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Principles of Plant-Microbe Interactions: Microbes for Sustainable Agriculture
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Principles of Plant-Microbe Interactions
Ben Lugtenberg
Editor
Principles of Plant-Microbe
Interactions
Microbes for Sustainable Agriculture
2123
Editor
Ben Lugtenberg
Molecular Microbiology and Biotechnology
Leiden University, Sylvius Laboratory
Leiden
The Netherlands
ISBN 978-3-319-08574-6 ISBN 978-3-319-08575-3 (eBook)
DOI 10.1007/978-3-319-08575-3
Springer Cham Heidelberg New York Dordrecht London
Library of Congress Control Number: 2014956088
© Springer International Publishing Switzerland 2015
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the
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does not imply, even in the absence of a specific statement, that such names are exempt from the relevant
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While the advice and information in this book are believed to be true and accurate at the date of publication,
neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or
omissions that may be made. The publisher makes no warranty, express or implied, with respect to the
material contained herein.
Printed on acid-free paper
Springer is part of Springer Science+Business Media (www.springer.com)
I dedicate this book to my wife Faina and my
children Annelieke, Martijn and Marjolein
Preface
The field of Plant Microbe Interactions is very broad. It covers all topics in which microbes influence or even determine plant activities. Plant enemies can be pathogenic
viruses, microbes or insects which cause pests. Fortunately, these enemies in turn
have natural enemies in the form of beneficial microbes, which can protect plants
against pathogens and pests. As is rather common in this field, we included nematodes and insects in the book. Although they are not microbes, they have in common
with microbes that some can cause harm to, and others help protect, the plant. Another group of microbes is beneficial for plant growth. Some microbes promote plant
growth, for example by producing “plant” hormones or by making nutrients available to the plant. Other beneficial microbes can alleviate plant stress or can inactivate
environmental pollutants, thereby cleaning the environment and allowing plants to
grow without toxic residues. The present market share of biologicals is estimated
at 1.6 billion USDs and is growing fast. In the past years the trend is that major
chemical companies buy smaller biotech companies.
For this book I have invited the world’s top scientists to summarize the basic
principles of all these topics in brief chapters which give a helicopter view on the
subjects. The book also contains important techniques, success stories and future
prospects. The topics include basic as well as applied aspects. Hereby we make an
attempt to close the gap that still exists between fundamental and applied research.
In my opinion the two fields need each other and cooperation will create a win-win
situation for both parties. Since space is limited, the authors have often referred to
reviews. For more detailed information, the reader can consult primary articles listed
as references in these reviews.
This book is meant for everybody who is interested in plant-microbe interactions
and in the roles microbes can play in making agriculture and horticulture more
sustainable. These include academic scientists, industrial professionals working in
agriculture, horticulture, biotech and food industry, students, teachers, as well as
government officials and decision makers who quickly want to make themselves
familiar with particular aspects of this broad field. Using this information as a basis,
also a non-specialist reader should be able to understand more complicated articles
and to discuss selected topics with colleagues. To read the book, basic knowledge of
plant science, microbiology, biochemistry, and molecular biology is helpful.
Ben Lugtenberg, editor
vii
Acknowledgement
I am very much indebted to all authors for their contributions. I am particularly
thankful to the following people who have contributed by useful advice and discussions: Gabriele Berg, Rainer Borriss, Frans de Bruijn, Faina Kamilova, Christoph
Keel, Corné Pieterse, and Clara Pliego. I am greatly obliged to Izabela Witkowska
and Melanie van Overbeek of Springer Dordrecht for their help and patience during
the preparation of the manuscript.
The following sponsors made the editing of the book more pleasant. Their contributions will go to a foundation which supports the promotion of knowledge about
plant-microbe interactions and their applications.
