Industrially Important Fungi for Sustainable Development: Volume 1: Biodiversity and Ecological Perspectives (Fungal Biology) 3030675602, 9783030675608

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Fungal Biology

Ahmed M. Abdel-Azeem Ajar Nath Yadav Neelam Yadav Zeba Usmani   Editors

Industrially Important Fungi for Sustainable Development Volume 1: Biodiversity and Ecological Perspectives

Fungal Biology Series Editors Dr. Vijai Kumar Gupta Biorefining and Advanced Materials Research Center Scotland’s Rural College (SRUC), SRUC Barony Campus, Parkgate Dumfries, Scotland United Kingdom 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

Ahmed M. Abdel-Azeem • Ajar Nath Yadav • Neelam Yadav • Zeba Usmani Editors

Industrially Important Fungi for Sustainable Development Volume 1: Biodiversity and Ecological Perspectives

Editors Ahmed M. Abdel-Azeem Botany and Microbiology Department Faculty of Science University of Suez Canal Ismailia, Egypt

Neelam Yadav Gopi Nath P.G. College Veer Bahadur Singh Purvanchal University Ghazipur, Uttar Pradesh, India

Ajar Nath Yadav Department of Biotechnology Dr. Khem Singh Gill Akal College of Agriculture Eternal University Baru Sahib Sirmour Himachal Pradesh, India Zeba Usmani Laboratory of Lignin Biochemistry Department of Chemistry and Biotechnology Tallinn University of Technology Tallinn, Estonia

ISSN 2198-7777 ISSN 2198-7785 (electronic) Fungal Biology ISBN 978-3-030-67560-8 ISBN 978-3-030-67561-5 (eBook) https://doi.org/10.1007/978-3-030-67561-5 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are solely and exclusively licensed 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

Foreword

Mankind is one of the living organisms that need uncountable products for their lifestyle and wellbeing and all those products are manufactured by humans whether they are medicines, foodstuffs, fabrics, or any other. Industries almost produce each and every product, and they have become an important part of our lifestyle without which we cannot imagine. Back when the industrial revolution began, the raw materials to make products used numerous chemicals that were hazardous for the whole planet and caused a lot of problems like pollution, and the depletion of biodiversity of plants and animals. Concerning the planet's health, a lot of chemicals were banned for use, but still there are some chemicals that are still in use. Such conditions were a big reason to worry; so scientists have discovered the use of microbes including bacteria, fungi, algae, and archaea for the production of various products including medicines, food, dyes, and many others. Among the microbes, fungi have received considerable attention in the formation of industrial products. Diverse ranges of industrially important fungi such as arbuscular mycorrhizal fungi, Aspergillus, Chaetomium, Cordyceps, Epicoccum, Fusarium, Ganoderma, Penicillium, Piriformospora, Saccharomyces Trichoderma, and Truffles are being used in the industries for various purposes. This volume of this book clearly describes the emerging taxonomical, biodiversity and ecological perspective of industrially important fungal communities from diverse habitats. In this regard, the editors and the authors have made an outstanding contribution in collecting and compiling past and current data on the role of fungal communities in each possible perspective with a major emphasis on industrial applications.

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I recommend this book to researchers and students working in the emerging and fascinating field of mycology. The book will advance the knowledge to a greater extent in these areas with significant broader research on fungal communities. The editors of this book deserve credit for such a splendid and innovative contribution of mycological research. Dr. Davinder Singh Vice Chancellor Eternal University Baru Sahib, Himachal Pradesh, India

Second Foreword

Fungi are a highly diverse clade of eukaryotes found in almost all ecological niches. Fungi have been used by mankind ever since the beginning of human civilization. The Sumerians and Egyptians domesticated Saccharomyces cerevisiae for brewing beer. However, it was not until around the end of the nineteenth century that scientists began to recognize and explore the interesting biology of fungal communities. Arbuscular mycorrhiza fungi (AMF) have been known to inhabit almost all major ecosystems worldwide ranging from arctic regions to tropical forests, from the deserts in the Arabic peninsula to the high Himalayans. AMF promotes many aspects of plant life, particularly improved nutrition, stress tolerance, and disease resistance. Another genus Aspergillus is cosmopolitan and prevalent in a wide range of environmental and climatic zones. Diverse species of Aspergillus have been extensively used in the production of foods, drinks, organic acids, and enzymes. The broad significance and economic importance of the Aspergillus have pushed it to the forefront of fungal research, with one of the largest academic and industrial research communities dedicated to this genus. Diverse species of Fusarium find applications in a broad range of fields such as biofuels, cosmetics, food, and pharmacy. The economic and historical perspective of Fusarium makes it the center of focus for future discussions about nomenclature and mycological diversity. The genus Penicillium is one of the most versatile mycofactories, comprising species with plant growth-promoting potential, biosurfactants, and bioemulsifier producers with advantages of low toxicity, biodegradability, and biocompatibility over chemically synthesized surfactants. Additionally, the ability of diverse species of this genus to produce enzymes makes them apt communities for microbiological break down of organic materials. Piriformospora indica, a root-colonizing endophytic fungus, possesses many fascinating features such as it allows plants to survive under stress vii

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conditions, and imparts resistance to toxins, heavy metals, and pathogenic organisms. Due to its inimitable characteristics, the fungus is being exploited for biotechnological applications in the area of agriculture, forestry, and flori-horticulture. This volume undoubtedly describes the biodiversity of fungal communities and their ecological perspective, the marvelous role these communities play in the biosphere, and how their interactions are significant drivers of many ecosystem functions. The book has taken into consideration the wonderful role of fungal communities in the industrial sector and environmental cleaning. The book also provides information about how utilizing fungal processes and products can help in achieving sustainability through more effectual use of natural resources. The significance of fungal interactions in environmental science, medicine, and biotechnology to a great extent has led to the emergence of a dynamic and multidisciplinary research field. This volume on Industrially Important Fungi for Sustainable Development, Volume 1: Biodiversity and Ecological Perspective is a very timely publication, which provides state-of-the-art information in the area of mycology, broadly involving fungi and fungal-based products for sustainable developments in the industry. The book comprises 17 chapters. The first chapter by Abdel-Azeem et al. describes the biodiversity and ecological perspective of industrially important fungi, whereas Singh et al. highlight biodiversity, the interaction of arbuscular mycorrhizal fungi (AMF) with plants, and their potential applications for sustainable agriculture in Chap. 2. Chapter 3 by Mohamed et al. describes Aspergillus from different habitats and their industrial applications. Chapter 4 by Leonardi et al. highlights the biodiversity, ecological significances, and biotechnological applications of genus Truffles. Abdel-Azeem et al. describe biodiversity and industrial applications of genus Chaetomium in Chap. 5. In Chap. 6, Nouh et al. have given the details of the diversity of Cordyceps from different environmental agroecosystems and potential applications. Rabab Majead Abed highlights the fungal biodiversity of the genus Epicoccum and their biotechnological potential in Chap. 7. In Chap. 8, Samiksha and Kumar describe the molecular taxonomy, diversity, and potential applications of genus fusarium. Gryzenhout et al. highlights the potential applications and biodiversity of genus Ganoderma in Chap. 9. Guillermo Fernandez-Bunster highlights diversity, phylogenetic profiling of genus Penicillium, and their potential applications in Chap. 10. Biodiversity, ecological significances and biotechnological applications of Piriformospora indica for agriculture and allied sectors have been described by Jha and Yadav in Chap. 11. Chapter 12 by Leo et al. describes Saccharomyces and their potential applications in food and food-processing industries. Adel Kamel Madbouly highlights the biodiversity of the genus Trichoderma and their potential applications in Chap. 13. Usmani et al. discuss the role of fungi in bioremediation of soil contaminated with persistent organic compounds in Chap. 14. Fungal biopesticides for agro-environmental sustainability is discussed by Waghunde et al. in Chap. 15. Refaey et al. describe the role of fungi in bioremediation of soil contaminated with heavy metals in Chap. 16. Finally, the conclusion and future prospects of biodiversity and biotechnological applications of industrially important fungi have been described by the editor and co-authors in the last chapter.

Second Foreword

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Overall, great efforts have been carried out by the editorial team, and scientists from different countries to compile this book as a highly unique and up-to-date source on Industrially Important Fungi for Sustainable Development, Volume 1: Biodiversity and Ecological Perspective for the students, researchers, scientists, and academicians. I hope readers will find this book highly useful and interesting in their educational pursuit in mycology. Amrik Singh Ahluwalia Pro-Vice Chancellor Eternal University Baru Sahib, Himachal Pradesh, India

Preface

Fungi are an understudied, biotechnologically valuable group of organisms. Due to the immense range of habitats that fungi inhabit, and the consequent need to compete against a diverse array of other fungi, bacteria, and animals, fungi have developed numerous survival mechanisms. However, besides their major basic positive role in the cycling of minerals, organic matter, and mobilizing insoluble nutrients, fungi have also other beneficial impacts. They are considered good sources of food and active agents for a number of industrial processes involving fermentation mechanisms as in the bread, wine, and beer industry. A number of fungi also produce biologically important metabolites such as enzymes, vitamins, antibiotics, and several products of important pharmaceutical use; still, others are involved in the production of single-cell proteins. The economic value of these marked positive activities has been estimated as approximating to trillions of US dollars. With regard to the edible fungi, P. Kirk had underlined that China presently exports these products to an estimate annual value of US$3.8 billion while its internal production of the same has reached a level of 268.3 billion Chinese Yuan ¥. The unique attributes of fungi thus herald great promise for their application in biotechnology and industry. Since ancient Egyptians mentioned in their medical prescriptions how they can use green molds in curing wounds as the obvious historical uses of penicillin, fungi can be grown with relative ease, making production at scale viable. The search for fungal biodiversity and the construction of a living fungi collection both have incredible economic potential in locating organisms with novel industrial uses that will lead to novel products. Fungi have provided the world with penicillin, lovastatin, and other globally significant medicines, and they remain an untapped resource with enormous industrial potential. The aim of this book volume Industrially Important Fungi for Sustainable Development, Volume 1: Biodiversity and Ecological Perspective is to provide understanding of fungal diversity from diverse habitats and their industrial application for future sustainability. The proposed book encompasses current advanced knowledge of fungal communities and their potential biotechnological applications

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in industry and allied sectors. The book will be useful to scientists, researchers and students related to microbiology, biotechnology, agriculture, molecular biology, environmental biology, and related subjects. Ismailia, Egypt Himachal Pradesh, India Uttar Pradesh, India Tallinn, Estonia

Ahmed M. Abdel-Azeem Ajar Nath Yadav Neelam Yadav Zeba Usmani

Contents

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Biodiversity and Ecological Perspective of Industrially Important Fungi: An Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Ahmed M. Abdel-Azeem, Hebatallah H. Abo Nahas, Mohamed A. Abdel-Azeem, Faiza Javaid Tariq, and Ajar Nath Yadav Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants, and Potential Applications . . . . . . . . . . . . . . . . . . . . . . Uma Singh, Ovaid Akhtar, Rani Mishra, Ifra Zoomi, Harbans Kaur Kehri, and Dheeraj Pandey Aspergillus from Different Habitats and Their Industrial Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Akram H. Mohamed, Bassem A. Balbool, and Ahmed M. Abdel-Azeem

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Truffles: Biodiversity, Ecological Significances, and Biotechnological Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107 Marco Leonardi, Mirco Iotti, Giovanni Pacioni, Ian R. Hall, and Alessandra Zambonelli

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Biodiversity and Industrial Applications of Genus Chaetomium . . . 147 Ahmed M. Abdel-Azeem, Abdelghafar M. Abu-Elsaoud, Hebatallah H. Abo Nahas, Mohamed A. Abdel-Azeem, Bassem A. Balbool, Mariam K. Mousa, Nehal H. Ali, and Amira M. G. Darwish

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Diversity of Cordyceps from Different Environmental Agroecosystems and Potential Applications . . . . . . . . . . . . . . . . . . . 207 Fatma A. Abo Nouh, Sara A. Gezaf, Hebatallah H. Abo Nahas, Yousef H. Abo Nahas, Celia Vargas-De-La-Cruz, Richard Andi Solorzano Acosta, and Ahmed M. Abdel-Azeem

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Exploring Fungal Biodiversity of Genus Epicoccum and Their Biotechnological Potential . . . . . . . . . . . . . . . . . . . . . . . . . . . 237 Rabab Majead Abed

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Molecular Taxonomy, Diversity, and Potential Applications of Genus Fusarium . . . . . . . . . . . . . . . . . . . . . . . . . . . 277 Samiksha and Sanjeev Kumar

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Ganoderma: Diversity, Ecological Significances, and Potential Applications in Industry and Allied Sectors . . . . . . . . . . . 295 Marieka Gryzenhout, Soumya Ghosh, James Michel Tchotet Tchoumi, Marcele Vermeulen, and Tonjock Rosemary Kinge

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Diversity, Phylogenetic Profiling of Genus Penicillium, and Their Potential Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . 335 Guillermo Fernandez-Bunster

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Piriformospora indica: Biodiversity, Ecological Significances, and Biotechnological Applications for Agriculture and Allied Sectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363 Yachana Jha and Ajar Nath Yadav

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Saccharomyces and Their Potential Applications in Food and Food Processing Industries . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393 Vincent Vineeth Leo, Vinod Viswanath, Purbajyoti Deka, Zothanpuia, Dwivedi Rohini Ramji, Lallawmsangi Pachuau, William Carrie, Yogesh Malvi, Garima Singh, and Bhim Pratap Singh

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Biodiversity of Genus Trichoderma and Their Potential Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429 Adel Kamel Madbouly

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Role of Fungi in Bioremediation of Soil Contaminated with Persistent Organic Compounds . . . . . . . . . . . . . . . . . . . . . . . . 461 Zeba Usmani, Minaxi Sharma, Tiit Lukk, and Vijai Kumar Gupta

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Fungal Biopesticides for Agro-Environmental Sustainability . . . . . . 479 Rajesh Ramdas Waghunde, Chandrashekhar U. Shinde, Puja Pandey, and Chandrakant Singh

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Role of Fungi in Bioremediation of Soil Contaminated with Heavy Metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 509 Maha Refaey, Ahmed M. Abdel-Azeem, Hebatallah H. Abo Nahas, Mohamed A. Abdel-Azeem, and Abeer A. El-Saharty

Contents

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Biodiversity and Biotechnological Applications of Industrially Important Fungi: Current Research and Future Prospects . . . . . . . 541 Ajar Nath Yadav, Tanvir Kaur, Rubee Devi, Divjot Kour, Ashok Yadav, Murat Dikilitas, Zeba Usmani, Neelam Yadav, Ahmed M. Abdel-Azeem, and Amrik Singh Ahluwalia

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573

Contributors

Ahmed M. Abdel-Azeem Botany and Microbiology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt Mohamed A. Abdel-Azeem Pharmacognosy Department, Faculty of Pharmacy and Pharmaceutical Industries, University of Sinai, El Arish, North Sinai, Egypt Rabab Majead Abed Department of Biology, Faculty of Education and Pure Science, University of Diyala, Baquba, Diyala, Iraq Hebatallah H. Abo Nahas Zoology Department, Faculty of Science, Suez Canal University, Ismailia, Egypt Yousef H. Abo Nahas Microbiology Department, Faculty of Medicine, Helwan University, Cairo, Egypt Fatma A. Abo Nouh Botany and Microbiology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt Abdelghafar M. Abu-Elsaoud Botany and Microbiology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt Richard Andi Solorzano Acosta Laboratory of Microbial Ecology and Biotechnology, Department of Biology, Faculty of Sciences, National Agrarian University La Molina (UNALM), Lima, Peru Faculty of Pharmacy and Biochemistry, Norbert Wiener Private University, Lima, Peru Amrik Singh Ahluwalia Department of Botany, Akal College of Basic Sciences, Eternal University, Baru Sahib, Sirmour, Himachal Pradesh, India Ovaid Akhtar Department of Botany, Kamla Nehru Institute of Physical and Social Sciences, Sultanpur, India Nehal H. Ali Zoology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt xvii

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Bassem A. Balbool Faculty of Biotechnology, October University for Modern Sciences and Arts, 6th October City, Egypt William Carrie Department of Biotechnology, Mizoram University, Aizawl, Mizoram, India Amira M. G. Darwish Food Technology Department, Arid Lands Cultivation Research Institute, City of Scientific Research and Technological Applications, Alexandria, Egypt Purbajyoti Deka Department of Biotechnology, Mizoram University, Aizawl, Mizoram, India Rubee Devi Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Sirmour, Himachal Pradesh, India Murat Dikilitas Department of Plant Protection, Faculty of Agriculture, Harran University, S. Urfa, Turkey Abeer A. El-Saharty National Institute of Oceanography and Fisheries, Alexandria, Egypt Guillermo Fernandez-Bunster School of Medical Technology, Universidad de Valparaíso, Camino la Troya S/N & El Convento, Circunvalación Ote., San Felipe, Valparaíso, San Felipe, Chile Sara A. Gezaf Botany and Microbiology Department, Faculty of Science, Arish University, North Sinai, Egypt Soumya Ghosh Department of Genetics, Faculty of Natural and Agricultural Sciences, University of the Free State, Bloemfontein, South Africa Marieka Gryzenhout Department of Genetics, Faculty of Natural and Agricultural Sciences, University of the Free State, Bloemfontein, South Africa Vijai Kumar Gupta Biorefining and Advanced Materials Research Center, Scotland’s Rural College (SRUC), Edinburgh, UK Ian R. Hall Truffles and Mushrooms (Consulting) Ltd., Dunedin, New Zealand Mirco Iotti Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy Yachana Jha N.V. Patel College of Pure and Applied Sciences, S.P. University, Anand, Gujarat, India Tanvir Kaur Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Sirmour, Himachal Pradesh, India Harbans Kaur Kehri Sadasivan Mycopathology Laboratory, Department of Botany, University of Allahabad, Allahabad, India

Contributors

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Tonjock Rosemary Kinge Department of Biological Sciences, Faculty of Science, The University of Bamenda, Bamenda, Cameroon Divjot Kour Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Sirmour, Himachal Pradesh, India Sanjeev Kumar Department of Genetics and Plant Breeding, School of Agriculture, Lovely Professional University, Jalandhar, India Vincent Vineeth Leo Department of Biotechnology, Mizoram University, Aizawl, Mizoram, India Marco Leonardi Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy Tiit Lukk Laboratory of Lignin Biochemistry, Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia Adel Kamel Madbouly Microbiology Department, Faculty of Science, University of Ain Shams, Cairo, Egypt Yogesh Malvi Department of Biotechnology, Mizoram University, Aizawl, Mizoram, India Rani Mishra Department of Botany, Rashtriya Kisan Post Graduate College, Shamli, India Akram H. Mohamed Microbial Genetic Resources Department, National Gene Bank, Agriculture Research Center, Giza, Egypt Mariam K. Mousa Botany and Microbiology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt Lallawmsangi Pachuau Department of Biotechnology, Mizoram University, Aizawl, Mizoram, India Giovanni Pacioni Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy Puja Pandey Department of Plant Pathology, B. A. College of Agriculture, Anand Agricultural University, Anand, Gujarat, India Dheeraj Pandey Sadasivan Mycopathology Laboratory, Department of Botany, University of Allahabad, Allahabad, India Dwivedi Rohini Ramji Department of Biotechnology, Mizoram University, Aizawl, India Maha M. Refaey Botany and Microbiology Department, Faculty of Science, Suez Canal University, Ismailia, Egypt Samiksha Department of Biotechnology, School of Biosciences, Lovely Professional University, Jalandhar, India

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Minaxi Sharma Department of Food Technology, Akal College of Agriculture, Eternal University, Baru Sahib, Himachal Pradesh, India Chandrashekhar U. Shinde Department of Entomology, N. M. College of Agriculture, Navsari Agricultural University, Navsari, Gujarat, India Garima Singh Department of Botany, Pachhunga University College, Aizawl, Mizoram, India Bhim Pratap Singh Department of Agriculture and Environmental Sciences (AES), National Institute of Food Technology Entrepreneurship & Management (NIFTEM), Sonepat, Haryana, India Chandrakant Singh Wheat Research Station, Junagadh Agricultural University, Junagadh, Gujarat, India Uma Singh Sadasivan Mycopathology Laboratory, Department of Botany, University of Allahabad, Allahabad, India Faiza Javaid Tariq Department of Microbiology, University of Health Sciences, Lahore, Pakistan James Michel Tchotet Tchoumi Institute for Agricultural Research for Development (IRAD), Yaoundé, Cameroon Zeba Usmani Laboratory of Lignin Biochemistry, Department of Chemistry and Biotechnology, Tallinn University of Technology, Tallinn, Estonia Celia Vargas-De-La-Cruz Faculty of Pharmacy and Biochemistry, Academic Department of Pharmacology, Bromatology and Toxicology, Latin American Center for Teaching and Research in Food Bacteriology (CLEIBA), Research Group Biotechnology and Omics in Life Sciences, Universidad Nacional Mayor de San Marcos, Lima, Peru Marcele Vermeulen Biogrip, Geology Department, Faculty of Natural and Agricultural Sciences, University of the Free State, Bloemfontein, South Africa Vinod Viswanath Department of Dairy Microbiology, College of Dairy Science & Technology, Kerala Veterinary and Animal Science University, Thrissur, Kerala, India Rajesh Ramdas Waghunde Department of Plant Pathology, College of Agriculture, Navsari Agricultural University, Bharuch, Gujarat, India Ajar Nath Yadav Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Sirmour, Himachal Pradesh, India Ashok Yadav Department of Botany, Institute of Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India

Contributors

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Neelam Yadav Gopi Nath P.G. College, Veer Bahadur Singh Purvanchal University, Ghazipur, Uttar Pradesh, India Alessandra Zambonelli Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy Ifra Zoomi Sadasivan Mycopathology Laboratory, Department of Botany, University of Allahabad, Allahabad, India Zothanpuia Department of Biotechnology, Mizoram University (a Central University), Pachhunga University College, Aizawl, Mizoram, India

About the Editors

Ahmed M. Abdel-Azeem is currently working as an academic staff member for the Botany Department, Faculty of Science, Suez Canal University, and as a mycologist with a particular interest in the ecology, taxonomy, biology, and conservation of fungi, especially on the members of the phylum Ascomycota. His research includes isolation, identification, and taxonomic assessments of these fungi with particular emphasis on those which produce bioactive materials from different ecological habitats. Most recently, his interests are on the effects of climate change on fungi. This in turn has led him to become involved in fungal conservation. He is a member of the IUCN Species Survival Commission Specialist Group for Cup Fungi, Truffles, and their Allies and also the founder of the Arab Society for Fungal Conservation. In 2014 and 2016, he proposed a good candidate for the celebration of Egypt’s National Fungus Day on 20 February. He, with the help of international societies, agencies, and mycologists, decreed Egypt’s National Fungus Day in Bibliotheca Alexandrina on 20 February 2016 for the first time. He has received various grants, fellowships, and national and international projects, e.g., EOL Fellowship in 2011, Mohamed bin Zayed Species Conservation Fund in 2014 and 2018, and National Geographic Society Fund in 2016. In 2018, he was elected to be a member of the Executive Committee of the International Mycological Association (IMA) for the next 4 years. He is the founder of Pan Arab Mycologists (PAM). He was hired for his experience in taxonomy, ecology, biology, and conservation of fungi to study the fungi in ancient air of unveiled Cheops Solar Boat Project and fungi that degraded ancient wood in Abydos Middle Cemetery Project. He studied the biodiversity of macrofungi in Romania, the UK, the USA, Finland, Sweden, Italy, Greece, Puerto Rico, Malta, and Poland. He is the editor in chief of Microbial

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Biosystems Journal (MBJ) and a reviewer of more than seven international journals. He has published more than 70 research paper journals, 27 book chapters in the books published by international publishers, and 5 books.

Ajar Nath Yadav is a Dean of Postgraduate Studies (Officiating) and Assistant Controller of Examinations at Eternal University, Baru Sahib, Himachal Pradesh, India. He has 5 years of teaching experience as an Assistant Professor (Senior Scale) at the UG, PG, and PhD level courses related to microbiology and microbial biotechnology at the Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University. He has 11 years of research experiences in the field of Microbial Biotechnology, Microbial Diversity, and Plant–Microbe Interactions. Dr. Yadav obtained a doctorate in Microbial Biotechnology, jointly from ICAR-Indian Agricultural Research Institute (IARI), New Delhi and Birla Institute of Technology, Mesra, Ranchi, India; MSc (Biotechnology) from Bundelkhand University and BSc (CBZ) from the University of Allahabad (A Central University), India. Dr. Yadav has 201 publications, with ah-index of 50, i10-index of 132, and 6554 citations (Google Scholar on 11/11/2020). Dr. Yadav is editor of 15 Springer-Nature, 06 CRC Press Taylor & Francis, 02 Elsevier, and 1 Wiley-Blackwell book. To his credit, he has one granted patent “Insecticidal formulation of novel strain of Bacillus thuringiensis AK 47.” Dr. Yadav has got 12 Best Paper Presentation Awards and 01 Young Scientist Award (NASISwarna Jayanti Purskar). Dr. Yadav received the “Outstanding Teacher Award” in 6th Annual Convocation 2018 by Eternal University, Baru Sahib, Himachal Pradesh. Dr. Yadav is currently handling two projects one funded by the Department of Environment, Science & Technology (DEST), Shimla and one by HP Council for Science, Technology & Environment (HIMCOSTE). Dr. Yadav has guided 01 PhD and 01 MSc Scholar and presently he is guiding 04 scholars for PhD and one MSc degree. He has to his credit ~6700 microbes (Archaea, bacteria, and fungi) isolated from diverse sources and ~550 potential and efficient microbes deposited at culture collection ICAR-National Bureau of Agriculturally Important Microorganisms (NBAIM), Mau, Uttar Pradesh, India. He has deposited 2423 nucleotide sequences and 03 whole-genome sequences (Bacillus thuringiensis AKS47, Arthrobacter agilis L77 and Halolamina pelagica CDK2) and 02 transcriptomes to NCBI GenBank databases: in the public domain. The niche-specific microbes from extreme environments were reported as specific bio-inoculants (Biofertilizers) for crops growing in normal and diverse abiotic stress conditions. Dr. Yadav and group have developed a technology for screening of archaea for phosphorus solubilization for the first time. He has been serving as an editor/editorial board member and reviewer for different national and international peer-reviewed journals. He has lifetime membership of the Association of Microbiologists in India, and Indian Science Congress Council, India. Please visit https://sites.google.com/site/ajarbiotech/ for more details.

About the Editors

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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 a research interest in the area of beneficial microbiomes and their biotechnological application in agriculture, medicine environment, and allied sectors. To her credit, she has 65 publications in different reputed international, national journals, and publishers with h-index 24, i10-index 46, and 1724 citations (Google Scholar on 11/11/2020). She is the editors of 02 books in Elsevier, 03 in CRC Press, Taylor & Francis, and 09 in Springer Nature. She has published 19 research communications in different conferences/symposiums/workshops. She got the 02 best paper presentations Award and 02 certificates of excellence in reviewing Award. She has to her credit >1700 microbes (Archaea, bacteria, and fungi) isolated from diverse sources and >115 potential and efficient microbes deposited at culture collection. She has deposited 295 nucleotide sequences to NCBI GenBank databases: in the public domain. She is Editor/ associate editor/reviewer of different international and national journals including Plos One, Extremophiles, Annals of Microbiology, Journal of Basic Microbiology, and Advance in Microbiology and Biotechnology. She has the lifetime membership of the Association of Microbiologists in India, Indian Science Congress Council, India, and National Academy of Sciences, India. Please visit https://sites.google. com/site/neelamanyadav/ for more details.

Zeba Usmani is currently working as a Research Scientist in the Department of Chemistry and Biotechnology at Tallinn University of Technology (TalTech). Her research focus lies at the intersection of environmental chemistry and microbiology, wherein she brings forth a diverse understanding of developing novel green methodologies for sustainable degradation of organic and inorganic chemicals. She brings in experience in analytical chemistry, microbial ecology, and marine ecology. Under the SUSFOOD 2 grant, she has worked on culturing of microbes and microbial and enzymatic degradation of organic chemicals and surfactants at a laboratory scale in order to ensure their sustainability. She completed her doctorate at Indian Institute of Technology (IIT-ISM), Dhanbad, India. Her research focus from doctorate include bio-based remediation of heavy metals from fly-ash for conversion into useful fertilizer, and uptake of heavy metals into terrestrial and aquatic ecosystems. She has 7 years of experience in the field of microbial biotechnology and

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About the Editors

environmental microbiology. To her credit, she has published many papers in peerreviewed journals with impact factors, a few good book chapters for publication houses of Elsevier and Springer, and a monolog for the Ministry of Environment and Forests. She was awarded the best poster presentation at the 4th International Conference on Natural Products Utilization, Bulgaria (2019). She has attended various other International Conferences in Estonia, Greece, and India. She is also a reviewer for multiple research paper across multiple journals PLOS One, MDPI journals, Water and Environment Journal, Environmental science and Pollution Research, Environmental Geochemistry, and Health and Scientific Reports. She is also the editor of some International journals: Microbial Biosystems and EUREKA: Life Sciences, Estonia. She has 5 upcoming books in the current year with reputed publishing houses of Elsevier and Springer. Her RG Score is 22.78 with 23 peerreviewed articles in well-reputed journals and 7 book chapters. She is a member of the Society for Bioinformatics and Biological Sciences (SBBS) and has been nominated for its Young Scientist Award 2020.

Chapter 1

Biodiversity and Ecological Perspective of Industrially Important Fungi An Introduction Ahmed M. Abdel-Azeem, Hebatallah H. Abo Nahas, Mohamed A. Abdel-Azeem, Faiza Javaid Tariq, and Ajar Nath Yadav

Contents 1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Fungal Enzymes and Their Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.1 Cellulases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.2 Xylanases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.3 Amylases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.4 Pectinase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.5 Lipases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.6 Laccases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.7 Proteases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.8 Chitinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.9 Tyrosinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.10 Phosphatases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.11 Antioxidant Compounds from Endophytic Chaetomium . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 4 4 7 10 12 13 16 18 20 21 22 23 24 25

A. M. Abdel-Azeem (*) Botany and Microbiology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt e-mail: [email protected] H. H. Abo Nahas Zoology Department, Faculty of Science, University of Suez Canal, Ismailia, Egypt M. A. Abdel-Azeem Pharmacognosy Department, Faculty of Pharmacy and Pharmaceutical Industries, University of Sinai, El Arish, North Sinai, Egypt F. J. Tariq Department of Microbiology, University of Health Sciences, Lahore, Pakistan A. N. Yadav Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Sirmour, Himachal Pradesh, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. M. Abdel-Azeem et al. (eds.), Industrially Important Fungi for Sustainable Development, Fungal Biology, https://doi.org/10.1007/978-3-030-67561-5_1

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1.1

A. M. Abdel-Azeem et al.

Introduction

Fungi are biologically and ecologically diverse. Biologically, they are heterotrophs obtaining their nutrients by absorption from external sources through three main strategies: saprobic, parasitic, and mutualistic. Saprobic forms have access to their energy via the enzymatic breakdown of organic materials such as sugars, cellulose, lignin, chitin, and keratin. The parasitic forms acquire the same directly from their living hosts whether plants or animals; the latter are ultimately destroyed or killed. The saprobic and parasitic forms are also often divided into biotrophs and necrotrophs (and more recently, as hemibiotrophs) according to their lifestyles. The former derive their energy from living cells and are found on or in living plants; they can have very complex nutrient requirements but they do not kill their host cells rapidly (Prasad et al. 2021). The latter derive their energy from dead cells; they invade and kill the host living tissue rapidly and then live saprobically on its remains. Finally, the hemibiotrophs have an initial period of biotrophy followed by a phase of necrotrophy (Moore et al. 2011). Ecologically, fungi are able to thrive in a wide range of ecosystems and habitats. They occur in aquatic and terrestrial environments and can grow on rocks as well as on many other surfaces (Mouchacca 1995). Most fungi prefer however moderate environmental conditions. Nonetheless some species are able to develop under stress conditions of extreme habitats induced by severe dryness and salinity and at low or high temperatures (Mouchacca 1997; Devi et al. 2020b). All aspects of human affairs are affected by fungi, either negatively or positively. The detrimental and beneficial activities of these microorganisms are marked. They are destructive to agriculture causing very serious plant diseases; they are also troublesome as they deteriorate foodstuffs, timber, textiles, seeds, and grains, as well as many other stored or manufactured materials (Fig. 1.1). Finally, they are also harmful to humans and animals by inducing superficial and deep mycotic infections. However, besides their major basic positive role in the recycling of minerals and organic matter and mobilizing of insoluble nutrients, fungi also have their proper beneficial impacts. They are considered as good sources of food and as active agents for a number of industrial processes involving fermentation mechanisms as in the bread, wine, and beer industry. A number of fungi also produce biologically important metabolites such as enzymes, vitamins, antibiotics, and several products of important pharmaceutical use; still others are involved in the production of singlecell proteins (Kour et al. 2019c; Rastegari et al. 2019a, b; Yadav et al. 2018). Fungi ubiquitous in distribution are extremely successful in survival due to their high plasticity and physiological versatility in secreting a wide range of enzymes involved in the degradation of complex polymers that allow them to use many biomass components as energy and carbon sources (Devi et al. 2020a; Yadav et al. 2019a, 2021). Fungi survive well in biologically intense, unfavorable environments because of their powerful enzyme systems. Production of extracellular enzymes is one of the varied mechanisms of fungi in adaptability, survival, and utilization of their ecological niche conditions (Gopinath et al. 2005). The ability to secrete

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

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Fig. 1.1 Diagram showing the potential use of fungi in biotechnology. Adapted from Hyde et al. (2019)

extracellular protein makes filamentous fungi attractive hosts for the production of proteins having immense value in agriculture, paper, pulp, and pharmaceutical industries (Carlsen and Nielsen 2001). Lignocellulose is the major structural component of plants and represents a major source of renewable organic matter (Howard et al. 2003). Besides being conspicuous producers of secondary metabolites that have potential as antibiotic, anticancer, antioxidant, and anti-parasitic compounds, used in the pharmaceutical industries, endophytic fungi are also reservoirs of a battery of enzymes (Rana et al. 2019a, b). Different types of extracellular enzymes secreted by fungi, especially endophytic fungi, have applications in food, textile, leather, confectionery, agriculture, beverage, nutrient translocations, and human health sectors (Abdel-Azeem et al. 2016a, b,

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2018, 2019; Mishra et al. 2017; Abd-ElGawad et al. 2020; Rana et al. 2019c). Furthermore, around 60% of enzymes exploited in industries are a product of fungal origin (Suryanarayanan et al. 2012). Fungal endophytes are one of the most favored candidates in enzyme production. In spite of these facts, their exploitation in enzyme production for biotech, pharmaceutical, and food industries or in human welfare is sparse (Uzma et al. 2018; Mishra et al. 2016). Endophytic fungi in conjunction with the hosts secrete proteins that are posibbly presumed to help in defense development and nutrition. Soluble sugar supply also contributes to the growth of fungal endophytes. As a result, cellulose and lignin production represents a strategic benefit for tissue decomposition (Oses et al. 2006; Yadav 2020). At present, endophytic fungi have a leading edge in the manufacture of industrially purposive enzymes like amylases, cellulases, chitinases, lipases, and proteases. The benefits of enzymes over chemical catalysts make them superior candidates for commercial and pharmaceutical uses as they function under comparatively moderate conditions of pH, temperature, and pressure, often stereoselective and specific (Tiwari 2015; Sharma et al. 2021). Extracellular hydrolases, such as cellulases, pectinases, lipases, and xylanases, produced by endophytic fungi equip the hosts with resistance mechanisms against pathogenic infiltration (Mhatre et al. 2017; Kour et al. 2019a). From biotechnological point of view, there are few relevant enzymes that are discussed further in the next sections. This chapter focuses on the current biotechnical applications of filamentous fungi and their related industrial processes and concludes with future prospects of the mycological biotechnology.

1.2 1.2.1

Fungal Enzymes and Their Applications Cellulases

Cellulose is considered one of the most abundant renewable polymers composed of β-1,4-linked glucose molecules. Cellulolytic microbiota produces a complex array of glycosyl hydrolases during the growth of cellulosic substrates. Endoglucanases and cellobiohydrolases, also called cellulases, are responsible for hydrolysis of cellulose. Hydrolysis of hemicellulose, a mixed polymer, occurs via the action of xylanases, mannanases, and other hydrolytic enzymes with broad substrate specificity. Cellulases possess a complex enzyme system comprising endo-1,4-β-D-glucanase, exo1,4-β-glucanase, and exo-1,4-D-glucosidase. These enzymes together with hemicellulases and pectinases are employed in the processing of lignocellulosic materials (Nigam and Singh 1995; Singh and Yadav 2020).

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

1.2.1.1

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Textiles

Some textile industries, e.g., stone washing of jeans, depend upon cellulases which give faded look to the jeans. Cellulases are used in the place of pumice stone, in a process known as biostoning that breaks minute fibrillar ends on the yarn surface. Stoning process involves more fiber damage and less machine productivity, is more work intensive, and is not environment friendly. These drawbacks are overcome by biostoning process.

1.2.1.2

Food Industry

Cellulases have comprehensive applications in food biotechnology too. Enriched methods of clarification, extraction, and stabilization are needed for vegetable and fruit juice production, in macerating enzyme complexes (xylanases, cellulases, and pectinases) to elevate the yield of juices; in enhancing properties such as flavor, texture, and aroma of vegetables and fruits; and in diminishing bitterness by infusion of enzymes such as β-glucosidases and pectinases.

1.2.1.3

Pulp and Paper

The process of mechanical pulping such as grinding and refining of the raw wood material leads to pulps containing high fibers, bulk, and stiffness. During biomechanical pulping, employing of cellulases has derived significant energy savings of 20–40% during grinding, improving, and refining of the raw wood material. Cellulases only, or in combination with xylanases, are profitable in the process of deinking waste papers. Various applications intended until now in exploiting cellulases are for the extraction of ink from the surface of fiber by limited hydrolysis of carbohydrate molecule.

1.2.1.4

Detergent Industry

Employment of cellulases conjointly with lipases and proteases in the manufacturing of detergents has been a contemporary introduction in the industry. The alkaline cellulases find their use as a detergent additive as an industrial practice is duly trailed as an aspect of selective cellulose contact within the fibers and dig out dirt from the interfibrillary spaces.

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Wine and Brewery Industry

Enzymes such as glucanases, pectinases, and hemicellulases play a determining aspect in wine formulation by correcting color, maceration of skin, filtration, and clarification and conclusively wine peculiarity and stability. Aromaticity of wines can be enhanced by β-glucosidases as they remodel glycosylated precursors. The assistance of using such enzymes in the course of wine preparation comprises reformed quality, finer maceration, apparent clarification, improved color extraction, elementary filtration, and improved stability.

1.2.1.6

Cellulases from Endophytic Fungi and Applications

One hundred and forty-nine taxa were recovered from 7 plant stems by Peng and Chen (2007). Out of the 149 fungal species, about 48.9% showed the presence of intercellular lipid bodies when observed under a microscope, of which 26 endophytic fungal strains represented larger lipid bodies. These strains were selected and grown on potato dextrose broth, which enhances the taste to accumulate 21.3–35% of lipid content of dry cell weight. When solid-state fermentation was carried out, these isolates were found positive for cellulase production and microbial oil with the yields of 0.31–0.69 filter paper unit as well as 19–42 mg/g initial dry substrate, respectively. Thus, the above results indicate that some endophytic fungal isolates associated with the oleaginous host plants possess the attributes of oil accumulation and cellulase production simultaneously. 1,4-β-D endoglucanase, 1,4-β-D cellobiohydrolase, and β-D glucosidase are the three main members of cellulolytic enzymes. Periconia sp. (BCC2871), an endophytic fungus, produces thermotolerant β-glucosidase. The full-length gene of β-glucosidase from this strain was cloned in Pichia pastoris KM71 strain. The recombinant enzyme was shown to have its optimal pH at 5 and 6 and the optimal temperature to be at 70  C. High enzyme activity was observed even after longer incubation periods at higher temperatures, thus retaining a 60% activity after 1.5 h at 70  C. The enzyme was found to be stable at higher pH conditions also and retained 100% activity recorded even after 2 h at pH 8. The inclusion of β-glucosidase into the hydrolysis reaction of rice straw encompassing a commercial cellulase, Celluclast 1.5L (Novozymes, Denmark), resulted in the boosting of reducing sugar release upon hydrolysis. This recombinant enzyme is apt and suitable for treating lignocellulosic substrates in the production of biofuels and other chemicals (Harnpicharnchai et al. 2009). Twelve endophytic fungal isolates of four medicinal plants were isolated; they were screened for cellulase activity, namely Adhatoda vasica, Costus igneus, Coleus aromatics, and Lawsonia inermis. Cladosporium cladosporioides and Curvularia vermiformis displayed a positive cellulase assay response among those 12 strains (Amrita et al. 2012).

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

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Wood-dwelling fungal endophytes were isolated from Drimys winteri, a Chilean tree, and Prumnopitys andina. Bjerkandera sp. isolated from D. winteri was positive to cellulase assay while T. versicolor, G. australe (A464), and C. subvermispora from P. andina were positive for cellulase activity (Oses et al. 2006). Cellobiohydrolase (CBHI)-encoding gene was isolated from a fungal endophyte Fusiccoccum sp. belonging to Ascomycota (Kanokratana et al. 2008). Expression of CBHI gene in Pichia pastoris KM71 was studied. The recombinant CBHI enzyme could degrade Avicel, filter paper, and 4-methylumbelliferyl β-Dcellobioside (MUC) but could not hydrolyze carboxymethylcellulose. CBHI was shown to have optimal activity at 40  C at pH 5.0 km and Vmax values were 0.57 mM and 3.086 nmol/min/mg, respectively, and the enzyme was stable at pH 3–11. CBHI retained its 50% activity at 70–90  C for 30 min. Since this enzyme has been observed to be stable in a wide range of pH, and moderately stable at high temperatures, it seems to have a promising potential in various biotechnological applications (Table 1.1).

1.2.2

Xylanases

Xylanases randomly hydrolyzed the β-1,4-glycosidic bonds of xylan, the major plant cell wall polysaccharide component of hemicelluloses. Xylan has a complex structure consisting of β-1,4-linked xylose residues in the backbone to which short side chains of O-acetyl, α-Larabinofuranosyl, D-α-glucuronic, and phenolic acid residues are attached (Coughlan and Hazlewood 1993). The use of xylanases in the biotech industry has increased remarkably. Xylanases have numerous applications in the food, paper and pulp, pharmaceutical, and textile industries.

1.2.2.1

Textiles

Xylanases have also been extensively used in the pretreatment of plant fibers. The xylanases employed in the process should be free from cellulolytic enzymes, for example, liberation of long cellulose fibers after the treatment of China grass stems. The need to use the strong bleaching step is no longer required, considering that the lignin does not go through oxidation that leads to darkening of the fibers (Prade 1996; Brühlmann et al. 2000).

