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Endophyte Biotechnology Potential for Agriculture and Pharmacology CABI Biotechnology SerieS Biotechnology, in particular the use of transgenic organisms, has a wide range of applica- tions including agriculture, forestry, food and health. There is evidence that it could make a major impact in producing plants and animals that are able to resist stresses and diseases, thereby increasing food security. There is also potential to produce pharmaceuticals in plants through biotechnology, and provide foods that are nutritionally enhanced. Genetically modified organisms can also be used in cleaning up pollution and contamination. However, the application of biotechnology has raised concerns about biosafety, and it is vital to ensure that genetically modified organisms do not pose new risks to the environment or health. To understand the full potential of biotechnology and the issues that relate to it, scientists need access to information that not only provides an overview of and background to the field, but also keeps them up to date with the latest research findings. This series, which extends the scope of CABI’s successful ‘Biotechnology in Agriculture’ series, addresses all topics relating to biotechnology including transgenic organisms, molecu- lar analysis techniques, molecular pharming, in vitro culture, public opinion, economics, development and biosafety. Aimed at researchers, upper-level students and policy makers, titles in the series provide international coverage of topics related to biotechnology, includ- ing both a synthesis of facts and discussions of future research perspectives and possible solutions. Titles available 1. Animal Nutrition with Transgenic Plants Edited by G. Flachowsky 2. Plant-derived Pharmaceuticals: Principles and Applications for Developing Countries Edited by K.L. Hefferon 3. Transgenic Insects: Techniques and Applications Edited by M.Q. Benedict 4. Bt Resistance: Characterization and Strategies for GM Crops Producing Bacillus thuringiensis Toxins Edited by Mario Soberón, Yulin Gao and Alejandra Bravo 5. Plant Gene Silencing: Mechanisms and Applications Edited by Tamas Dalmay 6. Ethical Tensions from New Technology: The Case of Agricultural Biotechnology Edited by Harvey James 7. GM Food Systems and Their Economic Impact Tatjana Brankov and Koviljko Lovre 8. Endophyte Biotechnology: Potential for Agriculture and Pharmacology Edited by Alexander Schouten Endophyte Biotechnology Potential for Agriculture and Pharmacology Edited by Alexander Schouten Laboratory of Phytopathology, Wageningen University & Research, Wageningen, The Netherlands CABI is a trading name of CAB International CABI CABI Nosworthy Way 745 Atlantic Avenue Wallingford 8th Floor Oxfordshire OX10 8DE Boston, MA 02111 UK USA Tel: +44 (0)1491 832111 T: +1 (617)682-9015 Fax: +44 (0)1491 833508 E-mail: [email protected] E-mail: [email protected] Website: www.cabi.org © CAB International 2019. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Names: Schouten, Alexander, editor. | C.A.B. International, issuing body. Title: Endophyte biotechnology : Potential for agriculture and pharmacology / edited by Alexander Schouten. Description: Wallingford, Oxfordshire, UK ; Boston, MA : CABI, [2019] | Includes bibliographical references and index. Identifiers: LCCN 2019016880| ISBN 9781786399427 (hbk : alk. paper) | ISBN 9781786399441 (epub) | ISBN 9781786399434 (epdf) Subjects: | MESH: Endophytes | Biotechnology | Symbiosis | Bacterial Physiological Phenomena | Fungi--physiology | Plants--metabolism Classification: LCC TP248.27.F86 | NLM TP248.27.M53 | DDC 660.6--dc23 LC record available at https://lccn.loc.gov/2019016880 ISBN-13: 978 1 78639 942 7 (hardback) 978 1 78639 943 4 (ePDF) 978 1 78639 944 1 (ePub) Commissioning Editor: David Hemming Editorial Assistant: Emma McCann Production Editor: Shankari Wilford Typeset by SPi, Pondicherry, India Printed and bound in the UK by Severn, Gloucester Contents Contributors vii Preface ix 1 Introduction 1 Alexander Schouten 2 Endophytic Fungi: Definitions, Diversity, Distribution and Their Significance in Plant Life 6 Alexander Schouten 3 Sources, Niches and Routes of Colonization by Beneficial Bacterial Endophytes 32 Stéphane Compant and Corinne Vacher 4 Analysing Seed Endophytes for Biotechnology 42 Alessandro Bergna, Tomislav Cernava, Christin Zachow and Gabriele Berg 5 Mitigating Climate Impacts on Crop Production via Symbiosis 59 Rusty Rodriguez, Alec Baird, Sang Cho, Zachery Gray, Evan Groover, Roman Harto, Marian Hsieh, Katie Malmberg, Ryan Manglona, Malia Mercer, Natalie Nasman, Tatiana Nicklason, Melissa Rienstra, Alex Van Inwegen, Andy VanHooser and Regina Redman 6 Endophytes as Novel Pest Control Agents: Myth or Reality? 68 Alan C. Gange, Amanda F. Currie and Jessica-Rose Spong 7 Improved Adaptation of Temperate Grasses through Mutualism with Fungal Endophytes 85 John R. Caradus and Linda J. Johnson 8 Interactive Effects of Co-occurring Epichloid Endophytes, Rhizobia and Arbuscular Mycorrhizal Fungi Modulating Their Benefits to Grasses and Legumes 109 Pablo Adrián García-Parisi and Marina Omacini v vi Contents 9 Saving Resources: The Exploitation of Endophytes by Plants for the Biosynthesis of Multi-functional Defence Compounds 122 Alexander Schouten 10 Bioprospecting of Endophytes 145 Weaam Ebrahim, Sherif S. Ebada and Peter Proksch 11 Prospects for Biotechnological Exploitation of Endophytes Using Functional Metagenomics 164 Melanie-Maria Obermeier and Christina A. Müller Bogotá 12 Interplay between Endophyte and Host Plant in the Synthesis and Modification of Metabolites 180 Jutta Ludwig-Müller Index 199 Contributors Alec Baird, University of California, Los