DIAMOND SPONSORS
ix
x Acknowledgement
GOLD SPONSORS
Contents
1 Introduction to Plant-Microbe Interactions ...................... 1
Ben Lugtenberg
Part I Introductory Chapters
2 The Importance of Microbiology in Sustainable Agriculture ........ 5
Thomas Schäfer and Tom Adams
3 Life of Microbes in the Rhizosphere ............................. 7
Ben Lugtenberg
4 Life of Microbes on Aerial Plant Parts . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Johan H. J. Leveau
5 Life of Microbes Inside the Plant. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Jesús Mercado-Blanco
6 Microbial Cell Surfaces and Secretion Systems . . . . . . . . . . . . . . . . . . . 33
Jan Tommassen and Han A. B. Wösten
7 Microbial Biofilms and Quorum Sensing . . . . . . . . . . . . . . . . . . . . . . . . . 45
Aurelien Carlier, Gabriella Pessi and Leo Eberl
8 Bacterial Volatiles as Airborne Signals for Plants and Bacteria . . . . . 53
Choong-Min Ryu
Part II Phytopathogens and Pest Insects
9 Phytopathogenic Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
Jan van der Wolf and Solke H. De Boer
10 Plant Pathogenic Fungi and Oomycetes . . . . . . . . . . . . . . . . . . . . . . . . . . 79
Pierre J. G. M. de Wit
xi
xii Contents
11 Phytopathogenic Nematodes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
Johannes Helder, Mariëtte Vervoort, Hanny van Megen, Katarzyna
Rybarczyk-Mydłowska, Casper Quist, Geert Smant and Jaap Bakker
12 Herbivorous Insects—A Threat for Crop Production . . . . . . . . . . . . . . 103
Eddy van der Meijden
13 Phytopathogenic Viruses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115
Carmen Büttner, Susanne von Bargen and Martina Bandte
14 Induced Disease Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
Corné M. J. Pieterse and Saskia C. M. Van Wees
15 Apologies to the Planet—Can We Restore the Damage? . . . . . . . . . . . . 135
Dulce Eleonora de Oliveira and Marc Van Montagu
16 Will the Public Ever Accept Genetically Engineered Plants? . . . . . . . 145
Inge Broer
Part III Control of Plant Diseases and Pests using Beneficial Microbes
17 Microbial Control of Phytopathogenic Nematodes . . . . . . . . . . . . . . . . 155
Xiaowei Huang, Keqin Zhang, Zefen Yu and Guohong Li
18 Microbial Control of Root-Pathogenic Fungi and Oomycetes . . . . . . . 165
Linda Thomashow and Peter A. H. M. Bakker
19 Control of Insect Pests by Entomopathogenic Nematodes . . . . . . . . . . 175
Vladimír Pu◦
ža
20 Bacillus thuringiensis-Based Products for Insect Pest Control . . . . . . 185
Ruud A. de Maagd
21 Post Harvest Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
Emilio Montesinos, Jesús Francés, Esther Badosa
and Anna Bonaterra
Part IV Plant Growth Promotion by Microbes
22 The Nitrogen Cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
Martine A. R. Kox and Mike S. M. Jetten
23 Biological Nitrogen Fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215
Frans J. de Bruijn
24 Phosphate Mobilisation by Soil Microorganisms . . . . . . . . . . . . . . . . . . 225
José-Miguel Barea and Alan E. Richardson
Contents xiii
25 Arbuscular Mycorrhizas: The Lives of Beneficial Fungi and Their
Plant Host . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235
Paola Bonfante and Alessandro Desirò
26 Plant Hormones Produced by Microbes. . . . . . . . . . . . . . . . . . . . . . . . . . 247
Stijn Spaepen
27 Stress Control and ACC Deaminase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
Bernard R. Glick
28 Plant-Microbe Interactions and Water Management in Arid
and Saline Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265
Daniele Daffonchio, Heribert Hirt and Gabriele Berg
29 Rhizoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277
Sofie Thijs and Jaco Vangronsveld
Part V Important Technologies
30 Microbial Communities in the Rhizosphere Analyzed
