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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
material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,


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now known or hereafter developed. Exempted from this legal reservation are brief excerpts in connection
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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 . . . . . . . . . . . . . . . . . . . . . .
Ben Lugtenberg

1

Part I Introductory Chapters

2

The Importance of Microbiology in Sustainable Agriculture . . . . . . . .
Thomas Schäfer and Tom Adams

5

3

Life of Microbes in the Rhizosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Ben Lugtenberg

7

4

Life of Microbes on Aerial Plant Parts . . . . . . . . . . . . . . . . . . . . . . . . . . .
Johan H. J. Leveau

17

5

Life of Microbes Inside the Plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Jesús Mercado-Blanco

25

6


Microbial Cell Surfaces and Secretion Systems . . . . . . . . . . . . . . . . . . .
Jan Tommassen and Han A. B. Wösten

33

7

Microbial Biofilms and Quorum Sensing . . . . . . . . . . . . . . . . . . . . . . . . .
Aurelien Carlier, Gabriella Pessi and Leo Eberl

45

8

Bacterial Volatiles as Airborne Signals for Plants and Bacteria . . . . .
Choong-Min Ryu

53

Part II Phytopathogens and Pest Insects
9

Phytopathogenic Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Jan van der Wolf and Solke H. De Boer

65

10

Plant Pathogenic Fungi and Oomycetes . . . . . . . . . . . . . . . . . . . . . . . . . .

Pierre J. G. M. de Wit

79

xi


xii

Contents

11

Phytopathogenic Nematodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Johannes Helder, Mariëtte Vervoort, Hanny van Megen, Katarzyna
Rybarczyk-Mydłowska, Casper Quist, Geert Smant and Jaap Bakker

91

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,
University Giessen, Giessen, Germany

Justus-Liebig-

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, The Netherlands

Wageningen University,

Martin Grube Institute of Plant Sciences, University of Graz, Graz, Austria
Johannes Helder Laboratory
Wageningen, The Netherlands

of

Nematology,

Wageningen

University,


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,
Netherlands

Berkel en Rodenrijs,

The

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
ˇ
Vladimír Pu◦ ža Institute of Entomology, Biology Centre of the AS CR, Ceské
Budˇejovice, Czech Republic


xviii

Contributors

Gabriella Pessi Institute of Plant Biology, University of Zurich, Zurich,
Switzerland
Corné M. J. Pieterse Plant-Microbe Interactions, Department of Biology, Faculty
of Science, Utrecht University, Utrecht, The Netherlands
Casper Quist Laboratory of Nematology, Wageningen University, Wageningen,
The Netherlands
Jos M. Raaijmakers Department of Microbial Ecology, Netherlands Institute of
Ecology, Wageningen, The Netherlands
Willem J. Ravensberg International Biocontrol Manufacturers Association
(IBMA), Brussels, Belgium
Koppert Biological Systems, Berkel en Rodenrijs, The Netherlands
Alan E. Richardson CSIRO Plant Industry, Canberra, Australia
Katarzyna Rybarczyk-Mydłowska Museum and Institute of Zoology PAS,
Warsaw, Poland
Choong-Min Ryu Molecular Phytobacteriology Laboratory, KRIBB, Daejeon,
Republic of Korea

Thomas Schäfer Novozymes A/S, Bagsvaerd, Denmark
Charikleia Schoina Laboratory of Phytopathology, Wageningen University,
Wageningen, The Netherlands
Susanne Schreiter Julius Kühn-Institut, Federal Research Centre for Cultivated
Plants (JKI), Braunschweig, Germany
Kornelia Smalla Julius Kühn-Institut, Federal Research Centre for Cultivated
Plants (JKI), Braunschweig, Germany
Geert Smant Laboratory of Nematology, Wageningen University, Wageningen,
The Netherlands
Stijn Spaepen Centre of Microbial and Plant Genetics, KU Leuven, Heverlee,
Belgium
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding
Research, Köln, Germany
Sofie Thijs Centre for Environmental Sciences, Hasselt University, Diepenbeek,
Belgium
Linda Thomashow USDA-ARS, Root Disease and Biological Control Research
Unit, Washington State University, Pullman, WA, USA
Jan Tommassen Section Molecular Microbiology, Department of Biology, Utrecht
University, Utrecht, The Netherlands


Contributors

xix

Eddy van der Meijden Institute of Biology, Leiden University, Leiden, The
Netherlands
Jan van der Wolf Plant Research International, Wageningen, The Netherlands
Hanny van Megen Laboratory of Nematology,
Wageningen, The Netherlands