1.2.2.2

Food Industry

Xylanases break down hemicelluloses present in wheat flour that results in a softer dough, increased volume of bread, higher water absorption, and resistance to fermentation process (Maat et al. 1992). Xylanases along with endoglucanases participate in arabinoxylan hydrolysis, separation of starch, and gluten isolation

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Table 1.1 Enzymes produced by endophytic fungi from different host plants Endophytic fungi Acremonium zeae, Acremonium sp. Cladosporium cladosporioides, Nigrospora, sphaerica, Colletotrichum gloeosporioides Curvularia brachyspora

Costus igneus Lawsonia inermis Adhatoda vasica

Curvularia vermiformis, Xylaria sp.

Coleus aromaticus

Drechslera hawaiiensis

Adhatoda vasica

Colletotrichum crassipes, Colletotrichum falcatum Phyllosticta sp.

Lawsonia inermis Adhatoda vasica, Lawsonia inermis Opuntia ficusindica Opuntia ficusindica Opuntia ficusindica

Aspergillus japonicus Monodictys castaneae

Host plant Corn

Enzyme Cellulases and hemicellulases Amylase, cellulose, protease

References Almeida et al. (2011) Amrita et al. (2012)

Amylase, laccase, lipase Cellulose, lipase, protease, amylase, laccase Amylase, lipase, protease Amylase, protease, lipase Amylase, lipase

Amrita et al. (2012) Amrita et al. (2012)

Cellulose, pectinase, protease, xylanase Xylanase

Bezerra et al. (2012) Bezerra et al. (2012) Bezerra et al. (2012)

Phoma tropica, Phomopsis archeri, Tetraploa aristata, Xylaria sp. Talaromyces flavus

Potentilla fulgens

Mortierella hyalina

Osbeckia stellata

Paecilomyces variabilis Penicillium sp.

Osbeckia chinensis Camellia caduca

Penicillium sp.

Schima khasiana

Acremonium zeae

Zea mays

Lipase, protease, xylanase Cellulase, lipase, protease, xylanase Amylase, lipase, protease, xylanase Cellulase, lipase, protease, xylanase Cellulase, lipase, protease, xylanase Xylanase

Colletotrichum musae

Musa cavendish

Acid phosphatase

Penicillium sp. Trichoderma sp., Penicillium sp., Aspergillus sp. Penicillium spp.

Centella asiatica Latrunculia corticata Dendronephthya hemprichi Glinus lotoides

Cellulase Cellulases

Chaetomium globosum

Protease, xylanase

Keratinase Laccase

Amrita et al. (2012) Amrita et al. (2012) Amrita et al. (2012)

Bhagobaty and Joshi (2012) Bhagobaty and Joshi (2012) Bhagobaty and Joshi (2012) Bhagobaty and Joshi (2012) Bhagobaty and Joshi (2012) Bischoff et al. (2009) Maccheroni and Azevedo (1998) Devi et al. (2012) El-Bondkly (2012) El-Gendy (2010) El-zayat (2008). Abdel-Azeem and Salem (2012) (continued)

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Table 1.1 (continued) Endophytic fungi Colletotrichum sp.

Host plant Abelmoschus esculentus

Acremonium sp. Fusarium sp. Alternaria chlamydospora, Pestalotiopsis sp.

Acrostichum aureum Acanthus ilicifolius

Lasiodiplodia theobromae

Coconut

Cylindrocephalum sp.

Alpinia calcarata (HAW.) Roscoe Eucalyptus benthamii, Platanus orientalis Glycine max Solanum tuberosum Saccharum officinarum

Aspergillus niger, Trichoderma atroviride, Alternaria sp., Annulohypoxylon stygium, Talaromyces wartmanni

Enzyme β-Galactosidase, rhamnogalacturonan lyase, acetyl esterase Amylase, cellulase, lipase Cellulase, lipase, protease, amylase, lipase Lipase Amylase Xylanase, hemicellulases

References Grünig et al. (2008) Maria et al. (2005a)) Maria et al. (2005b) Venkatesagowda et al. (2012) Sunitha et al. (2012) Robl et al. (2013)

from starch present in wheat flour (Gilbert et al. 1993). Xylanases are nowadays used in combination with amylases, pectinases, and cellulases to improve juice quality of fruits by means of liquefaction.

1.2.2.3

Paper and Pulp Industry

Xylanases are one of the favored enzymes in the cellulose and paper industries. Bridges between the xylan and lignin are acted upon by xylanases that open cellulosic pulp structure, concomitantly guiding xylan fragmentation and fragment extraction subsequently (Paice et al. 1992). Use of xylanase in pre-bleaching has received considerable attention as much lower amount of chlorine compounds is used (up to 30%), resulting in 20% reduction of organochlorine composition of effluents, as otherwise formation of organochlorines, during the decomposition of lignin, with the use of chlorine, is hazardous to biotic as well as abiotic environmental factors as they are extremely mutagenic, noxious, and threatening.

1.2.2.4

Xylanases from Endophytic Fungi and Their Applications

Thermotolerant extracellular xylanase from an endophytic fungal strain, Aspergillus terreus residing inside Memora peregrina, a native plant to Brazil, was purified and

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characterized. The fungal strain was shown to have high levels of xylanase activity when grown on wheat bran as carbon source at 30  C for 48 h, while cellulase activity was low. Xylanase was purified 45-fold with 67% of recovery by carboxymethylcellulose chromatography. A single purified band of 23 kD was observed in SDS-PAGE. Optimal enzyme activity was observed at 55  C and pH 4.5. Isolated enzyme was found to be thermotolerant at 45  C with a half-life of 55 min and at 50  C for 36 min, respectively. Enzyme kinetic studies have revealed xylanase activation (Sorgatto et al. 2012). A fungal strain (NRCF5) was isolated from the inner tissue of coral Rhytisma sp. (Egypt). Based on the morphological studies and ITS sequencing results, the species was confirmed as Aspergillus sp. As per the principles underlying the shuffling of genome to achieve cultivation of xylanase-producing fungi, the marine source Aspergillus NRCF5 was exploited as the starting strain and genetic variability was induced using different combinations and doses of mutagens. Ultraviolet irradiation (5 min) and N-methyl N-nitro-N-nitrosoguanidine (NTG, 100 mg/mL) for 30 (UNA) and 60 (UNB) min along with NTG (100 mg/mL) and ethidium bromide (250 mg/mL) for 30 (NEA) and 60 (NEB) min were used in combination as mutagens. This mutagenesis led to an increase in xylanase activity in five fungal strains and 0.25% (w/v) antimetabolite 2DG tolerance was also observed. Thereafter recursive protoplast fusion was carried out. Four rounds of genome shuffling led to the rise of seven high xylanase-producing fungal strains, and these also showed tolerance to 1.0% (w/v) 2DG. R4/31 strain was the best xylanase-producing strain among the seven strains. The recombinant xylanase has shown 6.13 higher folds of xylanase activity when compared with starting strain NCRF5 with 427.5 mL xylanase and 2.48 times more than that of the original (Mutant NEA51) (El-Bondkly 2012).

1.2.3

Amylases

Amylases are starch-degrading enzymes that catalyze starch by hydrolyzing internal glycosidic bonds in polysaccharides with the retention of anomeric configuration in products. Among starch-degrading enzymes are endo-amylases, exoamylases, debranching enzymes, and glycosyl transferases (Yadav et al. 2015; Khajeh et al. 2006). The enzymatic hydrolysis by amylases is preferred to acid hydrolysis in the starch processing industry due to the specificity of the reaction, the stability and lower energy requirements, and the elimination of neutralization steps (Satyanarayana et al. 2005; Kour et al. 2019a; Yadav et al. 2019b). There is an increasing demand for amylases with better properties such as raw starch-degrading amylases, which are suitable for industrial applications due to their cost-effective production techniques (Burhan et al. 2003). These enzymes account for about 30% of the world’s enzyme production (Maarel et al. 2002).

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

1.2.3.1

11

Textiles

Starch is extensively used in sizing process to prevent yarn from breaking, as it is easily available and cheap. After weaving process, the starch is removed by amylases as they act only on starch and do not interfere with fabrics. The starch thus removed, from the fabrics due to desizing by amylases, which break starch into dextrins, can be washed off (Hendriksen et al. 1999).

1.2.3.2

Paper and Pulp

Starch is used in the paper industry to size the paper. Sizing gives mechanical strength to the paper which involves applying less viscous and high-molecularweight starch to the paper. Usually, the starch is highly viscous. Upon sizing process, differences in viscosity of starch give different grades of paper (Godfrey and West 1996).

1.2.3.3

Detergent Industry

Approximately, 90% of liquid detergents contain amylases (Kottwitz et al. 1994). Amylases are stable at low temperatures and alkaline pH, and easily digest starch present in food particles that are attached to the clothes and form water-soluble oligosaccharides.

1.2.3.4

Bread and Baking Industry

Amylases are being used in the bread and baking industry for decades. Amylases give better color, higher volume, and softer crumb to the bread which improves the taste. Fungal amylases also got authorized as bread additives in the USA and in the UK in 1994 and 1963, respectively, after confirmation of their GRAS status (Pritchard 1992).

1.2.3.5

Amylases from Endophytic Fungi and Their Applications

Isolation of 14 endophytic fungi associated with Acanthus ilicifolius L., a mangrove angiosperm, and Acrostichum aureum L., a mangrove fern from Nethravathi mangrove, southwestern coast, India, was reported. Among these fungi, four of the fungal isolates from A. aureum host have shown positive activity when subjected to amylase plate assay (Maria et al. 2005a, 2005b). Endophytic fungi isolated from flowers and leaves of Alpinia calcarata were studied for amylolytic activity. Out of

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the 30 fungal strains, 1 strain (Cylindrocephalum sp. no. 7) has shown highest amylolytic activity. The influence of physical and chemical parameters on the production of amylase was additionally investigated with temperature, pH, carbon, and nitrogen sources as the parameters. Optimal amylase activity was observed at 30  C and at pH 7.0. The concentrations of 1.5% of maltose as carbon source and 0.3% sodium nitrate were recorded to be the best carbon and nitrogen sources, respectively, for the Cylindrocephalum sp. (Sunitha et al. 2012). Adhatoda vasica, Coleus aromaticus, Costus aromaticus, and Lawsonia inermis were processed for endophytic fungi and 12 fungal isolates were isolated. Out of the 12 fungi, four hyphomycetes, Cladosporium cladosporioides, Curvularia brachyspora, Drechslera hawaiiensis, and Nigrospora sphaerica, along with three coelomycetes, Colletotrichum crassipes, C. gloeosporioides, and Phyllosticta. sp., were found to be positive for amylase in the plate assay (Amrita et al. 2012). Αmylase-producing endophytic taxon, Preussia minima, has been recovered from Eremophila longifolia, a native plant of Australia. Zymogram of α-amylase has revealed it as a 70 kD enzyme. Its optimum activity was observed at 25  C and optimum pH was 9.0. Additional study of metal ion aftereffect was carried out. From these studies it was confirmed that manganese and calcium promote and stabilize amylase activity. The impact of different nitrogen and carbon sources on amylase activity was observed. L-asparaginase and starch were confirmed as the best nitrogen and carbon sources, respectively. Enzyme production during scale-up fermentation was encouraging as bioreactors revealed comparable production to that obtained in shaker cultures. The purified enzyme has shown similarity with the amylase of Magnaporthe oryzae, as confirmed from the partial sequence matching of the enzyme (Zaferanloo et al. 2014). A foliar endophytic fungus was isolated from Zea mays. The highest rate of production of glucoamylase was observed during initial growth phase, i.e., after 24-h incubation period at pH 8.0. The glucoamylase activity was lost at 100  C while being stable at 70  C, activity recorded was 158 U/mg protein, and 100% residual activity was retained for 30 min. Saturation of 60% yielded 421 U/mg protein which was 74% with a 2.7-fold purification.

1.2.4

Pectinase

Pectinase is a group of enzymes that break down pectin and depolymerize it by hydrolysis and by de-esterification reactions. Endopolygalacturonase, exopolygalacturonase, exo-polygalacturonase, endopectate lyase, oligo-Dgalactosiduronate lyase, and endopectinylase are depolymerizing enzymes that cleave glycosidic bonds of pectins by means of hydrolysis and transelimination (Alkorta et al. 1998). Pectin esterase is the pectolytic enzyme that catalyzes the hydrolysis of ester links between the carboxyl and methyl groups of complex polysaccharide known as pectin found in the cell wall of higher plants (Ceci and

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Lozano 1998). Pectic enzymes account for about 25% of world’s food enzyme production (Kashyap et al. 2001).

1.2.4.1

Wine Processing

Pectinolytic enzymes are added to fruits before the addition of inoculum. This process improves the characteristics of wine. Pectinases maximize juice yield, support wine extraction, facilitate filtration, and intensify color and flavor of wine.

1.2.4.2

Tea and Coffee Processing

Pectinases break down pectins present in the tea leaves, accelerate the fermentation process, and act as antifoaming agents for tea as the pectin of tea leaves is destroyed by pectinases. Pectinases are generally used in combination with other enzymes such as cellulases, hemicellulases, and proteinases. Crude enzyme extract from Aspergillus sp. is more effective for tea fermentation when compared to purified pectin enzyme alone used in the tea leaf fermentation. This is because of the crude fungal enzymes that contain other enzymes as well.

1.2.4.3

Pectinases from Endophytic Fungi and Their Applications

Coffee beans are coated with mucilaginous coat. It is composed of 89% moisture, 9% protein, 4% sugar, and 2.8% pectin. Demucilation process is required to carry out the fermentation of coffee beans. The demucilation process is performed with pectinases and proteases. Demucilation process leads to the reduction in pH and increased release of sugars. Murthy and Naidu (2011)) reported that crude pectinase obtained from Aspergillus niger (CFR) causes degradation of mucilaginous layer of about 54% after 1 h and 71% after 2 h, present in coffee beans, and complete decomposition of pectin was attained after 3.5 h.

1.2.5

Lipases

Lipases are the hydrolytic enzymes classified as a special class of esterases that in vivo break the ester bond of triacylglycerol releasing free acids and glycerol (Oliveira et al. 2014). These are able to catalyze interesterification, alcoholysis, acidolysis, esterification, and aminolysis reactions in nature and when under proper conditions in vitro (Diaz et al. 2006). Endophytes able to produce lipases have been the target of research in the last years. An endophytic strain Rhizopus oryzae isolated from Mediterranean plants was able to catalyze the esterification of fatty acids in isooctane (Torres et al. 2003). Recently, an effort has been successful in the

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production and stabilization of lipase from endophytic Cercospora kikuchii (CostaSilva et al. 2014a, b).

1.2.5.1

Pulp and Paper

Lipases are employed to remove the pitch, i.e., triacyl glycerides and waxes of wood. Lipases hydrolyze 90% of triacylglycerols into monoacylglycerols, making pulp hydrophilic and less sticky; increase pulping rate and witness of the paper; decrease chemical usage; reduce pollution; save energy; and prolong lifetime of equipment.

1.2.5.2

Leather

Proteins and lipids of collagen fibers of hides and skin should be totally removed before the tanning process of the leather. Non-fibril proteins are removed by proteases whereas fat is removed by lipases without damaging the leather.

1.2.5.3

Food Industry

Lipases have been extensively used in the food industry to synthesize flavors or flavor precursors. Selective hydrolysis of triacyl glycerides releases free fatty acids that act as flavors or flavor precursors (Alves Macedo et al. 2003). Lipases are used in flavor development of dairy products such as cheese, margarine, chocolate milk, butter, and sweets to remove the fat from the meat to produce lean meat and fish meat.

1.2.5.4

Detergent Industry

Lipases are used in detergents along with various other enzymes such as amylases, cellulases, and proteases (Benjamin and Pandey 1998). The ideal lipase should hydrolyze various lipids, withstand higher pH (pH 10–11) and temperatures (30–60  C), and are resistant to proteases used in the same detergent with an ability to act on greasy substances like lipsticks, frying fats, butter, and sauces (Jaeger and Reetz 1998).

1.2.5.5

Biodiesel Production

Biodiesel is produced from triacyl glycerides of animals, plants, algae, and fungi. Alga-based biodiesel production has been extensively used. Biodiesel synthesis involves removal of triacyl glycerides, digestion of triacyl glycerides into fatty acids, and transesterification of fatty acids into fatty acid methyl. Lipases are

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required to break the triacyl glycerides into free fatty acids, which is the second step in the production of biodiesel (Kaur et al. 2020; Yadav et al. 2020c).

1.2.5.6

Lipases from Endophytic Fungi and Their Application

A total of 212 endophytic fungi living in Amazon plant leaves and fruits have been screened for biocatalysts containing lipase-bound mycelium. Around 87% of the isolates may hydrolyze tributyrin substrate, and among these 30% were evaluated for their ability of esterification and transesterification reactions in organic solvents. Among these fungal isolates best nine isolates were investigated for enantioselectivity of mycelium-bound lipase activity in (R,S)-2-octanol resolution reaction. The endophyte UEA_115 was found to be the most ingenuous biocatalyst, demonstrating a splendid performance in esterification reactions (conversion >90%) and enhanced aptitude for the resolution of (R,S)-2-octanol (ees 29%; eep 99%; c 22%; E > 200). Thus, this investigation revealed the potent nature of the endophytic fungi as lipase suppliers in lipid biocatalysis. Immobilization and enzyme activity of lipases secreted by Cercospora kikuchii, an endophytic fungus, associated with the host Tithonia diversifolia, were studied. The maximum production of lipase obtained was when the fungal strain was grown on 2% soya bean oil after 6 days and the yield was 9 U/mL. The stability of the lipase was studied with spray-dried lipase with different adjuvants. The remaining enzymatic activity once dried with 10% (w/v) of lactose maltodextrin, β-cyclodextrin, gum apona, mannitol, as well as trehalose ranged from 63 to 100%. No lipase activity was observed when adjuvants were absent. After 8 months, the enzyme activity at 5  C and 25  C was 50% and 40%, respectively. When 10% of β-cyclodextrin was used to dry the lipase, the activity observed was 72% at 50  C. Lipase separation was carried out by butyl a ponaria column followed by partial purification (33.1%; 269.5 U/mg proteins). Spray drying of this enzyme in maltodextrin DE10 retained 100% of its activity (Costa-Silva et al. 2014b). The isolates and lipase-modified media have shown commendable development. In a study, the sesame, Pongamia, coconut, peanut, rubber, neem, and castor seeds were sampled from various sites in the state of Tamil Nadu, India, and then processed for endophytic fungal insulation. Totally 1279 endophytic fungal strains have been obtained from the seeds above. Nineteen strains were positive for lipolytic activity, of the 1279 strains, in addition to exhibiting cellulolytic, proteolytic, and amylolytic activities. These fungi belonged to the following genera: Aspergillus, Alternaria, Chalaropsis, Cladosporium, Colletotrichum, Curvularia, Drechslera, Fusarium, Lasiodiplodia, Mucor, Penicillium, Pestalotiopsis, Phoma, Phomopsis, Phyllosticta, Rhizopus, Stachybotrys, Sclerotinia, and Trichoderma. Five fungal strains, viz., Lasiodiplodia theobromae, Chalaropsis thielavioides, Colletotrichum gloeosporioides, Aspergillus niger, and Phoma glomerata, displayed highest lipase activity. Lasiodiplodia sp. was the best producer of lipase and the activity observed was 108 U/ml. This fungal strain was characterized by ITS sequencing of 18S rRNA (Venkatesagowda et al. 2012).

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Purification, characterization, stabilization, and enzyme kinetics of lipase production by fungal endophyte Cercospora kikuchii were studied (Costa-Silva et al. 2014b). The lipase was purified up to 9.31 times, with a reported recovery of 26.6%, whereas specific activity was found to be 223.6 U/mg. The optimal enzyme activity was observed at a temperature of 35  C and at pH of 4.6. Enzyme kinetic studies have shown that the Km was 0.0324 mM and Vmax 10.28 μmol/min/mg protein. The lipase possessed resistance attribute to Tween 80 and 20, Triton X, SDS, and proteases. In the presence of oxidants also lipase retained 100% of activity. After spray drying of the purified lipase, it possessed 85.2% of enzymatic activity. The lipase enzyme obtained from Cercospora kikuchii has several properties in relevance with industrial applications and depicted sufficing stabilization and retention of its enzymatic activity after spray drying.

1.2.6

Laccases

Laccases are glycosylated polyphenol oxidases (Thurston 1994). These enzymes find important commercial applications in the pulp and paper industry, animal biotechnology biotransformation, and detoxification of phenolic pollutants (Brenna and Bianchi 1994; Breen and Singleton 1999; Sahay et al. 2017; Singh et al. 2016). Laccase production is a common feature of many basidiomycete fungi, particularly those associated and involved in wood decay or terminal stages of decomposition (Gianfreda et al. 1999). Wang et al. (2006) reported the laccase production by endophytic Monotospora sp. isolated from Cynodon dactylon. In this study, maltose (2 g/L) and ammonium tartrate (10 g/L) were found to be the most suitable carbon and nitrogen sources, respectively, for enzyme production. Chen et al. (2011) reported the laccase production from endophytic Pestalotiopsis sp. isolated from sea mud collected from East China Sea under submerged and solid-state fermentation using various lignocellulosic by-products as substrates. The endophytic fungus Phomopsis liquidambari that grows on phenolic 4-hydroxybenzoic acid as the sole carbon and energy source is able to produce the ligninolytic enzymes laccase and lignin peroxidase when cultured in submerged fermentation (Chen et al. 2013).

1.2.6.1

Wine Stabilization

Laccase is used to improve the quality of drinks and for the stabilization of certain perishable products containing plant oils (Morozova et al. 2007). In the food industry, wine stabilization is the main application of laccase (Duran and Esposito 2000; Rosana et al. 2002). Polyphenols have undesirable effects on wine production and on its organoleptic characteristics, so their removal from the wine is very necessary (Rosana et al. 2002). Many innovative treatments, such as enzyme inhibitors, complexing agents, and sulfate compounds, have been proposed for the removal of phenolics responsible for discoloration, haze, and flavor changes but the

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possibility of using enzymatic laccase treatments as a specific and mild technology for stabilizing beverages against discoloration and clouding represents an attractive alternative (Cantarelli et al. 1989; Arora and Sharma 2010). Since such an enzyme is not yet allowed as a food additive, the use of immobilized laccase might be a suitable method to overcome such legal barriers as in this form it may be classified as a technological aid. So laccase could find application in preparation of must and wine and in stabilization of fruit juice (Minussi et al. 2002; Arora and Sharma 2010).

1.2.6.2

Baking Industry

In the bread-making process laccases affix bread and/or dough enhancement additives to the bread dough; this results in improved freshness of the bread texture and flavor and improved machinability (Minussi et al. 2002). Laccase is also one of the enzymes used in the baking industry. Laccase enzyme is added in the baking process which results in the oxidizing effect, and also improves the strength of structures in dough and/or baked products. Laccase imparts many characteristics to the baked products including an improved crumb structure and increased softness and volume. A flour of poor quality can also be used in this process using laccase enzyme (Minussi et al. 2002).

1.2.6.3

Textile Industry

Normally, from 10 to 50% of the initial dye load will be present in the dyebath effluent, giving rise to a highly colored effluent (Vandevivere et al. 1998; Moilanen et al. 2010). Therefore, the treatment of industrial effluents containing aromatic compounds is necessary prior to final discharge to the environment (Khlifia et al. 2010). Decolorization and detoxification of a textile industry effluent by laccase from Trametes trogii in the presence and absence of laccase mediators had been investigated. It was found that laccase alone was not able to decolorize the effluent efficiently even at the highest enzyme concentration tested: less than 10% decolorization was obtained with 9 U/mL reaction mixtures. To enhance effluent decolorization, several potential laccase mediators were tested at concentrations ranging from 0 to 1 mM. Most potential mediators enhanced decolorization of the effluent, with 1-hydroxybenzotriazole (HBT) being the most effective (Khlifia et al. 2010).

1.2.6.4

Pharmaceutical Industry

Laccases have been used for the synthesis of several products of the pharmaceutical industry (Arora and Sharma 2010; Abdel-Azeem et al. 2015; Abo Nahas 2019; Balbool and Abdel-Azeem 2020). One of the famous applications of laccases in industrial applications of laccase is actinocin that has been prepared from 4-methyl-

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3-hydroxyanthranilic acid. This compound has anticancer capability and works by blocking the transcription of DNA from the tumor cell (Burton 2003). Another example of the anticancer drugs is vinblastine, which is useful for the treatment of leukemia. The plant Catharanthus roseus naturally produces vinblastine. This plant produces a small amount of this compound. Katarantine and vindoline are the precursors of this pharmaceutically important compound. These precursors are produced in higher quantities and are easy to purify. Laccase is used to convert these precursors into vinblastine. A 40% conversion of these precursors into the final product has been obtained using laccase (Yaropolov et al. 1994). The use of laccase in such conversion reactions has made the preparation of several important compounds with useful properties, like antibiotics, possible (Pilz et al. 2003).

1.2.7

Proteases

Proteases (serine protease, cysteine protease, aspartic protease, and metalloprotease) are the most important class of enzymes that catalyze the total hydrolysis of proteins and have been studied extensively since the advent of enzymology (Nielsel and Oxenboll 1998). The inability of the plant and animal protease to meet current world demands has led to an increased interest in microbial proteases.

1.2.7.1

Food Industry

The principal applications of proteases in food processing are in brewing, cereal mashing, and beer haze clarification; in the coagulation step in cheese making; in altering the viscoelastic properties of dough in baking; and in the production of protein hydrolysates. The hydrolytic quality of proteases is exploited for degradation of the turbidity complex resulting from protein in fruit juices and alcoholic liquors, and improvement of quality of protein-rich foods, soy protein hydrolysis, gelatin hydrolysis, casein and whey protein hydrolysis, meat protein recovery, and meat tenderization (Yadav et al. 2020a, 2020b). The major application of proteases in the dairy industry is in the cheese manufacturing, where the primary function of enzymes is to hydrolyze the specific peptide bond to generate casein and macropeptides (Rao et al. 1998).

1.2.7.2

Detergent Industry

The use of enzymes as detergent additives represents the largest application of industrial enzymes. Proteases in laundry detergents account for approximately 25% of the total worldwide sales of enzymes (Demain and Adrio 2008). The use of enzymes in detergent formulations enhances the detergents’ ability to remove tough stains and makes the detergent environmentally safe. Nowadays, many

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laundry detergent products contain cocktails of enzymes including proteases, amylases, cellulases, and lipases (Hmidet et al. 2009). Alkaline proteases added to laundry detergents enable the release of proteinaceous material from stains. The performance of alkaline protease in detergent is influenced by several factors such as pH and temperature of washing solution as well as detergent composition. Ideally, proteases used in detergent formulations should have high activity and stability within a broad range of pH and temperatures, and should also be compatible with various detergent components along with oxidizing and sequestering (Jaouadi et al. 2008; Kumar and Takegi 1999; Savitha et al. 2011).

1.2.7.3

Leather Industry

Another industrial process which has received attention is the enzyme-aided dehairing of animal hides and skin in the leather industry. Leather making is a processing industry that has negative implications emanating from the wastes associated with industrial processing. In a tannery, a raw hide is subjected to a series of chemical treatments before tanning and finally converted to finished leather. Alkaline proteases may play a vital role in these treatments by replacing these hazardous chemicals especially involved in soaking, dehairing, and bating. Increased usage of enzymes for dehairing and bating not only prevents pollution problems, but also is effective in saving time with better quality leather (Zambare et al. 2011).

1.2.7.4

Pharmaceutical and Cosmetic Industries

Proteases might be utilized in the elimination of keratin in acne or psoriasis, elimination of human callus and degradation of keratinized skin, depilation, and preparation of vaccine for dermatophytosis therapy, and to increase ungual drug delivery (Randelli et al. 2010; Vignardet et al. 2001). Furthermore, these keratinases can remove the scar, regenerate the epithelia, and accelerate healing processes, and might also act in the medicine of trauma (Chao et al. 2007). In cosmetic products, proteases can hydrolyze the peptide bonds of keratin, collagen, and elastin of the skin. Enzymes such as papain, bromelain, and other proteases have been used on the skin for performing smoothing and peeling. The action of these proteases is related to cell renewal, exercising of keratinolytic activity, and promoting of the removal of dead cells in the epidermis and restoring of the same (Sim et al. 2000).

1.2.7.5

Proteases from Endophytic Fungi and Their Applications

Fungal endophytes possess the ability to produce proteases. An unidentified endophytic fungus, isolated from a marine soft coral Dendronephthya hemprichi, has shown highest keratinase activity when grown on different agricultural and poultry

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wastes in solid-state fermentation having a maximum activity of 1600 U/g. The maximum enzyme production was observed with rice straw as the carbon source at 26  C with moderate pH at 6 and the moisture content at 80%. Ahm1 and Ahm2, two types of keratinases, were purified and characterized by precipitation with diazanium sulfate (ammonium sulfate), DEAE aponaria, and gel-exclusion chromatography in a sequential manner. Molecular weight of enzyme Ahm1 was 19 kDa and Ahm2 was 40 kDa. For purified keratinases, various kinetic parameters were optimized, to investigate the hydrolysis of azokeratin by Ahm1 (pH range 7.0–8.0, at 50  C, stable in pH range of 6.0–8.0) and Ahm2 (pH range 10.0–11.0, at 60–65  C, stable in pH range of 6.0–11.0). Both the keratinases, Ahm1 and Ahm2, were reported to undergo inhibition by chelating agents such as EGTA and EDTA. Serine protease inhibitor phenylmethylsulfonyl fluoride and cysteine protease inhibitor iodoacetamide depicted inconsiderable consequences on keratinases (El-Gendy 2010). Jalgaonwala and Mahajan (2011) reported that 12 endophytic fungi had proteolytic activity of which a strain belonging to Mycelia Sterilia, from roots of Catharanthus roseus, showed a greater protease activity as compared to other fungal isolates tested. Alberto et al. (2016) examined four host trees, viz. Luehea divaricata, Sapindus saponaria, Trichilia elegans, Piper hispidum, and Saccharum spp., for production of various enzymes by fungal endophytes. Approximately 64% of endophytes were found to produce proteases. Isolation and partial purification of a protease produced by Acremonium sp., isolated from leaves of Saraca asoca, when grown on skim milk medium, has shown protease activity. Fructose and ammonium sulfate were found to be the prime carbon and nitrogen sources for the highest protease production and the optimum activity of the enzyme was recorded at pH 7.0. The enzyme activity was found to be 3.4 U/mL, the protein content 20 μg/mL, and the specific activity of enzyme 0.167 U/μg (Jain et al. 2012).

1.2.8

Chitinases

Chitin, a linear homopolymer of β-1,4-linked N-acetyl glucosamine, is a constituent of the exoskeleton of insects and shells of crustaceans and forms the basic structural component of the fungal cell wall. Chitinases are the enzymes that degrade this insoluble polymer, also known as chitinolytic enzymes. Fungal chitinases play an important role in the ecosystem by degrading and cycling carbon and nitrogen materials in chitin (Verma et al. 2015a, b, c, 2016; Kellner et al. 2009). Chitinases of fungi are also being studied for their potential in biocontrol of nematodes (Gan et al. 2007; Saxena et al. 2020) and pathogenic fungi (Klemsdal et al. 2006). Plants also produce chitinases as a defense response to infection by pathogens (El Gueddari et al. 2002). The products of chitinases have many desirable properties and find use in the control of microbes and tumors, wound healing, wastewater treatment, and drug delivery (Dai et al. 2006; Yadav et al. 2016a, b). Chitinases have been reported from the endophytic fungi Neotyphodium sp. and Colletotrichum musae (Borges et al.

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2009). It has been reported that the same endophytic fungi isolated from different host species showed varied capacity to produce enzymes; for example, Colletotrichum acutatum, Fusarium sp., Phomopsis sp., and Phyllosticta capitalensis isolated from different plant hosts varied in their ability to produce the different chitin-modifying enzymes (El Gueddari et al. 2002). Chitinases have a significant function in human health care. An important medical use for chitinases has also been recommended in augmenting the activity of antifungal drugs in therapy for fungal diseases. Due to their topical applications, they have a prospective use in antifungal creams and lotions. A number of artificial medical articles such as contact lenses, artificial skin, and surgical stitches have been formed from chitin derivatives. These derivatives have an extensive medical use because quite a few of these chitin derivatives are known to be nontoxic, nonallergic, biocompatible, and biodegradable.

1.2.9

Tyrosinases

Tyrosinase enzyme is a monooxygenase that belongs to class 3 copper-containing protein family. They catalyze the monophenolic oxidation (diphenolase or catecholase activity) or hydroxylation (monophenolase or cresolase activity) into respective o-quinones or catechols (Zaidi et al. 2014). Tyrosinase also catalyzes the melanin synthesis, by oxidation, in mammalian systems. Tyrosinase causes the hydroxylation of l-tyrosine to 3,4-dihydroxyphenylalanine (l-DOPA) which is involved in melanin biosynthesis (Parvez et al. 2006). Tyrosinase which is present in mushrooms, fruits, vegetables, etc. is responsible for the blackening during longterm storage. In humans, abnormalities such as flecks and defects during hyperpigmentation of skin are attributed to tyrosinases. Quite a significant role is played by tyrosinases in the agriculture industry. Tyrosinases are also used as biosensors to detect phenolic compounds in environment and thus find their applications in detoxification of wastewater and soils contaminated with phenols. Since tyrosinases are used as markers in melanoma patients and during the treatment of Parkinson’s disease, they are of therapeutic importance too. In the food industry also, they are used as food modifiers as they have the ability to cross-link proteins. Similarly, in the cosmetic industry also inhibitors of these enzymes are screened for skin treatments such as dermatological disorders associated with melanin hyperpigmentation. Tyrosinases also possess the property to degrade lignin, and thus the endophytic fungal production of tyrosinases implicates the characteristic association and recycling of natural ecosystem. Concomitantly, tyrosinase inhibitor production implicates host vegetative growth which represents a balance between the both. Several investigators have screened fungal endophytes for tyrosinase production on the hypothesis of change of ecological strategy of endophytes to saprobic lifestyle following senescence. Sun et al. (2011) screened endophytes from Acer truncatum

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for tyrosinase production and recorded that out of 21 strains, 10 endophytic taxa were positive.

1.2.10 Phosphatases Phosphorus present in soil is indispensable for plant growth, but is generally unavailable to plants in its native form. Phosphatases are the enzymes that make phosphorus available to the plants for enhancing their growth (Kour et al. 2020b, c). Endophytic fungi are also known to produce phosphatases (Kour et al. 2020d). Khan et al. (2016) screened various endophytes from frankincense tree for the secretion of extracellular enzymes. Species belonging to the genus Preussia exhibited higher enzyme secretion while a moderate activity was shown by Penicillium citrinum and Aureobasidium pullulans. Production of phosphatases also aids in the growth of hosts as monitored and reported in the above study with respect to the root/shoot length (Mondal et al. 2020). Previous studies also support the fact that inoculation of endophytes has resulted in a distinct growth as easily assimilable nutrients are made available by the action of phosphatases. Shubha and Srinivas (2017) reported phosphatase activity of endophytic fungi from Cymbidium aloifolium. Colletotrichum truncatum was reported to show the highest enzyme activity index of 1.58. They screened endophytes from flowers, roots, and leaves with 100%, 93.5%, and 77.7% of isolates positive for phosphatase activity, respectively. Except for two isolates, viz. A. alternate and Curvularia sp., all the other endophytic fungi were positive for phosphatase enzyme. Phosphate solubilization through phosphatase production or various organic acids is an attribute of plant growth-promoting fungi (Illmer et al. 1995; Hesham et al. 2021). Many reports clearly suggest that among different microbes, fungi are more capable of solubilizing phosphates (Nahas 1996; Kour et al. 2020a, 2019b). According to Wakelin et al. (2004), species belonging to Penicillium and Aspergillus are prominent endophytes known for competent phosphate solubilization. Endophytes thriving in extreme conditions such as high or low temperatures, nutrientdeficient soils, and lesser moisture are more potent in encouraging host growth (Chadha et al. 2015) and can support hosts by residing under such unfavorable conditions. Similar results were recorded by Chadha et al. (2015). All 12 isolates of endophytic fungi isolated from the roots of tomato plants from India displayed phosphatase-solubilizing activity. Trichoderma pseudokoningii showed the highest rate (37.45  2.78 to 64.32  2.87 μg/mL) of phosphate solubilization, with the rest showing lesser rate, viz. Chaetomium globosum (33.62  5.92 to 69.32  3.21 μg/ mL), Fusarium semitectum (32.64  1.89–57.63  2.11 μg/mL), and Aspergillus versicolor (31.63  2.02–63.72  2.36 μg/mL). The interest in Chaetomium enzymes almost had begun when one of the early researchers developed a method for testing the effectiveness of mildew proofing agents on cotton fabrics in which the fungus, Chaetomium globosum, is used as the test organism (Darwish and Abdel-Azeem 2020). This particular fungus was

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selected because it was found on nearly all outdoor fabrics as one of the most important organisms responsible for the loss of breaking strength of fabrics (Thom et al. 1934). In the 1940s, researchers determined the action of Chaetomium globosum on bleached cotton duck by measuring the changes in breaking strength, weight per square yard, thickness, staple length, fluidity, methylene blue absorption, moisture content, ash content, and rate of evolution of carbon dioxide as an indication of the rate of growth of the organisms on the fabric. After three decades, the interest switched to studying of the cellulolytic system in more detail, such as the effect of temperature on growth and cellulase production in the thermophilic compost fungus Chaetomium thermophile var. dissitum (Eriksen and Goksoyr 1977) and the isolation, taxonomy, and growth rate of the genus Chaetomium Kunze ex Fr. as a wheat straw decomposer for mushroom growth (Chahal and Hawksworth 1976). Later, stored useful books and important documents which were noticed to have moldy appearances were analyzed for isolation of cellulolytic fungi. Several fungi were isolated in pure form and identified, and the genus Chaetomium was the most dominant fungus. Thirteen different Chaetomium species were undertaken for screening of their cellulase-producing capability by the filter paper degradation ability (Yadav and Bagool 2015). Recent investigations were more specific in studying new Chaetomium cellulolytic fungal species, enzyme profiles, and genotypes of Chaetomium isolates, and isolation and screening of other Chaetomium enzymes such as L-methioninase, laccase, polysaccharide monooxygenase (PMO), β-1,3-glucanase, dextranase, pectinolytic, lipolytic, amylolytic, proteolytic, and chitinolytic and new classes of cellulose-degrading enzymes and synergistic enzyme systems (Abdel-Azeem et al. 2016a; Benhassine et al. 2016; Chen et al. 2018; Coronado-Ruiz et al. 2018; Hamed et al. 2016; Wanmolee et al. 2016). Based on the abovementioned data that emphasize the enduring interest and importance of fungal enzymes for sustainability, Chap. 5 in this book is focused on presenting various enzymes produced by Chaetomium species and their miscellaneous applications.

1.2.11 Antioxidant Compounds from Endophytic Chaetomium Recently, the genus Chaetomium has received attention as a rich source producing more than 200 small secondary metabolite compounds with diverse bioactivities, such as antitumor, phytotoxicity on numerous plants, immunomodulatory, antifungal, nematocidal, antimalarial, enzyme inhibitory, antibiotic, and other activities which have significance for drug development (Hu et al. 2018; Soytong et al. 2001). Chaetomium species can be antagonistic against various soil microorganisms and plant pathogens. Chaetoglobosins are well known for their robust cytotoxic

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bioactivity and potential pharmaceutical significance. Chaetoglobosins are grouped in the cytochalasin family of natural products and are actually polyketide derivatives found in fungi. They have unique biochemical property of binding eukaryotic actin proteins, disturbing the normal actin network in the cell. To date, more than eighty chaetoglobosins have been reported from different genera of filamentous fungi, including species of the genus Chaetomium (Wang et al. 2017). Chaetomium globosum CDW7, an endophyte from Ginkgo biloba, exhibited strong inhibitory antifungal activity against phytopathogens such as Fusarium graminearum, Rhizoctonia solani, Magnaporthe grisea, Pythium ultimum, and Sclerotinia sclerotiorum both in vitro and in vivo. Attia et al. (2020) studied the production of antimicrobial and extracellular enzymes and antioxidants by endophytic teleomorphic Ascomycota associated with medicinal plants. A total of 11 teleomorphic species were isolated from 4 medicinal plant species in Saint Katherine Protectorate in Egypt. Chaetomium grande and Sordaria fimicola were the most frequently isolated species and are represented by 12 (Chg1–Chg12) and 7 (Sf1–Sf7) isolates, respectively. In vitro, the antioxidant activity of the extracts was investigated using DPPH radical scavenging assay, and equal to 0.06% and 0.39%, respectively, in the extract of both taxa. In their recent study Darwish et al. (2020) documented the recent studies concerning antioxidants from the genus Chaetomium.

1.3

Conclusion

In order to achieve the goal of more mycological knowledge brought into use, for a more sustainable world of tomorrow, where the bioeconomy becomes an important pillar for our global society, we need fungi to be recognized with heightened visibility. They need to be higher up on global agendas. One way towards that goal could be to position mycology as a candidate for an Organisation de Cooperation et de Développement Économiques (OECD) Excellency Program. This could pave the way for increased (national and international) funding of international collaboration, increased global visibility, and hopefully higher priority among decision makers all over the world. We hope mycologists, and the mycological associations, will work together towards realizing this vision. Acknowledgment The authors are grateful to Prof. Magda M. Hagras, Vice President for Graduate Studies and Research, Suez Canal University, Ismailia 41522, Egypt, for her support and constant encouragement.

