Pandey A (2011) Slow and steady phosphate solubilization by a psychrotolerant strain of Paecilomyces hepiali (MTCC 9621). World J Microbiol Biotechnol 27:1055–1062 Rosenzweig WD, Ackroyd D (1983) Binding characteristics of lectins involved in the trapping of nematodes by fungi. Appl Environ Microbiol 46:1093–1096 Rosso LC, Finetti-Sialer MM, Hirsch PR, Ciancio A, Kerry BR, Clark IM (2011) Transcriptome analysis shows differential gene expression in the saprotrophic to parasitic transition of Pochonia chlamydosporia. Appl Microbiol Biotechnol 90(6):1981–1994 Schenck S, Chase T, Rosenzweig W, Pramer D (1980) Collagenase production by nematode-­ trapping fungi. Appl Environ Microbiol 40:567–570 Scholler M, Hagedorn G, Rubner A (1999) A reevaluation of predatory orbiliaceous fungi II A new generic concept. Sydowia 51:89–113 Segers R (1996) The nematophagous fungus Verticillium chlamydosporium: aspects of pathogenicity. PhD thesis, University of Nottingham, UK Segers R, Butt TM, Kerry BR, Peberdy JF (1994) The nematophagous fungus Verticillium chlamydosporium produces a chymoelastaselike protease which hydrolyses host nematode proteins in situ. Microbiol 140:2715–2723 Sharon E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels GJ, Spiegel Y (2007) Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118:247–258 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Soares FE, Braga FR, Araújo JV, dos Santos LW, Mozer LR, Queiróz JH (2012) In vitro activity of a serine protease from Monacrosporium thaumasium fungus against first-stage larvae of Angiostrongylus vasorum. Parasitol Res 110:2423–2437 Spiegel Y, Sharon E, Bar-Eyal M, Maghodia A, Vanachter A, Van Assche A et al (2007) Evaluation and mode of action of Trichoderma isolates as biocontrol agents against plant-parasitic nematodes. IOBC WPRS Bulletin 30(6/2):129 Stadler M, Mayer A, Anke H, Sterner O (1994a) Fatty acids and other compounds with nematicidal activity from cultures of basidiomycetes. Planta Med 60:128e132 Stadler M, Sheldrick WS, Dasenbrock J, Steglich W, Anke H (1994b) Antibiotics from the nematode-­trapping basidiomycete Nematoctonus robustus. Nat Prod Lett 4:209e216 Steyn PS (1970) The isolation, structure and absolute configuration of secalonic acid D, the toxic metabolite of Penicillium oxalicum. Tetrahedron Lett 26(1):51–57 Stirling GR (1991) Biological control of plant parasitic nematodes. CAB International, Wallingford, p 282 Stirling GR (2011) Biological control of plant parasitic nematodes: an ecological perspective, a review of progress and opportunities for further research. In: Davies KG, Spiegel Y (eds) Biological control of plant parasitic nematodes: building coherence between microbial ecology and molecular mechanisms. Springer, Dordrecht, pp 1–38 Stirling GR, Smith L (1998) Field tests of formulated products containing either Verticillium chlamydosporium or Arthrobotrys dactyloides for biological control of root-knot nematodes. Biol Contr 11:231–239 Su H, Zhao Y, Zhou J, Feng H, Jiang D, Zhang KQ, Yang J (2015) Trapping devices of nematode-­ trapping fungi: formation, evolution, and genomic perspectives. Biol Rev Camb Philos Soc 31:371–378

310

K. K. Kumar

Suarez B, Rey M, Castillo P, Monte E, Llobell A (2004) Isolation and characterization of PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 2413 displaying nematicidal activity. Appl Microbiol Biotechnol 65(1):46–55 Szabó M, Csepregi K, Gálber M, Virányi F, Fekete C (2012) Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: the role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biol Control 63(2):121–128 Szabó M, Urbán P, Virányi F, Kredics L, Fekete C (2013) Comparative gene expression profiles of Trichoderma harzianum proteases during in  vitro nematode egg-parasitism. Biol Control 67(3):337–343 Thorn RG, Barron GL (1984) Carnivorous mushrooms. Science 224(4644):76–78 Tikhonov VE, Lopez-Llorca LV, Salinas J, Jansson H-B (2002) Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V.suchlasporium. Fungal Genet Biol 35:67–78 Tosi S, Annovazzi L, Tosi I, Iadarola P, Caretta G (2002) Collagenase production in an Antarctic strain of Arthrobotrys tortor Jarowaja. Mycopathologia 153:157–162 Tunlid A, Ahrén D (2001) Application of genomics to the improvement of nematode-trapping. In: Vurro M, Gressel J, Butt T et al (eds) Enhancing biocontrol agents and handling risks. IOS Press, Amsterdam, pp 193–200 Tunlid A, Johansson T, Nordbring-Hertz B (1991) Surface polymers of the nematode-trapping fungus Arthrobotrys oligospora. J Gen Microbiol 137:1231–1240 Tunlid A, Jansson H-B, Nordbring-Hertz B (1992) Fungal attachment to nematodes. Mycol Res 96:401–412 Tunlid A, Rosen S, Ek B, Rask L (1994) Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys oligospora. Microbiology 140:1687–1695 Vasanthi D, Kumaraswamy K (1999) Efficacy of vermicompost to improve soil fertility and rice yield. J Ind Soc Soil Sci 47(2):268–272 Venkatesan T, Pattar S (2017) Intellectual property guidelines and commercialization of biocontrol agents/biopesticides technologies. In: Varshney R, Gupta A, Patil J (eds) Training manual on “identification, mass production and utilization of parasitoids, predators and entomopathogens for sustainable insect pest management”. ICAR-NBAIR, Bengaluru, pp 115–126 Wang ELH, Bergeson GB (1974) Biochemical changes in root exudates and xylem sap of tomato plants infected with Meloidogyne incognita. J Nematol 6:194–202 Wang M, Yang JK, Zhang KQ (2006a) Characterization of an extracellular protease and its cDNA from the nematode-trapping fungus Monacrosporium microscaphoides. Can J Microbiol 52:130–139 Wang RB, Yang JK, Lin C, Zhang KQ (2006b) Purification and characterization of an extracellular serine protease from the nematodetrapping fungus Dactylella shizishanna. Lett Appl Microbiol 42:589–594 Wang B, Wu WP, Liu XZ (2007) Purification and characterization of a neutral serine protease with nematicidal activity from Hirsutella rhossiliensis. Mycopathologia 163:169–176 Wang B, Liu X, Wu WP, Liu X, Li S (2009) Purification, characterization, and gene cloning of an alkaline serine protease from a highly virulent strain of the nematode-endoparasitic fungus Hirsutella rhossiliensis. Microbiol Res 164:665–673 Wang X, Guan T, Zhang L, Li H (2015) Cloning of a serine protease gene from the nematophagous fungus Esteya vermicola and expressed activity of the recombinant enzyme against Bursaphelenchus xylophilus. Nematology 17(9):1071–1080 Waweru B, Turoop L, Kahangi E, Coyne D, Dubois T (2014) Non-pathogenic Fusarium oxysporum endophytes provide field control of nematodes, improving yield of banana Musa sp. Biol Control 74:82–88 Whipps JM, Lumsden RD (2001) Comercial use of fungi as plant disease biological control agents: status and prospects. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents progress, problems and potential. CA National, New York, pp 9–22