by Cultivation-Independent DNA-Based Methods. . . . . . . . . . . . . . . . . 289
Susanne Schreiter, Namis Eltlbany and Kornelia Smalla
31 Visualization of Plant-Microbe Interactions . . . . . . . . . . . . . . . . . . . . . . 299
Massimiliano Cardinale and Gabriele Berg
Part VI Products for Plant Growth-promotion and Disease Suppression
32 Commercialisation of Microbes: Present Situation
and Future Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 309
Willem J. Ravensberg
33 Commercialization of Microbes: Manufacturing, Inoculation,
Best Practice for Objective Field Testing, and Registration . . . . . . . . . 319
Faina Kamilova, Yaacov Okon, Sandra de Weert and Katja Hora
34 Towards a New Generation of Commercial Microbial Disease
Control and Plant Growth Promotion Products. . . . . . . . . . . . . . . . . . . 329
Rainer Borriss
35 Important Organizations and Companies . . . . . . . . . . . . . . . . . . . . . . . . 339
Ben Lugtenberg
Part VII Paradigms in Plant-Microbe Interactions
36 Trichoderma: A Multi-Purpose Tool for Integrated Pest
Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 345
Matteo Lorito and Sheridan L. Woo
xiv Contents
37 Agrobacterium, The Genetic Engineer . . . . . . . . . . . . . . . . . . . . . . . . . . . 355
Paul J. J. Hooykaas
38 Take-All Decline and Beneficial Pseudomonads . . . . . . . . . . . . . . . . . . . 363
David M. Weller
39 The Oomycete Phytophthora infestans, the Irish Potato
Famine Pathogen. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 371
Charikleia Schoina and Francine Govers
40 Bacillus, A Plant-Beneficial Bacterium . . . . . . . . . . . . . . . . . . . . . . . . . . . 379
Rainer Borriss
41 Soybean Production in the Americas . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393
Woo-Suk Chang, Hae-In Lee and Mariangela Hungria
Part VIII Future Prospects and Dreams
42 Exploring the Feasibility of Transferring Nitrogen Fixation
to Cereal Crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403
Muthusubramanian Venkateshwaran
43 The Minimal Rhizosphere Microbiome . . . . . . . . . . . . . . . . . . . . . . . . . . 411
Jos M. Raaijmakers
44 The Edible Plant Microbiome: Importance and Health Issues . . . . . . 419
Gabriele Berg, Armin Erlacher and Martin Grube
45 From Nodulation to Antibiotics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427
Eva Kondorosi
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435
Contributors
Tom Adams Monsanto Company, St. Louis, MO, USA
Carmen Büttner Division Phytomedicine, Faculty of Life Sciences, HumboldtUniversität zu Berlin, Berlin, Germany
Esther Badosa Laboratory of Plant Pathology, Institute of Food and Agricultural
Technology, University of Girona, Girona, Spain
Jaap Bakker Laboratory of Nematology, Wageningen University, Wageningen,
The Netherlands
Peter A. H. M. Bakker Plant-Microbe Interactions, Institute of Environmental
Biology, Utrecht University, Utrecht, The Netherlands
Martina Bandte Division Phytomedicine, Faculty of Life Sciences, HumboldtUniversität zu Berlin, Berlin, Germany
José-Miguel Barea Soil Microbiology and Symbiotic Systems Department,
Estación Experimental del Zaidín, CSIC, Granada, Spain
Gabriele Berg Institute of Environmental Biotechnology, Graz University of
Technology, Graz, Austria
Anna Bonaterra Laboratory of Plant Pathology, Institute of Food and Agricultural
Technology, University of Girona, Girona, Spain
Paola Bonfante Department of Life Sciences and Systems Biology, University of
Torino, Torino, Italy
Rainer Borriss ABiTEP GmbH, Berlin, Germany
Inge Broer Agricultural and Environmental Faculty, University of Rostock,
Rostock, Germany
Massimiliano Cardinale Institute of Applied Microbiology, Justus-LiebigUniversity Giessen, Giessen, Germany
Aurelien Carlier Institute of Plant Biology, University of Zurich, Zurich,
Switzerland
xv
xvi Contributors