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References Abdel-Azeem AM, Salem FM (2012) Biodiversity of laccase producing fungi in Egypt. Mycosphere 3(5):900–920 Abdel-Azeem MA, Abdel-Aziz DM, Salem FM, Abdel-Azeem AM (2015) Surveying of Egyptian endophytic fungi for production of some pharmaceutical and industrial enzymes. 1st Scientific Forum for Student Research, Faculty of Science, Suez Canal University, Ismailia, Egypt. Abstract book 24 Abdel-Azeem AM, Gherbawy YA, Sabry AM (2016a) Enzyme profiles and genotyping of Chaetomium globosum isolates from various substrates. Plant Biosyst 150(3):420–428 Abdel-Azeem AM, Zaki SM, Khalil WF, Makhlouf NA, Farghaly LM (2016b) Anti-rheumatoid activity of secondary metabolites produced by endophytic Chaetomium globosum. Front Microbiol 7(1477):1–11 Abdel-Azeem AM, Omran MA, Mohamed RA (2018) Evaluation of the curative probability of bioactive metabolites from endophytic fungi isolated from some medicinal plants against paracetamol-induced liver injury in mice. LAP LAMBERT Academic Publishing. isbn:978613-9-89820-6 Abdel-Azeem AM, Abdel-Azeem MA, Khalil WF (2019) Endophytic fungi as a new source of antirheumatoid metabolites. In: Watson RR, Preedy VR (eds) Bioactive food as dietary interventions for arthritis and related inflammatory diseases. Elsevier, Amsterdam, pp 355–384. https://doi.org/10.1016/B978-0-12-813820-5.00021-0 Abd-ElGawad AM, Rashad YM, Abdel-Azeem AM, Al-Barati SA, Assaeed AM, Mowafy AM (2020) Calligonum polygonoides L. shrubs provide species-specific facilitation for the understory plants in coastal ecosystem. Biology 9(8):232. https://doi.org/10.3390/biology9080232 Abo Nahas HH (2019) Endophytic fungi: a gold mine of antioxidants. Microb Biosyst 4(1):58–79 Alberto RN, Costa AT, Polonio JC, Santos MS, Rhoden SA, Azevedo JL, Pamphile JA (2016) Extracellular enzymatic profiles and taxonomic identification of endophytic fungi isolated from four plant species. Genet Mol Res. https://doi.org/10.4238/gmr15049016 Alkorta I, Garbisu C, Llama MJ, Serra JL (1998) Industrial applications of pectic enzymes: a review. Process Biochem 33:21–28 Almeida MN, Guimaraes VM, Bischoff KM, Falkoski DL, Pereira OL, Goncalves DSPO et al (2011) Cellulases and hemicellulases from endophytic Acremonium species and its application on sugarcane bagasse hydrolysis. Appl Biochem Biotechnol 165:594–610 Alves Macedo G, Soberón Lozano MM, Pastore GM (2003) Enzymatic synthesis of short chain citronellyl esters by a new lipase from Rhizopus sp. Electron J Biotechnol 6:3–4 Amrita R, Nancy K, Namrata P, Sourav B, Arijit D, Subbaramiah SR (2012) Enhancement of protease production by Pseudomonas aeruginosa isolated from dairy effluent sludge and determination of its fibrinolytic potential. Asian Pac J Trop Biomed 2(3):S1845–S1851 Arora DS, Sharma RK (2010) Ligninolytic fungal laccases and their biotechnological applications. Appl Biochem Biotechnol 160:1760–1788 Attia EA, Singh BP, Dashora K, Abdel-Azeem AM (2020) A potential antimicrobial, extracellular enzymes, and antioxidants resource: endophytic fungi associated with medicinal plants. Int J Biosci 17(1):119–132 Balbool BA, Abdel-Azeem A (2020) Diversity of the culturable endophytic fungi producing L-asparaginase in arid Sinai, Egypt. Italian J Mycol 49:8–24 Benhassine S, Kacem CN, Destain J (2016) Production of laccase without inducer by Chaetomium species isolated from Chettaba forest situated in the east of Algeria. Afr J Biotechnol 15 (7):207–213. https://doi.org/10.5897/AJB2015.15001 Benjamin S, Pandey A (1998) Candida rugosa lipases: molecular biology and versatility in biotechnology. Yeast 14:1069–1087 Bezerra JDP, Santos MGS, Svedese VM, Lima DMM, Fernandes MJS, Paiva LM et al (2012) Richness of endophytic fungi isolated from Opuntia ficus-indica Mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 28:1989–1995

26

A. M. Abdel-Azeem et al.

Bhagobaty RK, Joshi SR (2012) Enzymatic activity of fungi endophytic on five medicinal plant species of the pristine sacred forests of Meghalaya, India. Biotechnol Bioprocess Eng 17:33–40 Bischoff KM, Wicklow DT, Jordan DB, de Rezende ST, Liu S, Hughes SR et al (2009) Extracellular Hemicellulolytic enzymes from the maize endophyte Acremonium zeae. Curr Microbiol 58:499–503 Borges W, Borges K, Bonato P, Said S, Pupo M (2009) Endophytic fungi: natural products, enzymes and biotransformation reactions. Curr Org Chem 13:1137–1163 Breen A, Singleton FL (1999) Fungi in lignocelluloses breakdown and biopulping. Curr Opin Biotechnol 10:252–258 Brenna O, Bianchi E (1994) Immobilized laccase for phenolic removal in must and wine. Biotechnol Lett 16:35–40 Brühlmann F, Leupin M, Erismann KH, Fiechter A (2000) Enzymatic degumming of ramie bast fibers. J Biotechnol 76(1):43–50 Burhan A, Nisa U, Gokhan C, Omer C, Ashabil A, Osman G (2003) Enzymatic properties of a novel thermostable, thermophilic, alkaline and chelator resistant amylase from an alkalophilic Bacillus sp. isolate ANT-6. Process Biochem 38:1397–1403 Burton S (2003) Laccases and phenol oxidases in organic synthesis. Curr Org Chem 7:1317–1331 Cantarelli C, Brenna O, Giovanelli G, Rossi M (1989) Beverage stabilization through enzymatic removal of phenolics. Food Biotechnol 3:203–214 Carlsen M, Nielsen J (2001) Influence of carbon source on alpha amylase production in Aspergillus oryzae. Appl Microbiol Biotechnol 57:346–349 Ceci L, Lozano JE (1998) Determination of enzymatic activities of commercial pectinases for the clarification of apple juice. Food Chem 61:237–241 Chadha N, Mishra M, Rajpal K, Bajaj R, Choudhary DK, Varma A (2015) An ecological role of fungal endophytes to ameliorate plants under biotic stress. Arch Microbiol 197:869–881 Chahal DS, Hawksworth DL (1976) Chaetomium cellulolyticum, a new thermotolerant and cellulolytic Chaetomium. I. Isolation, description and growth rate. Mycologia 68(3):600–610. https:// doi.org/10.1103/PhysRevB.46.4681 Chao YP, Xie FH, Yang J et al (2007) Screening for a new Streptomyces strain capable of efficient keratin degradation. J Environ Sci 19:1125–1128 Chen HY, Xue DS, Feng XY, Yao SJ (2011) Screening and production of ligninolytic enzyme by a marine derived fungal Pestalotiopsis sp. J63. Appl Biochem Biotechnol 165:1754–1769 Chen Y, Wang HW, Li L, Dai CC (2013) The potential application of the endophyte Phomopsis liquidambari to the ecological remediation of long term cropping soil. Appl Soil Ecol 67:20–26 Chen C, Chen J, Geng Z, Wang M, Liu N, Li D (2018) Regioselectivity of oxidation by a polysaccharide monooxygenase from Chaetomium thermophilum. Biotechnol Biofuels 11 (1):1–16. https://doi.org/10.1186/s13068-018-1156-2 Coronado-Ruiz C, Avendaño R, Escudero-Leyva E, Conejo-Barboza G, Chaverri P, Chavarría M (2018) Two new cellulolytic fungal species isolated from a 19th-century art collection. Sci Rep 8(1):1–9. https://doi.org/10.1038/s41598-018-24934-7 Costa-Silva TA, Souza CRF, Oliveira WP, Said S (2014a) Characterization and spray drying of lipase produced by the endophytic fungus Cercospora kikuchii. Braz J Chem Eng 31:849–858 Costa-Silva TA, Souza CRF, Oliveira WP, Said S (2014b) Characterization and spray drying of lipase produced by the endophytic fungus Cercospora kikuchii. Braz J Chem Eng 31:849–858 Coughlan MP, Hazlewood GP (1993) Beta-1, 4-d-xylan degrading enzyme systems: biochemistry molecular biology and applications. Biotechnol Appl Biochem 17(3):259–289 Dai J, Krohn K, Floerke U et al (2006) Metabolites from the endophytic fungus, Nodulisporium sp. from Juniperus cedre. Eur J Org Chem 15:3506–3498 Darwish AMG, Abdel-Azeem AM (2020) Chaetomium enzymes and their applications. In: AbdelAzeem AM (ed) Recent developments on genus Chaetomium, fungal biology. Springer Nature, Switzerland AG, pp 241–249 Darwish AMG, Abdelmotilib NM, Abdel-Azeem AM, Abo Nahas HH, Mohesien MT (2020) Applications of Chaetomium functional metabolites with special reference to antioxidants. In:

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

27

Abdel-Azeem AM (ed) Recent developments on genus Chaetomium, fungal biology. Springer Nature, Switzerland AG, pp 227–240 Demain AL, Adrio JL (2008) Contributions of microorganisms to industrial biology. Mol Biotechnol 38:41–55 Devi NN, Prabakaran JJ, Wahab F (2012) Phytochemical analysis and enzyme analysis of endophytic fungi from Centella asiatica. Asian Pac J Trop Biomed 2(3):S1280–S1284 Devi R, Kaur T, Guleria G, Rana K, Kour D, Yadav N et al (2020a) Fungal secondary metabolites and their biotechnological application for human health. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 147–161. https://doi.org/10.1016/ B978-0-12-820528-0.00010-7 Devi R, Kaur T, Kour D, Rana KL, Yadav A, Yadav AN (2020b) Beneficial fungal communities from different habitats and their roles in plant growth promotion and soil health. Microb Biosyst 5:21–47. https://doi.org/10.21608/mb.2020.32802.1016 Diaz MJC, Rodriguez JA, Roussos S, Cordova J, Abousalham A, Carriere F et al (2006) Lipase from the thermotolerant fungus Rhizopus homothallicus is more thermostable when produced using solid-state fermentation than liquid fermentation procedures. Enzym Microb Technol 39:1042–1050 Duran N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Cataly Env 28:83–99 El Gueddari NE, Rauchhaus U, Moerschbacher BM, Deising HB (2002) Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol 156:103–112 El-Bondkly AMA (2012) Molecular identification using ITS sequences and genome shuffling to improve 2-deoxyglucose tolerance and xylanase activity of marine-derived fungus, Aspergillus sp. NRCF5. Appl Biochem Biotechnol 167:2160–2173 El-Gendy MM (2010) Keratinase production by endophytic Penicillium spp. Morsy 1 under solid state fermentation using rice straw. Appl Bioche Biotechnol 162:780–794 El-Zayat SA (2008) Preliminary studies on laccase production by Chaetomium globosum an endophytic fungus in Glinus lotoides. Am Eurasian J Agric Environ Sci 3:86–90 Eriksen J, Goksoyr J (1977) Cellulases from Chaetomium thermophile var. dissitum. Eur J Biochem 77:445–450 Gan ZW, Yang JK, Tao N, Yu ZF, Zhang KQ (2007) Cloning and expression analysis of a chitinase gene Crchi1 from the mycoparasitic fungus Clonostachys rosea (syn. Gliocladium roseum). J Microbiol 45:422–430 Gianfreda L, Xu F, Bollag JM (1999) Laccases a useful group of oxidoreductive enzymes. Biorem J 3(1):1–25 Gilbert M, Yaguchi M, Watson DC, Wong KKY, Breuil C, Saddler JN (1993) A comparison of two xylanases from the thermophilic fungi Thielavia terrestris and Thermoascus crustaceus. Appl Microbiol Biotechnol 40:508–514 Godfrey T, West S (1996) Textiles. In: Godfrey T, West S (eds) Industrial enzymology, 2nd edn. MacMillan Press, London, UK, pp 360–371 Gopinath SCB, Anbu P, Hida A (2005) Extracellular enzymatic activity profiles in fungi isolated from oil rich environments. Mycoscience 46:119–126 Grünig CR, Duò A, Sieber TN, Holdenrieder O (2008) Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii sl- Acephala applanata species complex. Mycologia 100:47–67 Hamed SR, Abo Elsoud MM, Mahmoud MG, Asker MMS (2016) Isolation, screening and statistical optimizing of L-methioninase production by Chaetomium globosum. Afr J Microbiol Res 10(36):1513–1523. https://doi.org/10.5897/AJMR2016.8132 Harnpicharnchai P, Champreda V, Sornlake W, Eurwilaichitr L (2009) A thermotolerant betaglucosidase isolated from an endophytic fungi, Periconia sp., with a possible use for biomass conversion to sugars. Protein Expr Purif 67(2):61–69

28

A. M. Abdel-Azeem et al.

Hendriksen HV, Pedersen S, Bisgard-Frantzen H (1999) A process for textile warp sizing using enzymatically modified starches. Patent Application WO 99:35325 Hesham AE-L, Kaur T, Devi R, Kour D, Prasad S, Yadav N et al (2021) Current trends in microbial biotechnology for agricultural sustainability: conclusion and future challenges. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 555–572. https://doi.org/10.1007/978-981-15-6949-4_22 Hmidet N, El-Hadj Ali N, Haddar A et al (2009) Alkaline proteases and thermostable amylase co-produced by Bacillus licheniformis NH1: characterization and potential application as detergent additive. Biochem Eng J 47:71–79 Howard RL, Abotsi E, Rensberg EL, Howard S (2003) Lignocellulose biotechnology: issues of bioconversion and enzyme production. Afr J Biotechnol 2(12):602–619 Hu Y, Hao X, Chen L, Akhberdi O, Yu X, Liu Y, Zhu X (2018) Gα-cAMP/PKA pathway regulates pigmentation, chaetoglobosin a biosynthesis and sexual development in Chaetomium globosum. PLoS One 13(4):1–18. https://doi.org/10.1371/journal.pone.0195553 Hyde KD, Xu J, Rapior S et al (2019) The amazing potential of fungi: 50 ways we can exploit fungi industrially. Fungal Divers 97:1–136. https://doi.org/10.1007/s13225-019-00430-9 Illmer PA, Barbato A, Schinner F (1995) Solubilization of hardly soluble AlPO4 with P-solubilizing microorganisms. Soil Biol Biochem 27:260–270 Jaeger KE, Reetz MT (1998) Microbial lipases form versatile tools for biotechnology. Trends Biotechnol 16:396–403 Jain P, Aggarwal V, Sharma A, Pundir RK (2012) Isolation, production and partial purification of protease from an endophytic Acremonium sp. J Agric Technol 8:1979–1989 Jalgaonwala RE, Mahajan RT (2011) Evaluation of hydrolytic enzyme activities of endophytes from some indigenous medicinal plants. J Agric Technol 7:1733–1741 Jaouadi B, Ellouz-Chaabouni S, Rhimi M et al (2008) Biochemical and molecular characterization of a detergent-stable serine alkaline protease from Bacillus pumilus CBS with high catalytic efficiency. Biochimie 90:1291–1305 Kanokratana P, Chantasingh D, Champreda V, Tanapongpipat S, Pootanakit K, Eurwilaichitr L (2008) Identification and expression of cellobiohydrolase (CBHI) gene from an endophytic fungus, Fusiccoccum sp. (BCC4124) in Pichia pastoris. Protein Expr Purif 58:148–153 Kashyap DR, Vohra PK, Chopra S, Tewari R (2001) Applications of pectinases in the commercial sector: a review. Bioresour Technol 77:215–227 Kaur T, Devi R, Kour D, Yadav N, Prasad S, Singh A et al (2020) Advances in microbial bioresources for sustainable biofuels production: current research and future challenges. In: Yadav AN, Rastegari AA, Yadav N, Gaur R (eds) Biofuels production – sustainability and advances in microbial bioresources. Springer International Publishing, Cham, pp 371–387. https://doi.org/10.1007/978-3-030-53933-7_17 Kellner H, Luis P, Schlitt B, Buscot F (2009) Temporal changes in diversity and expression patterns of fungal laccase genes within the organic horizon of a brown forest soil. Soil Biol Biochem 41:1380–1389 Khajeh K, Shokri MM, Asghan SM, Moradian F, Ghasemi A (2006) Acidic proteolytic digestion of α-amylase from Bacillus licheniformis and Bacillus amyloliquefaciens: stability and flexibility analysis. Enzyme Microbial Technol 38:422–428 Khan AL, Al-Harrasi A, Al-Rawahi A, Al-Farsi Z, Al-Mamari A, Waqas M et al (2016) Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS One 11:e0158207 Khlifia R, Belbahria L, Woodwarda S, Ellouza M, Dhouiba A, Sayadia S et al (2010) Decolourization and detoxification of textile industry wastewater by the laccase-mediator system. J Hazard Mater 175:802–880 Klemsdal SS, Clarke JL, Hoell IA, Eijsink VG, Brurberg MB (2006) Molecular cloning, characterization, and expression studies of a novel chitinase gene (ech30) from the mycoparasite Trichoderma atroviride strain P1. FEMS Microbiol Lett 256(2):282–289

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

29

Kottwitz B, Upadek H, Carrer G (1994) Application and benefits of enzymes in detergents. Chim Oggi 12:21–24 Kour D, Rana KL, Kaur T, Singh B, Chauhan VS, Kumar A et al (2019a) Extremophiles for hydrolytic enzymes productions: biodiversity and potential biotechnological applications. In: Molina G, Gupta VK, Singh B, Gathergood N (eds) Bioprocessing for biomolecules production, pp 321–372. https://doi.org/10.1002/9781119434436.ch16 Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A et al (2019b) 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/10.1007/978-981-136536-2_13 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA et al (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, Perspective for value-added products and environments, vol 2. Springer International Publishing, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kour D, Kaur T, Devi R, Rana KL, Yadav N, Rastegari AA et al (2020a) Biotechnological applications of beneficial microbiomes for evergreen agriculture and human health. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 255–279. https://doi.org/10.1016/B978-0-12-820528-0.00019-3 Kour D, Kaur T, Yadav N, Rastegari AA, Singh B, Kumar V et al (2020b) Phytases from microbes in phosphorus acquisition for plant growth promotion and soil health. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 157–176. https:// doi.org/10.1016/B978-0-12-820526-6.00011-7 Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V et al (2020c) Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolor 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, Yadav N, Kumar M, Kumar V et al (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 Kumar CG, Takegi H (1999) Microbial alkaline proteases: from a bioindustrial viewpoint. Biotechnol Adv 17:561–594 Maarel V, Vanderveen MJEC, Uietdehaag JCM, Leemhuis JCM, Dijkuhizen L (2002) Properties and applications of starch converting enzymes of the α-amylase family. J Biotechnol 94:137–155 Maat J, Roza M, Verbakel J, Stam H, DaSilra MJS, Egmond MR, Hagemans MLD, VanGarcom RFM, Hessing JGM, VanDerhondel CAMJJ, van Rotterdam C (1992) Xylanases and their application in bakery. In: Visser J, Beldman G, VanSomeren MAK, Voragen AGJ (eds) Xylans and xylanases. Elsevier, Amsterdam, pp 349–360 Maccheroni JRW, Azevedo JL (1998) Synthesis and secretion of phosphatases by endophytic isolates of Colletotrichum musae grown under conditions of nutritional starvation. J Gen Appl Microbiol 44:381–387 Maria GL, Sridhar KR, Raviraja NS (2005a) Antimicrobial and enzyme activity of mangrove endophytic fungi of southwest coast of India. J Agric Technol 1:67–80 Maria GL, Sridhar KR, Raviraja NS (2005b) Antimicrobial and enzyme activity of mangrove endophytic fungi of southwest coast of India. J Agric Technol 1:67–80 Mhatre A, Narwankar R, Rawat A, Tembadmani K, Mishra S (2017) Characterization of endophytic fungi from medicinal plants for application in therapeutic enzyme extraction. In:

30

A. M. Abdel-Azeem et al.

Mishra S, Srinivas C, Singh S, Savant D (eds) Current perspectives in sustainable environment management. SIES Indian Institute of Environment Management, Nerul, pp 230–223 Minussi RC, Pastore GM, Duran N (2002) Potential applications of laccase in the food industry. Trends in Food Scien Technol 13:205–216 Mishra VK, Passari AK, Singh BP (2016) In vitro Antimycotic and biosynthetic potential of fungal endophytes associated with Schima wallichii. In: Kumar P, Gupta VK, Tiwari AK, Kamle M (eds) Current trends in plant disease diagnostics and management practices. Springer International Publishing, Cham, pp 367–381. https://doi.org/10.1007/978-3-319-27312-9_16 Mishra VK, Passari AK, Chandra P, Leo VV, Kumar B, Gupta VK (2017) Determination and production of antimicrobial compounds by Aspergillus clavatonanicus strain MJ31, an endophytic fungus from Mirabilis jalapa L. using UPLC-ESI-MS/MS and TD GC-MS. PLoS One 12(10):1–24 Moilanen U, Osma JF, Winquist E, Leisola M, Couto SR (2010) Decolorization of simulated textile dye baths by crude laccases from Trametes hirsute and Cerrena unicolor. Eng Life Sci 10 (3):1–6 Mondal S, Halder SK, Yadav AN, Mondal KC (2020) Microbial consortium with multifunctional plant growth promoting attributes: future perspective in agriculture. In: Yadav AN, Rastegari AA, Yadav N, Kour D (eds) Advances in plant microbiome and sustainable agriculture, Functional annotation and future challenges, vol 2. Springer, Singapore, pp 219–254. https:// doi.org/10.1007/978-981-15-3204-7_10 Moore D, Robson G, Trinci T (2011) 21st century guidebook to fungi. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511977022 Morozova OV, Shumakovich GP, Shleev SV, Yaropolov YI (2007) Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol 43(5):523–535 Mouchacca J (1995) Thermophilic fungi in desert soils: a neglected extreme environment. CAB INTERNATIONAL, Wallingford, pp 265–288 Mouchacca J (1997) Thermophilic fungi: biodiversity and taxonomic status. Cryptogam Mycol 18:19–69 Murthy PS, Naidu MM (2011) Improvement of robusta coffee fermentation with microbial enzymes. Eur J Appl Sci 3(4):130–139 Nahas E (1996) Factors determining rock phosphate solubilization by microorganism isolated from soil. World J Microb Biot 12:18–23 Nielsel RI, Oxenboll K (1998) Enzymes from fungi: their technology and uses. Mycologist 12:69–71 Nigam P, Singh D (1995) Enzymes and microbial enzymes involved in starch processing enzymes. Microbial Technol 17:770–778 Oliveira ACD, Fernades ML, Mariano AB (2014) Production and characterization of an extracellular lipase from Candida guilliermondii. Braz J Microbiol 45(4):1503–1511 Oses R, Valenzuela S, Freer J, Baeza J, Rodríguez J (2006) Evaluation of fungal endophytes for lignocellulolytic enzyme production and wood biodegradation. Int Biodeterior Biodegradation 57:129–135 Paice MG, Gurnagul N, Page DH, Jurasek L (1992) Mechanism of hemicellulose-directed prebleaching of Kraft pulps. Enzym Microb Technol 14:272–276 Parvez S, Kang M, Chung H, Cho C, Hong M, Shin M et al (2006) Survey and mechanism of skin depigmenting and lightening agents. Phytother Res 20:921–934 Peng XW, Chen HZ (2007) Microbial oil accumulation and cellulase secretion of the endophytic fungi from oleaginous plants. Ann Microbiol 57:239 Pilz R, Hammer E, Schauer F, Krag U (2003) Laccase catalyzed synthesis of coupling products of phenolic substrates in different reactors. Appl Microbiol Biotechnol 60:708–712 Prade RA (1996) Xylanases: from biology to biotechnology. Biotechnol Genet Eng Rev 13:101–132 Prasad S, Malav LC, Choudhary J, Kannojiya S, Kundu M, Kumar S et al (2021) Soil microbiomes for healthy nutrient recycling. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

31

microbial biotechnology for sustainable agriculture. Springer Singapore, Singapore, pp 1–21. https://doi.org/10.1007/978-981-15-6949-4_1 Pritchard PE (1992) Studies on the bread-improving mechanism of fungal alpha-amylase. J Biol Educ 26:12–18 Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN et al (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, Switzerland, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V et al (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 International Publishing, 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 Randelli A, Daroit DJ, Riffel A (2010) Biochemical features of microbial keratinases and their production and applications. Appl Microbiol Biotechnol 85:1735–1750 Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62:597–635 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/B978-0-44463504-4.00002-5 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/B978-0444-63504-4.00004-9 Robl D, Delabona PS, Santos Costa P, de Silva LJ, Rabelo C, Pinmentel IC (2013) Xylanase production by endophytic Aspergillus niger using pentose rich hydrothermal liquor from sugarcane bagasse. Biocatal Biotransformation 33(3):1–13 Rosana C, Minussi Y, Pastore GM, Durany N (2002) Potential applications of laccase in the food industry. Trends in Food Sci Technol 13:205–216 Sahay H, Yadav AN, Singh AK, Singh S, Kaushik R, Saxena AK (2017) Hot springs of Indian Himalayas: potential sources of microbial diversity and thermostable hydrolytic enzymes. 3. Biotech 7:1–11 Satyanarayana T, Rao JLUM, Ezhilvannan M (2005) α-Amylases. In: Pandey A, Webb C, Soccol CR, Larroche C (eds) Enzyme technology. Asia Tech Publishers, New Delhi, India, pp 189–220 Savitha S, Sadhasivam S, Swaminathan K et al (2011) Fungal protease: production, purification and compatibility with laundry detergents and their wash performance. J Taiwan Inst Chem Eng 42:298–304 Saxena AK, Padaria JC, Gurjar GT, Yadav AN, Lone SA, Tripathi M et al. (2020) Insecticidal formulation of novel strain of Bacillus thuringiensis AK 47. Indian Patent 340541. Sharma VP, Singh S, Dhanjal DS, Singh J, Yadav AN (2021) Potential strategies for control of agricultural occupational health hazards. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 387–402. https://doi.org/10.1007/978-981-15-6949-4_16 Shubha J, Srinivas C (2017) Diversity and extracellular enzymes of endophytic fungi associated with Cymbidium aloifolium L. Afr J Biotechnol 16:2248–2258 Sim YC, Lee SG, Lee DC et al (2000) Stabilization of papain and lysozyme for application to cosmetic products. Biotechnol Lett 22:137–140 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore

32

A. M. Abdel-Azeem et al.

Singh RN, Gaba S, Yadav AN, Gaur P, Gulati S, Kaushik R et al (2016) First, high quality draft genome sequence of a plant growth promoting and cold active enzymes producing psychrotrophic Arthrobacter agilis strain L77. Stand Genomic Sci 11:54. https://doi.org/10. 1186/s40793-016-0176-4 Sorgatto M, Guimarães NCA, Zanoelo FF, Marques MR, Peixoto-Nogueira SC, Giannesi GG (2012) Purification and characterization of an extracellular xylanase produced by the endophytic fungus, Aspergillus terreus, grown in submerged fermentation. Afr J Biotechnol 11:8076–8084 Soytong K, Kanokmedhakul S, Kukongviriyapa V, Isobe M (2001) Application of Chaetomium species (Ketomium) as a new broad spectrum biological fungicide for plant disease control: a review article. Fungal Divers 7:1–5 Sun X, Guo LD, Hyde KD (2011) Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47:85–95. https://doi.org/10.1007/s13225-0100086-5 Sunitha VH, Ramesha A, Savitha J, Srinivas C (2012) Amylase production by endophytic fungi Cylindrocephalum sp. isolated from medicinal plant Alpinia calcarata (Haw.) Roscoe. Braz J Microbiol 43:1213 Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Gopalan V (2012) Fungal endophytes: an untapped source of biocatalysts. Fungal Divers 54:19–30 Thom C, Humfeld H, Holman HP (1934) Laboratory tests for mildew resistance of outdoor cotton fabrics. Amer Dyestuff Rptr Illus 23(581):586 Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26 Tiwari K (2015) The future products: endophytic fungal metabolites. J Biodivers Biopros Dev 2:214–2376 Torres M, Dolcet MM, Sala N, Canela R (2003) Endophytic fungi associated with Mediterranean plants as a source of mycelium bound lipases. J Agric Food Chem 51(11):3328–3333 Uzma F, Hashem A, Murthy N, Mohan HD, Kamath PV, Singh BP (2018) Endophytic fungi— alternative sources of cytotoxic compounds: a review. Front Pharmacol 9(309):1–37 Vandevivere PC, Bianchi R, Verstraete W (1998) Treatment and reuse of wastewater from the textile wet-processing industry: review of emerging technologies. J Chem Technol Biotechnol 72:289–302 Venkatesagowda B, Ponugupaty E, Barbosa AM, Dekker RFH (2012) Diversity of plant oil seed associated fungi isolated from seven oil-bearing seeds and their potential for the production of lipolytic enzymes. World J Microbiol Biotechnol 28:71–80 Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK (2015a) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899 Verma P, Yadav AN, Shukla L, Saxena AK, Suman A (2015b) Alleviation of cold stress in wheat seedlings by Bacillus amyloliquefaciens IARI-HHS2-30, an endophytic psychrotolerant K-solubilizing bacterium from NW Indian Himalayas. Natl J Life Sci 12:105–110 Verma P, Yadav AN, Shukla L, Saxena AK, Suman A (2015c) Hydrolytic enzymes production by thermotolerant Bacillus altitudinis IARI-MB-9 and Gulbenkiania mobilis IARI-MB-18 isolated from Manikaran hot springs. Int J Adv Res 3:1241–1250 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 Vignardet C, Guillaume YC, Michel L, Friedrich J, Millet J (2001) Comparison of two hard keratinous substrates submitted to the action of a keratinase using an experimental design. Int J Pharm 224:115–122 Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium sp. closely associated with wheat roots. Biol Fertil Soils 40:36–43

1 Biodiversity and Ecological Perspective of Industrially Important Fungi. . .

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Wang JW, Wu JH, Huang WY, Tan RX (2006) Laccase production by Monotospora sp., an endophytic fungus in Cynodon dactylon. Bioresour Technol 97(5):786–789 Wang F, Jiang J, Hu S, Ma H, Zhu H, Tong Q, Zhang Y (2017) Secondary metabolites from endophytic fungus Chaetomium sp. induce colon cancer cell apoptotic death. Fitoterapia 121 (2016):86–93. https://doi.org/10.1016/j.fitote.2017.06.021 Wanmolee W, Sornlake W, Rattanaphan N, Suwannarangsee S, Laosiripojana N, Champreda V (2016) Biochemical characterization and synergism of cellulolytic enzyme system from Chaetomium globosum on rice straw saccharification. BMC Biotechnol 16(1):1–12 Yadav AN (2020) Recent trends in mycological research, volume 1: agricultural and medical perspective. Springer, Switzerland Yadav LS, Bagool RG (2015) Original research article isolation and screening of cellulolytic Chaetomium sp. from deteriorated paper samples. Int J Curr Microbiol Appl Sci 4(8):629–635 Yadav AN, Verma P, Sachan SG, Kaushik RK, Saxena AK (2015) Psychrotrophic microbes: diversity analysis and bioprospecting for industry and agriculture. In: 85th annual session of NASI & the symposium on “marine and fresh water ecosystems for National Development”, pp 1–2 Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016a) Cold active hydrolytic enzymes production by psychrotrophic Bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56:294–307 Yadav AN, Sachan SG, Verma P, Saxena AK (2016b) Bioprospecting of plant growth promoting psychrotrophic Bacilli from cold desert of north western Indian Himalayas. Indian J Exp Biol 54:142–150 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N et al (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 et al (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, Kour D, Sharma S, Sachan SG, Singh B, Chauhan VS et al (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, Rhizobacteria in abiotic stress management, vol 1. Springer Singapore, Singapore, pp 219–253. https://doi.org/10.1007/978981-13-6536-2_12 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 International Publishing, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020b) Agriculturally important fungi for sustainable agriculture, volume 2: functional annotation for crop protection. Springer International Publishing, Cham Yadav AN, Rastegari AA, Yadav N, Gaur R (2020c) Biofuels production – sustainability and advances in microbial bioresources. Springer, Cham Yadav AN, Singh J, Singh C, Yadav N (2021) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore Yaropolov AI, Skorobogatko OV, Vartanov SS, Varfolomeyev SD (1994) Laccase: properties, catalytic mechanism and applicability. Appl Biochem Biotechnol 49:257–280 Zaferanloo B, Bhattacharjee S, Ghorbani MM, Mahon n PJ, Palombo EA (2014) Amylase production by Preussia minima, a fungus of endophytic origin: optimization of fermentation conditions and analysis of fungal secretome by LC-MS. BMC Microbiol 14:5.

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Zaidi KU, Ali AS, Ali SA, Naaz I (2014) Microbial tyrosinases: promising enzymes for pharmaceutical, food bioprocessing, and environmental industry. Biochem Res Int 2014 Zambare V, Nilegaonkar S, Kanekar P (2011) A novel extracellular protease from Pseudomonas aeruginosa MCM B-327: enzyme production and its partial characterization. New Biotechnol 28:173–181

Chapter 2

Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants, and Potential Applications Uma Singh, Ovaid Akhtar, Rani Mishra, Ifra Zoomi, Harbans Kaur Kehri, and Dheeraj Pandey

Contents 2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Biodiversity of AM Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1 Biodiversity of AM Fungi in Alpine and Temperate Region . . . . . . . . . . . . . . . . . . . . . 2.2.2 Biodiversity of AM Fungi in Tropical Region . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3 Biodiversity of AM Fungi in Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4 Biodiversity of AM Fungi in Mangrove . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.5 Biodiversity of AM Fungi in HM-Contaminated Soils and Mining Fields . . . . . . . 2.2.6 Biodiversity of AM Fungi in Acidic Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.7 Biodiversity of AM Fungi in Alkaline Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.8 Biodiversity of AM Fungi in Saline Soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Interaction Between AM Fungi and Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1 Pre-symbiotic Phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2 Symbiotic Phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.3 Arbuscules: The Symbiotic Interface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.4 Common Mycorrhizal Network (CMN) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Application of AM Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.1 Application of AM Fungi Alleviates Water Stress in Plants . . . . . . . . . . . . . . . . . . . . . . 2.4.2 Application of AM Fungi Alleviates Salt Stress in Plants . . . . . . . . . . . . . . . . . . . . . . . . 2.4.3 Application of AM Fungi Alleviates Cold Stress in Plants . . . . . . . . . . . . . . . . . . . . . . . 2.4.4 Application of AM Fungi Improves the Phytoremediation of HM-Contaminated Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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U. Singh · I. Zoomi · H. K. Kehri · D. Pandey Sadasivan Mycopathology Laboratory, Department of Botany, University of Allahabad, Allahabad, India O. Akhtar (*) Department of Botany, Kamla Nehru Institute of Physical and Social Sciences, Sultanpur, India R. Mishra Department of Botany, Rashtriya Kisan Post Graduate College, Shamli, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. M. Abdel-Azeem et al. (eds.), Industrially Important Fungi for Sustainable Development, Fungal Biology, https://doi.org/10.1007/978-3-030-67561-5_2

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2.4.5 Application of AM Fungi Enhances Sustainable Agriculture Production . . . . . . . . 2.4.6 Application of AM Fungi Controls the Plant Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2.1

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Introduction

Arbuscular mycorrhizal (AM) fungi are important part and parcel of soil microbial ecosystems. AM fungi belong to the phylum Glomeromycota (Kehri et al. 2018; Kour et al. 2019b). They are symbiotically associated with the roots of land plants. The benefits of AM association to plants are limited not only to better nutrient uptake and access of water beyond the depletion zone, but also enhanced defense system against various biotic and abiotic stresses. Biologically AM fungi have intraradical (Fig. 2.1a–c) and extraradical phases (Fig. 2.1a–c). Intraradical phases are rootcolonizing structures. These include intraradical hyphae, spores, vesicles (Fig. 2.1a), hyphal coils (Fig. 2.1b), and arbuscules (Fig. 2.1c). Vesicle is however not reported in all AM fungi. Extraradical phase represents the AM fungal structure found outside the root in the soil (Fig. 2.1d). These include ramified hyphae, spores, and auxiliary cells. Auxiliary cells in the soils are characteristics of AM fungi lacking intraradical vesicles. Some commonly reported and taxonomically well-defined AM fungal genera are Glomus, Acaulospora, Gigaspora, Scutellospora, Entrophospora, etc. (Yadav et al. 2020b). Spores in nutshell have been utilized for identification and naming purposes. Some of the common spores of AM fungi are presented in Fig. 2.1e–j. Origin of AM fungi is traced back to the Devonian period (400 million years ago) probably since the evolution of the first land plant. Since then, AM fungi have been coevolving with the land plants and most of the plants, strictly speaking, “do not have roots, they have mycorrhiza.” AM fungi are associated with more than 72% of the land plants (Brundrett and Tedersoo 2018) and are distributed throughout the globe. Till date a total of 19 genus and 237 species of AM fungi have been identified, mentioned, and maintained at the world’s largest culture collection of AM fungi namely, The International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi (INVAM) accessed at https://invam.wvu.edu/. Since the origin of AM fungi, these are not much diversified as compared to the other soil fungi. However, they have established strong association with plants under various geoclimatic conditions in different biomes. The diversity of AM fungi is assessed in two ways: (i) by studying the AM fungal spores associated with the roots of plant and (ii) direct amplification of partial ribosomal RNA sequence from the host root or soils. Both the methods have their own pros and cons. Former method takes the advantage of AM spore extraction and identification by the method summarized by Kehri and Akhtar (2018). By employing either of the techniques, researchers have studied the diversity of AM fungi from various biomes on the earth. By isolation, establishment of culture in suitable host and also through the root-transformation

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Fig. 2.1 (a) Intraradical AM fungal structure showing vesicles and spores, (b) hyphal coils in the cortical cells, (c) an arbuscule, (d) AM-colonized root showing extraradical mycelium, (e) single spore of Funneliformis mosseae, (f) single spore of Gigaspora, (g) spore of Acaulospora scrobiculata with sporiferous saccule, (h) sporocarp of Rhizophagus fasciculatus, (i) broken sporocarp of Glomus sinuosum, (j) spore aggregates of Glomus aggregatum. Bar ¼ 100 μm (for a–d) and 20 μm (for e–j)

interaction between the AM fungi and plants has been studied extensively. The diversity of AM fungi in various biomes, their interaction with plants, and application have been summarized in the coming section of this chapter.

2.2 2.2.1

Biodiversity of AM Fungi Biodiversity of AM Fungi in Alpine and Temperate Region

Alpine region approximately expands 190,700 km2 and covers eight European countries, Italy, Austria, France, Germany, Liechtenstein, Slovenia, Monaco, and Switzerland, and India. It represents high altitude generally above 3600 m, where

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trees do not grow longer. It is suitable for vegetation mostly in stunted form due to extreme cold climate and is dominant by low shrubs, such as Rhododendron anthopogon, R. arboreum, R. campanulatum, R. barbatum, R. lepidotum, Catharanthus roseus, Ocimum sp., Asparagus racemosus, Stipa purpurea, Leontopodium nanum, and Potentilla bifurca (Rastegari et al. 2020a; Singh et al. 2020; Yadav et al. 2018b). Diversity of AM fungi associated with various plants growing in alpine region has been studied by various researchers. AM-colonizing plants along with their families from alpine biome are presented in Table 2.1. Another important terrestrial ecosystem is the temperate region (means moderate). Geographically, this region is situated between subtropics and polar circles. Average yearly temperatures in these regions are not extreme, neither burning hot nor freezing cold. Annual rainfall is 81 cm. Unlike in the tropics, temperature can change greatly between summers and winters. This region is suitable for vegetation such as Asparagus racemosus, Catharanthus roseus, Helianthus sp., and Ocimum sp.. Several plants of temperate region are found to be associated with AM fungi, which are listed in Table 2.1. Chaurasia et al. (2005) reported five different types of AM fungal genera, viz., Acaulospora, Gigaspora, Glomus, Sclerocystis, and Scutellospora in rhizospheric soil of plants, e.g., Rhododendron anthopogon, R. arboreum, R. campanulatum, R. barbatum, R. lepidotum, Catharanthus roseus, Ocimum sp., and Asparagus racemosus from Kumaun region, Central Himalaya. They have found Glomus as the most dominant AM fungi. Sharma et al. (2008) reported AM fungal spores from Haryana, India. AM fungal spores, viz., Glomus mosseae, G. fasciculatum, G. geosporum, G. macrocarpum, G. scintillans, G. diaphanum, and G. versiforme, were isolated from the rhizospheric soil of sunflower. Sharma et al. (2009a, b) reported AM fungal spores from Haryana, India. AM fungal species, viz., Acaulospora laevis, A. foveata, A. rehmii, A. scrobiculata, A. bireticulata, A. lacunose, and A. gerdemannii, were isolated from the rhizospheric soil of sunflower. Gaur and Kaushik (2011) collected rhizospheric soil and root samples of different medicinal plants, viz., Asparagus racemosus, Catharanthus roseus, and Ocimum sp., for the study of AM fungal association from different districts of Uttarakhand (Haridwar, Pauri Garhwal, Almora, Dehradun, and Udham Nagar). They have isolated 16 species of AM fungi from the rhizospheric soil of these plants. 50% of AM fungi species belonged to the Glomus: Glomus aggregatum, G. mosseae, G. fasciculatum, G. coronatum, G. intraradices, G. claroideum, G. geosporum, G. monosporum, and G. etunicatum. Gigaspora rosea, G. margarita, G. gigantea, Sclerocystis sinuosa, Acaulospora scrobiculata, and Acaulospora laevis were isolated from rhizospheric soil of Catharanthus roseus while Glomus aggregatum and G. fasciculatum were predominantly present in Ocimum sp. Glomus etunicatum, G. mosseae, G. fasciculatum, G. coronatum, Gigaspora margarita, G. gigantea, Sclerocystis sinuosa, and Acaulospora scrobiculata were observed in Asparagus racemosus.

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Table 2.1 Hosts of AM fungi in alpine and temperate regions Host plant Rhododendron anthopogon R. arboretum R. campanulatum R. barbatum R. lepidotum Catharanthus roseus Ocimum sp. Asparagus racemosus Helianthus annuus Helianthus annuus Asparagus racemosus Catharanthus roseus Ocimum sp. Quercus sp. Pinus sp. Agropyron yesoense Lespedeza cuneata Amphicarpaea edgeworthii Lotus corniculatus Artemisia annua Miscanthus sinensis Artemisia iwayomogi Orostachys japonica Artemisia princeps Persicaria blumei Artemisia scoparia Persicaria thunbergii Aster tripolum Phragmites communis

Family Ericaceae Ericaceae Ericaceae Ericaceae Ericaceae Apocynaceae Lamiaceae Liliaceae

Locality Kumaun, Central Himalaya

References Chaurasia et al. (2005)

Asteraceae

Haryana, India

Asteraceae

Haryana, India

Liliaceae Apocynaceae Lamiaceae

Uttarakhand (Haridwar, Pauri Garhwal, Almora, Dehradun, and Udham Nagar)

Sharma et al. (2008) Sharma et al. (2009a) Gaur and Kaushik (2011)

Fagaceae Pinaceae Poaceae Fabaceae Fabaceae Fabaceae Asteraceae Poaceae Asteraceae Crassulaceae Asteraceae Polygonaceae Asteraceae Polygonaceae Asteraceae Poaceae Ophioglossaceae Asparagaceae Poaceae Crassulaceae Fabaceae Poaceae Amaranthaceae Crassulaceae Commelinaceae Asteraceae Asteraceae Asteraceae

Kumaon region of Himalayan foothills Korea

Chaturvedi et al. (2012) Eo et al. (2014)

(continued)

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Table 2.1 (continued) Host plant

Family

Botrychium ternatum Polygonatum odoratum Calamagrostis epigejos Sedum oryzifolium Cassia mimosoides Setaria viridis Chenopodium ficifolium Sedum sarmentosum Commelina communis Sonchus brachyotus Chrysanthemum morifolium Sonchus oleraceus Desmodium oxyphyllum Sophora flavescens Digitaria sanguinalis Stellaria aquatic Disporum smilacinum Tephroseris kirilowii Erigeron bonariensis Themeda triandra Glycine soja Trifolium repens Impatiens balsamina Veronica undulata Imperata cylindrica Vicia amoena Isachne globosa Vicia unijuga Ixeris dentata

Fabaceae Fabaceae Poaceae Caryophyllaceae Colchicaceae Asteraceae Asteraceae Poaceae Fabaceae Fabaceae Balsaminaceae Scrophulariaceae Poaceae Fabaceae Poaceae Fabaceae Asteraceae Violaceae Fabaceae Poaceae Amaryllidaceae Solanaceae Amaryllidaceae Araliaceae Amaryllidaceae Asteraceae Fabaceae Fabaceae Brassicaceae Fabaceae Solanaceae Campanulaceae Cucurbitaceae Pedaliaceae Cucurbitaceae Solanaceae Polygonaceae Poaceae Fabaceae Fabaceae Convolvulaceae Fabaceae Asteraceae Poaceae Fabaceae Magnoliaceae Fabaceae Moraceae Rutaceae Fabaceae

Locality

References

(continued)

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

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Table 2.1 (continued) Host plant

Family

Viola mandshurica Kummerowia striata Zoysia japonica Allium cepa Lycopersicon esculentum Allium fistulosum Panax ginseng Allium scorodorpasum Petasites japonicas Arachis hypogaea Phaseolus angularis Brassica napus Phaseolus radiates Capsicum annum Platycodon grandiflorus Cucumis meto Sesamum indicum Cucumis sativus Solanum melongena Fagopyrum esculentum Sorghum bicolor Glycine max Vigna unguiculata Ipomoea batatas Vigna vexillata Lactuca sativa Zea mays Albizia julibrissin Liriodendron tulipifera Amorpha fruticose Morus alba Citrus unshiu Pueraria thunbergiana Chamaecyparis

Cupressaceae Ericaceae Cupressaceae Fabaceae Cupressaceae Rosaceae Araliaceae Anacardiaceae Fabaceae Rosaceae Fabaceae Styracaceae Fabaceae Symplocaceae Lauraceae Taxaceae Scrophulariaceae

Locality

References

(continued)

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U. Singh et al.