10  Fungi: A Bio-resource for the Control of Plant Parasitic Nematodes

311

Windham GL, Windham MT, Williams WP (1989) Effects of Trichoderma spp. on maize growth and Meloidogyne arenaria reproduction. Plant Dis 73:493–495 Yadav AN, Singh S, Mishra S, Gupta A (2019a) Recent advancement in white biotechnology through fungi. Volume 2: perspective for value-added products and environments. Springer, Cham Yadav AN, Singh S, Mishra S, Gupta A (2019b) Recent advancement in white biotechnology through fungi. Volume 3: perspective for sustainable environments. Springer, Cham Yadav AN, Rastegari AA, Yadav N, Kour D (2020a) Advances in plant microbiome and sustainable agriculture: diversity and biotechnological applications. Springer, Singapore Yadav AN, Rastegari AA, Yadav N, Kour D (2020b) Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges. Springer, Singapore Yadav AN, Singh J, Rastegari AA, Yadav N (2020c) Plant microbiomes for sustainable agriculture. Springer, Cham Yang JK, Huang XW, Tian BY, Wang M, Niu QH, Zhang KQ (2005) Isolation and characterization of a serine protease from the nematophagous fungus, Lecanicillium psalliotae, displaying nematicidal activity. Biotechnol Lett 27:1123–1128 Yang Y, Yang E, An Z, Liu X (2007a) Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proc Natl Acad Sci 104:8379–8384 Yang JK, Li J, Liang LM, Tian BY, Zhang Y, Chen CM, Zhang KQ (2007b) Cloning and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys conoides. Arch Microbiol 188:167–174 Yang JK, Liang LM, Zhang Y, Li J, Zhang L, Ye FP, Gan ZW, Zhang KQ (2007c) Purification and cloning of a novel serine protease from the nematode-trapping fungus Dactylellina varietas and its potential roles in infection against nematodes. Appl Microbiol Biotechnol 75:557–565 Yang JK, Ye FP, Mi QL, Tang SQ, Li J, Zhang KQ (2008) Purification and cloning of an extracellular serine protease from the nematodetrapping fungus Monacrosporium cystosporium. J Microbiol Biotechnol 18:852–858 Yang J, Wang L, Ji X, Feng Y, Li X, Zou C, Xu J, Ren Y, Mi Q, Wu J et al (2011) Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog 7:e1002179 Yang E, Xu L, Yang Y, Zhang X, Xiang M, Wang C, An Z, Liu X (2012) Origin and evolution of carnivorism in the Ascomycota (fungi). Proc Natl Acad Sci USA 109:10960–10965 Zaki FA (1994) Mode of action of nematode destroying organisms. In: Bhatti DS, Walia RK (eds) Nematode pest management in crops. CBS Publishers, Delhi, pp 239–256 Zhang K-Q, Hyde KD (2014) Nematode-trapping fungi. Springer, Dordrecht Zhang YJ, Liu XZ, Wang M (2008) Cloning, expression, and characterization of two novel cuticle-­degrading serine proteases from the entomopathogenic fungus Cordyceps sinensis. Res Microbiol 159:462–469 Zhang Y, Yu Z-F, Xu J, Zhang K-Q (2011) Divergence and dispersal of the nematode-trapping fungus Arthrobotrys oligospora from China. Environ Microbiol Rep 3:763–773 Zhang S, Gan Y, Xu B, Xue Y (2014) The parasitic and lethal effects of Trichoderma longibrachiatum against Heterodera avenae. Biol Control 72:1–8 Zhao ML, Mo MH, Zhang KQ (2004) Characterization of a neutral serine protease and its full-­ length cDNA from the nematodetrapping fungus Arthrobotrys oligospora. Mycologia 96:16–22 Zhao ML, Huang JS, Mo MH, Zhang KQ (2005) A potential virulence factor involved in fungal pathogenicity: serine-like protease activity of nematophagous fungus Clonostachys rosea. Fungal Divers 19:217–234 Zhao LL, Wei W, Kang L, Sun JH (2007) Chemotaxis of the pinewood nematode, Bursaphelenchus xylophilus, to volatiles associated with host pine, Pinus masso-niana, and its vector Monochamus alter-natus. J Chem Ecol 33:1207–1216 Zhao D, Liu B, Li LY, Zhu XF, Wang YY, Wang JQ, Duan YX, Chen LJ (2013) Simplicillium chinense: a biological control agent against plant parasitic nematodes. Biocontrol Sci Tech 23:980–986

Chapter 11

Global Scenario of Advance Fungal Research in Crop Protection Vanita Yadav, Murthy M. V. S. N. Lekkala, Challa Surekha, and Nageswara Rao Reddy Neelapu

Contents 11.1  I ntroduction 11.2  F  ungi as Biocontrol Agents 11.2.1  Fungi Mediated Biocontrol of Pests 11.2.2  Fungi Mediated Biocontrol of Soil Borne Plant Pathogens 11.2.3  Fungi Mediated Biocontrol of Weeds 11.2.4  Fungi Mediated Biocontrol of Nematodes 11.2.5  Mechanisms of Fungi Mediated Biocontrols 11.2.6  Advantages and Disadvantages of Fungi as Biocontrol Agents 11.3  Understanding the Biology of the Biocontrol Agents 11.3.1  Next Generation Sequencing Technologies 11.3.2  First Generation Sequencing Technologies 11.3.3  Second Generation of Sequencing Technologies 11.3.4  Third Generation of Sequencing Technologies 11.3.5  Fourth Generation of Sequencing Technologies 11.3.6  Fifth Generation Sequencing Technologies 11.4  Genome to Phenome Projects of Fungi 11.4.1  Genome Sequencing Projects 11.4.2  Transcriptome Sequencing Projects 11.4.3  Proteome Sequencing Projects 11.5  Synergism Between Different Biocontrol Agents 11.6  Synergism Between Plant Growth Promoting Rhizobacteria and Biocontrol Agents 11.7  Advances in Formulation of Biocontrol Agents 11.8  Understanding Interaction of Fungi with Plants 11.8.1  Colonization of Plant by Fungal Microbiome 11.8.2  Quorum Sensing Among Plant Microbiome and Interkingdom Species 11.8.3  Interaction Between Plants and Fungal Microbiome 11.8.4  Plants Immune System 11.8.5  Cross Talk Between Plants and Microbiomes 11.9  Conclusion and Future Directions References