Angeles, California, USA Gabriele Berg, Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria Alessandro Bergna, Austrian Centre of Industrial Biotechnology, Graz, Austria John R. Caradus, Grasslanz Technology Limited, Palmerston North, New Zealand Tomislav Cernava, Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria Sang Cho, Adaptive Symbiotic Technologies, Seattle, Washington, USA Stéphane Compant, Bioresources Unit, Center for Health & Bioresources, AIT Austrian Institute of Technology GmbH, Tulln, Austria Amanda F. Currie, School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK Sherif S. Ebada, Department of Pharmacognosy, Faculty of Pharmacy, Ain Shams University, Cairo; Department of Pharmaceutical Chemistry, Faculty of Pharmacy, Mu’tah University, Al-Karak, Jordan Weaam Ebrahim, Department of Pharmacognosy, Faculty of Pharmacy, Mansoura University, Mansoura, Egypt Alan C. Gange, School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK Pablo A. García-Parisi, IFEVA, Facultad de Agronomía, Universidad de Buenos Aires, CONICET, Buenos Aires, Argentina; Cátedra de Forrajicultura, Departamento de Producción Animal, Facultad de Agronomía, Universidad de Buenos Aires, Buenos Aires Zachery Gray, Adaptive Symbiotic Technologies, Seattle, Washington, USA Evan Groover, University of California, Berkeley, California, USA Roman Harto, Adaptive Symbiotic Technologies, Seattle, Washington, USA Marian Hsieh, Adaptive Symbiotic Technologies, Seattle, Washington, USA Linda J. Johnson, AgResearch Limited, Grasslands Research Centre, Palmerston North, New Zealand Jutta Ludwig-Müller, Institut für Botanik, Technische Universität Dresden, Dresden, Germany Katie Malmberg, Adaptive Symbiotic Technologies, Seattle, Washington, USA Ryan Manglona, Adaptive Symbiotic Technologies, Seattle, Washington, USA Malia Mercer, Adaptive Symbiotic Technologies, Seattle, Washington, USA vii viii Contributors Christina A. Müller Bogotá, Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria Natalie Nasman, Adaptive Symbiotic Technologies, Seattle, Washington, USA Tatiana Nicklason, Adaptive Symbiotic Technologies, Seattle, Washington, USA Melanie-Maria Obermeier, Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria; Austrian Centre of Industrial Biotechnology, Graz, Austria Marina Omacini, IFEVA, Facultad de Agronomía, Universidad de Buenos Aires, CONICET, Buenos Aires; Cátedra de Ecología, Departamento de Recursos Naturales y Ambiente, Facultad de Agronomía, Universidad de Buenos Aires, Buenos Aires Peter Proksch, Institute of Pharmaceutical Biology and Biotechnology, Heinrich- Heine- University Düsseldorf, Düsseldorf, Germany Regina Redman, Adaptive Symbiotic Technologies, Seattle, Washington, USA; Symbiogenics, Seattle, Washington, USA Melissa Rienstra, Adaptive Symbiotic Technologies, Seattle, Washington, USA Rusty Rodriguez, Adaptive Symbiotic Technologies, Seattle, Washington, USA; Symbiogenics, Seattle, Washington, USA; University of Washington, Seattle, Washington, USA Alexander Schouten, Laboratory of Nematology, Wageningen University & Research, Wageningen, The Netherlands. (Current address: Laboratory of Phytopathology, Wagenin- gen University & Research, Wageningen, The Netherlands) Jessica-Rose Spong, School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK Corinne Vacher, BIOGECO, INRA, University of Bordeaux, Pessac, France Alex Van Inwegen, Adaptive Symbiotic Technologies, Seattle, Washington, USA Andy VanHooser, Adaptive Symbiotic Technologies, Seattle, Washington, USA Christin Zachow, Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria Preface Virtually all plants in nature build intimate associations with microbes. Some microbes not only reside on the plant surface but are also capable of migrating into the plant without show- ing a distinct phenotype and eliciting disease responses. These rather elusive endophytic microbes are often closely related to plant pathogenic species and can even display the endophytic behaviour in one plant species while being pathogenic in another. Plants that have a persisting endophytic association with microbes often have a significant advantage over those that have not, because their performance and survival under stressful biotic and abiotic conditions, such as herbivory, disease, drought, extreme temperatures, or a combination of these, is positively affected by this association. Expanding the knowledge on plant–endophyte interactions is of crucial importance for future developments in plant breeding and sustain- able agricultural practices. What is more, as they are involved in biotrophic interactions, endophytes and, by combining their biosynthetic pathways, the plant–endophyte association may hold new peptides and metabolites with valuable properties for pharmacological and biotechnological purposes. In the past ten years, the fundamental and applied research on endophytes has significantly accelerated by using state-of-the-art molecular, biochemical, microscopical and biological techniques. This book aims at appreciating the added value of the current accumulated knowledge on endophytes by elaborating on the latest insights regarding microorganisms, their mesmerizing diversity and distribution, their intriguing interactions with plants, their ecological functions, and their benefits and applications in agriculture, biotechnology and medicine. I sincerely acknowledge all the colleagues who contributed, thus making this book possible: David Hemming at CABI for inviting me to edit this book in this series and both David Hem- ming and Emma McCann at CABI for their friendly support, advice and patience. Alexander Schouten Wageningen February 2019 ix

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