Table 2.1 (continued) Host plant obtusa Rhododendron mucronulatum Chamaecyparis pisifera Robinia pseudoaccasia Cryptomeria japonensis Rosa multiflora Dendropanax morbiferus Rhus javanica Indigofera kirilowii Stephanandra incisa Lespedeza bicolor Styrax obassia Lespedeza chiisanensis Symplocos sawafutagi Lindera obtusiloba Torreya nucifera Veronica undulata Stipa purpurea Leontopodium nanum Potentilla bifurca

Family

Locality

References

Poaceae Asteraceae Rosaceae

Northern Tibetan Plateau

Zhang et al. (2016)

Chaturvedi et al. (2012) studied the diversity and abundance of AM fungi in different ecosystems (oak forest, pure pine forest, pine-oak forest, and agricultural fields) from Kumaon region of Himalayan foothills. They have reported maximum diversity in pine-oak mixed forests and minimum in agriculture fields. On the basis of seasons maximum AM fungi were recorded in rainy seasons and minimum in winter seasons. In rainy season, Acaulospora scrobiculata, A. spinosa, and Glomus claroideum were reported from sites whereas in winter only G. intraradices was recorded. The dominant AM fungi species were Glomus intraradices, G. etunicatum, and Acaulospora scrobiculata. Eo et al. (2014) studied the distribution of AM fungi in local woody, herbaceous, and vegetable crop plants in the alpine region of Korea. They have recorded 89 AM fungal species in which Acaulospora and Glomus were the most dominant and abundant (19 species), followed by Scutellospora (15 species), Pacispora and

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Paraglomus (two species each), and Diversispora and Redeckera (one species each). Zhang et al. (2016) surveyed typical alpine steppe in the northern Tibetan Plateau and studied AM fungi association in Stipa purpurea, Leontopodium nanum, and Potentilla bifurca. They have recorded a total of eight genera including Glomus, Diversispora, Funneliformis, Archespora, Ambispora, Claroideoglomus, Paraglomus, and Rhizophagus.

2.2.2

Biodiversity of AM Fungi in Tropical Region

Tropical region is one of the important regions of terrestrial ecosystems on the earth. It is the region of the earth near the equator and between the Tropic of Cancer (23.43666 ) in the northern hemisphere and the Tropic of Capricorn (23.43666 ) in the southern hemisphere. It is characterized by the high annual rainfall, i.e., more than 200 cm. Achyranthes aspera, Axonopus scoparius, Brachiaria brizantha, B. humidicola, Bursera sp., Calotropis gigantea, Casuarina equisetifolia, Cocos nucifera, Caesalpinia eriostachys, Caesalpinia coriaria, Cordia alliodora, Eclipta prostrata, Flueggea sp., Hyptis suaveolens, Ipomoea biloba, Indigofera aspalathoides, I. tinctoria, Jatropha curcas, Jatropha simpetala, Lantana camara, Lonchocarpus constrictus, Paspalum sp., Ricinus communis, and Vitex trifolia were found to be associated with AM fungi in the tropical region. The plants associated with the AM fungi growing in the tropical region are listed in Table 2.2. Kulkarni et al. (1997) studied spore density of AM fungi in the rhizosphere of 12 plant species growing on sand dunes in the west coast of India during postmonsoon season. Rhizospheric soil contains AM fungal spores and total mean density was found to be 0.75 g. A total of 16 AM fungal species. Were found in rhizospheric soil; out of these nine species were related to Glomus. Among the spore communities, Gigaspora ramisporophora, Glomus albidum, Glomus clarum, and Scutellospora gregaria were dominant. Jaiswal and Rodrigues (2001) studied the occurrence of AM fungal spores in rhizospheric soil sample of different plants, viz., Achyranthes aspera, Calotropis gigantea, Casuarina equisetifolia, Cocos nucifera, Flueggea sp., Hyptis suaveolens, Ipomoea biloba, Lantana camara, and Vitex trifolia during March 1999, which occurs at one of the smallest states of India, Goa (Colva beach). The identified species of AM fungi include Acaulospora bireticulata, A. scrobiculata, A. spinosa, Gigaspora coralloidea, G. gregaria, G. margarita, Sclerocystis sinuosa, and Scutellospora verrucosa. Spores of Acaulospora sp. dominated in the rhizospheric zone of all plants with a percentage of 33–51% at every 100 g of a rhizospheric soil sample. Gavito et al. (2008) isolated Glomus, Acaulospora, and Gigaspora from common tree species (Bursera sp., Jatropha simpetala, Caesalpinia eriostachys, Caesalpinia coriaria, Cordia alliodora, and Lonchocarpus constrictus) from the study area located at the Pacific Coast in the State of Jalisco, Mexico. Sundar et al. (2011) studied the colonization of AM fungi in three different medicinal plants, viz., Eclipta prostrata, Indigofera aspalathoides, and I. tinctoria, from Tamil Nadu

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Table 2.2 Host of AM fungi in tropical region Host plant Ageratum conyzoides Emelia sonchifolia Launaea sarmentosa Tridax procumbens Polycarpaea corymbosa Ipomoea pes-caprae Leucas aspera Alysicarpus rugosus Canavalia rosea Borreria articularis B. pusilla Oldenlandia aspera Achyranthes aspera Calotropis gigantea Casuarina equisetifolia Cocos nucifera Flueggea sp. Hyptis suaveolens Ipomoea biloba Lantana camara Vitex trifolia Bursera sp. Jatropha simpetala Caesalpinia eriostachys Caesalpinia coriaria Cordia alliodora Lonchocarpus constrictus Eclipta prostrata Indigofera aspalathoides I. tinctoria

Family Asteraceae Asteraceae Asteraceae Asteraceae Caryophyllaceae Convolvulaceae Lamiaceae Papilionaceae Papilionaceae Rubiaceae Rubiaceae Rubiaceae

Locality Someshwara, Mangalore coast of India

References Kulkarni et al. (1997)

Amaranthaceae Apocynaceae Casuarinaceae Arecaceae Phyllanthaceae Lamiaceae Convolvulaceae Verbenaceae Lamiaceae

India, Goa (Colva beach)

Jaiswal and Rodrigues (2001)

Burseraceae Euphorbiaceae Fabaceae Fabaceae Boraginaceae Fabaceae

Pacific Coast, Jalisco, Mexico

Gavito et al. (2008)

Asteraceae Fabaceae Fabaceae

Tamil Nadu (Kanyakumari)

Sundar et al. (2011)

(continued)

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Table 2.2 (continued) Host plant Asclepias currasavica Bryophyllum pinnatum Costus igneus Cyclea peltate Dioscorea bulbifera Hemionitis arifolia Hemidesmus indicus Justicia sp. Leucas sp. Ocimum tenuiflorum Rauvolfia teraphylla Stevia rebaudiana Siegesbeckia orientalis Withania somnifera Borreria ocymoides Chonemorpha fragrans Elephantopus scaber Heracleum rigens Hydrocotyle javanica Canscora perfoliate Launaea acaulis Leucas hirta Peperomia pellucida Smilax zeylanica Apama siliquosa Centella asiatica Cyathula prostrata Piper nigrum Andrographis paniculata Begonia sp. Blepharis sp.

Family Asclepiadaceae Crassulaceae Costaceae Menispermaceae Dioscoreaceae Adiantaceae Apocynaceae Acanthaceae Lamiaceae Lamiaceae Apocynaceae Asteracecae Asteraceae Solanaceae

Locality Kodagu, Western Ghats of Karnataka

References Rajkumar et al. (2012)

Rubiaceae Apocynaceae Asteraceae Apiaceae Apiaceae Gentianaceae Asteraceae Lamiaceae Piperaceae Smilaceae

Dakshina Kannada, Western Ghats of Karnataka

Rajkumar et al. (2012)

Aristolochiaceae Apiaceae Amaranthaceae Piperaceae

Chikmagalur, Western Ghats of Karnataka

Rajkumar et al. (2012)

Acanthaceae Begoniaceae Acanthaceae Euphorbiaceae

Hassan, Western Ghats of Karnataka

Rajkumar et al. (2012)

(continued)

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Table 2.2 (continued) Host plant

Family

Locality

References

Breynia retusa Coffea arabica Eclipta alba Eclipta prostrate Lobelia nicotianaefolia Mentha piperita Naravelia zeylanica Pouzolzia indica Scoparia dulcis Triumfetta rhomboidea Canscora decussate Justicia adhatoda Ophiorrhiza mungos Tinospora cordifolia Tinospora sinensis Jatropha curcas Ricinus communis Axonopus scoparius Brachiaria brizantha B. humidicola Paspalum notatum Cocos nucifera

Rubiaceae Asteraceae Asteraceae Campanulaceae Lamiaceae Ranunculaceae Urticaceae Scrophulariaceae Tiliaceae

Gentianaceae Acanthaceae Rubiaceae Menispermaceae Menispermaceae

Udupi, Western Ghats of Karnataka

Rajkumar et al. (2012)

Euphorbiaceae Euphorbiaceae

Guantanamo (Cuba)

Alguacil et al. (2010)

Poaceae Poaceae Poaceae Poaceae

Amazon, Brazil

Leal et al. (2013)

Arecaceae

Malappuram, Kerala, India

Rajeshkumar et al. (2015)

(Kanyakumari). A total of 21 species of AM fungi were identified from the rhizospheric soil of these plants. In this study total five species were noticed 100% in all plants but out of these species, Glomus was the most dominant. Rajkumar et al. (2012) made a survey during the months of September and November in 2010 and 2011 for investigation of AM fungi status in 46 different medicinal plants in Western Ghats of Karnataka. They studied root colonization and spore density of rhizospheric soil and root samples and found that all the plants were mycorrhizal. The spore density of AM fungi ranged from 15 to 520 spores per 100 g of soil. A total of 40 different types of AM fungi were recorded; out of this only 4 were identified up to genus level. Among 36 identified up to species level Glomus species was very dominant in the rhizosphere of medicinal plants followed by Acaulospora sp., Gigaspora sp., Scutellospora sp., Paraglomus sp., and Pacispora sp.

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Alguacil et al. (2010) studied AM fungi biodiversity in a native vegetation soil and in a soil cultivated with Jatropha curcas and Ricinus communis in a tropical system in Guantanamo (Cuba) through PCR, cloning, sequencing, and phylogenetic analyses. A total of 20 AM fungi sequence types were identified: 19 belonged to the Glomeraceae and 1 to the Paraglomeraceae. Leal et al. (2013) collected soil sample from the host plants Axonopus scoparius, Brachiaria brizantha, B. humidicola, and Paspalum notatum and several invasive plants from forest and pasture of Benjamin Constant located in the Alto Solimões river region at the western portion of the Amazon state, Brazil. Most of the species (83%) pertained to the families Acaulosporaceae (Acaulospora) and Glomeraceae (Glomus and Rhizophagus). The genera Gigaspora, Diversispora, Archaeospora, and Ambispora were represented by only one species each while four species were identified in the genus Scutellospora. Rajeshkumar et al. (2015) reported the occurrence of AM fungi in Cocos nucifera which was cultivated in Malappuram district of Kerala, India. A total of 40 AM species were related to 10 genera, viz., Acaulospora, Claroideoglomus, Dentiscutata, Diversispora, Funneliformis, Gigaspora, Glomus, Redeckera, Scutellospora, and Septoglomus. Claroideoglomus, Glomus, and Gigaspora were dominant genera. Claroideoglomus etunicatum and Glomus aggregatum were the dominant species which showed 100% colonization in rhizospheric soil of coconut followed by Acaulospora scrobiculata, Glomus clavisporum, G. clarum, G. liquidambaris, and G. macrocarpum (78%) and rest of the species showed low level of colonization which belonged to different genera like Diversispora gibbosa, Acaulospora bireticulata, Acaulospora foveata, A. lacunose, Glomus cerebriforme, G. heterosporum, G. invermaium, G. pallidum, G. reticulatum, and G. tenebrosum.

2.2.3

Biodiversity of AM Fungi in Desert

Deserts are the regions that receive very little precipitation with an average annual rainfall of less than 25 cm. All deserts are arid and there is little availability of water for plants and animals. Earth has numerous land areas covered by deserts. Among all the terrestrial ecosystems, deserts are a unique ecosystem. Desert areas cover nearly one-third part of the land surface of the globe. Most of the major desert areas in the world are Sahara, the Arabian, the Kalahari deserts, and the Thar. Azadirachta indica, Acacia tortilis, A. aneura, Moringa concanensis, Mitragyna parvifolia, Cyperus conglomeratus, Salsola baryosma, Suaeda fruticose, Haloxylon recurvum, Phoenix dactylifera, and Sorghum bicolor are known for tolerating the hotter climate of the deserts. These plant communities show association with AM fungi, which are listed in Table 2.3. Bala et al. (1989) studied the root colonization in Azadirachta indica, Acacia tortilis, and A. aneura and reported that Gigaspora and Glomus are the most common AM fungi association in the roots of these plants. Panwar and Vyas (2002) studied AM fungi root colonization in the roots of Moringa concanensis

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Table 2.3 Host of AM fungi in desert region Host plant Azadirachta indica Acacia tortilis A. aneura A. catechu Moringa concanensis Mitragyna parvifolia

Family Meliaceae Fabaceae Fabaceae Fabaceae Moringaceae Rubiaceae

Cyperus conglomeratus Salsola baryosma Suaeda fruticose Haloxylon recurvum Phoenix dactylifera Phoenix dactylifera Phoenix dactylifera

Cyperaceae Amaranthaceae Amaranthaceae Amaranthaceae Arecaceae Arecaceae Arecaceae

Locality Indian Desert

References Bala et al. (1989)

Indian Thar Desert Indian Thar Desert

Panwar and Vyas (2002) Panwar and Tarafdar (2006) Chaudhry et al. (2006)

Cholistan Desert, Pakistan Arid zone of Rajasthan

Southern Arabia Arabian desert Arabian desert

Mathur et al. (2007)

Al-Yahya’ei et al. (2011) Symanczik et al. (2014) Symanczik et al. (2015)

and isolated different types of AM fungal species, viz., Acaulospora mellea, Gigaspora margarita, Gigaspora gigantea, Glomus deserticola, Glomus fasciculatum, Sclerocystis rubiformis, Scutellospora calospora, and Scutellospora nigra. Parmar and Tarafdar (2006) studied AM fungal association in plants belonging to Mitragyna parvifolia from Indian Thar desert and reported a total of 15 AM fungal species: Acaulospora elegans, Acaulospora sporocarpia, Gigaspora albida, Glomus aggregatum, Glomus ambisporum, Glomus constrictum, Glomus convolutum, Glomus fasciculatum, Glomus geosporum, Glomus intraradices, Glomus mosseae, Glomus rubiforme, Paraglomus occultum, Scutellospora minuta, and Scutellospora pellucida. Chaudhry et al. (2006) studied the root colonization in Cyperus conglomeratus and reported two different genera, viz., Gigaspora and Glomus. Mathur et al. (2007) studied AM fungal spore association in Salsola baryosma, Suaeda fruticose, and Haloxylon recurvum from arid zone of Rajasthan and reported five different genera: Glomus, Gigaspora, Acaulospora, Scutellospora, and Sclerocystis. Glomus was dominant in rhizospheric soil of these plants with eight species (Glomus aggregatum, G. ambisporum, G. mosseae, G. constrictum, G. deserticola, G. fasciculatum, G. geosporum, and G. sinuosum), followed by Gigaspora (Gigaspora gigantea, G. margarita, and G. rosea), Acaulospora (Acaulospora laevis, A. morrawae, and A. sporocarpia), and Scutellospora (Scutellospora calospora, S. nigra, and S. aurigloba) with three species each. Sclerocystis (Sclerocystis ceremoides and S. rubiformis) was detected with two species only. Al-Yahya’ei et al. (2011) reported unique AM fungi communities in date palm plantations and surrounding desert plant habitats of Southern Arabia. They isolated different species of AM fungal spores, viz., Glomus intraradices, G. mosseae, G. sinuosum, G. aggregatum, G. microaggregatum, G. eburneum, Racocetra

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gregaria, Acaulospora spinosa, Ambispora gerdemannii, Scutellospora calospora, and Racocetra fulgida. Symanczik et al. (2014) isolated Diversispora aurantia, Diversispora spurca, Claroideoglomus drummondii, and Funneliformis africanum species from Arabian desert during the study of root colonization of date palm. Symanczik et al. (2015) isolated Diversispora aurantia, Diversispora aurantia, Septoglomus africanum, and Paraglomus species from Arabian desert during the study of root colonization of Sorghum bicolor.

2.2.4

Biodiversity of AM Fungi in Mangrove

Mangrove ecosystem has many diverse plant communities grown in coastal region mainly known for many health benefits for humans. It grows between coastal and land area in tropical and subtropical regions of the world and is highly adapted for strong wind, extreme tidal waves, various temperature, salinity fluctuation, and anaerobic soil. The worldwide diversity of mangrove flora includes Acanthus ilicifolius, Aegiceras corniculatum, Ageratum conyzoides, Aglaia cucullata, Alysicarpus rugosus, Avicennia alba, Avicennia marina, Avicennia officinalis, Borreria articularis, Borreria pusilla, Bruguiera cylindrica, Bruguiera gymnorrhiza, Cerbera manghas, Derris heterophylla, Emilia sonchifolia, Excoecaria agallocha, Excoecariaag allocha, Heritiera fomes, Heritiera littoralis, Hibiscus tiliaceus, Pongamia pinnata, Rhizophora apiculate, Rhizophora mucronate, Sonneratia apetala, and Sonneratia caseolaris. Many of these mangrove vegetations are in strong association with AM fungi, which are listed in Table 2.4. Beena et al. (2001) studied AM fungal association in many host plants (Ageratum conyzoides, Alysicarpus rugosus, Borreria articularis, Borreria pusilla, Emilia sonchifolia, etc.) and observed different species of AM fungi belonging to genus Acaulospora, Glomus, Gigaspora, Sclerocystis, and Scutellospora from west coast of India. Kothamasi et al. (2006) studied AM fungal diversity in Bruguiera gymnorrhiza and observed different species of Glomus fasciculatum and G. magnicaule from mangrove ecosystem of Great Nicobar Island. Wang et al. (2010) reported Glomus aggregatum, G. geosporum, and G. rubiformis from the rhizospheric soil of Sonneratia apetala in South China. D’Souza and Rodrigues (2013a) studied AM fungal diversity in Acanthus ilicifolius, Excoecariaag allocha, and Rhizophora mucronate from two sites Terekhol and Zuari in Goa, India. They have reported a total of eleven AM fungal species representing five genera. Glomus was the dominant genus followed by Acaulospora, Rhizophagus, Funneliformis, and Racocetra. D’Souza and Rodrigues (2013b) isolated five different genera of AM fungi, viz., Acaulospora, Gigaspora, Glomus, Entrophospora, and Scutellospora, from Avicennia marina, Acanthus ilicifolius, Rhizophora apiculate, Sonneratia caseolaris, Rhizophora mucronate, Excoecaria agallocha, Bruguiera cylindrica, Rhizophora apiculate, Avicennia alba, etc. at the mangrove of Goa. Wang et al. (2015) recorded total six AM fungal genera, viz., Acaulospora, Claroideoglomus, Diversispora, Funneliformis, Paraglomus, and Rhizophagus, from four dominant

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Table 2.4 Host of AM fungi in mangroves Host plant Borreria articularis Borreria pusilla Oldenlandia aspera Hydrophylax maritima Emilia sonchifolia Ageratum conyzoides Launaea sarmentosa Tridax procumbens Wedelia biflora Polycarpaea corymbosa Cyperus arenarius Cyperus pedunculatus Fimbristylis argentea Euphorbia articulata Alysicarpus rugosus Canavalia cathartica Canavalia maritima Tephrosia purpurea Solanum xanthocarpum Spinifex littoreus Mollugo pentaphylla Scaevola sericea Bruguiera gymnorrhiza Sonneratia apetala Acanthus ilicifolius Excoecaria agallocha Rhizophora mucronate Avicennia marina Acanthus ilicifolius Rhizophora apiculate

Family Rubiaceae Rubiaceae Rubiaceae Rubiaceae Asteraceae Asteraceae Asteraceae Asteraceae Asteraceae Caryophyllaceae Cyperaceae Cyperaceae Cyperaceae Euphorbiaceae Fabaceae Fabaceae Fabaceae Fabaceae Solanaceae Poaceae Molluginaceae Goodeniaceae

Locality Karnataka, India

References Beena et al. (2001)

Rhizophoraceae

Great Nicobar Island

Kothamasi et al. (2006)

Lythraceae Acanthaceae Euphorbiaceae Rhizophoraceae

South China Terekhol and Zuari in Goa, India

Wang et al. (2010) D’Souza and Rodrigues (2013a)

Verbenaceae Acanthaceae Rhizophoraceae Lythraceae

Goa, India

D’Souza and Rodrigues (2013b)

(continued)

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Table 2.4 (continued) Host plant

Family

Sonneratia caseolaris Rhizophora mucronate Excoecaria agallocha Bruguiera cylindrica Rhizophora apiculate Avicennia alba Heritiera littoralis Pongamia pinnata Cerbera manghas Hibiscus tiliaceus Sonneratia apetala Heritiera fomes Excoecaria agallocha Derris heterophylla Bruguiera gymnorrhiza Avicennia officinalis Aglaia cucullata Aegiceras corniculatum

Rhizophoraceae Euphorbiaceae Rhizophoraceae Rhizophoraceae Acanthaceae

Malvaceae Fabaceae Apocynaceae Malvaceae Lythraceae Malvaceae Euphorbiaceae Fabaceae Rhizophoraceae Acanthaceae Meliaceae Primulaceae

Locality

References

Qi’Ao Mangrove Forest, China

Wang et al. (2015)

Mangrove site of Odisha

Gupta et al. (2016)

semi-mangrove species, including Heritiera littoralis, Pongamia pinnata, Cerbera manghas, and Hibiscus tiliaceus, from Qi’Ao Mangrove Forest. Gupta et al. (2016) reported 6 species of Acaulospora, 2 of Entrophospora, 2 of Gigaspora, 32 of Glomus, and 3 of Scutellospora from the mangrove site of Odisha which is highly saline. These AM fungi established mutualistic relationship with host plants including Sonneratia apetala, Heritiera fomes, Excoecaria agallocha, Derris heterophylla, Bruguiera gymnorhiza, Avicennia officinalis, Aglaia cucullata, and Aegiceras corniculatum.

2.2.5

Biodiversity of AM Fungi in HM-Contaminated Soils and Mining Fields

Metals having densities more than 5 g/cm3 are generally called as HMs and metalloids (Oves et al. 2012). Chemical fertilizers, sewage, and industrial effluents

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are the major sources of enhancement of HMs in the soil (Shen et al. 2002). Continuous increase in HM in the soil changes physical and chemical properties of soil such as acidification of soil, i.e., decrease in pH (Koomen et al. 1990). Presence of HM in the soil for a long time is detrimental to soil health due to their low mobility, nondegradable nature, and low solubility. From the agricultural point of view microorganisms play a very significant role in the reclamation of soil (Zoomi et al. 2017). Numerous studies reported AM fungal association in HM-tolerant plants, which are listed in Table 2.5. Mehrotra (1998) reported Acaulospora scrobiculata, Entrophospora colombiana, Glomus aggregatum, G. ambisporum, G. sp., and Scutellospora calospora from opencast coal mine site at Chandrapur, Maharashtra state, India. Chandra and Jamaluddin (1999) recorded AM fungi colonization in Acacia auriculiformis, Acacia catechu, Ailanthus excelsa, Acacia nilotica, Albizia procera, Cassia siamea, Dalbergia sissoo, Eucalyptus hybrid, Peltophorum sp., Pithecellobium dulce, and Gmelina arborea, in which the highest level of colonization was recorded in A. catechu followed by D. sissoo. Acaulospora was the dominant AM fungal species in coal mine soils of Kusmunda, Korba. Khan (2001) reported AM fungal species belonging to genera Gigaspora, Acaulospora, and Glomus associated with three tree species (Acacia arabica, Dalbergia sissoo, and Populus euroamericana) growing on a Cr-polluted site of Pakistan. Regvar et al. (2003) examined colonization of AM fungi in Pennycress (Thlaspi) belonging to Brassicaceae family. Members of this family are believed to be nonmycorrhizal. The author identified G. intraradices from the Zn-contaminated soil from different locations in Slovenia, Austria, Italy, and Germany. Selvaraj and Kim (2004) reported four species of AM fungi belonging to Glomus mosseae, Glomus geosporum, Glomus fasciculatum, and Sclerocystis sinuosa from the sewage effluent irrigated soil. Khade and Adholeya (2009) collected soil sample from adjoining Kanpur Tanneries, Uttar Pradesh, India, where the soil is contaminated with Cr, and recorded AM spores belonging to two genera, viz., Glomus and Scutellospora. Channabasava and Lakshman (2013) recorded AM fungal colonization in Jatropha curcas and Panicum miliaceum L. from the mined areas of Yellapur, Uttara Kannada, Karnataka. They reported a total of 16 species of AM fungi belonging to 4 genera, viz., Acaulospora (Acaulospora delicata, A. mellea, and A. foveata), Gigaspora (Gigaspora albida and G. decipiens), Glomus (Glomus claroides, G. aggregatum, G. clarum, G. fasciculatum, G. geosporum, G. macrocarpum, G. callosum, G. constrictum, G. microcarpum, G. fragile, G. mosseae, and G. reticulatum), and Scutellospora (Scutellospora calospora and S. erythropa). Glomus was the most dominant AM fungi. Krishnamoorthy et al. (2015) recorded AM fungi from metalloid- and metalcontaminated soil. They have identified Claroideoglomus claroideum, Funneliformis caledonium, Glomus constrictum, Glomus mosseae, Glomus clarus, and Rhizophagus intraradices. They have further reported that the AM fungi were associated with the Bidens tripartite, Cosmos bipinnatus, Conyza canadensis, Hymenachne amplexicaulis, and Phragmites sp. Leal et al. (2016) studied

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Table 2.5 Host of AM fungi in heavy metal-contaminated soils and mining areas Host plant Azadirachta indica Dalbergia sissoo Cassia siamea Cassia glauca Eucalyptus sp. Delonix elata Gmelina arborea Leucaena leucocephala Tectona grandis Emblica officinalis Ficus benghalensis Pithecellobium dulce Ficus religiosa Acacia auriculiformis Acacia catechu Acacia nilotica Ailanthus excelsa Albizia procera Cassia siamea Dalbergia sissoo Eucalyptus hybrid Gmelina arborea Peltophorum sp. Pithecellobium dulce Acacia arabica Dalbergia sissoo Populus euroamericana Thlaspi sp. (Pennycress) Prosopis juliflora Cynodon sp. Croton

Family Meliaceae Fabaceae Fabaceae Fabaceae Myrtaceae Fabaceae Verbenaceae Fabaceae Lamiaceae Euphorbiaceae Moraceae Leguminosae Moraceae

Locality Chandrapur, Maharashtra, India

References Mehrotra (1998)

Fabaceae Fabaceae Fabaceae Simaroubaceae Mimosaceae Fabaceae Fabaceae Myrtaceae Verbenaceae Fabaceae Fabaceae

Kusmunda (Korba)

Chandra and Jamaluddin (1999)

Fabaceae Fabaceae Salicaceae

Cr-polluted site of Pakistan

Khan (2001)

Brassicaceae

Zn-contaminated soil Slovenia, Austria, Italy, and Germany Southern peninsular, India

Regvar et al. (2003)

Fabaceae Poaceae Euphorbiaceae

Kanpur Tanneries, Uttar Pradesh

Selvaraj and Kim (2004) Khade and Adholeya (2009) (continued)

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Table 2.5 (continued) Host plant

Family

Locality

References

bonplandianum Desmostachya bipinnata Parthenium sp. Jatropha curcas Panicum miliaceum Bidens tripartite Cosmos bipinnatus Conyza canadensis Hymenachne amplexicaulis Phragmites sp. Brachiaria decumbens Eucalyptus camaldulensis Senecio inaequidens Sophora flavescens Vachellia sp. Senegalia sp. Cynodon dactylon Parthenium hysterophorus Croton bonplandianum Prosopis juliflora

Poaceae Asteraceae

Euphorbiaceae Poaceae

Yellapur, Uttara Kannada, Karnataka

Channabasava and Lakshman (2013)

Asteraceae Asteraceae Asteraceae Poaceae Poaceae

Metalloid- and metal-contaminated soil

Krishnamoorthy et al. (2015)

Poaceae Myrtaceae

Três Marias (Minas Gerais—MG— Brazil)

Leal et al. (2016)

Asteraceae

Site contaminated with Al, As, Cd, Cr, Cu, Ni, Pb, Zn Changzhi and Jincheng in Shanxi Province, China Gold and uranium mine tailings in South Africa Cr-laden technosols of Jajmau, Kanpur, India

Turrini et al. 2018)

Fabaceae Fabaceae Fabaceae Poaceae Asteraceae Euphorbiaceae Mimosaceae

Song et al. (2019) Buck et al. (2019) Akhtar et al. (2019)

rhizospheric soil sample of Brachiaria decumbens and Eucalyptus camaldulensis where soil is contaminated with Zn, Cd, Cu, and Pd and isolated Glomus, Acaulospora, Paraglomus, Gigaspora, Dentiscutata, Scutellospora, and Cetraspora from Votorantim Metals Company, Três Marias (Minas Gerais—MG—Brazil). Rhizoglomus venetianum, a new species of AM fungi associated with Senecio inaequidens, was reported from the site contaminated with Al, As, Cd, Cr, Cu, Ni, Pb, and Zn in Italy (Turrini et al. 2018). Song et al. (2019) studied the diversity of AM fungi from the cities of Changzhi and Jincheng in Shanxi Province, China. They recorded 14 genera of AM fungi. Glomus, Septoglomus, Rhizophagus, Kamienskia, and Sclerocystis were the dominant AM fungal genera in the root zone of Sophora flavescens. Seventeen AM fungi species including Claroideoglomus etunicatum, C. lamellosum, Diversispora celata, D. trimerales, D. spurca, Sclerocystis sinuosa,

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Rhizophagus intraradices, Scutellospora calospora, S. dipurpurescens, Redeckera fulvum, and Glomus iranicum were described by Buck et al. (2019) from the Vachellia and Senegalia trees growing on gold and uranium mine tailings in South Africa. Akhtar et al. (2019) reported seven AM fungi, viz., Rhizophagus intraradices, Funneliformis geosporus, Glomus sinuosum, Rhizophagus fasciculatus, Funneliformis mosseae, Glomus aggregatum, and Acaulospora scrobiculata, from the four host plants, viz., Cynodon dactylon, Parthenium hysterophorus, Croton bonplandianum, and Prosopis juliflora, growing over heavy Cr-laden technosols of Jajmau, Kanpur, India.

2.2.6

Biodiversity of AM Fungi in Acidic Soils

An acid soil occurs naturally by the continuous addition of acidic fertilizer in soil and decomposition of organic residue in soil. This type of soil frequently occurs in regions where annual precipitation is less than 600–800 mm. The soils are characterized by low pH between 4.5 and 7.5 depending on the crop. Acidification of soil also increases rainfall since rain has a pH of 5.7, depending on pollutants such as SO2, NO2, and others. For improvement of this type of soil one of the major symbiotic organisms which is AM fungi plays a very significant role in the enhancement of productivity of this type of soil. The plants colonized by AM fungi growing in the acid-tolerant soil are listed in Table 2.6. Morton (1986) reported three new species of Acaulospora, viz, Acaulospora dilatata, Acaulospora lacunosa, and Acaulospora rugosa, from host, i.e., Andropogon virginicus, which was growing in low pH and high aluminumcontaining soil in West Virginia. Hamel et al. (1994) collected soil sample from “old meadow” habitat (pH 5–6) in Gentilly, Quebec, Canada, from barley (Hordeum vulgare L.) as a host and recorded spores of 13 species from three genera, Glomus, Gigaspora, and Scutellospora. Moreira-Souza et al. (2003) recorded Acaulospora bireticulata, A. gerdemannii, A. laevis, A. scrobiculata, A. spinosa, A. rehmii, Acaulospora sp. 1, Acaulospora sp. 2, Entrophospora colombiana, Gigaspora margarita, G. decipiens, Glomus aggregatum, G. clarum, G. diaphanum, G. etunicatum, G. fasciculatum, G. geosporum, G. macrocarpum, G. microcarpum, G. pansihalos, Scutellospora gilmorei, S. nigra, S. pellucida, Table 2.6 Host of AM fungi in acidic soil Host plant Andropogon virginicus Hordeum vulgare Sorghum vulgare Zea mays Carica papaya Centrosema macrocarpum

Family Poaceae Poaceae Poaceae Poaceae Caricaceae Fabaceae

Locality West Virginia Quebec, Canada San Paulo, Brazil Brazil North Goa, India Venezuela

References Morton (1986) Hamel et al. (1994) Moreira-Souza et al. (2003) Oliveira et al. (2009) Khade et al. (2009) Alguacil et al. (2010)

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and Scutellospora sp. 1 from Araucaria forest, San Paulo, Brazil, where common plant community as a host is Araucaria (field) and pH of soil is 3.7, i.e., acidic soil pH. After further confirmation trap culture was established by the using Sorghum vulgare and same species was reported. Oliveira et al. (2009) reported AM fungi from slightly acidic soil of Brazil. Acaulospora, Glomus, Gigaspora, Sclerocystis, Funneliformis, Rhizophagus, and Dentiscutata were isolated from the host Zea mays. Khade et al. (2009) recorded a total of 11 fungal species from the Carica papaya L. growing in heavily acid soil of North Goa, India. These AM fungi belonged to genera Acaulospora, Dentiscutata, Gigaspora, Glomus, and Racocetra. Alguacil et al. (2010) selected legume pasture, Venezuela, as the study site where soil pH was 4.6–5.1. They isolated AM fungal spores belonging to Acaulospora mellea, A. rugose, A. spinosa, Rhizophagus intraradices, R. fasciculatum, and Glomus spp. (4) from Centrosema macrocarpum.

2.2.7

Biodiversity of AM Fungi in Alkaline Soils

Alkaline soil is a type of stressed soil common in arid and semiarid regions, covering more than 7% of land on the earth surface. It is associated with low rainfall and boron toxicity and pH greater than 7. These soils are highly porous, freely draining, and saturated with calcium carbonate. The abundance of calcium ions in soil solution limits the solubility of phosphorus in soil. In developing countries, calcareous soils sustain traditional rain-fed cultivation despite the intrinsic nutrient (P, Fe, and Co) unavailability, because the pH of soil in this region increases and there is abundance of cation. However, high-cost P fertilizers must be added to maintain a sustainable agriculture (Marschner 1995). For the reduction of alkalinity of soil and increase in production of crop plants make a special symbiotic relationship with AM fungi. The plants associated with AM fungi growing in alkaline soils are listed in Table 2.7. Oliveira et al. (2005) collected alkaline soil samples from Estarreja, Northern Portugal. They isolated AM fungi Glomus from host Conyza bilbaoana, Pinus pinaster, and Salix atrocinerea. They isolated Glomus geosporum, G. intraradices, G. mosseae, G. claroideum, G. fasciculatum, and G. etunicatum from the trap culture multiplied from the soils collected at the study site. Wang et al. (2008) collected soil samples from the alkaline field of Shandong and Hebei Provinces in the north of China. Vigna unguiculata, Pisum sativum, Phaseolus vulgaris, V. radiata, Cajanus cajan, and Acacia dealbata were growing at the sampling sites. They have recorded six different types of AM fungi, viz., Acaulospora (four species), Ambispora (one species), Glomus (20 species), Scutellospora (three species), Archaeospora (one species), and Paraglomus (one species) from the study site. Sharma et al. (2009) studied endangered anticancerous herb Curculigo orchioides in the alkaline soil of tropical semievergreen forest of the Western Ghats in Kolhapur district of India. A total of 18 AM fungal species belonging to three genera (Acaulospora, Glomus, and Gigaspora) were recorded. Glomus microcarpum was the most abundant.

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Table 2.7 Host of AM fungi in alkaline soil Host plant Conyza bilbaoana Pinus pinaster Salix atrocinerea Vigna unguiculate Pisum sativum Phaseolus vulgaris Vigna radiata Cajanus cajan Acacia dealbata Curculigo orchioides Vitis vinifera

Family Asteraceae Pinaceae Salicaceae

Locality Estarreja, Northern Portugal

References Oliveira et al. (2005)

Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae Fabaceae

Shandong and Hebei Provinces in the north of China

Wang et al. (2008)

Amaryllidaceae

Kolhapur, India

Vitaceae

Eastern Adriatic coast

Mangifera indica Vitis vinifera Citrus limon Citrus sinensis Corchorus olitorius Sorghum bicolor Saccharum officinarum Mentha sp. Cajanus cajan Allium cepa Abelmoschus esculentus Triticum durum

Anacardiaceae Vitaceae Rutaceae Rutaceae Malvaceae Poaceae Poaceae Lamiaceae Fabaceae Amaryllidaceae Malvaceae

Kosti province (western bank of the White Nile River)

Sharma et al. (2009a, b) Likar et al. (2013) Abdelhalim et al. (2014)

Poaceae

East of Algeria

Saccharum munja Hordeum vulgare

Poaceae

Varanasi, India

Poaceae

Central Anatolia, Turkey

Nadji et al. (2017) Parihar et al. (2019) Kaidzu et al. (2019)

Likar et al. (2013) studied AM fungal communities on the roots of grapevine plants growing in typical calcareous soils (with pH values above 7.0) collected from eastern Adriatic coast and isolated 30 different fungal taxa, which comprised 8 different Glomeromycota taxa, including Glomus sinuosum and Glomus indicum. Abdelhalim et al. (2014) studied AM fungal association in many crops (mango, grapefruit, lemon and sweet orange trees, Jew’s mallow, sorghum, sugarcane, mint, pigeon pea, onion, and okra) from the Kosti province (western bank of the White

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Nile River). The soil was moderately alkaline (pH 7.5–8.5). Claroideoglomus, Glomus, Funneliformis, and Paraglomus were found in almost all crops. The genus Kuklospora was recovered only in Sorghum. Nadji et al. (2017) collected alkaline soil from the eastern regions of Algeria and characterized the isolated AM fungi spores from Triticum durum Desf. by wet sieving methods. They found AM fungi belonging to the family Glomeraceae, Acaulosporaceae, and Scutellosporaceae with a predominance of Glomeraceae. Parihar et al. (2019) studied soil samples from Varanasi, India, and revealed the characteristics of soil neutral to alkali nature and that habituated six genera and eight different species of AM fungi, viz., Acaulospora (one), Cetraspora (one), Entrophospora (one), Funneliformis (two), Glomus (one), and Rhizoglomus (two) in the rhizosphere of native salt-tolerant vegetation Saccharum munja Roxb. Rhizoglomus fasciculatum was the most widely distributed species under strongly alkaline condition (52.96%) while Funneliformis mosseae was well distributed under slightly (22.99%) to moderately alkaline condition (35.78%). Kaidzu et al. (2019) collected soil sample from Hordeum vulgare and isolated Acaulospora, Claroideoglomus, Funneliformis, Gigaspora, and Glomus from the soil of Central Anatolia, Turkey. The soil of the study site was faced with salinity, alkalinity, and drought stresses.