 314  314   315   316   318   318   319  324  324   324   325   327   328   329  330  331   331   332  333  333  334  334  335   335   335  336  336  337  337  338

V. Yadav · M. M. V. S. N. Lekkala · C. Surekha · N. R. R. Neelapu (*) Department of Biochemistry and Bioinformatics, Institute of Science, Gandhi Institute of Technology and Management (GITAM), (Deemed-to-be University), Visakhapatnam, Andhra Pradesh, India

© Springer Nature Switzerland AG 2020 A. N. Yadav et al. (eds.), Agriculturally Important Fungi for Sustainable Agriculture, Fungal Biology, https://doi.org/10.1007/978-3-030-48474-3_11

313

314

V. Yadav et al.

11.1  Introduction Sustainable agriculture is one of the major challenges today, considering food security to growing human population and dependence of crop productivity on chemicals (Challa et al. 2019a) and (Kour et al. 2020). The ecological costs of the conventional agriculture approaches  are largely underestimated. There are five billion kilograms of pesticides being annually used worldwide (Verger and Boobis 2013) and it is estimated to result in around two lakh deaths every year (WHO 2004). There are number of rules and legislations implemented for limiting the usage of these harmful chemical insecticides to protect human health as well as our environment; however, a lot of efforts are still required to minimize the usage of insecticides. At the same time, there is a requirement of more sustainable methods for resolving these agronomic challenges and reducing the chemical pollution. Insect herbivory causes severe damage to plant in the natural systems, and their impact on agroecosystems is even more destructive (Meehan et al. 2011). Root pests have always caused huge damage to crops and the herbivores below ground sustain a wide diversity and feed on numerous plant tissues (Koppenhofer et  al. 2000a; Hunter 2001). The biological control is challenging and scientifically based risk analysis is required, i.e. to be experimented extensively before releasing the biological control agents into the field. Classical method is based on the capability of a pathogen to control host populations, depending on its ability to perpetuate and disperse. This method needs special care in selecting the agents that are strongly pathogenic; and ecologically and climatically apt for the target location. The pathogen has to be specific to the host and may also include their relatives if they do not have any economic or environmental importance. This review discusses in detail about global scenario of advance fungal research in biocontrol or crop protection as shown in Fig. 11.1.

11.2  Fungi as Biocontrol Agents Fungi are a phylogenetically diverse group of microorganisms which are heterotrophic in nature (absorptive nutrition). Fungi are employed for industrial or other applications like biocontrol, biomass degradation, bioremediation, bioenergy (biofuel), chemicals (organic acids), detergents, enzymes, food and feed, proteins, paper and pulp, pharmaceuticals (antibiotics, secondary metabolites, statins), and textiles due to its eco-friendly nature or bringing down greenhouse gas emissions (Lalitha et  al. 2011, 2013; Challa et  al. 2019a; Yadav et  al. 2019b, c). Entomopathogenic hyphomycetes are known to be active against a number of insects or pests, weeds, soil borne pathogens, nematodes, etc. in the agricultural ecosystems (Fig. 11.2).

11  Global Scenario of Advance Fungal Research in Crop Protection

315

Fig. 11.1  Global scenario of advance fungal research in biocontrol or crop protection

11.2.1  Fungi Mediated Biocontrol of Pests Entomopathogenic fungi are majorly known to be the natural enemies of pests of agricultural crops (Hajek and Leger 1994; Singh and Yadav 2020). Hyphomycetous fungi like Aspergillus, Beauveria, Culicinomyces, Hirsutella, Metarhizium, Nomuraea, Paecilomyces, Tolypocladium, and Verticillium are capable of causing natural outbreaks in the populations of the insects (Jyoti and Singh 2017). Entomopathogenic fungi Beauveria, Metarhizium, Nomuraea, Paecilomyces, and Verticillium belong to family Clavicipitaceae (Neelapu et  al. 2009; Challa and Neelapu 2019). The reproductive biology of the entomopathogenic fungi Beauveria bassiana and Nomuraea rileyi was reported to be both clonal and recombination (Padmavathi et al. 2003; Devi et al. 2006, 2007). Devi et al. (2004) reported that Beauveria bassiana is resistance to organophosphate based insecticide and this

316

V. Yadav et al.

Fig. 11.2  Fungi mediated biocontrol of insects or pests, weeds, soil borne pathogens, and nematodes in the agricultural ecosystems

resistance is mediated by esterase. Thus, these can be used for efficacious management of insect pests; however, they are not easy to produce at mass scale. They are host specific and have a huge impact on the host pest populations. These fungi have life cycles that coordinate with insect host stages and the environmental conditions. All the stages of insects can be killed by these pathogens. Fungi unlike other pathogens do not ingest to infect and kill the host; thus sap sucking phytophagous insects are also a target to them. They infect either by primary contact with fungal spore or by uptake of spores when sprayed on crops (Moore and Prior 1993). “Some entomopathogenic fungi have restricted and varied host ranges, for example, Aschersonia aleyrodes infects only scale insects, and whiteflies, whereas other fungal species have a wide host range” (Sandhu et al. 2012) (Fig. 11.3).

11.2.2  F  ungi Mediated Biocontrol of Soil Borne Plant Pathogens Soil food chain includes an array of predators (herbivore pests), like carabid, centipedes, mites, spiders, and beetles (Symondson et al. 2002). Till date, small number of commercial products based on arthropod predators had success. There are several reasons aligned for it and one among them is that interactions between predators and their prey cannot be predicted easily when multi-trophic systems are considered

11  Global Scenario of Advance Fungal Research in Crop Protection

317

Fig. 11.3  Morphology of (a) Beauveria bassiana, (b) Nomuraea rileyi, (c) Paecilomyces fumoroseus, and (d) Metarhizium anisopliae

which are under the influence of constantly changing biotic and abiotic parameters. The developing commercial products are based on the soil macro-fauna and numerous venues can be investigated (Yadav et al. 2020c, d). Trichoderma and Gliocladium are the fungal biocontrol agents which are used to control weeds (Bhuiyan et al. 2012). Gliocladium was known to control Pythium damping-off (Wilhite et  al. 1994). These BCAs produce antimicrobial compounds and suppress disease via antibiotics like gliovirin and gliotoxin.