Woo-Suk Chang Department of Biology, University of Texas-Arlington, Arlington,
Texas, USA
Daniele Daffonchio DeFENS, Department of Food, Environmental and Nutritional
Sciences, University of Milan, Milan, Italy
BESE Division, King Abdullah University of Science and Technology, Thuwal,
Kingdom of Saudi Arabia
Solke H. De Boer Emeritus Scientist, Charlottetown, PE, Canada
Frans J. de Bruijn INRA/CNRS Laboratory of Plant-Microbe Interactions,
Castanet-Tolosan Cedex, France
Ruud A. de Maagd Plant Research International, Wageningen UR, Wageningen,
The Netherlands
Dulce Eleonora de Oliveira VIB–Institute of Plant Biotechnology Outreach,
Department of Biotechnology and Bioinformatics, Ghent University, GentZwijnaarde, Belgium
Sandra de Weert Koppert Biological Systems, Berkel en Rodenrijs, The
Netherlands
Pierre J. G. M. de Wit Laboratory of Phytopathology, Wageningen University,
Wageningen, The Netherlands
Alessandro Desirò Department of Life Sciences and Systems Biology, University
of Torino, Torino, Italy
Leo Eberl Institute of Plant Biology, University of Zurich, Zurich, Switzerland
Namis Eltlbany Julius Kühn-Institut, Federal Research Centre for Cultivated Plants
(JKI), Braunschweig, Germany
Armin Erlacher Institute of Environmental Biotechnology, Graz University of
Technology, Graz, Austria
Institute of Plant Sciences, University of Graz, Graz, Austria
Jesús Francés Laboratory of Plant Pathology, Institute of Food and Agricultural
Technology, University of Girona, Girona, Spain
Bernard R. Glick Department of Biology, University of Waterloo, Waterloo, ON,
Canada
Francine Govers Laboratory of Phytopathology, Wageningen University,
Wageningen, The Netherlands
Martin Grube Institute of Plant Sciences, University of Graz, Graz, Austria
Johannes Helder Laboratory of Nematology, Wageningen University,
Wageningen, The Netherlands
Contributors xvii
Heribert Hirt BESE Division, King Abdullah University of Science and
Technology, Thuwal, Kingdom of Saudi Arabia
Paul J. J. Hooykaas Institute of Biology, Sylvius Laboratory, Leiden University,
Leiden, The Netherlands
Katja Hora Koppert Biological Systems, Berkel en Rodenrijs, The Netherlands
Xiaowei Huang Yunnan University, Kunming, People’s Republic of China
Mariangela Hungria Embrapa Soja, Londrina, Paraná, Brazil
Mike S. M. Jetten Department of Microbiology, Institute of Water and Wetland Research, Faculty of Science, Radboud University Nijmegen, Nijmegen, The
Netherlands
Faina Kamilova Koppert Biological Systems, Berkel en Rodenrijs, The
Netherlands
Eva Kondorosi Institute of Biochemistry, Biological Research Centre of the
Hungarian Academy of Sciences, Szeged, Hungary
Martine A. R. Kox Department of Microbiology, Institute of Water and
Wetland Research, Faculty of Science, Radboud University Nijmegen, Nijmegen,
The Netherlands
Hae-In Lee Department of Biology, University of Texas-Arlington, Arlington,
Texas, USA
Johan H. J. Leveau Department of Plant Pathology, University of California, Davis,
CA, USA
Guohong Li Yunnan University, Kunming, People’s Republic of China
Matteo Lorito Department of Agriculture, University of Naples Federico II, and
Institute of Plant Protection IPP–CNR, Portici (NA), Italy
Ben Lugtenberg Institute of Biology, Sylvius Laboratory, Leiden University,
Leiden, The Netherlands
Jesús Mercado-Blanco Department of Crop Protection, Institute for Sustainable
Agriculture, Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC),
Córdoba, Spain
Emilio Montesinos Laboratory of Plant Pathology, Institute of Food and
Agricultural Technology, University of Girona, Girona, Spain
Yaacov Okon Department of Plant Pathology and Microbiology, Faculty of
Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot,
Israel
Vladimír Pu◦
ža Institute of Entomology, Biology Centre of the AS CR, Ceské ˇ
Budˇejovice, Czech Republic