2.2.8

Biodiversity of AM Fungi in Saline Soil

Saline soil has many chemical and physical challenges as compared to normal soil; due to increase of salinity in soil it has reduced microbial biodiversity and agricultural productivity. In other words it is also known as dead soil from the point of agriculture. Saline soils are nutrient-deficient soil and have poor reproductive capacity. It contains toxic products like boron, carbonate, and aluminate ions. These soils contain less organic matter and biological activity (Rengasamy 2002; Yadav et al. 2020a). For the improvement of physical property of saline soil peoples cultivate salt-tolerant plants such as Phyla nodiflora, Acacia nilotica, Prosopis juliflora, and Dalbergia. These plants improve the uptake of water and nutrients in soil, reduce the toxicity of soil, and increase the soil organic matter which is necessary for plants. These salt-tolerant plants are reported to be associated with beneficial symbiotic microorganisms including AM fungi. These plants along with their families are listed in Table 2.8. Kannan and Lakshminarasimhan (1990) studied the AM fungi colonization in the host plant (Phyla nodiflora) growing in saline nutrient-deficient soil. They collected root and rhizospheric soil samples from the host monthly at a regular interval from February to June and determined the % of root bit infection as well as AM fungal spore population. They observed a number of AM fungal species. Thapar and Uniyal (1990) studied colonization of AM fungi spore in Acacia nilotica, Dalbergia sissoo, and Prosopis juliflora and also isolated saline soil sample and recorded ten AM fungi species, viz., Glomus caledonium, G. albidum, G. fasciculatus, G. macrocarpus,

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Table 2.8 Host of AM fungi in saline soil Host plant Prosopis juliflora Acacia nilotica Dalbergia sissoo Phyla nodiflora

Family Fabaceae Fabaceae Fabaceae

Locality Kurukshetra, Hisar (Haryana)

References Thapar and Uniyal (1990)

Verbenaceae

Not available

Prosopis juliflora Acacia nilotica Dalbergia sissoo Eucalyptus Spinifex littoreus Spinifex littoreus Asteriscus maritimus

Fabaceae Fabaceae Fabaceae Myrtaceae

Kurukshetra, Hisar (Haryana)

Kannan and Lakshminarasimhan (1990) Thapar and Uniyal (1990)

Poaceae

Tamil Nadu

Bhaskaran and Selvaraj (1997)

Poaceae

Not available

Selvaraj and Bhaskaran (1999)

Asteraceae

Cabo de Gata Natural Park, Spain

Estrada et al. (2013)

G. microcarpus, G. multicaulis, G. reticulatus, Gigaspora nigra, Sclerocystis coremoides, and Sclerocystis sinuosa. Thapar et al. (1991) collected saline-sodic soil (pH 9–10) sample from three districts (Kurukshetra, Hisar, and Rohtak) of Haryana state and recorded AM fungi diversity. They have isolated 16 species of AM fungi belonging to Glomus, Sclerocystis, and Scutellospora. Bhaskaran and Selvaraj (1997) studied AM fungi distribution on the basis of seasonal influence in the saline soil of Tamil Nadu. They isolated 15 different types of AM fungi species. Out of these Glomus aggregatum and Sclerocystis pakistanica were dominant. Selvaraj and Bhaskaran (1999) reported sporocarpic AM fungi associated with Spinifex littoreus and Aeluropus lagopoides in saline soil. A total of ten sporocarpic AM fungi species were reported and Glomus ambisporum was the dominant. Further, they reported the maximum colonization of Sclerocystis in the roots of Spinifex littoreus and the genera Glomus was found in the rhizospheric soil. Estrada et al. (2013) collected saline soil from Asteriscus maritimus which grows in Cabo de Gata Natural Park, Spain, and identified AM fungi species based on its spore morphology. Identified AM fungi were Rhizophagus intraradices, Claroideoglomus etunicatum, and Septoglomus constrictum.

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Interaction Between AM Fungi and Plants

The association between AM fungi and plants is obligate. AM fungi interact with the wide varieties of plants with their roots (Kour et al. 2020a; Yadav 2020; Yadav et al. 2021). Recently the interaction of AM fungi with plants and nanoparticles has been summarized by Akhtar et al. (2020a). They have concluded that the outcome of AM symbioses depends upon but is not limited to AM fungal species, host plant, and nature and concentration of nanoparticle(s) in the soil. It was a common thought that interactions of AM fungi with plants are always positive. However, in recent years it has been established that although obligatory the interaction may be neutral or negative. The association and nature of interaction depend upon AM fungi, host, growth stage of plants, soil condition, season of the climate, and environment (Kour et al. 2020d; Mondal et al. 2020). All these factors have their own fates in the establishment of AM fungal symbioses and the nature of interaction. The time when AM fungal hyphae find suitable host roots, a number of biochemical and cellular processes operate simultaneously, which could be understood under two phases: (i) the pre-symbiotic phase and (ii) symbiotic phase.

2.3.1

Pre-symbiotic Phase

The pre-symbiotic phase marks the sensation of AM fungi to roots in the soil and vice versa. AM fungi perceive the vicinity of a host via root-exuded molecules that induce spore germination and hyphal branching (Buée et al. 2000; Nagahashi and Douds Jr 2004). In this way the dialogue between the two partners starts even before the physical contact. Strigolactones (5-deoxystrigol) secreted by the host roots act as root recognition signals for AM fungi. Strigolactones are carotenoid-derived phytohormones (Al-Babili and Bouwmeester 2015), which have a primary role in plant development (Ruyter-Spira et al. 2013). It was identified in root exudates of Lotus japonicus that were responsible for hyphal branching and in germinating AM fungal spores (Akiyama et al. 2005). AM fungi sense strigolactones in root exudates at concentrations as low as 10 nM. In response to strigolactones, AM fungi secrete chitin oligomers (COs) and lipo-chitooligosaccharides (LCOs). COs and LCOs induce gene expression through the oscillation in intercellular calcium level (Besserer et al. 2006; Besserer et al. 2008; Bonfante and Genre 2015). The cascade of cellular events including gene expression and the molecules involved in the symbiotic establishment have been reviewed in detail by Gobbato (2015). The exudate-mediated communication promotes the attachment of AM fungal hyphae to the epidermis of the roots. AM fungi choose the site for initiating root penetration with utmost care. Hyphae are able to wander for quite a lot of centimeters along the root surface, hence forming hyphae which are long, straight, or gently curved, and then suddenly hyphae swell, flatten on the cell wall of some epidermal cells, and branch frequently to develop hyphopodium (Genre et al. 2005). From hyphopodium

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Fig. 2.2 Diagrammatic representation of interaction and establishment of symbiosis between AM fungi and plant. 1. In the vicinity of AM fungi root secretes strigolactones. 2. Strigolactones stimulate the germination of spore and branching in hyphae. 3. Hyphae of AM fungi secrete chitin oligomers (COs) and lipo-chitooligosaccharides (LCOs). COs and LCOs induce gene expression through the oscillation in intercellular calcium level. 4. Two-way communication approaches the AM fungal hyphae to the root epidermis and after wandering a few centimeters, it flattens to form hyphopodium. Meanwhile, host cell develops pre-penetrating apparatus (PPA). PPA is rich in endoplasmic reticulum, Golgi apparatus, secretory membranes, and cytoskeleton. 5. PPA guides the entry of hyphae into the epidermal cells. 6. In the inner cortical cell hyphae start ramifying to develop arbuscule. 7. A fully developed arbuscule. 8. Degenerating arbuscule

AM fungi enter the host epidermis and cortical cells to establish the symbiosis (Fig. 2.2).

2.3.2

Symbiotic Phase

As the hyphopodium is formed a pre-penetration apparatus (PPA) is assembled in the host cell at AM fungal contact site. This PPA is marked by the broad columnar cytoplasmic aggregation in the lumen of host cell formed by the stimulus of hyphopodium. PPA is rich in endoplasmic reticulum, Golgi apparatus, secretory membranes, and cytoskeleton (Lanfranco et al. 2017). PPA helps in the formation of perifungal membrane—an extension of host plasmalemma, which hosts the intracellular structure of the AM fungi. At this point hyphopodium branches and sends hyphae which penetrate the host cell wall and enter the cell lumen only through the PPA. PPA is also developed in other cortical cells where arbuscules are to be formed.

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At the arbuscule formation site, PPA is more extensive and forms perifungal membrane over all the fine branches of arbuscule. The perifungal membrane covering the arbuscular branches is the so-called periarbuscular membrane (PAM) that provides the symbiotic interface between the AM fungi and host (Lanfranco et al. 2017). Arbuscules collapse as well as degenerate within 2–3 days after maturity (Fig. 2.2) (Gutjahr and Parniske 2013; Kobae and Hata 2010), whereas the host cell recovers its original structure and would now be ready to host new arbuscules. A number of transport proteins, e.g., symbiotic phosphate transporter and ATP-binding cassettes, are localized in the PAMs (discussed in coming sections). These PAM-localized proteins are synthesized as a result of gene transcription and exocytosis toward the developing PAM (Lanfranco et al. 2017). The plants’ transcription factors required for the development of arbuscules were summarized by Lanfranco et al. (2017). They include RAD1 (required for arbuscule development 1), CYCLOPS, DELLAs (gibberellin repressor protein), RAM1, MtERF1, and DELLA interacting protein 1. RAM1 and RAD1 that regulate the genes required for arbuscular branching are in turn regulated by DELLA proteins (Park et al. 2015).

2.3.3

Arbuscules: The Symbiotic Interface

During the symbiotic phase of arbuscule development, a number of transporters are localized in the PAM (Fig. 2.3). These transporters provide the passage for various molecules across the PAM, e.g., phosphorus (P), nitrogen (N), sulfur (S), carbon (C), and other HMs. Wang et al. (2017) summarized the transporters for various molecules localized in the PAM and the transporters which are of plant origin and upregulated by AM fungal association. The transporters of a molecule at the soilAM fungi interface are usually different from transporters working at the AM fungiplant interface (i.e., in arbusculate cells). In plant-AM fungi interaction AM fungi are almost dependent upon the plant carbon, while it provides many of the other nutrients to the host. The transporters for carbon and other molecules, which are exclusively localized in the PAMs, are summarized in Table 2.9.

2.3.3.1

Transporter for Phosphorus (Pi)

AM fungi transport phosphorus to the plant through the arbuscule-containing cortical cell. Phosphorus is transported in the form of Pi (inorganic phosphorus) at the arbuscular interface through the transporters depicted in Fig. 15.3 and mentioned in Table 2.9. Harrison and Vanbuuren (1995) reported P-transporter GvPT in Glomus versiforme colonizing Medicago truncatula. MtPT4, a P-transporter, was described by Harrison et al. (2002) from Glomus versiforme and Gigaspora gigantea colonizing Medicago truncatula. GmosPT is a P-transporter reported by Balestrini et al. (2007) in Glomus mosseae colonizing Lycopersicon esculentum. Recently Xie et al.

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Fig. 2.3 Transporters of phosphorus, nitrogen, sulfur, and carbon identified at the arbuscular interface. These transporters are exclusively localized in the periarbuscular membrane of arbusculate cells. Phosphorus, nitrogen, and sulfur are transported from arbuscule to the host cell, while carbon (in the form of monosaccharides) is taken into the arbuscule

(2016) reported P-transporter GigmPT in Gigaspora margarita colonizing Astragalus sinicus.

2.3.3.2

Transporter for Nitrogen (NH4+)

At the arbuscular interface nitrogen is transferred in the form of NH4+ through various N-transporters depicted in Fig. 2.3 and mentioned in Table 2.9. LjAMT2;2, a N-transporter, was reported in Gigaspora margarita colonizing Lotus japonicus by Guether et al. (2009). Kobae et al. (2010) reported another N-transporter GmAMT4.1 in Glomus intraradices colonizing Glycine max. RiPTR2, a N-transporter, was described by Belmondo et al. (2014) in Rhizophagus irregularis colonizing transformed roots of Cichorium intybus. GintAMT2, a N-transporter, was identified

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Table 2.9 Identified transporters of nutrients located in the periarbuscular membrane of arbusculate cells Nutrients Phosphorus (Pi)

Transporter GvPT MtPT4

GmosPT GigmPT Nitrogen (NH4+)

LjAMT2;2 GmAMT4.1 RiPTR2 GintAMT2 GintAMT3

Sulfate

LjSultr1;2

Carbon

GpMST1 SWEET1b

AM fungi Glomus versiforme Glomus versiforme Gigaspora gigantea Glomus mosseae Gigaspora margarita Gigaspora margarita Glomus intraradices Rhizophagus irregularis Glomus intraradices Rhizophagus irregularis Rhizophagus irregularis Geosiphon pyriformis Rhizophagus irregularis

Host plant Medicago truncatula Medicago truncatula

References Harrison and Vanbuuren (1995) Harrison et al. (2002)

Lycopersicon esculentum Astragalus sinicus

Balestrini et al. (2007)

Lotus japonicus

Guether et al. (2009)

Glycine max

Kobae et al. (2010)

Cichorium intybus

Belmondo et al. (2014)

Daucus carota

Perez-Tienda et al. (2011) Calabrese et al. (2016)

Sorghum bicolor Lotus japonicus Nostoc punctiforme Medicago truncatula

Xie et al. (2016)

Giovannetti et al. (2014) Schüßler et al. (2006) An et al. (2019)

by Perez-Tienda et al. (2011) in Glomus intraradices colonizing transformed roots of Daucus carota. Recently, GintAMT3, a N-transporter, was described by Calabrese et al. (2016) in Rhizophagus irregularis colonizing Sorghum bicolor.

2.3.3.3

Transporter for Sulfate

LjSultr1;2 located in the PAM (depicted in Fig. 15.3 and mentioned in Table 2.9) of Rhizophagus irregularis colonizing Lotus japonicus was identified by Giovannetti et al. (2014). It transported sulfate from AM fungi to the host cell across the PAM.

2.3.3.4

Transporter for Heavy Metals (HMs)

HMs are found in soil which influence plant growth. AM fungal association provides the tolerance against toxic HM (Akhtar et al. 2019), but promotes the uptake of macro and micronutrients to the plant in nutrient deficiency. A number of HM

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transporters are identified in the extraradical as well as intraradical mycelium of AM fungi (Ferrol et al. 2016) that are crucial for the HM homoeostasis in AM-plant interaction. Transfer of HM from the AM fungi to the host plant at arbuscular interface is well established (González-Guerrero et al. 2016). However, such transporters localized to the PAM are yet to be identified.

2.3.3.5

Transporter for Carbon

In exchange of nutrients, AM fungi get photosynthates from the host plants. Carbon is transferred to the AM fungi at the arbuscular interface in the form of monosaccharides (MS). MS transporters localized in the PAM are depicted in Fig. 2.3 and mentioned in Table 2.9. These transports assist the transfer of fixed carbon to the AM fungi. The first sugar transporter of monosaccharide, i.e., GpMST1, was identified by Schüßler et al. (2006) in Geosiphon pyriformis (which is a symbiont with Nostoc punctiforme). SWEET1b, another sugar transporter, was identified by An et al. (2019) in the PAM of Rhizophagus irregularis colonizing Medicago truncatula. This transporter was able to maintain the arbuscule development and degeneration by transporting the glucose from host to arbuscule. A paradigm shift is about to happen with the identification of several genes found in extraradical mycelium responsible for the uptake of glucose and xylulose from the medium. The presence of RiMST2 transporter (Helber et al. 2011) and MST2 transporter (Lanfranco et al. 2017) in extraradical hyphae, which can take up glucose and xylose, suggested a partial metabolic independence of AM fungi from host plants. Two more MS transporters (i.e., RiMST5 and RiMST6) were identified by Lahmidi et al. (2016) from extraradical mycelium as well as intraradical mycelium of Rhizophagus irregularis. These are also the transporters of sugar from the soil to extraradical mycelium and from the arbusculate cells.

2.3.4

Common Mycorrhizal Network (CMN)

AM fungi play a major role in plant community dynamics and interaction among plants. Extraradical mycelium of AM fungi connects individual plants of the same or different species (Fig. 2.4) in “common mycorrhizal network” (CMN). Transfer of C via CMNs has been demonstrated from photosynthetic to non-photosynthetic plants, but its transfer within autotrophic plants remains controversial (Selosse and Roy 2009; Jalonen et al. 2009). Similarly, transfer of N via CMNs between plants is not so clear (Lekberg et al. 2010). Walder et al. (2012) by monitoring C-stable isotope tracing and 15N and 33P labeling studied the CMN Rhizophagus intraradices or Funneliformis mosseae between flax and sorghum. They found an asymmetrical exchange of C, N, and P via CMN. They also found enhanced biomass when grown together as compared to monoculture. The exchange of water through these CMNs is not untouched. Singh

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Fig. 2.4 Red lines showing common mycorrhiza network (CMN) connecting the roots of plants. 1: Big tree, 2: shallow-rooted plant, 3: deep-rooted plants. CMN provides a channel for flow of nutrient, water, and defense among the plants

et al. (2020a, b) in their study on bio-irrigation between deep-rooted pigeon pea and shallow-rooted finger millet reported the hydraulic lift of water column via CMN. They have found that CMN provided by Rhizophagus fasciculatus and Ambispora leptoticha could have promoted the water to the shallow-rooted finger millet even in drought stress. In addition to this CMN provides the passage of defense signals between the plants on pathogenic attack. Song et al. (2010) reported upregulation of six defense-related genes in an uninfected plant, which was connected via CMN to a plant attacked by pathogenic fungus Alternaria solani. Similar finding was also obtained by Song et al. (2014) in insect-attacked plants.

2.4 2.4.1

Application of AM Fungi Application of AM Fungi Alleviates Water Stress in Plants

Deficiency of water is known as drought. It means the absence of sufficient water that is needed for the growth and development of plants. Drought is one of the major serious abiotic stresses in the soil. Around the globe approximately one-third of soils are subjected to drought stress, which limits plant growth and development and

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decreases the total crop production in numerous regions of the world (Calvo-Polanco et al. 2016; Kour et al. 2019a). Drought stress increases cell dehydration, lowers soil water potential and ultimately resulting in inhibition of cell expansion and division, root proliferation, nutrient uptake, stem elongation, and water-use efficiency (Kour et al. 2020b, c). AM fungal symbiosis can improve plant growth by improving plant biomass, leaf area, root length, and nutrient uptake under drought condition (Kapoor et al. 2013; Gong et al. 2013; Pagano 2014; Latef et al. (2016). Application of AM fungi under water-stressed condition exhibited greater level of photosynthetic pigments (Yooyongwech et al. 2016), transpiration rates, stomatal conductivity, relative water condition, higher water potential, and lower leaf temperature (Wu and Xia 2006). AM fungi application resulted in enhanced P uptake (Farahani et al. 2008) and improved antioxidant defense system (Zhang et al. 2015; Wu and Zou 2017) in plants under water-scarce condition. AM fungi do so by hormonal cross talk with plants (Bernardo et al. 2019).

2.4.2

Application of AM Fungi Alleviates Salt Stress in Plants

Salinity in soil is the most serious problem in the world that is decreasing the soil productivity day by day. Approximately more than 1 billion ha of total land in arid and semiarid regions of the world (Abdel Latef 2010) is salt stressed. Plants growing in salt-affected land are showing stunted growth, low nutrient uptake, and decreased distribution of ions. Higher accumulation of salt (Na+ and Cl) in plant tissue leads to oxidative damage, affecting the integrity of plant membranes (damage to lipids, proteins, and nucleic acids), impairing activities of biocatalysts and functioning of photosynthetic apparatus, which causes deleterious effects of the reactive oxygen species (Kumar et al. 2014; Kumar et al. 2019; Sharaff et al. 2020). Microorganisms present in the rhizosphere, viz., nitrogen-fixing bacteria, phosphate solubilizers, and mycorrhizae, can be useful, which alleviate the detrimental effects of salt stress (Rai et al. 2020; Rajawat et al. 2020; Yadav et al. 2018a). AM fungi are considered as the most effective biological tool for alleviation of salt stress in plants. A number of studies suggested that AM fungi improve salt tolerance in different plant species such as clover, tomato, cucumber, fenugreek, maize, lettuce, sesbania, and acacia (Ruiz-Lozano et al. 1996; Al-Karaki 2000; Feng et al. 2002; Giri et al. 2003, 2007; Giri and Mukerji 2004; Evelin et al. 2012, 2013). Application of AM fungi for improving stomatal conductance, root hydraulic conductivity, photosynthetic capacity, accumulation of enzymatic and nonenzymatic antioxidants, water-use efficiency, detoxification of damaging reactive oxygen species, and osmotic adjustment has been evidenced in AM plants growing under salinity stress (Sharifi et al. 2007; Sheng et al. 2008; Evelin et al. 2009; Abdel Latef and Chaoxing 2011; Porcel et al. 2012; Kumar et al. 2014; Auge et al. 2014). AM fungi play an important role in the alleviation of salt stress by increasing Ca, P, and K uptake and K/Na and Ca/Na ratios, while also increasing carbon assimilation

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by promoting the conductance of stomata (Hajiboland et al. 2010). Application of AM fungi regulates many mechanisms such as control of water and ionic homeostasis, accumulation of osmolytes (compatible organic solutes), reduction in the oxidative damage, maintenance of photosynthetic processes, and control over ultrastructure alteration for survival of plants under salt stresses (Latef et al. 2016; Saxena et al. 2017; Porcel et al. 2012; Atakan et al. 2018; Kehri et al. 2016).

2.4.3

Application of AM Fungi Alleviates Cold Stress in Plants

Low temperature is one of the serious abiotic stresses for growth, development, and production of plants (Zhu et al. 2011). Low temperature can cause deleterious effect on plants such as plasma membrane integrity, cellular osmotic potential, and restriction of antioxidant metabolism that lead to loss of structural stability of major proteins (Paredes and Quiles 2015; Yadav et al. 2015a, b, 2016). Visible effects caused due to low temperature include growth retardation, reduced leaf area, wilting, chlorosis, loss of stomatal movements, reduction in hydraulic conductance, and decreased photosynthesis (Paredes and Quiles 2015). A number of studies have been conducted by researchers (Duhamel and Vandenkoornhuyse 2013; Latef et al. 2016; Zhu et al. 2017; Hashem et al. 2018; Begum et al. 2019) to alleviate the cold stress in plants by application of AM fungi.

2.4.4

Application of AM Fungi Improves the Phytoremediation of HM-Contaminated Soils

Contamination of soil with HMs may impose negative effects on natural resources as well as ecosystem that pose danger effects on human health by contamination of food chain (Peuke and Rennenberg 2005; Ren et al. 2015). However some metals are essential for plant growth and its activity but in limited concentration; for example, iron (Fe), copper (Cu), nickel (Ni), zinc (Zn), and manganese (Mn) help in electron transfer in plants and also parts of several enzymes (Zenk 1996); Cu and Zn are involved in seed production, flowering, and growth in plants (Vamerali et al. 2010). In contrast, several HMs, viz., cadmium (Cd), lead (Pb), mercury (Hg), and arsenic (As), are nonessential (Mertz 1981). An increased metal concentration in soil in higher amount can lead to negative effects upon ecosystem as well as human health (Sharma et al. 2021). AM fungi have been well applied in phytoremediation. Phytoremediation is one of the best strategies to remediate HMs from the soil by using several organisms including AM fungi. This method is eco-friendly that uses plants to extract HMs from contaminated soil to a level that makes them available for private and public

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use. Application of AM fungi modulates the HM extraction from soil, when associated with hyperaccumulator plants (Zoomi et al. 2019). Concomitant to the enhanced HM uptake (Khan et al. 2014), application of AM fungi enhances the nutrient acquisition from the soil (Leung et al. 2013). Application of AM fungi alleviates the Zn (Christie et al. 2004), Pb (Bahraminia et al. 2016; Yang et al. 2016), and Hg (Yu et al. 2010) toxicity in plants. AM fungi have also been applied in phytoremediation of lead-zinc mining area (Yang et al. 2015). AM fungi improved the growth performance of tomato plant raised under Cr-rich substrate without causing any translocation of Cr to the edible parts (Akhtar et al. 2020b)

2.4.5

Application of AM Fungi Enhances Sustainable Agriculture Production

Maintenance of high agricultural productivity for fulfilling global food demands has been a major challenge for developed and developing countries. As a result of extensive use of fertilizers, the agrochemicals and agronomic practices commonly adopted in intensive production systems have generated environmental problems including deterioration of soil quality, surface water, and groundwater, and reduced biodiversity and function of ecosystems. If agricultural systems are to be sustainable in terms of sustained soil fertility and soil structure over a long period of time, management strategies that are environmentally safe, economically viable, and socially fair are needed (Subrahmanyam et al. 2020; Prasad et al. 2021; Hesham et al. 2021; Rastegari et al. 2020a, b). For the maintenance of sustainable agriculture productivity microbial biodiversity plays a major role. These microorganisms reside surrounding the zone of root, the so-called rhizosphere. AM fungi are one of the important biological tools used in the agriculture field for the maintenance of sustainable agriculture and an increase in food production (Pandey et al. 2019). AM fungi are well known for its beneficial activities such as uptake and transfer of nutrient (P, N, Zn), suppression of soil plant pathogen, enhancement of stress tolerance activity, and reduction of toxicity from the polluted soil (Rastegari et al. 2020b). AM inoculants are being commercialized as fertilizers to enhance agriculture production. Application of Rhizophagus irregularis through seed coating in Triticum aestivum resulted in growth improvement (Oliveira et al. 2016). The improvement was the consequence of enhanced nutrient absorption. Applications of AM fungi as biofertilizers have been used by Igiehon and Babalola (2017) and Akyol et al. (2018) to enhance agricultural production.

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Application of AM Fungi Controls the Plant Diseases

AM fungal symbioses improve host resistance against pathogens and pests and act as biocontrol agents (Whipps 2004; Pozo and Azcon-Aguilar 2007; Smith and Read 2008; Jung et al. 2012). Application of Glomus bagyarajii was proved to be a good biocontrol agent against wilt disease in tomato caused by Ralstonia solanacearum and Phytophthora capsica (Kumar et al. 2018). Glomus deserticola and Glomus clarum have been applied as a biocontrol agent against ear rot of Zea mays caused by Fusarium verticillioides (Olowe et al. 2018). The efficiency of AM fungi as a biocontrol agent is further enhanced when applied in combination with Trichoderma harzianum or T. viride. Combination of both the biocontrol agents was proved to be much more effective against diseases such as tobacco bacterial wilt caused by Ralstonia solanacearum (Yuan et al. 2016), stem rust disease caused by Puccinia graminis f. sp. tritici (El-Sharkawy et al. 2018), and basal rot of onion caused by Fusarium oxysporum f. sp. cepae (Rajeswari et al. 2019).

2.5

Conclusion

Across the 9 major biomes (i.e., alpine, temperate, tropical region, deserts, mangroves, HM-polluted and mining field, acidic, alkaline, and saline soils) of the world a total of 63 research articles dealing with the diversity of AM fungi were summarized under 8 subheadings and tables. Many of the research articles were not included in this chapter because of lack of specified host in natural ecosystems or redundancy in publication. A total of 77 families and 347 genera of vascular plants (pteridophytes, gymnosperms, and angiosperms) were showing the AM fungal association. The families, e.g., Amaranthaceae and Chenopodiaceae, which are generally non-mycorrhizal were reported to be mycorrhizal. Among 9 major biomes diversity was most studied in Fabaceae, followed by Asteraceae, Poaceae, Euphorbiaceae, Lamiaceae, and Rubiaceae (Fig. 2.5). The diversity of AM fungi was also studied in Pinaceae and Taxaceae of gymnosperm and Ophioglossaceae of pteridophyte. Interaction between plants and AM fungi is reciprocal as bidirectional exchange of nutrients takes place through the wide array of transporters located at the PAM in the arbusculate cell. Many of the transporters for P, N, and S are identified, but HM transporters localized in the PAM are unidentified. Much work is needed in understating the symbiotic interaction at the carbon edge. It was a common thought that AM fungi are fully dependent upon its host for carbon; however, it is now clear that AM fungi have several carbon transporter genes of their own, which can take up monosaccharides from the medium directly through extraradical mycelium. AM fungi as CMN provide a very extensive system of underground network between intercropped plants in terms of exchange of nutrients, water, and defense signals. However, our understanding is meager on CMN communication system and

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Fabaceae Apocynaceae Solanaceae Convolvulaceae Rosaceae Gentianaceae Adiantaceae Burseraceae Costaceae Moringaceae Smilaceae

Asteraceae Rhizophoraceae Verbenaceae Cupressaceae Rutaceae Liliaceae Aristolochiaceae Campanulaceae Dioscoreaceae Ophioglossaceae Styracaceae

Poaceae Amaranthaceae Crassulaceae Lythraceae Scrophulariaceae Meliaceae Asclepiadaceae Caricaceae Fagaceae Pedaliaceae Symplocaceae

Euphorbiaceae Ericaceae Cyperaceae Menispermaceae Anacardiaceae Pinaceae Asparagaceae Casuarinaceae Goodeniaceae Phyllanthaceae Taxaceae

Lamiaceae Malvaceae Myrtaceae Mimosaceae Araliaceae Piperaceae Balsaminaceae Colchicaceae Lauraceae Primulaceae Tiliaceace

Rubiaceae Amaryllidaceae Apiaceae Moraceae Brassicaceae Salicaceae Begoniacaece Commelinaceae Magnoliaceae Ranunculaceae Urticaceae

Acanthaceae Arecaceae Caryophyllaceae Polygonaceae Cucurbitaceae Vitaceae Boraginaceae Companulaceae Molluginaceae Simaroubaceae Violaceae

Fig. 2.5 Pie chart showing the cumulative diversity of AM fungi in 77 families of land plants inhabiting various habitats. Number in front of families represents the number of plant genera found to be associated with AM fungi. The data is cumulative of a total of 63 research studies dealing with biodiversity of AM fungi

still there is much more to be explored. More is to be worked out on CMN in the field ecosystems, where these associations become robust because of coexistence of multiple soil microorganisms in the microhabitat. AM fungi have numerous potential applications such as biofertilizer and biocontrol agent. AM fungi have been successfully applied in the restoration of degraded habitats. Consortium and monoxenic cultures of AM fungi have been well applied in sustainable agricultural production, phytoremediation, and protection of plants from biotic as well as abiotic stresses. Application of AM fungi protects the plants from cold, drought, acidic, alkaline, and saline stresses.

References Abdel Latef A (2010) Changes of antioxidative enzymes in salinity tolerance among different wheat cultivars. Cereal Res Commun 38(1):43–55 Abdel Latef AA, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127:228–233. https://doi.org/10.1016/j.scienta.2010.09.020 Abdelhalim TS, Finckh MR, Babiker AG, Oehl F (2014) Species composition and diversity of arbuscular mycorrhizal fungi in White Nile state, Central Sudan. Arch Agron Soil Sci 60 (3):377–391. https://doi.org/10.1080/03650340.2013.793453 Akhtar O, Mishra R, Kehri HK (2019) Arbuscular mycorrhizal association contributes to Cr accumulation and tolerance in plants growing on Cr contaminated soils. Proc Natl Acad Sci India Sect B Biol Sci 89:63–70. https://doi.org/10.1007/s40011-017-0914-4

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Akhtar O, Kehri HK, Zoomi I (2020b) Arbuscular mycorrhiza and Aspergillus terreus inoculation along with compost amendment enhance the phytoremediation of Cr-rich technosol by Solanum lycopersicum under field conditions. Ecotoxicology and Environmental Safety, 201, p.110869. https://doi.org/10.1016/j.ecoenv.2020.110869 Akhtar O, Zoomi I, Pandey D, Kehri HK, Narayan RP (2020a) Tripartite interaction among nanoparticles, symbiotic microbes and plants: current scenario and future perspectives. In: Bhushan I, Singh V, Tripathi D (eds) Nanomaterials and environmental biotechnology. Nanotechnology in the life sciences. Springer, Cham, pp 55–64. https://doi.org/10.1007/978-3-03034544-0_4 Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827. https://doi.org/10.1038/nature03608 Akyol TY, Niwa R, Hirakawa H, Maruyama H, Sato T, Suzuki T, Saito M (2018) Impact of introduction of arbuscular Mycorrhizal fungi on the root microbial community in agricultural fields. Microbes Environ 34(1):23–32. https://doi.org/10.1264/jsme2.ME18109 Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186. https://doi.org/10.1146/annurev-arplant-043014-114759 Alguacil MD, Lozano Z, Campoy M, Roldan A (2010) Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol Biochem 42:1114–1122. https://doi.org/10.1016/j.soilbio.2010.03.012 Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10:51–54 Al-Yahya’ei MN, Oehl F, Vallino M, Lumini E, Redecker D, Wiemken A, Bonfante P (2011) Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of Southern Arabia. Mycorrhiza 21(3):195–209. https://doi.org/10. 1007/s00572-010-0323-5 An J, Zeng T, Ji C, de Graaf S, Zheng Z, Xiao TT, Deng X, Xiao S, Bisseling T, Limpens E, Pan Z (2019) A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytol 224(1):396–408. https://doi.org/10.1111/nph. 15975 Atakan A, Özkaya HÖ, Erdoğan O (2018) Effects of Arbuscular Mycorrhizal Fungi (AMF) on heavy metal and salt stress. TURJAF 6(11):1569–1574. https://doi.org/10.24925/turjaf.v6i11. 1569-1574.1992 Auge RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front Plant Sci 5:562–574. https://doi.org/10. 3389/fpls.2014.00562 Bahraminia M, Zarei M, Ronaghi A, Ghasemi-Fasaei R (2016) Effectiveness of arbuscular mycorrhizal fungi in phytoremediation of lead-contaminated soil by vetiver grass. Int J Phytoremediation 18(7):730–737. https://doi.org/10.1080/15226514.2015.1131242 Bala K, Rao AV, Tarafdar JC (1989) Occurrence of VAM associations in different plant species of the Indian desert. Arid Land Res Manag 3(3):391–396. https://doi.org/10.1080/ 15324988909381215 Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant-Microbe Interact 20:1055–1062 Beena KR, Arun AB, Raviraja NS, Sridhar KR (2001) Association of arbuscular mycorrhizal fungi with plants of coastal and dunes of west coast of India. Trop Ecol 42(2):213–222 Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ahmed N, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068 Belmondo S, Fiorilli V, Pérez-Tienda J, Ferrol N, Marmeisse R, Lanfranco L (2014) A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase. Front Plant Sci 5:1–11. https://doi.org/10.3389/fpls.2014.00436

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

73

Bernardo L, Carletti P, Badeck FW, Rizza F, Morcia C, Ghizzoni R, Lucini L (2019) Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol Bioch 137:203–212. https://doi.org/10.1016/j.plaphy.2019.02.007 Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4(7):1239–1247. https://doi.org/10.1371/journal.pbio. 0040226 Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413. https://doi. org/10.1104/pp.108.121400 Bhaskaran C, Selvaraj T (1997) Seasonal incidence and distribution of VA-mycorrhizal fungi in native saline soils. J Environ Biol 18(3):209–212 Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154. https://doi.org/10.1016/j.tplants.2014.12.002 Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115 Buck MT, Straker CJ, Mavri-Damelin D, Weiersbye IM (2019) Diversity of arbuscular mycorrhizal (AM) fungi colonising roots of indigenous Vachellia and Senegalia trees on gold and uranium mine tailings in South Africa. S Afr J Bot 121:34–44. https://doi.org/10.1016/j.sajb.2018.10.014 Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant-Microbe Interact 13:693–698. https://doi.org/10.1094/MPMI.2000.13.6. 693 Calabrese S, Perez-Tienda J, Ellerbeck M, Arnould C, Chatagnier O, Boller T, Schussler A, Brachmann A, Wipf D, Ferrol N, Courty PE (2016) GintAMT3-a low-affinity ammonium transporter of the arbuscular mycorrhizal Rhizophagus irregularis. Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.00679 Calvo-Polanco M, Sánchez-Romera B, Aroca R (2016) Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environ Exp Bot 131:47–57 Chandra KK, Jamaluddin (1999) Distribution of vesicular arbuscular mycorrhizal fungi in coal mine overburden dumps. Indian Phytopathol 52(3):254–258 Channabasava A, Lakshman HC (2013) Diversity and efficacy of AM fungi on Jatropha curcas L., and Panicum miliaceum L., in mine spoils. J Agric Technol 9(1):83–93 Chaturvedi S, Tewari V, Sharma S, Oehl F, Wiemken A, Prakash A, Sharma AK (2012) Diversity of arbuscular mycorrhizal fungi in Oak-Pine forests and agricultural land prevalent in the Kumaon Himalayan Hills, Uttarakhand, India. Br Microbiol Res J 2(2):82 Chaudhry MS, Nasim FH, Khan AG (2006) Mycorrhizas in the perennial grasses of Cholistan Desert, Pakistan. Int J Bot 2(2):210–218. https://doi.org/10.3923/ijb.2006.210.218 Chaurasia B, Pandey A, Palni LMS (2005) Distribution, colonization and diversity of arbuscular mycorrhizal fungi associated with central Himalayan rhododendrons. Forest Ecol Manag 207 (3):315–324. https://doi.org/10.1016/j.foreco.2004.10.014 Christie P, Li X, Chen B (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261(1-2):209–217 D’Souza J, Rodrigues BF (2013a) Biodiversity of Arbuscular Mycorrhizal (AM) fungi in mangroves of Goa in West India. J For Res 24(3):515–523. https://doi.org/10.1007/s11676-0130342-0 D’Souza J, Rodrigues BF (2013b) Seasonal diversity of arbuscular mycorrhizal fungi in mangroves of Goa, India. Int J Biodivers Sci Ecosyst Serv Manag 2013:1–7. https://doi.org/10.1155/2013/ 196527

74

U. Singh et al.

Duhamel M, Vandenkoornhuyse P (2013) Sustainable agriculture: possible trajectories from mutualistic symbiosis and plant neodomestication. Trends Plant Sci 18(11):597–600. https:// doi.org/10.1016/j.tplants.2013.08.010 El-Sharkawy HH, Rashad YM, Ibrahim SA (2018) Biocontrol of stem rust disease of wheat using arbuscular mycorrhizal fungi and Trichoderma spp. Physiol Mol Plant P 103:84–91. https://doi. org/10.1016/j.pmpp.2018.05.002 Eo JK, Park SH, Lee EH, Eom AH (2014) Biodiversity and distribution of Arbuscular mycorrhizal fungi in Korea. Kor J Mycol 42:255–261. https://doi.org/10.4489/KJM.2014.42.4.255 Estrada B, Beltrán-Hermoso M, Palenzuela J, Iwase K, Ruiz-Lozano JM, Barea JM, Oehl F (2013) Diversity of arbuscular mycorrhizal fungi in the rhizosphere of Asteriscus maritimus (L.) Less., a representative plant species in arid and saline Mediterranean ecosystems. J Arid Environ 97:170–175. https://doi.org/10.1016/j.jaridenv.2013.05.019 Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280. https://doi.org/10.1093/aob/mcp251 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 22:203–217. https://doi.org/10.1007/s00572-011-0392-0 Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23(1):71–86. https://doi.org/10.1007/s00572-0120449-8 Farahani HA, Lebaschi MH, Hamidi A (2008) Effects of arbuscular mycorrhizal fungi, phosphorus and water stress on quantity and quality characteristics of coriander. ANAS 2(2):55–60 Feng G, Zhang FS, Xl L (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190. https://doi.org/10.1007/s00572-002-0170-0 Ferrol N, Tamayo E, Vargas P (2016) The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. J Exp Bot 67:6253–6265. https://doi.org/10.1093/ jxb/erw403 Gaur S, Kaushik P (2011) Analysis of vesicular arbuscular mycorrhiza associated with medicinal plants in Uttarakhand state of India. World Appl Sci J 14(4):645–653 Gavito ME, Pérez-Castillo D, González-Monterrubio CF, Vieyra-Hernández T, Martínez-Trujillo M (2008) High compatibility between arbuscular mycorrhizal fungal communities and seedlings of different land use types in a tropical dry ecosystem. Mycorrhiza 19(1):47–60. https:// doi.org/10.1007/s00572-008-0203-4 Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499. https://doi.org/10.1105/tpc.105.035410 Giovannetti M, Tolosano M, Volpe V, Kopriva S, Bonfante P (2014) Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619. https://doi.org/10.1111/nph.12949 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 14:307–312. https://doi.org/10.1007/s00572-003-0274-1 Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175. https://doi.org/10.1007/s00374-003-0636-z 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. https://doi.org/10.1007/s00248-007-9239-9 Gobbato E (2015) Recent developments in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 26:1–7. https://doi.org/10.1016/j.pbi.2015.05.006

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

75

Gong M, Tang M, Chen H, Zhang Q, Feng X (2013) Effects of two Glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. New For 44:399–340. https://doi.org/10.1007/s11056-012-9349-1 González-Guerrero M, Escudero V, Saéz Á, Tejada-Jiménez M (2016) Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia. Front Plant Sci 7:1088. https://doi.org/10.3389/fpls.2016.01088 Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83. https://doi.org/10.1104/pp.109. 136390 Gupta N, Bihari KM, Sengupta I (2016) Diversity of arbuscular mycorrhizal fungi in different salinity of mangrove ecosystem of Odisha, India. Adv Plant Agric Res 3(1):85. https://doi.org/ 10.15406/apar.2016.03.00085 Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617. https://doi.org/10.1146/annurev-cellbio-101512-122413 Hajiboland R, Aliasgharzadeh N, Laiegh SF (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327. https://doi.org/10.1007/s11104-009-0255-z Hamel C, Dalpé Y, Lapierre C, Simard RR, Smith DL (1994) Composition of the vesiculararbuscular mycorrhizal fungi population in an old meadow as affected by pH, phosphorus and soil disturbance. Agric Ecosyst Environ 49(3):223–231. https://doi.org/10.1016/0167-8809(94) 90051-5 Harrison MJ, Vanbuuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629 Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429. https://doi.org/10.1105/tpc.004861 Hashem A, Abd Allah EF, Alqarawi AA, Egamberdieva D (2018) Arbuscular mycorrhizal fungi and plant stress tolerance. In: Egamberdieva D, Ahmed P (eds) Plant microbiome: stress response. Springer, Singapore, pp 81–103. https://doi.org/10.1007/978-981-10-5514-04 Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823. https://doi.org/10.1105/tpc. 111.089813 Hesham AE-L, Kaur T, Devi R, Kour D, Prasad S, Yadav N et al (2021) Current trends in microbial biotechnology for agricultural sustainability: conclusion and future challenges. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 555–572. https://doi.org/10.1007/978-981-15-6949-4_22 Igiehon NO, Babalola OO (2017) Biofertilizers and sustainable agriculture: exploring arbuscular mycorrhizal fungi. Appl Microbiol Biotechnol 101(12):4871–4881. https://doi.org/10.1007/ s00253-017-8344-z Jaiswal V, Rodrigues BF (2001) Occurrence and distribution of arbuscular mycorrhizal fungi in coastal sand dune vegetation of Goa. Curr Sci 80(7):826–827 Jalonen R, Nygren P, Sierra J (2009) Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant Cell Environ 32:1366–1376. https://doi.org/10.1111/j.1365-3040.2009.02004.x Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defences. J Chem Ecol 38:651–666. https://doi.org/10.1007/s10886-012-01346 Kaidzu T, Suzuki K, Sugiyama H, Akca MO, Ergül A, Turgay OC, Nonaka M, Harada N (2019) The composition characteristics of arbuscular mycorrhizal fungal communities associated with barley in saline-alkaline soils in Central Anatolia. J Soil Sci Plant Nutr:1–7. https://doi.org/10. 1080/00380768.2019.1706432