318

V. Yadav et al.

11.2.3  Fungi Mediated Biocontrol of Weeds Weeds are the major constraint to the worldwide agricultural production and impact of weeds on crop production is calculated with average losses of around 20%. Human resources can be better invested in more meaningful pursuits; but the social costs are hindering their development. The use of herbicides has limited due to the increase in population of herbicide-resistant weeds, majorly in wheat and maize (Rastegari et al. 2020a, b). This has led to the development of new strategies for long-term management of agricultural weeds. The result of global trade is that more plant species with potentially weedy traits are on move, resulting in the rise of new weed issues mainly in natural ecosystems and non-agricultural lands. Such situations lead to exotic weeds that contribute to the massive threat to our biodiversity after habitat destruction (Yadav et al. 2019a). Fungal biological control agents (BCAs) are exploited for the management of weed. The risk analysis and safety issues of biological control using fungal pathogens are still in the learning phase. The two major methods for biological control are (1) classical biological control for management of exotic or alien weeds and (2) inundative application of BCAs for biological control of endemic weeds. The potential of fungal pathogens as classical BCAs is aptly defined as the “use of living organisms to control pest species” (Waage and Greathead 1988; Watson 1991). Fungi Colletotrichum gloeosporioides f.sp. malvae is used for the control of round leaf mallow (Malva pusilla) (Mortensen 1988; PMRA 2006). Same fungi C. gloeosporioides f.sp. aeschynomene was used to control Aeschynomene virginica. BCA, Colletotrichum gloeosporioides f.sp. is commercially available in the name of BioMal. Similarly, fungi Sclerotinia minor was used to control broadleaf plantain (Plantago major), dandelion (Taraxacum officinale), white clover (Trifolium repens), and in turf (PMRA 2010). BCA, Sclerotinia minor is commercially available in the name of Sarritor.

11.2.4  Fungi Mediated Biocontrol of Nematodes Nematophagous fungi are the potential biological control agents to control nematodes effectively. Phytophagus nematodes, migrating in soil to new host plants or deprived of proper hosts, face survival in an environment abundantly populated with fungal enemies. Fungal spores of Harposporium are ingested by nematode and these spores germinate in the esophagus to develop and consume the nematode (Aschner and Kohn 1958). These fungi then recycle carbon, nitrogen, and other important elements from biomass of nematodes. Fungal species such as Arthrobotrys, Verticillium chlamydosporium, Acremonium, Fusarium oxysporum, and Dactylella oviparasitica are used to control nematodes. Arthrobotrys which is commercially available in the name of Royal 350 is used to control root-knot nematode against tomato crop (Cayrol and Frankowski 1979). Verticillium chlamydosporium and

11  Global Scenario of Advance Fungal Research in Crop Protection

319

another nonsporulating “contortion fungus” are used to control eggs of Heterodera schachtii and H. avenae cysts (Tribe 1977). Further, Acremonium and Fusarium oxysporum are also used to control H. schachtii in sugar beet soils of California (Nigh 1979). Furthermore, these fungi are used to control Sarisodera africanus cysts of Panicum roots in West Africa. Dactylella oviparasitica is used to control root-knot nematode Meloidogyne populations and their eggs in peach orchards on Lovell rootstock in California’s San Joaquin valley (Stifling 1978).

11.2.5  Mechanisms of Fungi Mediated Biocontrols Biological control is an outcome of many different types of interactions among the organisms. The different biocontrol mechanisms are antagonism, antibiosis, and competition (Fig. 11.4). 11.2.5.1  Antagonism Antagonism is defined as “lysis of the pathogen by other microorganism. This is also called as hyperparasitism and fungi that are parasitic on other fungi are known as mycoparasites” (Bakers and Cook 1974). Cook (1993) classified the mycoparasitic interactions as (a) unilateral antagonism, (b) mutual antagonism, and (c) no antagonism. Ampelomyces quisqualis has been the subject of numerous investigations on biological control of powdery mildews for over the 50 years. The fungus Ampelomyces quisqualis occurs on Erysiphales (powdery mildews) which is a naturally occurring deuteromycete hyperparasite and it infects to form pycnidia (fruiting bodies) within powdery mildew hyphae, conidiophores, and cleistothecia (the closed fruiting bodies of powdery mildews). Hyperparasitism “reduces the growth and eventually kills the mildew colony. The mycoparasitic competence of

Fig. 11.4  Mechanisms of biological control (a) antagonism (Tricohoderma viride vs Fusarium solani) (Source: Villamizar-Gallardo et al. 2017), (b) antibiosis (Trichoderma spp. on M. phaseolina) (Source: Mendoza et al. 2015), and (c) competition (Trichoderma harzianum and Ambrosiella grosmanniae) (Source: Castrillo et al. 2016)

320

V. Yadav et al.

Trichoderma species against economically important plant pathogens has allowed the development of biocontrol strategies” (Harman et al. 2004; Motlagh and Samimi 2013). Weindling in 1932, “observed and reported that the Trichoderama lignorum (T. viride) parasitize the hyphae of Rhizoctonia solani and recommended that the Trichoderma can be used control damping-off of citrus seedlings” (Lo 1997). There are several fungal parasites like Coniothyrium minitans which attack plant pathogen like sclerotia, while Pythium oligandrum attack living hyphae belonging to Botrytis, Fusarium, and Phytophthora. Single fungal pathogen “can be attacked by multiple hyperparasites, for example, Acremonium alternatum, Acrodontium crateriforme, Ampelomyces quisqualis, Cladosporium oxysporum, and Gliocladium virens have the capacity to parasitize powdery mildew pathogens” (Kiss 2003). 11.2.5.2  Antibiosis Antibiosis is the “procedure of secretion of antimicrobial compounds by fungi to suppress or kill pathogenic fungi in the vicinity of its growth area. Most fungi are capable of secreting one or more compounds. The secondary metabolites with the antibiotic activity are often correlated to specific stages of morphological differentiation, and are associated with the phase of active growth. Interestingly, some fungal secondary metabolites can modify the growth and the metabolism of plants, while others seem to target specific fungal processes such as sporulation and hyphal elongation. Thus, the expression of secondary metabolites may occur at a predictable point during the normal life cycle of some fungi, including those used for agriculture applications” (Keller et al. 2005). Menendez and Godeas (1998) reported “a biocontrol study of Trichoderma harzianum against Sclerotinias clerotiorum—a soil borne plant pathogen attacking many economically important crops, such as soybean”. Menendez and Godeas (1998) studied “about antibiosis of T. harzianum against the plant pathogen and assumed that the beneficial effect was due to concurrent mycoparasitism and competition” (Inbar et  al. 1996; Ghisalberti 2002). In another example, despite close contact between hyphae of Trichoderma spp. and Fusarium moniliforme/Aspergillus flavus on coculturing, hyphal penetration was absent. This suggested that mycoparasitism was not the sole cause for the observed inhibitory effects (Calistru et  al. 1997). Therefore, metabolites produced by Trichoderma spp. (e.g., volatiles, extracellular enzymes, and/or antibiotics) were considered to be the probable elements involved in antibiosis. Trichoderma spp. has been effective against a wide host range and in hindering the longevity of sclerotia of pathogenic fungi. Szekeres et al. (2005) reviewed about “antagonistic metabolites produced by Trichoderma spp. The metabolites are linear, amphipathic polypeptides, namely peptaibols and peptaibiotics. The physico-chemical and biological properties of these antibiotic compounds included disruption of lipid membranes, antimicrobial activities, and induction of plant resistance. Some biocontrol agents exhibit predatory behavior under nutrient-limited conditions. However, such activity generally is not expressed under typical growing conditions. For example, some species of Trichoderma produce a range of enzymes that are

11  Global Scenario of Advance Fungal Research in Crop Protection

321

directed against cell walls of fungi. Peptaibols and the related peptaibiotics are linear, amphipathic polypeptides and the compounds are composed of 5–20 amino acids. These are generally produced in microheterogeneous mixtures that have strong antimicrobial activity”. Gram-positive bacteria and fungi act synergistically with cell-wall-degrading enzymes (CWDEs) to inhibit the growth of fungal pathogens and elicit plant resistance to pathogens (Wiest et  al. 2002; Szekeres et  al. 2005). Peptaibols and peptaibiotics with unusual amino acid content are the result of non-ribosomal biosynthesis. Large multifunctional enzymes known as peptide synthetases assemble these molecules by the multiple carrier thio-template mechanism from a remarkable range of precursors, which can be N-methylated, acylated, or reduced (Szekeres et  al. 2005). Peptaibols and peptaibiotics show interesting physico-chemical and biological properties including the formation of pores in bilayer lipid membranes. In tobacco plants, exogenous applications of peptaibols trigger a defense response and reduce susceptibility to tobacco mosaic virus (Wiest et al. 2002). A peptaibol synthetase from T. virens has been purified, and the corresponding gene, when cloned, will facilitate studies of this compound and its contribution to biocontrol. An extensive review on antibiosis and production of Trichoderma secondary metabolites elaborated the significance of secondary metabolites (antibiotic activity) in antagonistic action of Trichoderma spp. against pathogenic fungi Pythium ultimum and Rhizoctonia solani (Hutchinson 1999; Hanson and Howell 2002). However, there seems to be a general consent on the combined synergistic effect of the two factors (enzymes and antibiotic compounds) (Schirmbock et al. 1994). 11.2.5.3  Competition Starvation is the most “common cause of death for microorganisms, so that competition for limiting nutrients results in biological control of fungal phytopathogens” (Chet et al. 1997). Celar (2003) directed a study on the forms of nutrients mostly available to phytopathogenic and antagonistic fungi. Earlier study reconfirmed the findings of Blakeman (1978) that shortage of easily accessible nutrients for microorganisms, especially of those living in soil and on plant surfaces, results in open nutrient competition among microorganisms (Sivan and Chet 1986; Lewis and Papavizas 1991). Biocontrol based on competition for rare but essential micronutrients, such as iron, which is extremely limited in the rhizosphere, depending on soil pH has been observed. In highly oxidized and aerated soil, iron is present in ferric form (Lindsay 1979), which is insoluble in water (pH 7.4) and the concentration may be as low as 10–18 M. This concentration is too low to support the growth of microorganisms, which generally need concentrations approaching 10–6 M. To survive in such an environment, organisms were found to secrete iron-binding ligands called siderophores having high affinity to sequester iron from the micro-environment. Largely most filamentous fungi uptake iron as essential mineral for viability and under iron starvation, and mostly fungi excrete low-molecular-weight ferric-

322

V. Yadav et al.

iron specific chelators, termed siderophores, to mobilize environmental iron (Eisendle et al. 2004). Then, iron from the ferri-siderophore complexes is recovered via specific uptake mechanisms. In Aspergillus fumigates and Aspergillus nidulans, siderophore biosynthesis is negatively regulated by carbon source (Eisendle et al. 2004). In Ustilago maydis, gene products related to iron uptake affect the development of plant (McIntyre et  al. 2004). Some Trichoderma and biocontrol agents produce highly efficient siderophores that chelate iron and stop the growth of other fungi (Chet and Inbar 1994). For this reason, soil composition influences the biocontrol effectiveness of Pythium by Trichoderma according to iron availability. In addition, T. harzianum T35 controls Fusarium oxysporum by competing for both rhizosphere colonization and nutrients, with biocontrol becoming more effective as the nutrient concentration decreases (Tjamos 1992). Competition has proved to be particularly important for the biocontrol of phytopathogens such as Botrytis cinerea, the main pathogenic. The increased efficiency in iron uptake of the commensal microorganisms is thought to be a contributing factor to their ability to aggressively colonize plant roots and an aid to the displacement of the deleterious organisms from potential sites of infection. Thus, the cited examples confirm the significance of competition for nutrients during biocontro. 11.2.5.4  Biocontrol Agents This section discusses in detail about biocontrol agents like Beauveria bassiana, Paecilomyces fumosoroseus, Nomuraea rileyi, Metarhizium anisopliae, Verticillium lecanii, and Trichoderma. Beauveria bassiana is a filamentous entomopathogenic fungus which is highly adapted to specific insect hosts. This fungus naturally grows in soil and is a well-known pathogen on insects that causes white muscardine disease (Sandhu et al. 2001; Thakur et al. 2005; Jain et al. 2008). Paecilomyces fumosoroseus is a both nematophagous and entomopathogenic fungus, which kills harmful nematodes and insects by pathogenesis and causes disease in them. This fungus is used as a bionematicide for controlling nematodes by applying it directly to the soil. P. lilacinus infects and ingests the eggs of root-knot and even cyst nematodes. Hyphomycetes are the natural enemies of whiteflies worldwide and cause “Yellow Muscardine” disease (Nunez et  al. 2008). Usually, certain species of fungi are known for their competence causing high level mortality, and developing natural epizootics that is dependent on the environmental conditions and also biased by various practices of crop production. P. lilacinus is known for its potential as biological control agent specifically in subtropical and tropical soils. P. lilacinus has the ability to grow on leaf surface in humid conditions and it is known to spread rapidly in whitefly populations (Wraight et al. 2000). Nomuraea rileyi is dimorphic hyphomycetous fungi that cause epizootic on numerous insects and arthropods and thus it is a very efficient biocontrol agent against insects and arthropods. It is known that many insect species that belong to