76

U. Singh et al.

Kannan K, Lakshminarasimhan C (1990) Development of endomycorrhizae in Phyla nodiflora. In: Bagyaraj DJ, Manjunath A (eds) Mycorrhizal symbiosis and plant growth. U. A. S. Bangalore, Bangalore, pp 18–20 Kapoor R, Evelin H, Mathur P, Giri B (2013) Arbuscular mycorrhiza: approaches for abiotic stress tolerance in crop plants for sustainable agriculture. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, Cham, pp 359–401. https://doi.org/10.1007/978-1-46145001-6_14 Kehri HK, Akhtar O (2018) Approaches in studying the diversity of arbuscular mycorrhizal fungi. In: Singh S (ed) Biodiversity: monitoring management and utilization. Astral International (P) Ltd, New Delhi, pp 91–110 Kehri HK, Khare V, Akhtar O, Zoomi I (2016) Arbuscular Mycorrhizal Fungi; Potential Inoculants for Cultivation of Aromatic Plant Vetiveria zizanioides in Alkaline Soil. J Ind Bot Soc 95 (1&2):125–134 Kehri HK, Akhtar O, Zoomi I, Pandey D (2018) Arbuscular mycorrhizal fungi: taxonomy and its systematics. Int J Life Sci Res 6(4):58–71 Khade SW, Adholeya A (2009) Arbuscular mycorrhizal association in plants growing on metalcontaminated and noncontaminated soils adjoining Kanpur tanneries, Uttar Pradesh, India. Water Air Soil Pollut 202(1-4):45–56. https://doi.org/10.1007/s11270-008-9957-8 Khade SW, Rodrigues BF, Sharma PK (2009) Arbuscular mycorrhizal status and root phosphatase activities in vegetative Carica papaya L. varieties. Acta Physiol Plant 32:565–574. https://doi. org/10.1007/s11738-009-0433-x Khan AG (2001) Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent-polluted soil. Environ Int 26(5-6):417–423. https://doi.org/10.1016/S0160-4120(01)00022-8 Khan A, Sharif M, Ali A, Shah SNM, Mian IA, Wahid F, Ali N (2014) Potential of AM fungi in phytoremediation of heavy metals and effect on yield of wheat crop. Am J Plant Sci 5:1578–1586. https://doi.org/10.4236/ajps.2014.511171 Kobae Y, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353. https://doi.org/10.1093/pcp/pcq013 Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415. https://doi.org/10.1093/pcp/pcq099 Koomen I, McGram SP, Giller KE (1990) Mycorrhizal infection of clover is delayed in soils contaminated with heavy metals from past sewage sludge applications. Soil Biol Biochem 22 (6):871–873 Kothamasi D, Kothamasi S, Bhattacharyya A, Kuhad RC, Babu CR (2006) Arbuscular mycorrhizae and phosphate solubilising bacteria of the rhizosphere of the mangrove ecosystem of Great Nicobar island, India. Biol Fertil Soils 42(4):358–361. https://doi.org/10.1007/s00374-0050035-8 Kour D, Rana KL, Yadav AN, Yadav N, Kumar V, Kumar A et al (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/10.1007/978-981-136536-2_13 Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA et al (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 International Publishing, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1 Kour D, Kaur T, Devi R, Rana KL, Yadav N, Rastegari AA et al (2020a) Biotechnological applications of beneficial microbiomes for evergreen agriculture and human health. In:

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

77

Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 255–279. https://doi.org/10.1016/B978-0-12-820528-0.00019-3 Kour D, Rana KL, Sheikh I, Kumar V, Yadav AN, Dhaliwal HS et al (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 B. https://doi. org/10.1007/s40011-019-01151-4 Kour D, Rana KL, Yadav AN, Sheikh I, Kumar V, Dhaliwal HS et al (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 3:23–34. https://doi.org/ 10.1007/s42398-020-00094-1 Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V et al (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 Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM (2015) Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One 10(6):0128784. https:// doi.org/10.1371/journal.pone.0128784 Kulkarni SS, Raviraja NS, Sridhar KR (1997) Arbuscular mycorrhizal fungi of tropical sand dunes of west coast of India. J Coast Res 13:931–936 Kumar A, Dames JF, Gupta A (2014) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Rev Biotechnol 35:461–474. https://doi.org/10.3109/07388551.2014.899964 Kumar MR, Ashwin R, Bagyaraj DJ (2018) Screening arbuscular mycorrhizal fungi in order to select the best for alleviating wilt disease complex of capsicum. Proc Natl Acad Sci India Sect B Biol Sci 88(2):679–684. https://doi.org/10.1007/s40011-016-0804-1 Kumar V, Joshi S, Pant NC, Sangwan P, Yadav AN, Saxena A et al (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/10.1007/978-981-15-06901_8 Lahmidi NA, Courty PE, Brule D, Chatagnier O, Arnould C, Doidy J, Berta G, Lingua G, Wipf D, Bonneau L (2016) Sugar exchanges in arbuscular mycorrhiza: RiMST5 and RiMST6, two novel Rhizophagus irregularis monosaccharide transporters, are involved in both sugar uptake from the soil and from the plant partner. Plant Physiol Biochem 107:354–363 Lanfranco L, Bonfante P, Genre A (2017) The mutualistic interaction between plants and arbuscular mycorrhizal fungi. In: Heitman J, Howlett BJ, Crous PW (eds) The fungal kingdom. American Society for Microbiology, Washington, DC, pp 727–747. https://doi.org/10.1128/ microbiolspec.FUNK-0012-2016 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. https://doi.org/10.1007/s12374-016-0237-7 Leal PL, Siqueira JO, Stürmer SL (2013) Switch of tropical Amazon forest to pasture affects taxonomic composition but not species abundance and diversity of arbuscular mycorrhizal fungal community. Appl Soil Ecol 71:72–80. https://doi.org/10.1016/j.apsoil.2013.05.010 Leal PL, Varón-López M, de Oliveira Prado IG, dos Santos JV, Soares CRFS, Siqueira JO, de Souza Moreira FM (2016) Enrichment of arbuscular mycorrhizal fungi in a contaminated soil after rehabilitation. Braz J Microbiol 47(4):853–862. https://doi.org/10.1016/j.bjm.2016.06.001 Lekberg Y, Hammer EC, Olsson PA (2010) Plants as resource islands and storage units: adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345. https://doi.org/10.1111/j.1574-6941.2010.00956.x

78

U. Singh et al.

Leung HM, Zhen-Wen W, Zhi-Hong YE, Kin-Lam Y, Xiao-Ling P, Cheung KC (2013) Interactions between arbuscular mycorrhizae and plants in phytoremediation of metal-contaminated soils: a review. Pedosphere 23(5):549–563 Likar M, Hančević K, Radić T, Regvar M (2013) Distribution and diversity of arbuscular mycorrhizal fungi in grapevines from production vineyards along the eastern Adriatic coast. Mycorrhiza 23(3):209–219. https://doi.org/10.1007/s00572-012-0463-x Marschner H (1995) Mineral nutrition of higher plants. (Academic Press Limited: London). Mineral nutrition of higher plants, 2nd edn. Academic Press Limited, London Mathur N, Singh J, Bohra S, Vyas A (2007) Arbuscular mycorrhizal status of medicinal halophytes in saline areas of Indian Thar Desert. Int J Soil Sci 2(2):119–127 Mehrotra VS (1998) Arbuscular mycorrhizal associations of plants colonizing coal mine spoil in India. J Agric Sci 130(2):125–133. https://doi.org/10.1017/S0021859697005091 Mertz W (1981) The essential trace elements. Science 213:1332–1338 Mondal S, Halder SK, Yadav AN, Mondal KC (2020) Microbial consortium with multifunctional plant growth promoting attributes: future perspective in agriculture. In: Yadav AN, Rastegari AA, Yadav N, Kour D (eds) Advances in plant microbiome and sustainable agriculture, vol 2. Functional annotation and future challenges. Springer, Singapore, pp 219–254. https://doi. org/10.1007/978-981-15-3204-7_10 Moreira-Souza M, Trufem SFB, Gomes-da-Costa SM, Cardoso EJBN (2003) Arbuscular mycorrhizal fungi associated with Araucaria angustifolia (Bert.) O. Ktze. Mycorrhiza 13:211–215. https://doi.org/10.1007/s00572-003-0221-1 Morton J (1986) Three new species of Acaulospora (Endogonaceae) from high aluminum, low pH soils in West Virginia. Mycologia 78:641–648. https://doi.org/10.1080/00275514.1986. 12025300 Nadji W, Belbekri N, Ykhlef N, Djekoun A (2017) Diversity of arbuscular mycorrhizal fungi of durum Wheat (Triticum durum Desf.) fields of the East of Algeria. J Agric Sci 9(3):117–127. https://doi.org/10.5539/jas.v9n3p117 Nagahashi G, Douds DD Jr (2004) Isolated root caps, border cells, and mucilage from host roots stimulate hyphal branching of the arbuscular mycorrhizal fungus, Gigaspora gigantea. Mycol Res 108(9):1079–1088. https://doi.org/10.1017/S0953756204000693 Oliveira RS, Vosátka M, Dodd JC, Castro PML (2005) Studies on the diversity of arbuscular mycorrhizal fungi and the efficacy of two native isolates in a highly alkaline anthropogenic sediment. Mycorrhiza 16(1):23–31. https://doi.org/10.1007/s00572-005-0010-0 Oliveira CA, Sa NMH, Gomes EA, Marriel IE, Scotti MR, Guimaraes CT, Schaffert RE, Alves VMC (2009) Assessment of the mycorrhizal community in the rhizosphere of maize (Zea mays L.) genotypes contrasting for phosphorus efficiency in the acid savannas of Brazil using denaturing gradient gel electrophoresis (DGGE). Appl Soil Ecol 41:249–258. https://doi.org/ 10.1016/j.apsoil.2008.11.005 Oliveira RS, Rocha I, Ma Y, Vosátka M, Freitas H (2016) Seed coating with arbuscular mycorrhizal fungi as an ecotechnological approach for sustainable agricultural production of common wheat (Triticum aestivum L.). J Toxicol Environ Health A 79(7):329–337. https://doi.org/10.1080/ 15287394.2016.1153448 Olowe OM, Olawuyi OJ, Sobowale AA, Odebode AC (2018) Role of arbuscular mycorrhizal fungi as biocontrol agents against Fusarium verticillioides causing ear rot of Zea mays L. (Maize). Curr Plant Biol 15:30–37. https://doi.org/10.1016/j.cpb.2018.11.005 Oves M, Khan MS, Zaidi A, Ahmad E (2012) Soil contamination, nutritive value, and human health risk assessment of heavy metals: an overview. In: Zaidi A, Wani PA, Khan MS (eds) Toxicity of heavy metals to legumes and bioremediation. Springer, New York, pp 1–27. https://doi.org/10. 1007/978-3-7091-0730-0_1 Pagano MC (2014) Drought stress and mycorrhizal plants. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer, New York, pp 97–110. https://doi.org/10.1007/978-14614-9466-9_5

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

79

Pandey D, Kehri HK, Zoomi I, Akhtar O, Singh AK (2019) Mycorrhizal fungi: biodiversity, ecological significance, and industrial applications. In Recent Advancement in White Biotechnology Through Fungi (pp. 181-199). Springer, Cham. https://link.springer.com/chapter/ 10.1007/978-3-030-10480-1_5 Panwar J, Tarafdar JC (2006) Distribution of three endangered medicinal plant species and their colonization with arbuscular mycorrhizal fungi. J Arid Environ 65(3):337–350. https://doi.org/ 10.1016/j.jaridenv.2005.07.008 Panwar J, Vyas A (2002) AM fungi: a biological approach towards conservation of endangered plants in Thar desert, India. Curr Sci Bangalore 82(5):576–577 Paredes M, Quiles MJ (2015) The effects of cold stress on photosynthesis in hibiscus plants. PLoS One 10(9):1–13. https://doi.org/10.1371/journal.pone.0137472 Parihar M, Rakshit A, Singh HB, Rana K (2019) Diversity of arbuscular mycorrhizal fungi in alkaline soils of hot sub humid eco-region of Middle Gangetic Plains of India. Acta Agr Scand B-Soil Plant Sci 69(5):386–397. https://doi.org/10.1080/09064710.2019.1582692 Park H-J, Floss DS, Levesque-Tremblay V, Bravo A, Harrison MJ (2015) Hyphal branching during arbuscule development requires reduced arbuscular mycorrhiza. Plant Physiol 169:2774–2788. https://doi.org/10.1104/pp.15.01155 Perez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcon-Aguilar C, Ferrol N (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055. https://doi.org/10.1016/j.fgb. 2011.08.003 Peuke AD, Rennenberg H (2005) Phytoremediation. EMBO Rep 6(6):497–450. https://doi.org/10. 1038/sj.embor.7400445 Porcel R, Aroca R, Ruíz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi - a review. Agron Sustain Dev 32:181–200. https://doi.org/10.1007/s13593-011-0029-x Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. https://doi.org/10.1016/j.pbi.2007.05.004 Prasad S, Malav LC, Choudhary J, Kannojiya S, Kundu M, Kumar S et al (2021) Soil microbiomes for healthy nutrient recycling. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 1–21. https://doi. org/10.1007/978-981-15-6949-4_1 Rai PK, Singh M, Anand K, Saurabhj S, Kaur T, Kour D et al (2020) Role and potential applications of plant growth promotion rhizobacteria for sustainable agriculture. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 49–60. https://doi. org/10.1016/B978-0-12-820526-6.00004-X Rajawat MVS, Singh R, Singh D, Yadav AN, Singh S, Kumar M et al (2020) Spatial distribution and identification of bacteria in stressed environments capable to weather potassium aluminosilicate mineral. Braz J Microbiol 51:751–764. https://doi.org/10.1007/s42770-019-00210-2 Rajeshkumar PP, Thomas GV, Gupta A, Gopal M (2015) Diversity, richness and degree of colonization of arbuscular mycorrhizal fungi in coconut cultivated along with intercrops in high productive zone of Kerala, India. Symbiosis 65(3):125–141. https://doi.org/10.1007/ s13199-015-0326-2 Rajeswari E, Latha P, Kamalakannan A (2019) Eco friendly management of onion basal rot disease using Trichoderma viride and AM fungi. J Pharmac Phytochemistry 8(2):892–896 Rajkumar HG, Seema HS, Sunil Kumar CP (2012) Diversity of arbuscular mycorrhizal fungi associated with some medicinal plants in Western Ghats of Karnataka region, India. World J Sci Technol 2(1):13–20 Rastegari AA, Yadav AN, Yadav N (2020a) New and future developments in microbial biotechnology and bioengineering: trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam

80

U. Singh et al.

Rastegari AA, Yadav AN, Yadav N (2020b) New and future developments in microbial biotechnology and bioengineering: trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam Regvar M, Vogel K, Irgel N, Wraber T, Hildebrandt U, Wilde P, Bothe H (2003) Colonization of pennycresses (Thlaspi spp.) of the Brassicaceae by arbuscular mycorrhizal fungi. J Plant Physiol 160(6):615–626 Ren W, Geng Y, Ma Z, Sun L, Xue B, Fujita T (2015) Reconsidering brownfield redevelopment strategy in China’s old industrial zone: a health risk assessment of heavy metal contamination. Environ Sci Poll Res Int 22(4):2765–2775. https://doi.org/10.1007/s11356-014-3548-6 Rengasamy P (2002) Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust J Exp Agric 42(3):351–361. https://doi.org/10.1071/EA01111 Ruiz-Lozano JM, Azcón R, Goméz M (1996) Alleviation of salt stress by arbuscular-mycorrhizal Glomus species in Lactuca sativa plants. Physiol Plant 98:767–772. https://doi.org/10.1111/j. 1399-3054.1996.tb06683.x Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83. https://doi.org/10.1016/j.tplants.2012.10.003 Saxena B, Shukla K, Giri B (2017) Arbuscular mycorrhizal fungi and tolerance of salt stress in plants. In: Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 67–97. https://doi.org/10.1007/978-981-10-4115-0_4 Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444(7121):933–936. https://doi. org/10.1038/nature05364 Selosse M-A, Roy M (2009) Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70. https://doi.org/10.1016/j.tplants.2008.11.004 Selvaraj T, Bhaskaran C (1999) Some sporocarpic VA-mycorrhizal fungi associated with Spinifex littoreus and Aeluropus lagopoides in saline soil. In: Abstract, National conference on Mycorrhiza. Barkatulla University, Bhopal, p 40 Selvaraj T, Kim H (2004) Ecology of vesicular-arbuscular mycorrhizal (VAM) fungi in coastal areas of India. J Appl Biol Chem 47(2):71–76 Sharaff MS, Subrahmanyam G, Kumar A, Yadav AN (2020) Mechanistic understanding of rootmicrobiome interaction for sustainable agriculture in polluted soils. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 61–84. https://doi. org/10.1016/B978-0-12-820526-6.00005-1 Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151. https://doi. org/10.1016/j.jplph.2006.06.016 Sharma S, Parkash V, Aggarwal A (2008) GLOMALES I: a monograph of Glomus spp. (Glomaceae) in the sunflower rhizosphere of Haryana, India. Helia 31(49):13–18. https://doi. org/10.2298/HEL0849013S Sharma D, Kapoor R, Bhatnagar AK (2009a) Differential growth response of Curculigo orchioides to native arbuscular mycorrhizal fungal (AMF) communities varying in number and fungal components. Eur J Soil Biol 45(4):328–333. https://doi.org/10.1016/j.ejsobi.2009.04.005 Sharma S, Parkash V, Kaushish S, Aggarwal A (2009b) A monograph of Acaulospora spp. (VAM fungi) in sunflower rhizosphere in Haryana, India. Helia 32(50):69–76. https://doi.org/10.2298/ HEL0950069S Sharma VP, Singh S, Dhanjal DS, Singh J, Yadav AN (2021) Potential strategies for control of agricultural occupational health hazards. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 387–402. https://doi.org/10.1007/978-981-15-6949-4_16 Shen ZG, Li XD, Wang CC, Chen HM, Chua H (2002) Lead Phytoextraction from contaminated soil with high-biomass plant species. J Environ Qual 31:1893–1900. https://doi.org/10.2134/ jeq2002.1893

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

81

Sheng M, Tang M, Chan H et al (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296. https://doi.org/10.1007/ s00572-008-0180-7 Singh A, Kumar R, Yadav AN, Mishra S, Sachan S, Sachan SG (2020a) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–15. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Singh D, Mathimaran N, Boller T, Kahmen A (2020b) Deep-rooted pigeon pea promotes the water relations and survival of shallow-rooted finger millet during drought—Despite strong competitive interactions at ambient water availability. PLoS One 15(2):e0228993. https://doi.org/10. 1371/journal.pone.0228993 Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5(10):1–11. https://doi. org/10.1371/journal.pone.0013324 Song YY, Ye M, Li C, He X, Zhu-Salzman K, Wang RL, Su YJ, Luo SM, Zeng RS (2014) Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Sci Rep 4:3915. https://doi.org/10.1038/srep03915 Song J, Han Y, Bai B, Jin S, He Q, Ren J (2019) Diversity of arbuscular mycorrhizal fungi in rhizosphere soils of the Chinese medicinal herb Sophora flavescens Ait. Soil Till Res 195:104423. https://doi.org/10.1016/j.still.2019.104423 Subrahmanyam G, Kumar A, Sandilya SP, Chutia M, Yadav AN (2020) Diversity, plant growth promoting attributes, and agricultural applications of rhizospheric microbes. In: Yadav AN, Singh J, Rastegari AA, Yadav N (eds) Plant microbiomes for sustainable agriculture. Springer, Cham, pp 1–52. https://doi.org/10.1007/978-3-030-38453-1_1 Sundar SK, Palavesam A, Parthipan B (2011) AM fungal diversity in selected medicinal plants of Kanyakumari District, Tamil Nadu, India. Indian J Microbiol 51(3):259–265. https://doi.org/10. 1007/s12088-011-0112-7 Symanczik S, Błaszkowski J, Koegel S, Boller T, Wiemken A, Al-Yahya’Ei MN (2014) Isolation and identification of desert habituated arbuscular mycorrhizal fungi newly reported from the Arabian Peninsula. J Arid Land 6(4):488–497. https://doi.org/10.1007/s40333-014-0021-9 Symanczik S, Courty PE, Boller T, Wiemken A, Al-Yahya’ei MN (2015) Impact of water regimes on an experimental community of four desert arbuscular mycorrhizal fungal (AMF) species, as affected by the introduction of a non-native AMF species. Mycorrhiza 25(8):639–647. https:// doi.org/10.1007/s00572-015-0638-3 Thapar HS, Uniyal K (1990) Survey of some VAM fungi in saline soils of Haryana State. In: Jalali BL, Chand H (eds) Current trends in mycorrhizal research, Proc Natl conference on mycorrhiza. HAU, Hisar, pp 16–17 Thapar HS, Uniyal K, Verma RK (1991) Survey of native VAM fungi of sodic soils of Haryana State. Ind Forest 117(12):1059–1069 Turrini A, Saran M, Giovannetti M, Oehl F (2018) Rhizoglomus venetianum a new arbuscular mycorrhizal fungal species from a heavy metal-contaminated site downtown Venice in Italy. Mycol Prog 17(11):1213–1224. https://doi.org/10.1007/s11557-018-1437-y Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17. https://doi.org/10.1007/s10311-009-0268-0 Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797. https://doi.org/10.1104/pp.112.195727 Wang YY, Vestberg M, Walker C, Hurme T, Zhang X, Lindström K (2008) Diversity and infectivity of arbuscular mycorrhizal fungi in agricultural soils of the Sichuan Province of mainland China. Mycorrhiza 18(2):59–68. https://doi.org/10.1007/s00572-008-0161-x

82

U. Singh et al.

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. https://doi.org/10.1007/s11104-0090244-2 Wang Y, Li T, Li Y, Qiu Q, Li S, Xin G (2015) Distribution of arbuscular mycorrhizal fungi in four semi-mangrove plant communities. Ann Microbiol 65(2):603–610. https://doi.org/10.1007/ s13213-014-0896-x Wang C, White PJ, Li C (2017) Colonization and community structure of arbuscular mycorrhizal fungi in maize roots at different depths in the soil profile respond differently to phosphorus inputs on a long-term experimental site. Mycorrhiza 27(4):369–381 Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1122. https://doi.org/10.1139/b04-082 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. https://doi.org/10.1016/j.jplph.2005.04.024 Wu QS, Zou YN (2017) Arbuscular mycorrhizal fungi and tolerance of drought stress in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 25–41. https://doi.org/10.1007/978-981-10-4115-0_2 Xie XA, Lin H, Peng XW, Xu CR, Sun ZF, Jiang KX, Huang A, Wu XH, Tang NW, Salvioli A (2016) Arbuscular mycorrhizal symbiosis requires a phosphate transceptor in the Gigaspora margarita fungal symbiont. Mol Plant 9:1583–1608. https://doi.org/10.1016/j.molp.2016.08. 011 Yadav AN (2020) Recent trends in mycological research, volume 1: agricultural and medical perspective. Springer, Switzerland 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. https://doi.org/10.1016/j.jbiosc.2014.11.006 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. https://doi.org/10.1007/s11274-014-1768-z Yadav AN, Sachan SG, Verma P, Saxena AK (2016) Bioprospecting of plant growth promoting psychrotrophic Bacilli from cold desert of north western Indian Himalayas. Indian J Exp Biol 54:142–150 Yadav AN, Kumar V, Dhaliwal HS, Prasad R, Saxena AK (2018a) Microbiome in crops: diversity, distribution, and potential role in crop improvement. In: Crop improvement through microbial biotechnology. Elsevier, Amsterdam, pp 305–332. https://doi.org/10.1016/B978-0-444-639875.00015-3 Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N et al (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, Kaur T, Kour D, Rana KL, Yadav N, Rastegari AA et al (2020a) Saline microbiome: biodiversity, ecological significance and potential role in amelioration of salt stress in plants. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 283–309. https://doi.org/10.1016/B978-0-12-820526-6.00018-X Yadav AN, Singh J, Rastegari AA, Yadav N (2020b) Plant microbiomes for sustainable agriculture. Springer, Cham Yadav AN, Singh J, Singh C, Yadav N (2021) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore Yang Y, Liang Y, Ghosh A, Song Y, Chen H, Tang M (2015) Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead–zinc

2 Arbuscular Mycorrhizal Fungi: Biodiversity, Interaction with Plants. . .

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mine area: potential applications for phytoremediation. Environ Sci Pollut Res 22 (17):13179–13193. https://doi.org/10.1007/s11356-015-4521-8 Yang Y, Liang Y, Han X, Chiu TY, Ghosh A, Chen H, Tang M (2016) The roles of arbuscular mycorrhizal fungi (AMF) in phytoremediation and tree-herb interactions in Pb contaminated soil. Sci Rep 6:1–14. https://doi.org/10.1038/srep20469 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. https://doi.org/10.1016/j.scienta.2015.11.002 Yu Y, Zhang S, Huang H (2010) Behavior of mercury in a soil–plant system as affected by inoculation with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 20 (6):407–414. https://doi.org/10.1007/s00572-009-0296-4 Yuan S, Li M, Fang Z, Liu Y, Shi W, Pan B, Wu K, Shi J, Shen B, Shen Q (2016) Biological control of tobacco bacterial wilt using Trichoderma harzianum amended bioorganic fertilizer and the arbuscular mycorrhizal fungi Glomus mosseae. Biol Control 92:164–171. https://doi.org/10. 1016/j.biocontrol.2015.10.013 Zenk MH (1996) Heavy metal detoxification in higher plants-A review. Gene 179:21–30 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):1–11. https://doi.org/10.1007/s11557-015-1108-1 Zhang J, Wang F, Che R, Wang P, Liu H, Ji B, Cui X (2016) Precipitation shapes communities of arbuscular mycorrhizal fungi in Tibetan alpine steppe. Sci Rep 6(1):1–10. https://doi.org/10. 1038/srep23488 Zhu XC, Song FB, Liu SQ (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346:189–199. https://doi.org/10. 1007/s11104-011-0809-8 Zhu X, Song F, Liu F (2017) Arbuscular mycorrhizal fungi and tolerance of temperature stress in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 163–194. https://doi.org/10.1007/978-981-10-4115-0_8 Zoomi I, Narayan RP, Akhtar O, Srivastava P (2017) Role of plant growth promoting rhizobacteria in reclamation of wasteland. In: Patra J, Vishnuprasad C, Das G (eds) Microbial Biotechnology. Springer, Singapore. https://doi.org/10.1007/978-981-10-6847-8_3 Zoomi I, Kehri HK, Pandey D, Akhtar O (2019) Effect of AM fungi on growth performance of Capsicum annum L. raised in heavy metals contaminated soil. Int J Pharm Biol Sci 9 (3):230–238

Chapter 3

Aspergillus from Different Habitats and Their Industrial Applications Akram H. Mohamed, Bassem A. Balbool, and Ahmed M. Abdel-Azeem

Contents 3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Biodiversity of Aspergillus from Different Habitats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1 Soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2 Endophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.3 Airborne . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.4 Pathogenic Aspergillus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.5 Human . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Industrial Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1 Metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2 Enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.3 Organic Acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.4 Pigments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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A. H. Mohamed (*) Microbial Genetic Resources Department, National Gene Bank, Agriculture Research Center, Giza, Egypt B. A. Balbool Faculty of Biotechnology, October University for Modern Sciences and Arts, 6th October City, Egypt A. M. Abdel-Azeem Botany and Microbiology Department, Faculty of Science, Suez Canal University, Ismailia, Egypt © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. M. Abdel-Azeem et al. (eds.), Industrially Important Fungi for Sustainable Development, Fungal Biology, https://doi.org/10.1007/978-3-030-67561-5_3

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Introduction

Genus Aspergillus is considered as one of the most diverse fungal species as it can colonize different substrates and can live under different environmental conditions (Klich 2002; Abdel-Azeem et al. 2016, 2019, 2020). Aspergilli could be recovered from soil, salt marshes, endophytes, stones, water, and humans (Klich 2002; AbdelAzeem 2013; Conley et al. 2006; Tang et al. 2012; Balbool and Abdel-Azeem 2020). The biodiversity of Aspergillus species is highly affected by some conditions such as the climate, substrate availability, ecological interactions, and water activity (Abdel-Azeem 2013; Grishkan and Nevo 2010; Petterson and Leong 2011). Genus Aspergillus contains more than 340 approved species with both pathogenic and industrially important species (Samson et al. 2014; Abdel-Azeem et al. 2016). Genus Aspergillus species can act as plant and human pathogens such as A. fumigatus and A. terreus; it can also produce the cariogenic ochratoxins such as A. ochraceus. Also, this important genus can produce a wide variety of useful metabolites such as organic acids, dyes, and enzymes which can be included in several industries as pharmaceutical, food, textile, and beverage industries, e.g., A. niger and A. oryzae. Due to the previously mentioned economic and medical importance of this widely distributed genus, researchers made a huge effort to study the biodiversity, classification, and secondary metabolites of genus Aspergillus since Aspergillus species is considered one of the most diverse fungal species and could be found in several habitats. Also, due to its economic and pharmaceutical applications, this chapter sheds light on the biodiversity, habitats, and industrial and pharmaceutical application of genus Aspergillus.

3.2

Biodiversity of Aspergillus from Different Habitats

Aspergillus consists of about more than 340 species (Fig. 3.1). These species may be pathogenic and/or beneficial for humans, plants, and animals; also Aspergillus can be found as insect pathogen (Samson et al. 2014; Abdel-Azeem et al. 2016; Sahayaraj et al. 2012). Aspergillus genus is considered as a cosmopolitan group since it can live in a wide range of ecosystems and environmental and climatic zones (Lević et al. 2013). These genera can be found in different habitats in the environment, as epiphytic or endophytic with plants, soil, and air; in addition it can be found in both fresh and marine habitat. Aspergilli are able to utilize different types of organic substrate (Cray et al. 2013). Due to the biodiversity of Aspergillus genus and because it is widespread, there was an emerging interest to maximize the use and application of Aspergillus in many biotechnological and industrial fields. Aspergilli are considered as one of the most important genera for large-scale production of organic acids as well as enzymes which occupy a big share of the world market. Since these genera could tolerate acidic medium and could utilize a broad spectrum of natural substrate, Aspergilli

3 Aspergillus from Different Habitats and Their Industrial Applications

Fig. 3.1 Classification of the valid 339 Aspergillus species (Gautier et al. 2016)

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produce a high number of hydrolytic enzymes through solid-state fermentation (Schuster et al. 2002). Aspergillus showed a great share in the pharmaceutical industry through production of a wide range of bioactive metabolites such as antibiotics, antifungal, as well as lipid/cholesterol-lowering products (Bok et al. 2006; Pecyna and Bizukojc 2011). Aspergilli attract attention to be used in the agricultural section by acting in growth promotion activity or protecting plant against plant pathogens (Hung and Rutgers 2016).

3.2.1

Soil

Soil is considered as a big reservoir for many organisms which is considered as a complex biological system in which fungi are the dominant soil microorganisms in terms of different species in soil including Aspergillus (Oliveira et al. 2013). According to Houbraken et al. (2014) and Hubka et al. (2015) Aspergillus species are classified into subgenera, Aspergillus, Circumdati, Fumigati, and Nidulantes, and 20 sections. These genera are widely distributed all over the world (Klich and Pitt 1988). More than 270 studies included information about the diversity of Aspergillus species in the soil between 0 and 46 degrees north or south with high relative percentage of Aspergillus, the greatest between 25 and 35 degrees N/S, except many rare species and new species reported from tropical and subtropical soils (Hong et al. 2006; Klich and Pitt 1988). Limited studies showed biodiversity of Aspergillus in certain crop or agroecosystem (Tedersoo et al. 2014; Rastegari et al. 2020a, b). Kredics et al. (2014) reported that many factors including plant species, soil physicochemical characters, application of pesticides and/or fertilizers, and geographical location affect the diversity of fungal communities. The inoculation of A. niger isolated from wheat crop rhizosphere into soil significantly affects the content of other pathogenic fungi, including Gibberella, Fusarium, Monographella, Bipolaris, and Volutella, which cause soilborne diseases in various crops (Wang et al. 2018). In a study conducted in Turkey by Kucuk and Kyvanc (2011) on maize crop to evaluate the most dominant species, they reported that A. ustus, A. versicolor, and Gliocladium viride were dominant in the maize soil. In a study conducted in Southwest Ethiopia, about 93 species belonging to Aspergillus genera were isolated from different crops like haricot bean (31 sp.), cabbage (20 sp.), faba bean (17 sp.), tomato (15 sp.), and sugarcane (9 sp.). The high phosphate solubilization efficiency showed that Aspergillus sp. can be used as a potential biofertilizer (Elias et al. 2016). Also soil of medicinal plants and wild plants affects the quality of bioactive compounds of medicinal plants; thus rhizosphere fungi enhance the medicinal plant properties. Shaikh and Nadaf (2013) reported that many Aspergillus sp. from aromatic rice rhizosphere are responsible for synthesizing 2-acetyl-1-pyrroline. In Egypt, a study conducted by El-Zayat et al. (2008) reported that Aspergillus sp. especially was the most common genus associated with the rhizosphere of Hyoscyamus muticus medicinal plants which are distributed in many regions of Aswan city.

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Despite the vital role of soil fungi in different ecosystems, soil phytopathogenic fungi are associated with crop diseases, where the effects of their infection may transmit from field to human and animal consumers putting their health at risk (Winter and Pereg 2019; Yadav et al. 2020a, b). These soilborne fungi are the main producers of mycotoxins where their presence in foods is of global concern and is considered as a threat to the agricultural industry (Lee and Ryu 2017; Milićević et al. 2010). Aspergillus is considered as the main producer of aflatoxins (AFs) (Marin et al. 2013). The AFs can contaminate many crops, including peanuts, rice (Oryza sativa L.), and maize. Widespread contamination occurs in the hot and humid regions of the world (Marin et al. 2013). Aspergillus sp. dominates many polluted ecosystems and can be used as biological markers of pollution and at the same time as bioremediation agents to control the pollution in the area as reported by Rodrigues et al. (2020) who isolated Aspergillus niger and Aspergillus tamarii as the most dominant fungi from the Jansen Lagoon State Park, Brazil.

3.2.2

Endophytes

Endophytic fungi were first defined by de Bary (1866) as the fungi or bacteria that could colonize tissues of healthy plants without causing any symptomatic disease (Rana et al. 2019a, b; Suman et al. 2016). As reported by Hawksworth and Rossman in 1997, one million different fungal endophytic species were present in their investigated plants. Aspergillus is considered as the most dominant genus which is rich in many compounds with many biological activities (Sadorn et al. 2016). Presence of endophytic Aspergillus in such tissues of plants depends mainly on the age, where Aspergillus sp. and Penicillium sp. were isolated only from old leaves of Ensete ventericosum and were totally absent in young leaves as recorded by Chauhan et al. (2019). Endophytic Aspergillus plays a vital role in health and provides growth parameters of many crops (Yadav 2020; Yadav et al. 2020a, b). A. japonicas isolated from wild plant Euphorbia indica showed high concentrations of indoleacetic acid (IAA), salicylic acid (SA), flavonoids, and phenolics which could improve plant biomass and other nutritive values of soybean and sunflower plants under temperature stress (40  C) in comparison to endophyte-free plants (Hamayun et al. 2018). Aspergillus is responsible for the production of most secondary metabolites of medicinally important plants, such as fungal endophyte Aspergillus iizukae which is isolated from leaves of milk thistle (Silybum marianum) that could produce three important compounds, silybin A, silybin B, and isosilybin A, which are present mainly as the main constituent of S. marianum seeds (El-Elimat et al. 2014). Endophytic Aspergillus can also inhabit marine environment. Endophytic fungi are also found in symbiotic relationship inside tissues of marine macroalgae (Yadav 2020). As reported by Kamat et al. (2020) who observed that Aspergillus sp. was the most dominant and abundant endophytic fungus present in the sampled algal species

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collected from Konkan Coast, India, these Aspergillus produce antimicrobial, antioxidant, and anticancer activities. Marine sponges are considered as a rich source for pharmaceutical products with many biological activities, e.g., anticancer, antioxidant, anti-inflammatory, and antimicrobial activities. Endophytic fungi inhabiting marine sponge are responsible for the production of majority of biologically active secondary metabolites (Almeida et al. 2012). Endophytic Aspergillus sp. isolated from marine sponge Xestospongia testudinaria produced two disydonols A and B which showed anticancer activity against HepG-2 and CaSki human tumor cell lines (Sun et al. 2012). As one of the richest economic and ecological sources, mangroves are halotolerant plants distributed in coastal wetlands (Gopal and Chauhan 2006). Mangrove shows species diversity of flora and fauna as well as is known as the hot spot for marine fungi (Shearer et al. 2007). Mangroves are considered as a big reservoir for numerous endophytic Aspergillus, Penicillium, and Phoma (Bharathidasan and Panneerselvam 2011). Aspergillus ustus is an endophytic fungus isolated from Acrostichum aureum mangroves from Guangxi Province in China (Zhou et al. 2011). Also, Aspergillus flavus and Aspergillus tamari have been isolated from mangroves of Jaffna Peninsula, Sri Lanka (Ravimannan and Sepali 2020). In Egypt, A. terreus has been isolated from the mangrove plant A. marina collected from Abu Ghoson area, south Marsa Alam city, Red Sea coast (El-Gendy et al. 2014). Elsbaey et al. (2019) reported that endophytic fungus Aspergillus versicolor was isolated from fruits of the mangrove Avicennia marina from Safaga, Red Sea, Egypt. As endophytic fungi can live inside healthy plant tissue, there were endolichenic fungi which can act as endosymbionts inside lichen thalli (Arnold et al. 2009). Aspergillus versicolor was isolated from the lichen Lobaria retigera obtained from Mount Laojun, Yunnan Province, China (Dou et al. 2014). In India, Aspergillus niger was isolated as endolichenic fungi from Parmotrema ravum lichen (Padhi et al. 2018). Also, Aspergillus quandricinctus is isolated as the endophyte of Usnea longissima collected from eastern Indian Himalayan regions, south 107 Sikkim districts, Kupup, Nathang (Bajpai et al. 2020).

3.2.3

Airborne

As members of genus Aspergillus have low weight and small-size (2.5–3.5 lm) fungal spores, they can be transferred to large distance by many environmental factors such as convection currents and wind. Aspergillus and Penicillium are considered the most dominant. Fungi are ubiquitous in all atmospheres which can cause respiratory problems (Araujo and Cabral 2010). According to Pasanen et al. (1991) the term airborne fungi is related to the release of its spores in the air which is affected by different factors such as humidity and wind speed. Yan et al. (2016) recorded high abundancy of Aspergillus and Penicillium spores in heavy haze days

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which was more than Cladosporium species. Aspergillus and Penicillium spores are usually released at an air velocity less than that required for Cladosporium spores (Pasanen et al. 1991). On the other hand, the study conducted on farm workers in an area of the Apulia region, southern Italy, in 2011 revealed that there was strong relationship between occurrence of airborne Aspergillus spp. and environmental and geographical data, so there is higher presence of Aspergillus in sheds located at 90 m above sea level, with temperature and humidity higher than 29  C and 50%, respectively (Cafarchia et al. 2014). A study conducted on Iranian air samples collected from 22 districts of Tehran revealed that 38 Aspergillus isolates represented by 12 species, i.e., A. niger (28.94%, 11 isolates), A. flavus (18.42%, 7 isolates), A. tubingensis (13.15%, 5 isolates), A. japonicus (10.52%, 4 isolates), A. ochraceus (10.52%, 4 isolates), and 2.63% of 1 isolate each from A. nidulans, A. amstelodami, A. oryzae, A. terreus, A. versicolor, A. flavipes, and A. fumigatus were obtained by settle plate method (Kermani et al. 2016). In India a study conducted in Dongargarh showed high contribution of Aspergillus sp. as follows: Aspergillus niger (18.08%), Aspergillus flavus (14.69%), Aspergillus versicolor (12.43%), and Aspergillus fumigates (09.04%) (Sharma 2011). Aspergillus section versicolor is considered as the most common indoor air fungal species, as they can be present in different temperatures, humidity, and broad range of substrates with different water activity (Nielsen 2003). As an example, studies carried out in Croatia showed high distribution and biodiversity of A. section versicolor in indoor environments such as basements and apartments (Amend et al. 2010; Jurjevic et al. 2012). According to CaM sequences, indoor air isolates were seven different species among which some were just recently described including A. jensenii, A. creber, A. tennesseensis, A. venenatus (Jurjevic et al. 2012), and A. griseoaurantiacus (Visagie et al. 2014), followed by other distinctive species including A. amoenus and A. protuberus, as well as three isolates assigned to undescribed species from the section versicolor. A. jensenii and A. creber dominated over other identified sections. On the other hand, airborne Aspergillus were medically important, which comprise A. fumigatus, A. flavus, A. niger, and A. terreus. Also, Conidia Aspergillus spp. can be detected inside and outside of buildings year-round (Boff et al. 2013; Vonberg and Gastmeier 2006; Brenier-Pinchart et al. 2009). Presence of these microorganisms in hospitals is very dangerous especially for immunocompromised patients which could result in 40–90% mortality rates (Alangaden 2011). The mechanism of Aspergillosis infection is mainly by inhalation of Aspergillus conidia, but duration and quantity of conidia to make an infection are not clear (Hope et al. 2005). For example, inhalation of A. fumigatus spores into lungs may cause many diseases including invasive pulmonary aspergillosis and aspergillum, in addition to many hypersensitivity diseases (allergic asthma, pneumonitis, and allergic bronchopulmonary aspergillosis) (Latgé 1999; Greub and Bille 1998).

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Pathogenic Aspergillus

Phytopathogenic Aspergilli attract attention to be controlled, not only for their ability to destroy many important crops, but also due to their ability to produce many types of mycotoxins which are highly toxic to poultry, livestock, fish, and humans (Forgacs and Carll 1962). Black Aspergilli are reported as a main cause of pre- and postharvest diseases in maize, cereal grain, bunch grapes, onions, garlic, soybeans, apples, and peanuts (Magnoli et al. 2006; Dalcero et al. 2002; Pitt 1975; Pozzi et al. 1995; Magnoli et al. 1999). The main sources of Aspergillus inoculum are litter, soil, and vineyard soils (Klich 2002; Hayden and Maude 1992; Leong et al. 2007; Griffin et al. 2001). The source of Aspergillus infection may be seeds or fruits of most crops (Palencia et al. 2009a; Hayden and Maude 1992; Leong et al. 2007). It was reported that not all black Aspergilli were epiphytic; some of those fungi isolated from surface-sterilized maize seeds indicated that the fungi were endophytic which were characterized as symptomless infection not dormant but actively producing their toxic secondary metabolites into the host plant (Hayden and Maude 1992; Palencia et al. 2009b). As mentioned by Aybeke (2020) that Aspergillus alliaceus reported as parasite on Orobanche parasitic plant by altering the hormones and phenolic metabolism leads to slow and continuous death of Orobanche plant, these characteristics recommend the use of this fungus as a biological agent against Orobanche plant. Aspergillus flavus can cause ear rot disease of maize; the disease symptoms can appear at any growth stage of maize plant from flowering to harvest time (Latterell and Rossi 1983; Vollmeister et al. 2012). Aspergillus sp. can also cause serious problems with high economic losses, wherein their mycotoxins can be accumulated inside the tissues of maize grains resulting in high risk on animal and human health (Logrieco et al. 2003; Balazs and Schepers 2007). Aspergillus flavus is considered as an opportunistic pathogen causing economic damage especially for oil-containing crops such as cottonseed, maize, and peanuts. A. flavus can present as conidia, sclerotia, or mycelia in infected plant tissues. Sclerotia of both A. flavus and A. parasiticus can survive in soil up to 3 years (Horn et al. 2009; Wicklow et al. 1993). Colonization and infection by fungus depend mainly on the growth stage of the crop, as in maize kernel which is most susceptible to infection, while colonization is higher on the silk of mature maize ears than young ones (Zuber and Lillehoj 1979). In addition to environmental condition the colonization of fungus is also enhanced by insect and bird damage which facilitates the sites for fungus (Horn and pitt 1997; Payne 1998). In another point of view, there was host association between cultivated crop and soil contamination by Aspergillus sp., as observed by Garber and Cotty (2014) in Rio Grande Valley of Texas, and there was association between A. parasiticus in soil cultivated by sugarcane crop and they observed low proportions of Aspergillus section flavi communities in soil when cultivated by another crop.