11  Global Scenario of Advance Fungal Research in Crop Protection

323

Lepidoptera including Spodoptera litura and some to Coleoptera are very susceptible to N. rileyi. The host specificity and the eco-friendly nature of N. rileyi fortify its use in insect pest management. On the other hand, its mode of infection and development is examined and reported for numerous insect hosts (for instance, Trichoplusia ni, Heliothis zea, Plathypena scabra, Bombyx mori, Pseudoplusia). In another example, insect Spilosoma was found to be severely attacked by N. rileyi (Mathew et al. 1998). Metarhizium anisopliae is a pathogen for insect pests and is very well known for biological control of notorious insect pests (Sandhu et al. 1993; Sandhu and Mishra 1994). This species is specifically used for the control of locusts, grasshoppers, cockroaches, termites, and other major pests worldwide. Oil is used for spreading the green spores to the parts of the insect with high relative humidity (parts like the back of the neck or under the wing where cuticle is thin) where the fungus can grow easily. This fungus is very effective; it holds the capability to kill 90% of locusts with its application in 7–21  days, depending on the number of infected spores. Complete biological activity of M. anisopliae is tested on Eutectona machaeralis (teak skeletonizer) and is analyzed to be a potential fungal biological control agent of teak pest (Sandhu et al. 2000). Verticillium lecanii is widely distributed entomopathogenic fungus that causes large epizootic in warm and humid environments (Nunez et  al. 2008, Kim et  al. 2002). It is known to be a very effective agent of biological control against Trialeurodes vaporariorum in South Korean greenhouses. In the year 1970, V. lecanii was developed for controlling whitefly and several aphids species including green peach aphids for use in greenhouse Chrysanthemums (Hamlen 1979). It is considered to be major parasite and can cause massive fall in cereal-cyst nematode populations (Kerry et al. 1982). Another species V. chlamydosporium has an extensive host range among cyst and root-knot nematodes. It is not much consistent and only few isolates have potential as commercial biological control agents. Species of Trichoderma are used in biological control of pests and soil borne pathogens, and as PGPR. This mechanism of biological control has led to improvement in application of the different strains as biocontrol agents. These are developed into commercial products of biocontrol that are used in the fields, greenhouse systems (Harman et al. 2004), and also well known for controlling various soil borne diseases. The soil borne diseases known are “Pythium ultimum Trow. (Naseby et al. 2000), Sclerotinia sclerotiorum (Lib.) de Bary (Inbar et al. 1996) and Fusarium oxysporum Schlechtend (Sivan and Chet 1993)” Trichoderma spp. easily extracts nutrients from complex substrates (e.g. protein, glucosamine, and tannin) in the soil. Trichoderma viride mediated reprogramming of plant defense mechanism in Vigna mungo, Cajanus cajan, Vigna radiata, was  reported  against plant pathogens Fusarium oxysporum and Alternaria alternata (Surekha et al. 2013, 2014; Rao et al. 2015). Thus, this potential is an additional advantage as it leads to improvement in soil minerals where excessive use of herbicides needs to be limited.

324

V. Yadav et al.

11.2.6  A  dvantages and Disadvantages of Fungi as Biocontrol Agents Fungi as biocontrol agents have number of features that gathers public support. The best part is the usage of these has limited the chemical products that are poisonous to human population as well as to environment. Currently these biocontrol products are just 2% in global pesticide market. Chemical approach is easier and more effective on pests which actually led to chemical revolution from green revolution (Pimentel et  al. 1992; Yadav et  al. 2020a). Fungi are dignified biological agents with diverse benefits such as they are self-generating either on the surface of plants or inside them which efficiently provide protection constantly and are absolutely safe to use. Fungi are easy to produce and also quite adaptable with current application technology. Additionally, vast usage of fungi can lead in control of numerous pests with a single product. There are certain limitations with biocontrol fungi like narrow host range of the beneficial organisms, and increase in mortality rate with age of biocontrol fungi. Environmental factors play a huge role in their success, for example, biocontrol to be effective, moist/humid weather is necessary. The above-mentioned major reasons limit their usage in pest control (Yadav et al. 2020b, e).

11.3  Understanding the Biology of the Biocontrol Agents Understanding the biology of the biocontrol agents is possible when we understand the next generation sequencing (NGS) technologies and NGS data.

11.3.1  Next Generation Sequencing Technologies Deoxyribonucleic acid (DNA) is the ultimate code of any living organisms genome and is composed of four bases [A, T, G, C] in enormous numbers and in different combinations. DNA sequencing utilizes the DNA composition for analysis and translates the code of all the biota on earth. The emergence of sequencing technologies performed a substantial role in studying genomic sequences of individuals. The sequence constitutes string of nucleotides [A,T,G,C] and N [represent ambiguity]. The first sequencing technologies were developed by Sanger et al. in the year 1977 and later by Maxam et al. in the year 1980. Their discovery unlocked the door for genetic code studies and lead to the development of faster and competent sequencing technologies. As we are heading towards the age of synthetic genomics and personalized medicine, there is an increased need of highly efficient sequencing technologies. Determination of order and composition of nucleic acid in a sample is a vital element for a number of research applications. Since, five decades large num-

11  Global Scenario of Advance Fungal Research in Crop Protection

325

bers of researchers are involved in advancements of these technologies for fast and accurate results. Also there is a stupendous improvement in recorded with time from sequencing short oligonucleotides to millions of bases. There was also hard time in deducing coding sequence of a single gene to broadly available data of whole genomes (Neelapu and Surekha 2016; Kchouk et al. 2017). This section discusses in detail about the next generation technologies used for generation of NGS data (Fig. 11.5).

11.3.2  First Generation Sequencing Technologies First generation sequencing technology includes Sanger and Maxam Gilbert DNA sequencing technologies introduced in the year 1977. Sanger sequencing follows the chain termination method, i.e. dideoxynucleotide method (Sanger et al. 1977). Sanger sequencing uses oligonucleotide primers to find certain specific regions of DNA.  The process is initiated with denaturation of double stranded to single stranded DNA which forms the template for the process of sequencing. The resultant single strand is then annealed with oligonucleotide primers. Later, elongated in

Fig. 11.5  Next generation sequencing technologies used for generation of NGS data

326

V. Yadav et al.

the mixture of deoxynucleotide triphosphates (dNTPs) that provides the nucleotides (A,T,G,C) to build new double stranded model. Along with these a few chain terminating dideoxynucleotide triphosphates (dNTPs) of each nucleotide are added, which help in termination of the strand. Each strand will be varying in their length depending on the ddNTPs attaching. Each ddNTP is associated with a fluorescent marker, when attached to the sequence will emit and illuminate light depending on the nucleotide base. According to the protocol each nucleotide is associated with specific color fluorescence, namely A by green, T by red, G by black, and C by blue. And then a laser depicts the sequence depending on the intensity color of light emitted and which is translated into peak. If a heterozygous variant is present in the sequence, peak will be captured by two fluorescent dyes and the dye color is replaced by completely new base pair’s color. The types of variants include silent, missense, nonsense, truncating, deletion, insertion, and splicing. Sanger sequencing is the robust testing strategy that has the capability to diagnose point mutation/ deletion or duplication. It is definitely a promising approach to cover desired regions but is costly for multiplex testing systems. Therefore, the latest Sanger sequencing approach is gene specific (Masoudi-Nejad et  al. 2013; El-Metwally et al. 2014). Maxam–Gilbert sequencing is another method that belongs to the first generation of sequencing which was developed in the year 1976–1977 by Allan Maxam and Walter Gilbert. It is well known as chemical degradation/chemical cleavage method for DNA sequence determination. The method depends on nucleotide cleaving and is most efficient with small nucleotide polymers. This method permits sequencing of at least 100 bases from the point of labelling (Maxam and Gilbert 1977). In accordance to this method, the sequence of the nucleotides is determined by terminally labelled DNA molecule by breaking it at any of the bases (ATGC) with the aid of chemical agents (Shackelford 2019). It is gel based sequencing method which uses four different base specific enzymes known as restriction endonucleases for cleaving at specific sequence. Postpurification, phosphate from 3′ end is cleaved with the help of phosphatase and replaced with radioactive phosphate 32P. Then the radioactive DNA fragment is treated with restriction endonucleases and the resultant DNA fragments are ran through gel electrophoresis to separate labelled and unlabelled end subfragments. And the fragment is purified whose sequence needs to be identified from its other end labelled subfragment. Four base specific samples are prepared and the end labelled DNA fragment is divided further and placed in these chemical solutions. Each solution treats a particular base and the bond of that specific base is broken and the base is removed. Electrophoresis is performed for the DNA fragments in the four reaction samples, and by autoradiography, the bands of DNA fragments are revealed according to their length in each individual lane. The sequence is read depending on the density of bands. The dark band in each reaction depicts the base present in position. Maxam–Gilbert method was more popular when compared to Sanger, but was not preferred because of its technical complexity and extensive usage of hazardous radioactive chemicals (Mahboob 2010).

11  Global Scenario of Advance Fungal Research in Crop Protection

327

11.3.3  Second Generation of Sequencing Technologies The first generation sequencing technologies remained prominent for almost three decades, specifically Sanger sequencing. However, cost and time were the major drawbacks that have led to development of second generation sequencing technologies which are based on two approaches, namely sequencing by ligation and sequencing by synthesis. The basic characteristics of the second generation of sequencing are (1) generation of millions of short reads in parallel, (2) speeding up the process of sequencing when compared to first generation, and (3) detection of sequencing output directly without electrophoresis. The second generation sequencing technologies include Roche/454 sequencing, Ion torrent sequencing, Illumina/ Solexa sequencing, and ABI/SOLiD sequencing. Roche/454 sequencing was introduced in the market in the year 2005 and uses pyrosequencing technique which follows sequencing by synthesis method and detects pyrophosphate released after each nucleotide is incorporated in the new synthetic DNA. Each of the randomly fragmented DNA samples is attached to a bead which carries primers carrying oligonucleotides complementary to the DNA fragment. Each fragment is associated with a single bead and each bead is isolated, amplified using PCR producing a million copies of each fragment. The beads are now transferred onto a plate of wells which undergoes a series of reactions producing light at addition of each nucleotide that in turn deduce the sequence of DNA fragments. It has the capability to generate long reads which are easier to map a reference genome (Mardis 2008) Ion torrent semiconductor sequencing technology was bought into market by Life Technologies in the year 2010. It is similar to 454 pyrosequencing, except that it does not use fluorescent labelled nucleotides. It is particularly based on hydrogen ion detection that is released during the process of sequencing. It uses microwell containing chip that has bead with several identical fragments. The change in pH while incorporating each nucleotide with fragment in the pearl is detected by the sensor and converted into a voltage signal that is proportional to the number of nucleotides incorporated. This method holds the capability to produce read of 200–600 base pairs. The major benefit of this technology is longer read length and speed of sequencing. The disadvantage on the other hand is difficulty in interpreting homopolymer sequences that cause indel errors (Rothberg et al. 2011). Illumina/Solexa sequencing by synthesis approach is developed by Solexa which was acquired by Illumina and commercialized the sequencer Illumina/Solexa Genome Analyzer (GA) (Shendure and Ji 2008; Balasubramanian 2015). The DNA samples are fragmented and adapters ligated to either ends. These adapters are fixed to respective complementary adapters, then hooked on a slide with number of variants on a solid plate. Then each sequence attached to the solid plate is amplified by PCR bridge amplification creating several identical copies of sequences that are known as cluster and each cluster contains almost a million copies of the original sequence. Then sequence of nucleotide is determined via sequencing by synthesis approach of Illumina. This approach employs reversible terminators, add primers,

328

V. Yadav et al.

modified nucleotides along with DNA polymerase. The modified nucleotide sequence helps in extending primers by polymerases. Each nucleotide is labelled with a fluorescent so that each one is unique and has one 3′-hydroxyl group assuring addition of a single nucleotide. Clusters are excited by lasers for emitting a signal that is unique for each nucleotide. The signal is then detected by a coupled-charge device (CCD) camera which is in turn translated by certain computer programs. Initially, it produces very short reads of 35 bp and they had the advantage in which they could produce paired end (PE) short reads. The sequence of both ends of each DNA cluster is recorded. However, the latest version is capable of sequencing more than 600 Gbp and short read length is about 125 bp (Reuter et al. 2015; Heo 2015). ABI/SOLiD sequencing is incorporated in market by Life Technologies which was later taken over by Applied Biosystems (ABI) in the year 2007. Supported Oligonucleotide Ligation and Detection (SOLiD) developed sequencing technique following the Sequencing By Ligation (SBL) approach which supports oligonucleotide ligation and detection. This process consists of multiple sequencing rounds which starts by attaching adapters to the DNA fragment, fix on beads, and then clone by PCR emulsion. Then the beads are placed on glass slide consisting of 8-mer with fluorescent label at the end of the fragment and the emitted color is recorded (Alic et al. 2016; Goodwin et al. 2016).