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Human

Aspergillus is widely distributed in different habitats such as plants, dead organic matter, soil, air, animal systems, and water. Aspergilli could be found in surfaces of buildings, indoor air, home appliances, and even dust and drinking water. Aspergilli produce asexual conidia which are considered airborne and stress tolerant, and it would also produce sexual ascospores (Stevenson et al. 2015; Wyatt et al. 2015). Although Aspergilli comprise hundreds of species, few species would show an impact on animals and humans. Usually infections are caused by Aspergillus flavus, Aspergillus fumigatus, Aspergillus nidulans, Aspergillus niger, and Aspergillus terreus (Baddley et al. 2001; Perfect et al. 2001; Enoch et al. 2006). A. fumigatus is responsible for about 90% of human infections, followed by A. flavus and A. niger (Lass-Flörl et al. 2005). The ability of different Aspergillus species to cause human infections varies from one country to another depending on the population under study. Usually inhaled conidial spores could be eliminated by the macrophages and innate immune system in immunocompetent individuals. Infection depends on the virulence factor of the fungal species, host’s immunological state, and pulmonary functions; Aspergilli infections cause a variety of reactions such as allergy and other infectious diseases in immunocompromised individuals. Aspergillosis causes lethal and invasive respiratory infections and maybe in other organs/tissues, and would be followed by organ dissemination in a condition called invasive aspergillosis. Mild immunodeficiency patients and patients with chronic lung diseases are usually susceptible to chronic necrotizing pulmonary aspergillosis. On the other hand, noninvasive Aspergillus species induce some other lung diseases including aspergilloma and allergic bronchopulmonary aspergillosis (Kosmidis and Denning 2015a, b). The increased number of immunocompromised people recently is due to different factors such as pollution, alcoholism, HIV, use of immunosuppressive drugs, radiation, and personal hygiene (Maschmeyer et al. 2007). This has resulted in increased number of research studies on aspergillosis and its severity among different populations.

3.3 3.3.1

Industrial Applications Metabolites

Microorganisms produce a wide variety of compounds as a defensive mechanism against harsh environment or another organism (Singh and Yadav 2020). The produced compounds are referred to as metabolites, which would be a final metabolic process product or even an intermediate. Metabolites are mostly restricted to molecules or low molecular weight. Metabolites regulate several functions as enzymatic inhibitors or activators and cell signaling. Metabolites are classified into

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primary and secondary metabolites; primary metabolites are responsible for the regulation of growth and reproduction, and secondary metabolites are used as antibacterial, antifungal, anticancer, and anti-inflammatory agents; herbicides; and immunosuppressants (Devi et al. 2020a, b). Some metabolites are used to treat several biological disorders which were untreated till the discovery of the fungal products (Rastegari et al. 2019a, b). Genus Aspergillus was reported to produce several extracellular enzymes and organic acids which led to its extensive use in several biotechnological industries. This section covers some of the important Aspergilli products and its industrial applications.

3.3.2

Enzymes

Fungi produce a wide variety of enzymes (Table 3.1) which have been used extensively in industrial processes such as the food and pharmaceutical industries. Scientists reported the ability of endophytic fungi to produce several enzymes as peroxidases, laccases, chitinase, and glucanases (Sieber et al. 1991; Moy et al. 2002; Kour et al. 2019). Since Aspergilli are widely distributed and include a huge number of species, there is an increased demand on Aspergilli enzymes to be used in industrial applications (Abdel-Azeem et al. 2016). By 2010, FDA considered A. oryzae and A. niger safe to be used (GRAS) (Contesini et al. 2010).

3.3.2.1

Lipase

Lipases (EC 3.1.1.3) are responsible for the hydrolysis of triacylglycerols to fatty acids and glycerol. Lipases could be produced by a wide variety of organisms such as animals, plants, and microorganisms. Animal lipases are involved in the gastric processes and could be found in the pancreas (Yadav et al. 2019). Lipases produced by microbes are found to be more stable than other lipases and hence it is used in several processes. Lipases carry out several reactions such as acidolysis, alcoholysis, esterification, and hydrolysis. Lipases are used in different applications such as the hydrolysis of oils from fabrics, ester synthesis in food, and biodiesel production (Contesini et al. 2010; Sahay et al. 2017). Lipases produced under solid-state fermentation process by Aspergillus ibericus, A. niger, and A. uvarum showed a remarkable result for the valorizations of oil mills and winery wastes (Salgado et al. 2014).

3.3.2.2

Laccases

Laccases (EC. 1.10.3.2) are classified among the blue multicopper oxidase enzymes. Laccase was purified from Rhus vernicifera and described firstly by Yoshida in 1883. Several trials carried out to discover the nature of laccases ended with the

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Table 3.1 Examples of enzymes produced by Aspergillus species and their application (Park et al. 2017) Enzyme a-Amylase

Classification Hydrolase

Aminopeptidase

Hydrolase

AMP deaminase Catalase

Hydrolase Oxidoreductase

Source Aspergillus Niger Aspergillus oryzae A. niger A. oryzae Aspergillus sojae Aspergillus melleus A. niger

Cellulase

Hydrolase

A. niger

Chymosin

Hydrolase

A. niger

Esterase

Hydrolase

A. niger

a-Galactosidase b-Glucanase

Hydrolase Hydrolase

Glucose oxidase

Oxidoreductase

A. niger A. niger Aspergillus aculeatus A. niger

Glutaminase

Hydrolase

b-D-glucosidase

Hydrolase

A. oryzae A. Sojae A. niger

Inulinase Lactase

Hydrolase Hydrolase

A. niger A. niger

Lipase

Hydrolase

A. niger A. oryzae

Xylanase

Hydrolase

A. niger

Application Brewing, beverage, textile, and pulp

References Suganuma et al. (2007)

Brewing and soy sauce fermentation

Marui et al. (2010)

Food and beverage production Food processing, textile, and rubber production Drink, detergent, textile, and pulp production Milk and dairy products Perfumes and cosmetics Soy milk production Grain feed industry

Okado et al. (2015) Pariza and Johnson (2001)

Breadmaking, dairy, and wine/beer processing Soy sauce fermentation

Wong et al. (2008)

Dyeing textiles

Song et al. (2010) Ohta et al. (1993) Tosa and Shibatani (1995) Singh and Mukhopadhyay (2012) Elgharbi et al. (2015)

Ethanol production Milk and dairy products Paper, food, detergent, and textile industries Breadmaking and beverage production

Villena and Gutiérrez-Correa (2006) Pariza and Johnson (2001) Giuliani et al. (2001) Patil et al. (2009) Mathlouthi et al. (2003)

Ito et al. (2013)

discovery that it is a metalloprotein associated with copper (Yousfi et al. 2002). Laccases are widely distributed and it could be found in plants, insects, bacteria, and also fungi (Kunamneni et al. 2008). Fungal laccases possess a high redox activity other than other laccases; laccases could be involved in various applications such as

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the degradation of phenolic compounds and lignin, and also melanin synthesis, ethanol production, wine purification, herbicide degradation, and biodegradation of dyes, and in the textile industries (Mayer and Staples 2002; Giardina et al. 2010; Prasad et al. 2021; Sharma et al. 2021). Many Aspergilli showed an ability to produce laccases with a promising activity such as Aspergillus nidulans, A. niger, A. fumigatus, and A. oryzae (Thurston 1994; Scherer and Fischer 1998). Since laccases are considered as an important industrial requirement, several trials have been carried out to purify and produce the industrially important enzyme in a large scale with low cost and Aspergilli could be considered as a promising source.

3.3.2.3

Pectinases

Pectinases are responsible for breaking down pectin; pectin is a heteropolysaccharide that could be found in the cell wall of plants, fibers, fruits, and vegetables. Henri Braconnot (1825) was the first scientist who isolated and described pectinases. Pectinases comprise pectin lyase, polygalacturonase, and pectozyme. Polygalacturonase was widely studied and was used commercially in a wide scale. Pectinases have been used in processes involving the degradation of plant materials, which will allow the speeding up of fruit juices like apples and sapota. Generally fungal enzymes could be preferred commercially as they are secreted extracellularly, and thus it will be easy to be recovered from culture media (Soares et al. 2012). Aspergillus niger is one of the most famous fungal taxa that produce pectinases, as it produces the enzyme to facilitate the breaking down of the plant’s middle lamella and then the fungus will extract the plant nutrients using its hyphae. Pectinases resemble around 25% of the global market of food enzymes and around 10% of the global market (Anisa et al. 2013; Kohli and Gupta 2015; Kumar et al. 2017). Several experiments are carried out to optimize the pectinase production and explore other Aspergillus species that produce it efficiently. Solid-state fermentation showed a higher enzymatic production compared to submerged fermentation (Maheshwari 2003). Wheat bran, rice straw, and Tween 80 were used as a substrate to enhance pectinase production (Debing et al. 2006). Some experiments were carried out to optimize the medium condition for maximum production of pectinases such as that of Esawy et al. (2013) who produced pectinases from A. niger using Egyptian citrus peels as a carbon source. This was followed by immobilization of the produced pectinase in polyvinyl alcohol, where the immobilized enzyme showed a promising result compared to the free enzyme.

3.3.2.4

Proteases

Proteases may be named after peptidases or proteinases; they catalyze the breaking down of protein into smaller units (polypeptides or amino acids). The discovery of proteases is quite linked to the production of milk curd. Desert nomads used to carry milk in bags furbished from goat stomachs and after long journeys they discovered

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the milk in a denser/sour state and did not understand the reason behind this. Proteases are involved in many industries such as food, textiles, leather making, animal nutrition, and detergents (Negi and Banerjee 2006; Hamada et al. 2017). Proteases resemble around 60% of the enzyme market, and thus it has got attention to optimize its activity and production (Jinka et al. 2009). Negi and Banerjee (2006) produced proteases efficiently from Aspergillus awamori using wheat bran as substrate under solid-state fermentation conditions. Also, Chutmanop et al. (2008) produced protease under solid-state fermentation condition from rice bran from A. oryzae. Use of rice bran showed low output of the proteases compared to wheat bran, which was related to the low porosity of the rice bran which leads to low oxygen penetration. Scientists started to use a mix of 75% rice bran and 25% wheat bran which enhanced the production of proteases and reduced its production costs.

3.3.3

Organic Acids

Organic acids as carboxylic acids are considered the most common acids. Organic acids occupy a huge sector in industrial production processes (Magnuson and Lasure 2004; Liaud et al. 2014). Fungal biotechnology facilitated the production of organic acids from natural safe sources. Organic acids are widely used in different fields starting with the food industry, pharmaceutical industry, and industrial processes. The production of organic acids was mainly facilitated by the shared efforts by engineers, chemists, and microbiologists which could be considered as important as the production of penicillin. Filamentous fungi showed a higher ability to produce organic acids in a large-safe scale compared to those from bacterial sources. Filamentous fungi were mentioned to produce several important organic acids such as malic, oxalic, gluconic, itaconic, kojic and citric acids. The critical parameters for citric acid production by A. niger were defined empirically and include high carbohydrate concentration, low but finite manganese concentrations, maintenance of high dissolved oxygen, constant agitation, and low pH (Schreferl et al. 1986; Zhang and Roehr 2002). Itaconic acid was obtained from the distillation of citric acid in 1960 by fermentation of carbohydrates by A. terreus (Okabe et al. 2009). Itaconic acid has been applied in a numerous range of industries with the largest producers in the world being the United States, Japan, Russia, and China. Kojic acid (5-hydroxy-2(hydroxymethyl)-4-pyrone; KA) is an organic acid that has a wide variety of applications where it could be used as antibiotic, antioxidant, and food additive (Chaudhry et al. 2014; Bentley 2006); also it could be used in cosmetics as skinwhitening compound; medically it could be used in the treatment of chloasma (Terabayashi et al. 2010). It can be produced by several Aspergillus species as A. tamarii, A. parasiticus, and A. oryzae (Bentley 2006).

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Pigments

Pigments from natural sources have been obtained since long time and with time interest in production of natural colorants has increased due to toxic effects of synthetic ones. Natural pigments like carotenoids, flavonoids (anthocyanins), chlorophylls, phycobiliproteins, betalains, and quinones are common ones that are in use. Among these, due to the ease of cultivation, extraction, and genetic diversity, fungi and bacteria are the most promising. Bacteria and fungi such as Bacillus, Achromobacter, Yarrowia, Rhodotorula, Phaffia, and Monascus produce a large number of pigments. Carotenoids that are yellow, red, and orange are widely used as food and feed supplements and as antioxidants in the pharmaceutical industry (Mukherjee et al. 2017). Fungal pigments are secondary metabolites that are sometimes produced due to scarcity in the nutritional value. When the nutritional supply of essential nutrients decreases or there is some disfavoring environmental condition, mycelium produces secondary metabolites (Hesham et al. 2021; Singh et al. 2020). There are some fungi including Aspergillus, Fusarium, Penicillium, and Trichoderma that produce various pigments as intermediate metabolites during their growth. Fungal pigments are classified as carotenoids and polyketides. Fungal polyketides are made up of tetraketides and octaketides having eight C2 units forming polyketide chain (Mukherjee et al. 2017). Anthraquinone is the most common class that is proved to be potentially safe (Mapari et al. 2010). Pigment anthraquinone is widely used in the dyestuff industry and is most commonly produced by Trichoderma, Aspergillus, and Fusarium (Durán et al. 2002). It is now known that single fungal species can produce a mixture of different pigments, having various biological properties.

3.4

Conclusion

The high biodiversity characteristics shown by the different Aspergillus taxa made it possible for this genus to become one of the most interesting genera across the fungal genera. Aspergillus species showed the ability to grow over various habitats across the normal habitats to most extreme ones. Aspergilli secondary products have been included into several industries and have showed very promising results and applications. It is highly recommended to mine the genetic characteristics of various Aspergilli from several habitats; also studying its metabolomics becomes necessary as we expect that by deep mining its genes and metabolites will reveal more novel products and secrets about this interesting genus.t Acknowledgments We would like to express our gratitude and deep pleasure to Prof. Ajar Nath Yadav and all of the book editors for their efforts. Also, we would like to extend our gratitude to October University for Modern Sciences and Arts, Suez Canal University, and Agricultural Research Center in Egypt.

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References Abdel-Azeem AM (2013) Ecological and taxonomical studies: on ascospore-producing fungi in Egypt. LAP LAMBERT Academic Publishing, Palestine Abdel-Azeem AM, Salem FM, Abdel-Azeem MA, Nafady NA, Mohesien MT, Soliman EA (2016) Biodiversity of the genus Aspergillus in different habitats. In: Gupta VK (ed) Aspergillus system properties and applications. New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 3–28. https://doi.org/10.1016/B978-0-444-63505-1. 00001-4 Abdel-Azeem AM, Abdel-Azeem MA, Abdul-Hadi SY, Darwish AG (2019) Aspergillus: biodiversity, ecological significances, and industrial applications. In: Yadav AN et al (eds) Recent advancement in white biotechnology through fungi, fungal biology. Springer Nature, Switzerland AG, pp 121–179. https://doi.org/10.1007/978-3-030-10480-1_4 Abdel-Azeem AM, Abu-Elsaoud A, Darwish A, Balbool B, Abo Nouh F, Abo Nahas H., Abd El-Azeem M, Ali N, Kirk P. (2020) The Egyptian ascomycota 1: genus Aspergillus. Microb Biosyst 5(1):61–99. https://doi.org/10.21608/mb.2020.100044. Alangaden GJ (2011) Nosocomial fungal infections: epidemiology, infection control, and prevention. Infect Dis Clin 25:201–225 Almeida C, Hemberger Y, Schmitt SM et al (2012) Marilines A–C: novel Phthalimidines from the sponge-derived fungus Stachylidium sp. Chem A Eur J 18:8827–8834. https://doi.org/10.1002/ chem.201103278 Amend AS, Seifert KA, Samson R, Bruns TD (2010) Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proc Natl Acad Sci 107:13748–13753 Anisa S, Ashwini S, Girish K (2013) Isolation and screening of Aspergillus spp. for pectinolytic activity. Electron J Biol 9:37–41 Araujo R, Cabral JP (2010) Fungal air quality in medical protected environments. Air Qual 357:382–382 Arnold AE, Miadlikowska J, Higgins KL et al (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283–297 Aybeke M (2020) Aspergillus alliaceus infection fatally shifts Orobanche hormones and phenolic metabolism. Braz J Microbiol 51:883–892 Baddley JW, Stroud TP, Salzman D, Pappas PG (2001) Invasive mold infections in allogeneic bone marrow transplant recipients. Clin Infect Dis 32:1319–1324 Bajpai R, Yusuf MA, Upreti DK et al (2020) Endolichenic fungus, Aspergillus quandricinctus of Usnea longissima inhibits quorum sensing and biofilm formation of Pseudomonas aeruginosa PAO1. Microb Pathog 140:103933–103933 Balazs E, Schepers JS (2007) The mycotoxin threat to food safety. Int J Food Microbiol 119:1–2 Balbool BA, Abdel-Azeem AM (2020) Diversity of the culturable endophytic fungi producing L-asparaginase in arid Sinai, Egypt. Italian J Mycol 49:8–24 Bentley R (2006) From miso, sake and shoyu to cosmetics: a century of science for kojic acid. Nat Prod Rep 23:1046–1062 Bharathidasan R, Panneerselvam A (2011) Isolation and identification of endophytic fungi from Avicennia marina in Ramanathapuram District, Karankadu, Tamil Nadu. India Eur J Exp Biol 1:31–36. https://doi.org/10.1016/j.ijfoodmicro.2007.07.018 Boff C, Zoppas BCDA, Aquino VR et al (2013) The indoor air as a potential determinant of the frequency of invasive aspergillosis in the intensive care. Mycoses 56:527–531 Bok JW, Hoffmeister D, Maggio-Hall LA et al (2006) Genomic mining for Aspergillus natural products. Chem Boil 13:31–37 Braconnot H (1825) Recherches sur un nouvel acide universellement répandu dans tous les vegetaux. Annales de chimie et de physique, 2(28):173–178

100

A. H. Mohamed et al.

Brenier-Pinchart M-P, Lebeau B, Quesada J-L et al (2009) Influence of internal and outdoor factors on filamentous fungal flora in hematology wards. Am J Infect Control 37:631–637 Cafarchia C, Camarda A, Iatta R et al (2014) Environmental contamination by Aspergillus spp. in laying hen farms and associated health risks for farm workers. J Med Microbiol 63:464–470 Chauhan NM, Gutama AD, Aysa A (2019) Endophytic fungal diversity isolated from different agro-ecosystem of Enset (Ensete ventericosum) in Gedeo zone, SNNPRS. Ethiopia BMC Microbiol 19:172–172 Chutmanop J, Chuichulcherm S, Chisti Y, Srinophakun P (2008) Protease production by Aspergillus oryzae in solid-state fermentation using agroindustrial substrates. J Chem Technol Biotechnol 83:1012–1018 Conley CA, Ishkhanova G, Mckay CP, Cullings K (2006) A preliminary survey of non-lichenized fungi cultured from the hyperarid Atacama Desert of Chile. Astrobiology 6:521–526 Contesini FJ, Lopes DB, Macedo GA et al (2010) Aspergillus sp. lipase: potential biocatalyst for industrial use. J Mol Catal B Enzym 67:163–171 Cray JA, Bell ANW, Bhaganna P et al (2013) The biology of habitat dominance; can microbes behave as weeds? Microb Biotechnol 6:453–492 Dalcero A, Magnoli C, Hallak C et al (2002) Detection of ochratoxin A in animal feeds and capacity to produce this mycotoxin by Aspergillus section Nigri in Argentina. Food Addit Contam 19:1065–1072 de Bary A (1866) Morphologie und physiologie der pilze, flechten und myxomyceten. Engelmann Debing J, Peijun L, Stagnitti F et al (2006) Pectinase production by solid fermentation from Aspergillus niger by a new prescription experiment. Ecotoxicol Environ Saf 64:244–250 Devi R, Kaur T, Guleria G, Rana K, Kour D, Yadav N et al (2020a) Fungal secondary metabolites and their biotechnological application for human health. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam, pp 147–161. https://doi.org/10.1016/ B978-0-12-820528-0.00010-7 Devi R, Kaur T, Kour D, Rana KL, Yadav A, Yadav AN (2020b) Beneficial fungal communities from different habitats and their roles in plant growth promotion and soil health. Microbial Biosystems 5:21–47. https://doi.org/10.21608/mb.2020.32802.1016 Dou Y, Wang X, Jiang D et al (2014) Metabolites from Aspergillus versicolor, an endolichenic fungus from the lichen Lobaria retigera. Drug Discov Ther 8:84–88 Durán N, Teixeira MF, De Conti R, Esposito E (2002) Ecological-friendly pigments from fungi. Crit Rev Food Sci Nutr 42:53–66 El-Elimat T, Raja HA, Graf TN et al (2014) Flavonolignans from Aspergillus iizukae, a fungal endophyte of milk thistle (Silybum marianum). J Nat Prod 77:193–199 El-Gendy MMA, El-Bondkly AMA, Yahya SMM (2014) Production and evaluation of antimycotic and antihepatitis C virus potential of fusant MERV6270 derived from mangrove endophytic fungi using novel substrates of agroindustrial wastes. Appl Biochem Biotechnol 174:2674–2701 Elgharbi F, Hmida-Sayari A, Zaafouri Y, Bejar S (2015) Expression of an Aspergillus niger xylanase in yeast: application in breadmaking and in vitro digestion. Int J Biol Macromol 79:103–109 Elias F, Woyessa D, Muleta D (2016) Phosphate solubilization potential of rhizosphere fungi isolated from plants in Jimma zone, Southwest Ethiopia. Int J Microbiol 2016:1–11 Elsbaey M, Tanaka C, Miyamoto T (2019) New secondary metabolites from the mangrove endophytic fungus Aspergillus versicolor. Phytochem Lett 32:70–76 El-Zayat SA, Nassar MSM, El-Hissy FT et al (2008) Mycoflora associated with Hyoscyamus muticus growing under an extremely arid desert environment (Aswan region, Egypt). J Basic Microbiol 48:82–92 Enoch D, Ludlam H, Brown N (2006) Invasive fungal infections: a review of epidemiology and management options. J Med Microbiol 55:809–818

3 Aspergillus from Different Habitats and Their Industrial Applications

101

Esawy MA, Gamal AA, Kamel Z et al (2013) Evaluation of free and immobilized Aspergillus niger NRC1ami pectinase applicable in industrial processes. Carbohydr Polym 92:1463–1469 Forgacs J, Carll WT (1962) Mycotoxicoses. Adv Vet Sci 7:273–882 Garber NP, Cotty PJ (2014) Aspergillus parasiticus communities associated with sugarcane in the Rio Grande Valley of Texas: implications of global transport and host association within Aspergillus section Flavi. Phytopathology 104:462–471 Gautier M, Normand A-C, Ranque S (2016) Previously unknown species of Aspergillus. Clin Microbiol Infect 22:662–669 Giardina P, Faraco V, Pezzella C et al (2010) Laccases: a never-ending story. Cell Mol Life Sci 67:369–385 Giuliani S, Piana C, Setti L et al (2001) Synthesis of pentylferulate by a feruloyl esterase from Aspergillus niger using water-in-oil microemulsions. Biotechnol Lett 23:325–330 Gopal B, Chauhan M (2006) Biodiversity and its conservation in the Sundarban mangrove ecosystem. Aquat Sci 68:338–354 Greub G, Bille J (1998) Aspergillus species isolated from clinical specimens: suggested clinical and microbiological criteria to determine significance. Clin Microbiol Infect 4:710–716 Griffin MA, Patterson MG, West MA (2001) Job satisfaction and teamwork: the role of supervisor support. J Organ Behav 22:537–550 Grishkan I, Nevo E (2010) Spatiotemporal distribution of soil microfungi in the Makhtesh Ramon area, Central Negev desert, Israel. Fungal Ecol 3:326–337 Hamada S, Kubota K, Sagisaka M (2017) Purification and characterization of a novel extracellular neutral metalloprotease from Cerrena albocinnamomea. J Gen Appl Microbiol 63:51–57 Hamayun M, Hussain A, Iqbal A et al (2018) Endophytic fungus Aspergillus japonicus mediates host plant growth under normal and heat stress conditions. Biomed Res Int 2018:1–11 Hayden NJ, Maude RB (1992) The role of seed-borne Aspergillus niger in transmission of black mould of onion. Plant Pathol 41:573–581 Hesham AE-L, Kaur T, Devi R, Kour D, Prasad S, Yadav N et al (2021) Current trends in microbial biotechnology for agricultural sustainability: conclusion and future challenges. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 555–572. https://doi.org/10.1007/978-981-15-6949-4_22 Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi?. Phytopathology 87: 888–891 Hong S-B, Cho H-S, Shin H-D et al (2006) Novel Neosartorya species isolated from soil in Korea. Int J Syst Evol Microbiol 56:477–486 Hope WW, Walsh TJ, Denning DW (2005) The invasive and saprophytic syndromes due to Aspergillus spp. Med Mycol 43:S207–S238 Horn BW, Pitt JI (1997) Yellow mold and aflatoxin. Compendium of Peanut diseases. 2:40–42 Horn BW, Moore GG, Carbone I (2009) Sexual reproduction in Aspergillus flavus. Mycologia 101:423–429 Hubka V, Nováková A, Kolařík M et al (2015) Revision of Aspergillus section Flavipedes: seven new species and proposal of section Jani sect. nov. Mycologia 107:169–208 Hung R, Rutgers SL (2016) Applications of Aspergillus in plant growth promotion. In: Gupta K (ed) Microbial Cellulase system properties and applications: new and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 223–227 Houbraken J, de Vries RP, Samson RA (2014) Modern taxonomy of biotechnologically important Aspergillus and Penicillium species. In: Advances in applied microbiology. Elsevier, pp 199–249 Ito K, Koyama Y, Hanya Y (2013) Identification of the glutaminase genes of Aspergillus sojae involved in glutamate production during soy sauce fermentation. Biosci Biotechnol Biochem 77:1832–1840 Jinka R, Ramakrishna V, Rao SK, Rao RP (2009) Purification and characterization of cysteine protease from germinating cotyledons of horse gram. BMC Biochem 10:28

102

A. H. Mohamed et al.

Jurjevic Z, Peterson SW, Horn BW (2012) Aspergillus section versicolor: nine new species and multilocus DNA sequence based phylogeny. IMA fungus 3:59–79 Kamat S, Kumari M, Taritla S, Jayabaskaran C (2020) Endophytic fungi of marine alga from Konkan coast, India—a rich source of bioactive material. Front Mar Sci 7:31–31 Kermani F, Shams-Ghahfarokhi M, Gholami-Shabani M, Razzaghi-Abyaneh M (2016) Diversity, molecular phylogeny and fingerprint profiles of airborne Aspergillus species using random amplified polymorphic DNA. World J Microbiol Biotechnol 32:96–96 Klich MA (2002) Biogeography of Aspergillus species in soil and litter. Mycologia 94:21–27 Klich MA, Pitt JI (1988) A laboratory guide to the common Aspergillus species and their teleomorphs. Commonwealth scientific and industrial research organization. Division of Food Processing North Ryde, New South Wales, Australia Kohli P, Gupta R (2015) Alkaline pectinases: a review. Biocatal Agric Biotechnol 4:279–285 Kosmidis C, Denning DW (2015a) Republished: the clinical spectrum of pulmonary aspergillosis. Postgrad Med J 91:403–410 Kosmidis C, Denning DW (2015b) The clinical spectrum of pulmonary aspergillosis. Thorax 70:270–277 Kour D, Rana KL, Kaur T, Singh B, Chauhan VS, Kumar A et al (2019) Extremophiles for hydrolytic enzymes productions: biodiversity and potential biotechnological applications. In: Molina G, Gupta VK, Singh B, Gathergood N (eds) Bioprocessing for biomolecules production, pp 321–372. https://doi.org/10.1002/9781119434436.ch16 Kredics L, Hatvani L, Naeimi S, Körmöczi P, Manczinger L, Vágvölgyi C et al (2014) Biodiversity of the genus Hypocrea/Trichoderma in different habitats. In: Gupta VG, Schmoll M, HerreraEstrella A, Upadhyay RS, Druzhinina I, Tuohy M (eds) Biotechnology and biology of Trichoderma. Elsevier, Newnes, pp 3–24. https://doi.org/10.1016/C2012-0-00434-6 Kucuk C, Kyvanc M (2011) In vitro interactions and fungal populations isolated from maize rhizosphere. J Biol Sci 11:492–495 Kumar V, Yadav AN, Verma P et al (2017) β-Propeller phytases: diversity, catalytic attributes, current developments and potential biotechnological applications. Int J Biol Macromol 98:595–609 Kunamneni A, Plou FJ, Ballesteros A, Alcalde M (2008) Laccases and their applications: a patent review. Recent Pat Biotechnol 2:10–24 Lass-Flörl C, Griff K, Mayr A et al (2005) Epidemiology and outcome of infections due to Aspergillus terreus: 10-year single Centre experience. Br J Haematol 131:201–207 Latgé J-P (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12:310–350 Latterell FM, Rossi AE (1983) Gray leaf spot of corn: a disease on the move. Plant Dis 67:842–847 Lee HJ, Ryu D (2017) Worldwide occurrence of mycotoxins in cereals and cereal-derived food products: public health perspectives of their co-occurrence. J Agric Food Chem 65:7034–7051 Leong SL, Hocking AD, Scott ES (2007) Aspergillus species producing ochratoxin A: isolation from vineyard soils and infection of Semillon bunches in Australia. J Appl Microbiol 102:124–133 Lević J, Gošić-Dondo S, Ivanović D et al (2013) An outbreak of Aspergillus species in response to environmental conditions in Serbia. Pestic Fitomed 28:167–117 Liaud N, Giniés C, Navarro D et al (2014) Exploring fungal biodiversity: organic acid production by 66 strains of filamentous fungi. Fungal Biol Biotechnol 1(1) Logrieco A, Bottalico A, Mulé G, Moretti A, Perrone G (2003) Epidemiology of toxigenic fungi and their associated mycotoxins for some Mediterranean crops. In: Xu X, Bailey JA, Cooke BM (eds) Epidemiology of mycotoxin producing fungi, Springer, Cham, pp 645–667. https://doi. org/10.1007/978-94-017-1452-5 Magnoli CE, Saenz MA, Chiacchiera SM, Dalcero AM (1999) Natural occurrence of Fusarium species and fumonisin-production by toxigenic strains isolated from poultry feeds in Argentina. Mycopathologia 145:35–41 Magnoli C, Hallak C, Astoreca A et al (2006) Occurrence of ochratoxin A-producing fungi in commercial corn kernels in Argentina. Mycopathologia 161:53–53

3 Aspergillus from Different Habitats and Their Industrial Applications

103

Magnuson J, Lasure L (2004) Organic acid production by filamentous fungi. In: Tkacz JS, Lange L (eds) Advances in fungal biotechnology for industry, agriculture and medicine. Springer, Boston, MA, pp 307–340 Maheshwari M (2003) Microbial production of pectinases from coffee pulp waste. In: 44th annual conference of Association of Microbiologists of India, 12–14. Mapari SAS, Thrane U, Meyer AS (2010) Fungal polyketide azaphilone pigments as future natural food colorants? Trends Biotechnol 28:300–307 Marin S, Ramos AJ, Cano-Sancho G, Sanchis V (2013) Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem Toxicol 60:218–237 Marui J, Ohashi-Kunihiro S, Ando T et al (2010) Penicillin biosynthesis in Aspergillus oryzae and its overproduction by genetic engineering. J Biosci Bioeng 110:8–11 Maschmeyer G, Haas A, Cornely OA (2007) Invasive aspergillosis. Drugs 67:1567–1601 Mathlouthi N, Juin H, Larbier M (2003) Effect of xylanase and β-glucanase supplementation of wheat- or wheat-and barley-based diets on the performance of male turkeys. Br Poult Sci 44:291–298 Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565 Milićević DR, Škrinjar M, Baltić T (2010) Real and perceived risks for mycotoxin contamination in foods and feeds: challenges for food safety control. Toxins 2:572–592 Moy M, Li HM, Sullivan R et al (2002) Endophytic fungal β-1, 6-glucanase expression in the infected host grass. Plant Physiol 130:1298–1308 Mukherjee G, Mishra T, Deshmukh SK (2017) Fungal pigments: an overview. In: Satyanarayana T, Deshmukh SK, Johri BN (eds) Developments in fungal biology and applied mycology. Springer, Cham, pp 525–541. https://doi.org/10.1007/978-981-10-4768-8L Negi S, Banerjee R (2006) Optimization of amylase and protease production from Aspergillus awamori in single bioreactor through EVOP factorial design technique. Food Technol Biotechnol 44:257–261 Nielsen KF (2003) Mycotoxin production by indoor molds. Fungal Genet Biol 39:103–117 Ohta K, Hamada S, Nakamura T (1993) Production of high concentrations of ethanol from inulin by simultaneous saccharification and fermentation using Aspergillus niger and Saccharomyces cerevisiae. Appl Environ Microbiol 59:729–733 Okabe M, Lies D, Kanamasa S, Park EY (2009) Biotechnological production of itaconic acid and its biosynthesis in Aspergillus terreus. Appl Microbiol Biotechnol, Sep;84(4):597–606. https://doi. org/10.1007/s00253-009-2132-3. Epub 2009 Jul 21. PMID:19629471 Okado N, Sugi M, Ueda M et al (2015) Safety evaluation of AMP deaminase from Aspergillus oryzae. Food Chem Toxicol 86:342–350 Oliveira LG, Cavalcanti MAQ, Fernandes MJS, Lima DMM (2013) Diversity of filamentous fungi isolated from the soil in the semiarid area, Pernambuco, Brazil. J Arid Environ 95:49–54 Padhi S, Masi M, Panda SK, Luyten W, Cimmino A, Tayung K, Evidente A (2018) Antimicrobial secondary metabolites of an endolichenic Aspergillus niger isolated from lichen thallus of Parmotrema ravum. Nat Prod Res 34(18):2573–2580 Palencia ER, Glenn AE, Bacon CW (2009a) Colonization of maize seedlings under drought conditions by two ochratoxin A producer species within the Aspergillus section Nigri. Phytopathology 99:S99–S99 Palencia ER, Klich MA, Glenn AE, Bacon CW (2009b) Use of a rep-PCR system to predict species in the Aspergillus section Nigri. J Microbiol Methods 79:1–7 Pariza MW, Johnson EA (2001) Evaluating the safety of microbial enzyme preparations used in food processing: update for a new century. Regul Toxicol Pharmacol 33:173–186 Park HS, Jun SC, Han KH, Hong SB, Yu JH (2017) Diversity, application, and synthetic biology of industrially important Aspergillus fungi. In: Sariaslani S, Gadd GM (eds) Advances in applied microbiology. Elsevier, Amsterdam, pp 161–202 Pasanen A-L, Pasanen P, Jantunen MJ, Kalliokoski P (1991) Significance of air humidity and air velocity for fungal spore release into the air. Atmos Environ Part A 25:459–462

104

A. H. Mohamed et al.

Patil AGG, Kote NV, Mulimani V (2009) Enzymatic removal of flatulence-inducing sugars in chickpea milk using free and polyvinyl alcohol immobilized α-galactosidase from Aspergillus oryzae. J Ind Microbiol Biotechnol 36:29–33 Payne GA (1998) Process of contamination by aflatoxin-producing fungi and their impact on crops. Mycotoxins Agric Food Saf 1998:279 Pecyna M, Bizukojc M (2011) Lovastatin biosynthesis by Aspergillus terreus with the simultaneous use of lactose and glycerol in a discontinuous fed-batch culture. J Biotechnol 151:77–86 Perfect J, Cox G, Lee J et al (2001) The impact of culture isolation of Aspergillus species: a hospitalbased survey of aspergillosis. Clin Infect Dis 33:1824–1833 Petterson OV, Leong S (2011) Fungal Xerophiles (Osmophiles). In: eLS (encyclopaedia of life sciences). John Wiley and Sons, Chichester. Pitt JI (1975) Xerophilic fungi and the spoilage of foods of plant origin. Water relations of foods 273–307 Pozzi CR, Corrêa B, Gambale W et al (1995) Postharvest and stored corn in Brazil: mycoflora interaction, abiotic factors and mycotoxin occurrence. Food Addit Contam 12:313–319 Prasad S, Malav LC, Choudhary J, Kannojiya S, Kundu M, Kumar S et al (2021) Soil microbiomes for healthy nutrient recycling. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 1–21. https://doi. org/10.1007/978-981-15-6949-4_1 Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN et al (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, Switzerland, pp 1–62 Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V et al (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 International Publishing, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6 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/B978-0-44463504-4.00002-5 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/B978-0444-63504-4.00004-9 Rastegari AA, Yadav AN, Yadav N (2020a) New and future developments in microbial biotechnology and bioengineering: trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam Rastegari AA, Yadav AN, Yadav N (2020b) New and future developments in microbial biotechnology and bioengineering: trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health. Elsevier, Amsterdam Rodrigues IVP, Borges KRA, Custódio Neto da Silva MA et al (2020) Diversity of soil filamentous fungi influenced by marine environment in São Luís, Maranhão, Brazil. Sci World J 2020:1–6 Sadorn K, Saepua S, Boonyuen N et al (2016) Allahabadolactones A and B from the endophytic fungus, Aspergillus allahabadii BCC45335. Tetrahedron 72:489–495 Ravimannan N, Sepali E (2020) Antibacterial activity of endophytic fungi isolated from mangroves of Jaffna Peninsula, Sri Lanka. African Journal of Plant Science 14:243–247 Sahay H, Yadav AN, Singh AK et al (2017) Hot springs of Indian Himalayas: potential sources of microbial diversity and thermostable hydrolytic enzymes. 3 Biotech 7:1–11 Sahayaraj K, Borgio JAF, Kumar SM (2012) First record of Aspergillus flavus as a fungal pathogen of reduviid predator, Rhynocoris marginatus (Fab.) (Hemiptera: Reduviidae). EntomoBrasilis 5:80–81

3 Aspergillus from Different Habitats and Their Industrial Applications

105

Salgado JM, Abrunhosa L, Venâncio A et al (2014) Integrated use of residues from olive mill and winery for lipase production by solid state fermentation with Aspergillus sp. Appl Biochem Biotechnol 172:1832–1845 Samson RA, Visagie CM, Houbraken J et al (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173 Scherer M, Fischer R (1998) Purification and characterization of laccase II of Aspergillus nidulans. Arch Microbiol 170:78–84 Schreferl G, Kubicek CP, Röhr M (1986) Inhibition of citric acid accumulation by manganese ions in Aspergillus niger mutants with reduced citrate control of phosphofructokinase. J Bacteriol 165:1019–1022 Schuster E, Dunn-Coleman N, Frisvad JC, Van Dijck PW (2002) On the safety of Aspergillus niger – a review. Appl Microbiol Biotechnol 59:426–435 Shaikh MN, Nadaf AB (2013) Qualitative analysis of 2-acetyl-1-pyrroline from the rhizosphere fungal species of basmati rice varieties by GC-FID. Int J Curr Res 5:1663–1665 Sharma K (2011) Concentration and species diversity of airborne fungi of Dongargarh. Int Multidiscip Res J 1(9):34–36 Sharma VP, Singh S, Dhanjal DS, Singh J, Yadav AN (2021) Potential strategies for control of agricultural occupational health hazards. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 387–402. https://doi.org/10.1007/978-981-15-6949-4_16 Shearer CA, Descals E, Kohlmeyer B, et al (2007) Fungal biodiversity in aquatic habitats. Biodiversity and Conservation 16:49–67 Sieber TN, Sieber-Canavesi F, Dorworth C (1991) Endophytic fungi of red alder (Alnus rubra) leaves and twigs in British Columbia. Can J Bot 69:407–411 Singh AK, Mukhopadhyay M (2012) Overview of fungal lipase: a review. Appl Biochem Biotechnol 166:486–520 Singh J, Yadav AN (2020) Natural bioactive products in sustainable agriculture. Springer, Singapore Singh A, Kumar R, Yadav AN, Mishra S, Sachan S, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–15. https://doi.org/10.1016/B978-0-12-820526-6.00001-4 Soares I, Távora Z, Barcelos RP, Baroni S (2012) Microorganism-produced enzymes in the food industry. In: Valdez B (ed) Scientific, health and social aspects of the food industry, vol 1. BoD– Books on Demand, Croatia, pp 83–94 Song J, Imanaka H, Imamura K et al (2010) Development of a highly efficient indigo dyeing method using indican with an immobilized β-glucosidase from Aspergillus niger. J Biosci Bioeng 110:281–287 Stevenson A, Cray JA, Williams JP et al (2015) Is there a common water-activity limit for the three domains of life? ISME J 9:1333–1351 Suganuma T, Fujita K, Kitahara K (2007) Some distinguishable properties between acid-stable and neutral types of α-amylases from acid-producing koji. J Biosci Bioeng 104:353–362 Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity, vol 1Research Perspectives. Springer, New Delhi, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7 Sun L-L, Shao C-L, Chen J-F et al (2012) New bisabolane sesquiterpenoids from a marine-derived fungus Aspergillus sp. isolated from the sponge Xestospongia testudinaria. Bioorg Med Chem Lett 22:1326–1329. https://doi.org/10.1016/j.bmcl.2011.12.083 Tang Y, Lian B, Dong H et al (2012) Endolithic bacterial communities in dolomite and limestone rocks from the Nanjiang Canyon in Guizhou karst area (China). Geomicrobiol J 29:213–225

106

A. H. Mohamed et al.

Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346(6213):12566881–125668810 Terabayashi Y, Sano M, Yamane N et al (2010) Identification and characterization of genes responsible for biosynthesis of kojic acid, an industrially important compound from Aspergillus oryzae. Fungal Genet Biol 47:953–961 Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26 Tosa T, Shibatani T (1995) Industrial application of immobilized biocatalysts in Japan. Ann N Y Acad Sci 750:364–375 Villena G, Gutiérrez-Correa M (2006) Production of cellulase by Aspergillus niger biofilms developed on polyester cloth. Lett Appl Microbiol 43:262–268 Visagie CM, Hirooka Y, Tanney JB et al (2014) Aspergillus, Penicillium and Talaromyces isolated from house dust samples collected around the world. Stud Mycol 78:63–139 Vollmeister E, Schipper K, Baumann S et al (2012) Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev 36:59–77 Vonberg R, Gastmeier P (2006) Nosocomial aspergillosis in outbreak settings. J Hosp Infect 63:246–254 Wang Y, Wang Li WA, Huang J (2018) Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One 13(4):e0196408 Wicklow DT, Wilson DM, Nelsen TC (1993) Survival of Aspergillus flavus sclerotia and conidia buried in soil in Illinois or Georgia. Phytopathology 83:1141–1141 Winter G, Pereg L (2019) A review on the relation between soil and mycotoxins: effect of aflatoxin on field, food and finance. Eur J Soil Sci 70:882–897 Wong CM, Wong KH, Chen XD (2008) Glucose oxidase: natural occurrence, function, properties and industrial applications. Appl Microbiol Biotechnol 78:927–938 Wyatt TT, Golovina EA, van Leeuwen R et al (2015) A decrease in bulk water and mannitol and accumulation of trehalose and trehalose-based oligosaccharides define a two-stage maturation process towards extreme stress resistance in ascospores of Neosartorya fischeri (Aspergillus fischeri). Environ Microbiol 17:383–394 Yadav AN (2020) Recent trends in mycological research, volume 1: agricultural and medical perspective. Springer, Switzerland Yadav AN, Kour D, Rana KL, Yadav N, Singh B, Chauhan VS et al (2019) 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, Kour D, Yadav N, Kumar A (2020a) Agriculturally important fungi for sustainable agriculture, volume 1: perspective for diversity and crop productivity. Springer International Publishing, Cham Yadav AN, Mishra S, Kour D, Yadav N, Kumar A (2020b) Agriculturally important fungi for sustainable agriculture, volume 2: functional annotation for crop protection. Springer International Publishing, Cham Yan D, Zhang T, Su J et al (2016) Diversity and composition of airborne fungal community associated with particulate matters in Beijing during haze and non-haze days. Front Microbiol 7:487 Yousfi M, Nadjemi B, Bellal R, Ben Bertal D, Palla G (2002) Fatty acids and sterols of Pistacia atlantica fruit oil. JAOCS, 79(10):1049–1050 Zhang A, Roehr M (2002) Citric acid fermentation and heavy metal ions-II. The action of elevated manganese ion concentrations. Acta Biotechnol 22:375–382 Zhou H, Zhu T, Cai S et al (2011) Drimane sesquiterpenoids from the mangrove-derived fungus Aspergillus ustus. Chem Pharm Bull 59:762–766 Zuber MS, Lillehoj EB (1979) Status of the aflatoxin problem in corn. J Environ Qual 8:1–5

Chapter 4

Truffles: Biodiversity, Ecological Significances, and Biotechnological Applications Marco Leonardi, Mirco Iotti, Giovanni Pacioni, Ian R. Hall, and Alessandra Zambonelli

Contents 4.1 4.2 4.3 4.4 4.5

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Truffle Industry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tuber Biodiversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ecological Significance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biotechnological Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.1 Truffle Farming: First Steps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.2 Spore Inoculation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.3 Inoculating with Mycorrhizal Roots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.4 Inoculation with Pure Cultures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.5 Transformed Strains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.6 Double Cropping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6 Conclusion and Future Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

108 109 110 122 125 125 126 128 128 130 130 132 133

M. Leonardi · M. Iotti · G. Pacioni (*) Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy e-mail: [email protected] I. R. Hall Truffles and Mushrooms (Consulting) Ltd., Dunedin, New Zealand A. Zambonelli Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy © The Author(s), under exclusive license to Springer Nature Switzerland AG 2021 A. M. Abdel-Azeem et al. (eds.), Industrially Important Fungi for Sustainable Development, Fungal Biology, https://doi.org/10.1007/978-3-030-67561-5_4

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4.1

M. Leonardi et al.

Introduction

Many species of fungi produce their fruiting bodies underground and these are loosely referred to as “truffles” whereas strictly speaking the true truffles are the hypogeous fruit bodies of the genus Tuber (Ascomycota, Pezizales). The remainder are better termed false truffles, truffle-like, or desert truffles. The fruiting bodies produced underground are considered as the result of the adaptation of mushrooms to drought (Bonito et al. 2013; Yadav et al. 2020a, b). The development of a hypogeous habitat protects against water loss, extreme temperatures, and browsing by animals before a fruiting body is mature. In this adaptation to the underground habitat, the fruiting bodies are more or less globular with the spores produced inside. The spores are dispersed by mycophagous animals (Pacioni et al. 1989) which locate truffles by the attractive aromas they produce. During the digestion process the spores are released from the truffle and the surface of the spores is etched by the animal’s digestive juices (Zambonelli et al. 2017). Later, when the animal has perhaps moved some distance away from the point of ingestion the spores are deposited in a well-manured patch of soil that is likely to attract the roots hopefully of a suitable host tree in search of nutrients. Truffle aromas are predominantly sulfur-based volatile organic compounds (VOCs) such as dimethyl sulfide, the main attractant (Talou et al. 1990; Pacioni et al. 1991). During the development of Tuber fruiting bodies, a considerable activity of the enzyme tyrosinase is recorded. Tyrosinase is responsible for the production of melanins and the thickening and hardening of the ascospore walls (Ragnelli et al. 1992). In turn melanins are related to the production of the natural endocannabinoid anandamide (AEA). This has psychotropic effects on animals and is known as the “happiness hormone.” This might be an added bonus for animals that eat truffles— maybe even humans (Pacioni et al. 2015b)! Each species of truffle produces a unique blend of aromas including alcohols, ketones, aldehydes, aromatic compounds, as well as a range of sulfur compounds. The concentration of these also varies with time and peaks when the truffle reaches maturity (Strojnik et al. 2020). Some insects most likely coevolved with truffles and dine exclusively on truffles, like the beetle Leiodes cinnamomea and the fly Suillia gigantea. There are also many other animals, like snails-slugs, reptiles, birds, and mammals, that prefer to eat truffle if these are available (Zambonelli et al. 2017; Ori et al. 2018b). The different hydnophagous animals have a capacity to digest fruiting bodies, free the spores from the asci, and degrade the spore walls which assists in germination (Piattoni et al. 2014; Ori et al. 2018b). Since animals are the main sporedispersing agents of truffle, it is likely that there are no poisonous truffles. Truffles in the soil can be found in five different states (De la Varga Pastor et al. 2017): – Free mycelium (haploid) connected with the root systems of symbiotic plants and that extends into the soil from which it takes water and solutes and transfers it to the plants.