11.3.4  Third Generation of Sequencing Technologies The third generation sequencing technologies run at low cost and are significantly faster when compared to second generation sequencing technologies. The sample preparation is easy without the need of PCR amplification. These advanced methodologies produce long reads in kilobases resolving the assembly problem and repetitive regions of complex genome. The two major approaches in third generation sequencing are Single Molecule Real Time (SMRT) sequencing approach and Oxford Nanopore Technology (ONT) sequencing approach. SMRT was developed by Pacific Biosciences and uses same fluorescent labelling as other technologies, but instead of executing cycles of amplification nucleotide, it detects signals in real time. Pacific biosciences sequencing platforms have a high error rate about 13% dominated by insertions and deletion errors. These errors are randomly distributed along the long read (Kchouk et al. 2017). Oxford Nanopore Technology sequencing (ONT) was developed for determining the order of nucleotides in a DNA. MinION, the device that promised generation of long reads and enhanced resolution of structural genomic variants, was released by Oxford Nanopore Technologies in the year 2014 (Mikheyev and Tin 2014; Laehnemann et al. 2015). It is a small 4 in device that can be connected to a system (Laver et al. 2015). In this technique the initial DNA strand is linked to its complementary strand by a hairpin. A protein nanopore is used to pass the DNA fragment (Heo 2015). With the action of motor protein DNA fragment is translated through the pore generating ionic current variations that are caused by differences in moving

11  Global Scenario of Advance Fungal Research in Crop Protection

329

nucleotides in the pore. The variance is recorded and then interpreted to analyze the sequence. In this the direct strand is sequenced to generate “template read” followed by hairpin and then the inverse strand that generates “complement read,” the resulting consensus sequence is the “two direction read (2D)” (Jain et al. 2016; Lu et al. 2016). Low cost, small sizes are the major advantages of this technique over the rest. Also, the sequenced data is displayed on the screen for the sample loaded which is easy to read and reduces delay. MinION is capable of obtaining very long reads of more than 150 kbps, however, has a pretty high error rate ~12% (Ip et al. 2015). This technology has evolved and another device “PrometION” was released which is a sequencer with 48 individual flow cells and each one with 3000 pores that operates at 500 bp/s. Thus it holds the capability to sequence huge genomes (such as the human genome) (Lu et al. 2016).

11.3.5  Fourth Generation of Sequencing Technologies Nanopore based sequencing is considered as the fourth generation sequencing technology which is also known as single molecule nanopore technology. The significance of the technology can be analyzed by its applications and this technology has a major impact on personalized medicine. It holds the capability to sequence the entire human genome in less than $1000 and at the same time is very quick and reliable. DNA that is the blueprint of life is the molecule that encodes genetic instructions. The other technologies require sample preparation and complex data processing algorithms resulting in low throughput, short read lengths, and high cost. The advantage of this technology over other generations is it is label-free; highthroughput generating ultra-long reads with minimum requirement of materials. This technology originated from Coulter counter and ion channels and the external voltage is applied and the particles that are smaller than pore are passed through. These pores are either made of solid state film or embedded in biological membrane which separates the reservoir with cis and trans compartments consisting of conductive electrolytes. Electrodes are immersed in each chamber and biased voltage is passed which results in electrolyte ions in the solution to pass through the pores electrophoretically resulting in ionic current signal. The pore is blocked by an analyte and the negatively charged cis DNA is added to the chamber blocking the current flowing through the chamber. The properties (physical and chemical) can be statistically calculated by analyzing duration and amplitude of current blockades with these translocation events. Nanopore technology can be broadly classified into two categories: biological nanopore technology and solid state nanopore technology. Biological nanopores are the transmembrane protein channels that are usually inserted in the substrate (bilipid layer, polymer films, or liposomes). The major advantages with biological nanopore are reproducibility, size and structure along with the ability of modifying in combination with molecular biology techniques. The common biological nanopores include α-Hemolysin, MspA (for reading info from 4 nucleotides simultaneously), Bacteriophage phi29, and Oxford Nanopore

330

V. Yadav et al.

Technologies (ONT). α-Hemolysin also known as α-toxin is the most common biological nanopore, and it is an exotoxin secreted by a human pathogenic bacterium Staphylococcus aureus. The inner diameter of α-HL and size of ss-DNA are pretty close in size that aids in identifying the identifying nucleotides using ionic current in the nanopore making it a promising tool for the molecular interaction analyses. The only limitation is its limited pore size restricting it to the analysis of ss DNA or RNA or small molecules or length of β-barrel which is very long to distinguish each nucleotide in long chain DNA. Solid state nanopore are nano-sized holes formed from drilling the opening in a solid substrate (Dekker 2007; Storm et al. 2003). These are specifically used in the study of molecular translocation. Growth in microfabrication technologies has gained more attention towards solid state nanopore. The advantage over biological nanopore is its thermal, chemical, and mechanical stability; along with size adjustability (Cheley et al. 2002; Abiola et al. 2003; Venkatesan et al. 2009), additionally they can even work under various experimental conditions and can be produced in bulk. Over the past few years the method is also applied in multiple fields such as DNA sequencing, protein detection, and disease diagnosis (Traversi et  al. 2013). Some of the major examples of solid state nanopore include: Si3N4 and SiO2 nanopores (widely used a substrate because of their high chemical stability and low mechanical stress) (Kim et al. 2007), Al2O3 membranes (have improved electrical performance, low noise in DNA translocation, and higher signal-to-noise ratio (Feng et  al. 2015), over single layer membranes, hybrid biological/solid state nanopore.

11.3.6  Fifth Generation Sequencing Technologies Fourth generation sequencing technologies suffer with lower accuracy and cannot sequence ultra-short DNA.  An alternative to sequencing-by-synthesis methods, a portable and affordable is offered by nanopore sequencing. There are two approaches—high-fidelity nanopore sequencing of ultra-short DNA targets and cyclomics and ultra-sensitive nanopore sequencing of cell free tumor DNA. Highfidelity nanopore sequencing of ultra-short DNA targets is a nanopore based sequencing strategy that has been reported to overcome the shortcomings in which short target sequences are first circularized and then amplified via rolling-circle amplification to produce long stretches of concatemeric repeats. These are sequenced on the MinION platform and the resulting repeat sequences are aligned in order to obtain highly accurate consensus which reduces the error rate in the individual repeats. For the first time the ability to obtain unbiased and accurate nanopore data for target DNA sequences of