4 Truffles: Biodiversity, Ecological Significances. . .

109

– Mycorrhizal symbiotic mycelium (haploid) that produces different types of symbiosis with plant roots (ecto-, septate endo-, arbutoid, ectendomycorrhiza, and endophytism) (Pacioni et al. 2014a; Schneider-Maunoury et al. 2018, 2020; Ori et al. 2019; also see Sect. 4.4). – Ascoma (haploid peridium and sterile veins, dikaryotic fertile veins) which goes through six stages of development (hyphal, peridial, veined, ascal, sporal, and pigmented stages) and takes several months to reach maturity (Zarivi et al. 2015; De la Varga Pastor et al. 2017). – Ascospores (haploid plurinucleate), produced by meiosis of the zygote in which the two mating-type (MAT) idiomorphs are segregated (Martin et al. 2010; Rubini et al. 2011b). – Conidia (mitospores, haploid) have not been determined so far in species of clades other than Maculatum and Puberulum; they are non-cultivable and incapable of producing mycorrhizae and could be involved as spermatia in fertilization during sexual reproduction as much as ascospores (Urban et al. 2004; Healy et al. 2013; Leonardi et al. 2020). In the Mediterranean area and the Middle East, for at least a couple of millennia, man has been discovering the gastronomic qualities of truffles, and for more than two centuries has been able to cultivate black truffles (Tuber aestivum and T. melanosporum). The first rational methods for truffle cultivation were developed about 30 years ago and have since become increasingly technologically advanced, thanks also to the use of molecular biology and new electronic devices (Pacioni et al. 2014a). In this chapter, the state of knowledge in the fields of biodiversity and ecology, biotechnological applications, and cultivation of truffles is reported. Due to their economic importance, a brief history of the truffle industry is also discussed.

4.2

Truffle Industry

There are seventeenth-century documents that show that there was a trade of small barrels filled with black truffles boiled in wine and preserved in oil between central Italy and Germany (Pacioni et al. 2015a). In the first half of the nineteenth century it was possible to find food products based on truffles, such as hare pâté or canned woodcock, even in India, thanks to appertisation (pasteurization), introduction of tin cans (Tannahill 1973), as well as older methods for conservation such as drying and preservation in vinegar, brine, fat, glycerine, or alcohol (Ferry de La Bellone 1888). Since then only steam sterilization and freezing have introduced an element of innovation in the long-term conservation of truffles. There is scant economic data available for truffles. FAOSTAT data (http://www. fao.org/faostat/en/#data) combines truffle production with those for mushrooms, and in every truffle-producing region there is a predominant black market especially for fresh products that are impossible to quantify. Even in Italy, which together with France and Spain controls and markets a large part of the world’s truffle production,

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the data are also aggregated to those for mushrooms, a large sector second only to China (http://data.istat.it/Index.aspx?QueryId¼8910). Aggregate data on the quantity of truffles processed by the world’s food industry is also unavailable although there are rare references that do demonstrate the importance of truffles to the economies of the Abruzzo, Tuscany, and Piedmont regions of Italy (Brun and Mosso 2010; Damiani et al. 2011; Pacioni et al. 2015a). In addition to the fresh and preserved truffle markets there is also a demand for truffle flavors where the first industrial patents date back to the early twentieth century (Pacioni et al. 2013). In more recent times cosmetic products and food supplements have been marketed by famous brands. The most recent patents for these were awarded to Akridge (2020) and Coquet and Chabert (2020) and new drugs (Stanikunaite et al. 2007; El Enshasy et al. 2013; Patel et al. 2017).

4.3

Tuber Biodiversity

In the early 2010s, Bonito et al. (2010, 2013) estimated that there were between 180 and 220 species within the Tuber genus. About 80 species were considered valid by Zambonelli et al. (2016). Since then about 50 new species have been typified in the last few years (Table 4.1). Since many type materials of the eighteenth and nineteenth centuries have been lost (e.g., Vittadini’s herbarium) several truffle species need to be typified. Most of the new species have been added to the Puberulum and Rufum clades and come from China and Northern-Central America, showing that a huge portion of the boreal hemisphere is still unexplored. However, even after this latest update, many lineages have still to be described, particularly in the Puberulum and Maculatum clades (whitish truffles), as well as several cryptic lineages within some species complexes. There is no doubt that some of these newly described species will have significant culinary potential so it is worth highlighting them here. However, this very thing that might make a new species so interesting is often omitted from taxonomic descriptions and as a consequence they might be condemned to be mere taxonomic curiosities. In the Aestivum clade two new European species, Tuber alcaracense and Tuber pulchrosporum, have been identified. Tuber pulchrosporum has ascospores bearing a uniquely crested ornamentation and it is phylogenetically closest to T. panniferum. Tuber alcaracense shows morphological features overlapping with the Tuber mesentericum species complex (Benucci et al. 2016). There are five new species in the Excavatum clade with four from China and one from Iran which mostly differ for the characteristics of spore ornamentations (Puliga et al. 2020). For example, the Chinese T. badium is closely related to T. depressum (94–95% of similarity between ITS sequences) and these species can be identified only through spore morphology: ellipsoid and subglobose (T. depressum) rather than fusiform (T. badium). The Japonicum group was first recognized by Kinoshita et al. (2011) and thereafter supported by Bonito et al. (2013) although no species were officially described

FM205596 AJ002509

MK113975 JN896352

MB 833685 MB 325082 MB 184470 MB 180551 MB 249434 MB 828883 MB 563565

MB 818791 MB 818795 MB 226823 MB 222226 MB 833874

Tuber alcaracense Ant. Rodr. & Morte

Tuber malençonii Donadini, Riousset, G. Riousset & G. Chev. Tuber magnatum Picco

Tuber mesentericum Vittad.

Tuber panniferum Tul. & C. Tul.

Tuber pulchrosporum Konstantinidis, Tsampazis, Slavova, Nakkas, Polemis, Fryssouli & Zervakis Tuber sinoaestivum J.P. Zhang & P.G. Liu

Excavatum clade Tuber badium S.P. Wan

Tuber depressum S.P. Wan

Tuber excavatum Vittad. Tuber fulgens Quél. Tuber iranicum F. Puliga, M. Illice, M. Iotti, D. Baldo & A. Zambonelli

HM485355 HM485358 MN854634

KX904892

KX904889

AF132507

AF132508

MN810047

MycobBank# MB 218597

Species Tuber aestivum Vittad.

ITS Ref. Seq. AF516779

CMI Unibo 4939

HKAS 95396

HKAS 88789

KUN-HKAS 59105

ACAM 2016-007 (ACAM!)

JC. D sub n 136-78

MUB Fung-971

Holotype voucher/specimen #

Europe Europe Iran

China

China

China

Greece-Bulgaria

France-ItalySpain Europe, Western Asia, Thailand Southern and Central Europe Southern Europe

Geographic distribution Europe, North Africa, Iran Spain

(continued)

Wan et al. (2017b) Wan et al. (2017b) Vittadini (1831) Quélet (1880) Puliga et al. (2020)

Tulasne and Tulasne (1844) Polemis et al. (2019) Zhang et al. (2012)

Vittadini (1831)

Crous et al. (2020) Donadini et al. (1978) Picco (1788)

References Vittadini (1831)

Table 4.1 List of the genotyped and morphotyped species in the Tuber genus. In bold the species characterized after recognition made by Bonito et al. (2010, 2013) and Zambonelli et al. (2016)

4 Truffles: Biodiversity, Ecological Significances. . . 111

MycobBank# MB 801128 MB 818793

MB 568737

MB 185088 MB 832580

MB 815830 MB 815829 MB 814490 MB 807668

MB 814192 MB 227990 MB 804231 MB 190290

Species Tuber neoexcavatum L. Fan & Yu Li

Tuber verrucosivolvum S.P. Wan

Gennadii clade Tuber gennadii (Chatin) Pat.

Tuber lacunosum Mattir.

Tuber lucentum Bordallo

Japonicum/Turmericum clade Tuber flavidosporum Hir. Sasaki, A. Kinosh. & Nara

Tuber japonicum Hir. Sasaki, A. Kinosh. & Nara

Tuber turmericum L. Fan Tuber xanthomonosporum Qing & Yun Wang

Macrosporum clade Tuber calosporum S.P. Wan

Tuber canaliculatum Gilkey Tuber glabrum L. Fan & S. Feng Tuber macrosporum Vittad.

Table 4.1 (continued)

JQ925643 KF002731 HM485373

KT444598

KT758837 KJ162154

AB553444

AB553446

MN437515

HM485360

HM485361

KY013650

ITS Ref. Seq. JX458715

UC 620892 BJTC FAN228

HKAS88790

BJTC FAN473 YAAS L3185

TFM: S16001

TFM: S16012

MUB Fungj825

HKAS 88863

Holotype voucher/specimen # BJTC FAN184

USA China Western Europe

China

China China

Japan

Japan

GreeceMorocco-SpainTunisia Italy-MoroccoPortugal-Spain Spain

China

Geographic distribution China

Wan et al. (2016) Gilkey (1920) Fan et al. (2014) Vittadini (1831)

Kinoshita et al. (2016) Kinoshita et al. (2016) Fan et al. (2015) Qing et al. (2015)

Crous et al. (2019)

Mattirolo (1900)

Patouillard (1903)

References Fan et al. (2013a) Wan et al. (2017b)

112 M. Leonardi et al.

KU186913

MB 816348 MB 819367

MB 564391 MB 803258 MB 819798 MB564391 MB 221960 MB 819799 MB564393 MB 564394 MB 307170 MB 190092 MB 564395 MB 563657 MB564391

Tuber aztecorum G. Guevara, Bonito & M.E. Sm.

Tuber beyerlei Trappe, Bonito & G. Guevara

Tuber bomiense K. M. Su & W. P. Xiong Tuber brennemanii A. Grupe, Healy & M.E. Sm.

Tuber castilloi G. Guevara, Bonito & Trappe

Tuber foetidum Vittad. Tuber floridanum Grupe, Sulzbacher & M.E. Sm.

Tuber guevarae Bonito & Trappe

Tuber lauryi Trappe, Bonito & G. Guevara

Tuber linsdalei Gilkey Tuber maculatum Vittad. Tuber mexiusanum G. Guevara, Bonito & Cázares

Tuber microverrucosum L. Fan & C.L. Hou

Tuber miquihuanense G. Guevara, Bonito & Cázares

NR119868

JN870099

HM85370 AF003919 NR119867

NR119862

JF419305

AJ557544 MF611781

NR119865

KC517480 MF611779

NR119866

KY271791

KF002729

MB 550860

Tuber sinomonosporum J.Z. Cao & L. Fan Maculatum clade Tuber arnoldianum Healy, Zurier & Bonito

Guevara 885 (ITCV)

BJTC FAN142

G. Guevara 181 (ITCV)

OSC 130885

G. Guevara 180 (ITCV)

FLAS-F-61240

Cázares 149 (ITCV)

SKM101 FLAS-F-61235

Trappe 32597 (OSC 130875)

Guevara 993 (ITCV [José Castillo Tovar herbarium])

FH 00377353

BJTC FAN150

Mexico

China

USA Europe Mexico

USA

Mexico

Western Europe USA-Brazil

Mexico

China USA

USA

Mexico

USA

China

(continued)

Healy et al. (2016b) GuevaraGuerrero et al. (2018) Guevara et al. (2013) Su et al. (2013) Grupe et al. (2018) Guevara et al. (2013) Vittadini (1831) Grupe II et al. (2018) Guevara et al. (2013) Guevara et al. (2013) Gilkey (1954) Vittadini (1831) Guevara et al. (2013) Fan et al. (2012b) Guevara et al. (2013)

Fan et al. (2014)

4 Truffles: Biodiversity, Ecological Significances. . . 113

LC312201

MB 188017 MB 821786 MB 192144 MB 808639 MB 445492 MB 538392 MB 134661

Tuber indicum Cooke & Massee

Tuber longispinosum A. Kinosh.

Tuber melanosporum Vittad. Tuber pseudobrumale Y. Wang & Shu H. Li Tuber pseudoexcavatum Y. Wang, G. Moreno, Riousset, Manjón & G. Riousset Tuber regimontanum G. Guevara, Bonito & Julio Rodr. Tuber himalayense B.C. Zhang & Minter MB 570492

NR_121340

MB 228019 MB 815399

Melanosporum clade Tuber brumale Vittad. Tuber cryptobrumale Merényi, T. Varga & Bratek

Tuber yigongense L. Fan & W.P. Xiong Puberulum clade

AF132515 KJ742703 DQ329374

MB 357109

Tuber whetstonense J.L. Frank, D. Southw. & Trappe

MF663714

AB553423

JQ638998

AF132504 KU203777

NR119864

DQ011845 HM485389 JF419265

MB 245393 MB 150586 MB 564397

Tuber scruposum R. Hesse Tuber shearii Harkn. Tuber walkeri Healy, Bonito & G. Guevara

ITS Ref. Seq. DQ011850

MycobBank# MB 237266

Species Tuber rapaeodorum Tul. & C. Tul.

Table 4.1 (continued)

BJTC FAN731

K(M)32236

Guevara 909 (ITCV)

YAAS L3181 herb. Riousset, 01140395

TFM: S17009

K(M)39493

BP 107922

J.L. Frank 756 (SOC)

R. Healy 521 (ISC)

Holotype voucher/specimen #

China

Southern Asia

Mexico

Southern Europe China China

Japan

India

Europe Hungary

USA

Central Europe USA USA

Geographic distribution Europe

Vittadini (1831) Merényi et al. (2017) Cooke and Massee (1892) Kinoshita et al. (2018) Vittadini (1831) Li et al. (2014) Wang et al. (1998) Guevara et al. (2008) Zhang and Minter (1988) Fan et al. (2018)

References Tulasne and Tulasne (1843) Hesse (1891) Murrill (1920) Guevara et al. (2013) Frank et al. (2006)

114 M. Leonardi et al.

NR119983 AF003917

GQ221447 KP276177

MB 814687

MB 118774 MB 814688

MB 228144 MB811138 MB 563686 MB 216094 MB 824068 MB 819588 MB 812784 MB 563658 MB 824931 MB 811139

Tuber bonitoi G. Guevara & Trappe

Tuber borchii Vittad. Tuber brunneum G. Guevara, Bonito & Trappe

Tuber californicum Harkn. Tuber caoi L. Fan

Tuber cistophilum P. Alvarado, G. Moreno, Manjón, Gelpi & Jaime Muñoz Tuber dryophilum Tul. & C. Tul.

Tuber elevatireticulatum K.F. Wong & H.T. Li Tuber griseolivaceum L. Fan & K.B. Huang

Tuber hubeiense L. Fan

Tuber huizeanum L. Fan & C.L. Hou

Tuber incognitum Piña Páez, Bonito, Guevara & Castellano Tuber jinshajiangense L. Fan

JQ910651

KT067688

MF540618 KY428921

HM485351 MB 811138

FJ554490 KT897474

KT897472

KX262075

MB 817165

Tuber baoshanense S.P. Wan

KJ742702 NR 119860

MB 808638 MB 437836

Tuber alboumbilicum Y. Wang & Shu H. Li Tuber anniae W. Colgan & Trappe

BJTC FAN124

OSC 150066

BJTC FAN144

HMAS 60233

XTAM3 - TAIF Fan 469 - BJTC

AH 39275

Colln Harkness 150 BJTC FAN271

Trappe 33835 (OSU)

Trappe 32421 (OSU)

wsp002, HKAS88788

YAAS L2324 OSC 58992

China

Mexico

China

China

China China

Europe

Spain

USA China

Europe Mexico

Mexico

China

China USA

(continued)

Li et al. (2014) Colgan and Trappe (1997) Wan et al. (2017a) GuevaraGuerrero et al. (2015) Vittadini (1831) GuevaraGuerrero et al. (2015) Harkness (1899) Fan et al. (2016b) Alvarado et al. (2012a) Tulasne and Tulasne (1845) Lin et al. (2018) Huang et al. (2017) Fan et al. (2016a) Fan et al. (2012b) Piña Paez et al. (2018) Fan et al. (2016b)

4 Truffles: Biodiversity, Ecological Significances. . . 115

MycobBank# MB 505743 MB 519470 MB 460825 MB 564356 MB 325083 MB 467502

MB 801143 MB 811140 MB 817164 MB 564521 MB 814689

MB 803932 MB 147428

Species Tuber latisporum Juan Chen & P.G. Liu

Tuber lijiangense L. Fan & J.Z. Cao

Tuber liui A-S. Xu Tuber microsphaerosporum L. Fan & Y. Li

Tuber oligospermum (Tul. & C. Tul.) Trappe

Tuber pacificum Trappe, Castellano & Bushnell

Tuber panzhihuanense X. J. Deng & Y. Wang

Tuber parvomurphium L. Fan

Tuber polymorphosporum S.P. Wan

Tuber pseudomagnatum L. Fan

Tuber pseudoseparans G. Guevara, G. Bonito & J. Trappe

Tuber pseudosphaerosporum L. Fan

Tuber puberulum Berk. & Broome

Table 4.1 (continued)

AJ969626

KF744063

KT897480

NR111718

KX262072

KP276186

NR120126

HM485378

KF021624

DQ898182 KP276187

KF805727

ITS Ref. Seq. NR119620

BJTC FAN250

OSU, Trappe 33778

BJTC FAN163

HKAS 88793

BJTC FAN298

HKAS72015

OSC Trappe 12493

XZE 984 BJTC FAN152

HKAS 52005

Holotype voucher/specimen # HKAS 44315

Europe

China

Mexico

China

China

China

China

Southern Europe, North Africa USA

China China

China

Geographic distribution China

Trappe and Castellano (2000) Deng et al. (2013) Fan et al. (2016b) Wan et al. (2017a) Fan and Cao (2012) GuevaraGuerrero et al. (2015) Fan and Yue (2013) Berkeley and Broome (1846)

References Chen and Liu (2007) Fan et al. (2011a) Xu (1999) Fan et al. (2012d) Trappe (1979)

116 M. Leonardi et al.

MB 254781 MB 814690

MB 811502 MB 564483 MB 811141] MB 488927 MB 487925 MB 130788

Tuber sphaerosporum Gilkey

Tuber tequilanum G. Guevara, Bonito & Trappe

Tuber thailandicum Suwannar, Kumla & Lumyong

Tuber vesicoperidium L. Fan

Tuber xuanhuaense L. Fan

Tuber zhongdianense X.Y. He, Hai M. Li & Y. Wang Regianum clade Tuber bernardinii Gori Tuber regianum Montecchi & Lazzari MB 819574

KY420104 KY420099

MB 800677

Tuber sinosphaerosporum L. Fan, J.Z. Cao & Yu Li

Tuber magentipunctatum Merényi, I. Nagy, Stielow & Bratek Rufum clade

NR119621

MB 818667 MB 564482

Tuber sinoniveum S.P. Wan Tuber sinopuberulum L. Fan & J.Z. Cao

JQ288909

KP276179

JQ690071

KP196329

KT897482

HM485390

JX092086

KX904882 JQ690073

KX555454

MB 817704

Tuber shii L. Fan & Y.W. Wang

HM485387 KT444595

MB 150287 MB 814191

Tuber separans Gilkey Tuber shidianense S.P. Wan & F.Q. Yu

ZB 4293 - BP107924

MCVE 970 87/002 (MuSe)

Y. Wang 0299 (IFS)

HMAS 60213

BJTC FAN155

SDBR-CMU-MTUF001

MycoBank Typification #136858 Trappe 33796 (OSU)

BJTC FAN135

HKAS 88792 BJTC FAN157

BJTC FAN409

HKAS 88770

Italy Italy-SlovakiaSpain Hungary-Italy

China

China

China

Thailand

Mexico

USA

China

China China

China

North America China

(continued)

Gori (2003) Montecchi and Lazzari (1987) Crous et al. (2017)

GuevaraGuerrero et al. (2015) Suwannarach et al. (2015) Fan et al. (2012c) Fan et al. (2016b) He et al. (2004)

Gilkey (1916) Wan et al. (2016) Wang et al. (2016) Xu et al. (2017) Fan et al. (2012c) Fan et al. (2012a) Gilkey (1939)

4 Truffles: Biodiversity, Ecological Significances. . . 117

JX402095 JX402090 MH115318

MB 824804 MB 226599 MB 563693 MB 356056 MB 383644 MB 415319 MB 824805 MB807402 MB 547003 MB 270389 MB 801007 MB 204496 MB 824806

Tuber crassitunicatum L. Fan & X.Y. Yan Tuber ferrugineum Vittad. Tuber formosanum H.T. Hu & Y. Wang

Tuber furfuraceum H.T. Hu & Y.I. Wang

Tuber huidongense Y. Wang

Tuber liaotongense Y. Wang

Tuber lishanense L. Fan & X.Y. Yan Tuber luomae Trappe, Eberhart, Piña Páez & Bonito

Tuber lyonii Butters

Tuber malacodermum E. Fisch.

Tuber melosporum (G. Moreno, J. Díez & Manjón) P. Alvarado, G. Moreno, Manjón & J. Díez Tuber nitidum Vittad. Tuber piceatum L. Fan, X.Y. Yan & M.S. Song

FJ748910

MH115303 FJ809887

HM485369

FJ797877

FJ859900

MH115295 AF106892 JN655530

HM485348

MB 227470

Tuber candidum Harkn.

ITS Ref. Seq. MT006095

MycobBank# MB 834191

Species Tuber buendiae Ant. Rodr. & Morte

Table 4.1 (continued)

HMAS 97125

OSC#58742 (ISOTYPE) – Trappe 17730 Nov 1907, leg. Sassella (holotype BERN) MA-Fungi 3359

87062 Coll Wang Yun 8-28-1987 BJTC FAN718 OSC 148707

IFP, Wang 89923

H.T. Hu 0201

KUN–HKAS62628

BJTC FAN465

Harkness 195 (BPI)

Holotype voucher/specimen # MUB Fung-0974

All Europe China

Spain-Italy

Switzerland

USA

China USA

China

China

China

China Southern Europe China

North America

Geographic distribution Spain

Alvarado et al. (2012b) Vittadini (1831) Yan et al. (2018)

Fischer (1923)

Yan et al. (2018) Eberhart et al. (2020) Butters (1903)

References Crous et al. (2020) Phillips and Harkness (1899) Yan et al. (2018) Vittadini (1831) Qiao et al. (2013) Hu and Wang (2005) Wang and He (2002) Wang (1990)

118 M. Leonardi et al.

AY918957

GU979033 MK211283 FJ797879

MB 357108 MB 819602 MB 519841 MB 325085

MB 800576 MB 104836 MB 828724 MB 357098 MB 824807 MB 800577

Tuber rufum Picco Tuber sinoalbidum L. Fan & J.Z. Cao

Tuber spinoreticulatum Uecker & Burds.

Tuber subglobosum L. Fan & C.L. Hou

Tuber taiyuanense B. Liu Tuber theleascum M. Leonardi, A. Paz, G. Guevara & Pacioni Tuber umbilicatum Juan Chen & P.G. Liu

Tuber wanglangense L. Fan Tuber wenchuanense L. Fan & J.Z. Cao DQ478637 JX267044

JX267043

FJ748913

AY112894 JF921164

MK211278

MB 828722

Tuber pustulatum M. Leonardi, A. Paz, G. Guevara & Pacioni Tuber quercicola J.L. Frank, D. Southw. & Trappe

HMAS 60220 HMAS 60239

HKAS 44316

HMAS 75888A ITCV908

BJTC FAN153

Uecher188

BJTC FAN105

J. L. Frank 738

BCN-Myc IC10011503

China China

China

China Mexico

China

USA

All Europe China

North America

Spain-France

Leonardi et al. (2019) Frank et al. (2006) Picco (1788) Fan et al. (2011b) Uecker and Burdsall Jr (1977) Fan et al. (2013b) Liu (1985) Leonardi et al. (2019) Chen et al. (2006) Yan et al. (2018) Fan et al. (2013b)

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until 2015. Although Kinoshita and colleagues assumed that this group was endemic to Japan, two studies described two species from China (Fan et al. 2015; Qing et al. 2015) by renaming the clade as “Turmericum” (Fan et al. 2015). However, phylogenetic analysis conducted by Kinoshita et al. (2016) shows that the Chinese species T. xanthomonosporum and T. turmericum fall into a group with low ITS variability (99.6–99.9% similarity). Moreover, the lack of morphological differences between the two species suggests that they may be synonyms. All the species in this clade have one ascospore per ascus (T. flavidosporum, T. turmericum, and T. xanthomonosporum) except for T. japonicum that usually has two ascospores per ascus. Four new species have been identified in the Maculatum clade, all of which come from North and Central America. Tuber arnoldianum was found as ascomata and ectomycorrhizas of native and non-native Fagaceous roots at the Arnold Arboretum in Massachusetts (Healy et al. 2016b). Tuber brennemanii and T. floridanum were previously indicated by Bonito et al. (2010) as Tuber sp. 36 and Tuber sp. 47, respectively, after analyzing ectomycorrhizal communities in pecan orchards. Their ascomata were described later from both disturbed habitats and natural forests. The last new species T. aztecorum was found in central Mexico. Ascoma morphology features and phylogenetic analysis demonstrated that T. aztecorum is easily distinguishable from all other species in the Maculatum clade distributed in northeastern Mexico, such as T. castilloi and T. guevarai. There are three new species in the Melanosporum clade. Merényi et al. (2017) identified Tuber cryptobrumale, as a cryptic species in the T. brumale species complex, through different approaches of integrative taxonomy. The other two, T. longispinosum and T. yigongense, are from Japan and China (Tibet), respectively. Tuber yigongense is probably a cryptic lineage of the Tuber indicum complex which has not yet been resolved in a rigorous and satisfactory manner. In fact, Fan et al. (2018) support the hypothesis that the Chinese truffles previously identified as Tuber indicum and Tuber himalayense could be genetically different from Indian species and thus their correct names should be Tuber sinense K. Tao & B. Liu and T. formosanum H.T. Hu & Y. Wang. Unfortunately, holotypes of T. indicum and T. himalayense deposited in the Kew Herbarium have not been barcoded (molecular typed). Because of the worldwide importance of T. melanosporum and the large number of superficially similar Chinese species, flavor would be a useful taxonomic feature for the applied scientist even if these were just blunt comments such as “not so good,” “disgusting,” “stunning,” or “best forgotten.” However, these are rarely to be seen in a taxonomist’s vocabulary. Twenty-one new species have been added to the Puberulum complex. Only two of the new species match with the undescribed lineages identified by Lancellotti et al. (2016b) and many lineages from all continents remain unnamed. GuevaraGuerrero et al. (2015) and Piña Paez et al. (2018) have described five new taxa from Mexico: Tuber bonitoi, T. brunneum, T. pseudoseparans, T. tequilanum, and T. incognitum. The first four new species have phylogenetic affinity to Tuber separans, described from the USA. The other species were from the Far East: 15 in China and 1 in Thailand. Fan et al. (2016b) proposed the creation of the

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“Latisporum” clade including only Puberulum species from Asia. The Latisporum group should include nine Chinese species (T. polymorphosporum, T. baoshanense, T. latisporum, T. panzhihuanense, T. alboumbilicum, T. pseudosphaerosporum, T. parvomurphium, T. caoi, Tuber sp. 3), four Japanese species (Tuber sp. 10, Tuber sp. 11, Tuber sp. 12, Tuber sp. 13), and the unique species from Thailand (T. thailandicum) (Wan et al. 2017a). The Chinese species T. microsphaerosporum, T. sinopuberulum, and T. vesicoperidium have also been defined by Fan et al. (2012c, d) but could be synonyms of T. lijiangense, a complex species that needs a more detailed investigation. Healy et al. (2016a) reviewed the diversity and taxonomy of the Rufum clade by removing erroneous species names and considering only verified specimen-based sequences. The group share spiny ascospore ornamentation with the Melanosporum clade where several species show a range of spiny-alveolate spore ornamentation. In addition, T. melosporum is the only Tuber species having smooth ascospores (Lancellotti et al. 2016a). Eight species were newly described in the Rufum clade. Tuber buendiae from Spain was previously identified as a hypothetical undescribed species Tuber sp. 83 by Healy et al. (2016a). It is similar to T. pustulatum, another new species described by Leonardi et al. (2019) from Spain and France (Corsica) and firstly identified as T. malacodermum by Cabero (2009) and Bonito et al. (2010, 2013). Leonardi et al. (2019) described also T. theleascum from Mexico belonging to T. lyonii species complex (sensu Healy et al. 2016a) and previously identified as the undescribed species Tuber sp. 65 (Bonito et al. 2010, 2013). T. malacodermum, T. pustulatum, and T. theleascum share the typical peridial structure with T. luomae, a new species from the Pacific Northwest, USA. Eberhart et al. (2020) emphasize this character of the peridiopellis that is uncommon in the Rufum clade which has been found in geographically disjunct species. The other four new Tuber species belonging to the Rufum clade were described from China by Yan et al. (2018). Tuber crassitunicatum is very similar to the previously described species T. taiyuanense and T. huidongense because of its brown ascomata with ellipsoidal and spinoreticulate ascospores. Tuber lishanense and T. piceatum are very similar to the European T. nitidum and the North American T. candidum, while T. wanglangense is a sister species of T. wenchuanense, which is found in the same region. With regard to the other clades, T. calosporum was described as a new Chinese member of the Macrosporum clade, Tuber lucentum was the third species described among the Gennadii clade, while no new species have been added to the Gibbosum and Multimaculatum clades. Tuber bernardinii, T. regianum, and the recently described T. magentipunctatum seem to be a clade of its own but phylogenetic analysis involving these species is still poor and not resolved.

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Ecological Significance

Research conducted over the past 20 years has shown that true truffles have a worldwide distribution and are common in many terrestrial ecosystems. They can be found from natural forests to strongly anthropized areas such as urban parks and gardens and in boreal, temperate, Mediterranean, subtropical, or tropical climates (Morris et al. 2009; Hynson et al. 2013; Wang et al. 2013; Zambonelli et al. 2014; Suwannarach et al. 2015; Lin et al. 2018; Yadav 2020). Like many species of ectomycorrhizal mushrooms, Tuber is characterized by a high continental or local endemism (Bonito et al. 2010) so it is rare to find species shared between two continents or species widespread over a whole continent. While the true truffles are native to the Northern Hemisphere applied scientists have ensured that T. melanosporum, T. borchii, and T. aestivum are now not uncommon in all Southern Hemisphere countries with land south of 33 S: New Zealand, Australia, Chile, South Africa, Argentina, Brazil, and probably Uruguay (Reyna and Garcia-Barreda 2014; Zambonelli et al. 2015; Hall et al. 2017). Other species, in particular those of the Puberulum clade s.l. (the whitish truffles, Lancellotti et al. 2016a, b), were probably spread into Southern Hemisphere during the nineteenth and twentieth centuries on the roots of trees imported by early settlers for timber, fruit, nuts, or landscaping and are often found in nurseries (Barroetaveña et al. 2006, 2010; Southworth et al. 2009; Pietras et al. 2013). Ascomata or ectomycorrhizae of whitish truffles such as T. maculatum, T. dryophilum, and T. rufum are now common members of ectomycorrhizal communities of tree species introduced into New Zealand (Bulman et al. 2010) and have been found under Nothofagus alpina in Northern Patagonia (Nouhra et al. 2013). The range of distribution varies considerably depending on the Tuber species. Tuber aestivum seems to be the species with the highest ecological adaptation to climate and soil conditions (Molinier et al. 2016; Robin et al. 2016), probably supported by its high intraspecific genetic diversity (Molinier et al. 2015; Riccioni et al. 2019). It can be found in almost all countries throughout Europe as well as in northern Africa, the Middle East, and as far east as Iran (Zambonelli et al. 2014; Molinier et al. 2016; Jamali 2017). The distribution area of T. borchii roughly coincides with that of T. aestivum although they do not share the same habitats. However, T. borchii seems to include two cryptic species (Bonuso et al. 2010) whose ascomata have been rarely collected in the same sites (Iotti M, personal observation). Some other Tuber species have a wide distribution area but they also include cryptic lineages whose phylogeography is unknown. Three main clades have been identified in Tuber anniae after analyzing sequences of ascomata and ectomycorrhizae from North America and North Europe (Wang et al. 2013). Tuber indicum sl is spread throughout a vast area from Himalaya to Japan and the presence of different cryptic species has been stressed by many authors (Wang et al. 2006; Chen et al. 2011; Belfiori et al. 2013; Kinoshita et al. 2018; Qiao et al. 2018). Reports of Tuber malacodermum were from both Europe and Central America but a recent work (Leonardi et al. 2019) identified Tuber pustulatum (Spain and Corsica)

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and Tuber theleascum (Mexico) as new species in addition to T. malacodermum type clade. In-depth phylogeographic and ecological investigations should be done for these entire species complex in Tuber, in particular for T. mesentericum, T. brumale, T. rufum, and T. excavatum which have a number of unexplored lineages spread mostly everywhere in Europe (Iotti et al. 2007; Benucci et al. 2016; Healy et al. 2016a, b; Merényi et al. 2016; Puliga et al. 2020). Most Tuber species have a relatively narrow geographic distribution. The worldwide cultivated truffle T. melanosporum is naturally spread only in few western European countries (mainly Italy, France, and Spain) but it can adapt both to warm Mediterranean and colder continental climates, provided that no extreme drought or freeze events occur (Hall et al. 2007; Chen et al. 2016). The soil type (well drained and structured, mineralized, alkaline, and calcareous) seems to be the limiting factor affecting the spread of this truffle (Jaillard et al. 2016; Ori et al. 2018a). Other Tuber species appear to have narrow ecological requirements and are confined to specific habitats or areas. Tuber magnatum mainly grows in floodplains and riparian areas of the Italian and Balkan peninsulas, with porous soils rich in sediments and high water availability (Marjanović et al. 2015; Bragato and Marjanović 2016; Iotti et al. 2018). On the contrary, Tuber oligospermum, T. cistophilum, and T. melosporum have only been detected in typical Mediterranean environments of Iberian Peninsula, Morocco, and Sardinia (Alvarado et al. 2012a, b; Boutahir et al. 2013; Lancellotti et al. 2016a, b). Many other species in the genus, as Tuber bernardinii (Gori 2003), are extremely rare and it is difficult to define their ecological preferences from the current literature. Tuber members have very low host specificity although the range of symbiotic associations has been studied in detail only for valuable species. The most common host plants are trees within Pinaceae and Fagaceae but truffles can also establish ectomycorrhizae with Betulaceae, Myrtaceae, Juglandaceae, Malvaceae, Salicaceae, and many shrubs in the Cistaceae (Gryndler 2016). Moreover, Tuber species can form other types of mycorrhizae with plants belonging to Ericaceae and Orchidaceae. Truffles in the Puberulum and Rufum clades were found to establish arbutoid mycorrhizae with Arbutus spp. in the wild (Kennedy et al. 2012; Lancellotti et al. 2014) but, at present, no ericoid or monotropoid mycorrhizae were described with other Ericales. On the contrary, many Tuber species have been detected as fungal partner in orchid mycorrhizae (Selosse et al. 2004; Julou et al. 2005; OguraTsujita and Yukawa 2008; Ouanphanivanh 2008; Illyés et al. 2010; Jacquemyn et al. 2017; Schiebold et al. 2017). The presence of Tuber mycelium which appeared to be a weak parasite in the roots of otherwise healthy non-ectomycorrhizal herbaceous plants was first detected using ELISA by Plattner and Hall (1995) (Fig. 4.1). A variety of publications have been published since then (Gryndler et al. 2014; Schneider-Maunoury et al. 2020; Taschen et al. 2020). While some studies showed the fungi to be confined to the apoplastic compartment of fine roots (SchneiderMaunoury et al. 2020) Ian Hall (pers. comm.) remains convinced that T. melanosporum is a wolf in sheep’s clothing and the brûlé is the result of a general aggressive trait in some Tuber species. Indeed, like many other ectomycorrhizal fungi, Tuber species are able to colonize and connect to a wide range of plants at the

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Fig. 4.1 Fungal infections in the roots of Anthoxanthum odoratum, a short-lived perennial grass, stained with trypan blue, were shown by ELISA to be formed by Tuber melanosporum (Plattner and Hall 1995)

same time, contributing to driving the evolution and functioning of many terrestrial ecosystems (Smith and Read 2008). Despite their wide distribution and diversity, Tuber species are patchily distributed and rarely dominate ectomycorrhizal community in natural forests. This condition changes in truffle plantations where the use of nursery-inoculated plants confers a competitive advantage to the cultivated truffle (Zambonelli et al. 2000; Zambonelli et al. 2005) as long as the other ectomycorrhizal fungi do not take over. The decline rate of Tuber ectomycorrhizae depends on climate and soil conditions of the plantation site but also on the repertoire of the local ectomycorrhizal fungi that can coexist with or replace them. Specific studies on the composition of ectomycorrhizal communities in natural and cultivated truffle grounds have been only carried out for the valuable species T. melanosporum (Belfiori et al. 2012; Taschen et al. 2015), T. magnatum (Murat et al. 2005; Bertini et al. 2006; Leonardi et al. 2013), T. aestivum (Benucci et al. 2011), T. borchii (Iotti et al. 2010), and Tuber macrosporum (Benucci et al. 2014). The experimental sites investigated by these authors have alkaline (pH >7) and calcareous soils with a low content of organic matter (