Wageningen University,

Marc Van Montagu VIB–Institute of Plant Biotechnology Outreach, Department
of Biotechnology and Bioinformatics, Ghent University, Gent-Zwijnaarde, Belgium
Saskia C. M. Van Wees Plant-Microbe Interactions, Department of Biology,
Faculty of Science, Utrecht University, Utrecht, The Netherlands
Jaco Vangronsveld Centre for Environmental Sciences, Hasselt University,
Diepenbeek, Belgium
Muthusubramanian Venkateshwaran School of Agriculture, University of
Wisconsin-Platteville, Platteville, WI, USA
Mariëtte Vervoort Laboratory
Wageningen, The Netherlands

of

Nematology,

Wageningen

University,

Susanne von Bargen Division Phytomedicine, Faculty of Life Sciences, HumboldtUniversität zu Berlin, Berlin, Germany
Han A. B. Wösten Section Molecular Microbiology, Department of Biology,
Utrecht University, Utrecht, The Netherlands
David M. Weller United States Department of Agriculture-Agricultural
Research Service, Root Disease and Biological Control Research Service,
Pullman, Washington, USA
Sheridan L. Woo Department of Agriculture, University of Naples Federico II, and
Institute of Plant Protection IPP–CNR, Portici (NA), Italy

Zefen Yu Yunnan University, Kunming, People’s Republic of China
Keqin Zhang Yunnan University, Kunming, People’s Republic of China


Abbreviations

ABA
ACC
AFM
AHL
AMF
ARISA
BC
BCA
BCPC
BNF
BPSG
Bt
CFU
CIPAC
CK
c-LP
CLSM
CMV
CNN
CRAfT
CSP
DAMP
DAPG
DGGE

DIC
DSF
EBIC
ECM
EPA
EPN
EPPO
ET

abscisic acid
1-aminocyclopropane-1-carboxylate
atomic force microscopy
N-acyl homoserine lactone
arbuscular mycorrhizal fungus
Automated rRNA Intergenic Spacer Analysis
biocontrol
biocontrol agent
British Crop Production Council
Biological nitrogen fixation
BioPesticide Steering Group
Bacillus thuringiensis
colony forming units
Collaborative International Pesticides Analytical Council
cytokinin
cyclic lipopeptide
confocal laser scanning microscopy
Cassava mosaic virus
competition for nutrients and niches
Cre Reporter Assay for Translocation
Common Symbiotic Pathway

damage-associated molecular patterns
2,4-diacetylphloroglucinol
denaturing gradient gel electrophoresis
Differential Interference Contrast
diffusible signal factor
European Biostimulant Industry Council
Ectomycorrhizal fungi
Environmental Protection Agency
Entomopathogenic nematode
European and Mediterranean Plant Protection Organization
Ethylene
xxi


xxii

ETI
ETS
FAME
FAO
FeMoCo
GA
GAP
GAs
GFP
GM
GMO
GOGAT
GS
HR

HR
HSL
IAA
IAM
IBCA
IJ
IncP-1
InsP5
IPM
IPyA
ISO
ISR
ITS fragments
JA
LCO
LPS
LysM
MALDI MSI
MAMP
MGE
MHB
MRL
Myc factor
N2 H 4
N2 O
NB-LRR
NH2 OH
NHEJ

Abbreviations


effector-triggered immunity
effector-triggered susceptibility
Fatty Acid Methyl Esters
Food and Agriculture Organization
Iron-molybdenum cofactor
gibberellin
Good agricultural practice
gibberellins
Green fluorescent protein
genetically modified
genetically modified organism
Glutamine oxoglutarate aminotransferase
Glutamine Synthase
Homologous recombination
hypersensitive response
homoserine lactone
indole-3-acetic acid
indole-3-acetamide
invertebrate biocontrol agent
infective juvenile
incompatibility groups of plasmids
1D-myo-inositol 1,2,4,5,6 pentakisphosphate
Integrated pest management
indole-3-pyruvate
international organization for standardization
induced systemic resistance
internal transcribed spacer ribosomal DNA (used as the universal
barcode for fungi)
Jasmonic Acid

lipochitooligosaccharide
lipopolysacchide
lysine-motif
Matrix-Assisted Laser Desorption/Ionization Mass Spectrometry Imaging
microbe associated molecular pattern
mobile genetic element (DNA fragments, which can be transferred from cell to cell)
mycorrhiza helper bacteria
maximum residue limit
mycorrhization factor
hydrazine
nitrous oxide
nucleotide binding-leucine-rich repeat
hydroxylamine
Non-homologous end-joining


Abbreviations

nif gene
NO
Nod factor
NOx
OECD
OMZ
OTU
PAHs
PAMP
PCA
PCB
PCN

PCR
PCWDE
PGP
PGPB
PGPF
PGPM
PGPR
PhyloChip
Pi
PIP
PIR
PIT
PKS
PMRA
PPA
PPP
PP-transferase
PQQ
PR
PRR
PSM
PTI
PZN
qPCR
QS
rDNA
RLP
RNAi
ROL
ROS

RP

xxiii

nitrogen fixation gene
nitric oxide
nodulation factor
nitrogen oxides
organisation for economic co-operation and development
oxygen minimum zone
operational taxonomic unit (used as species equivalent)
polycyclic aromatic hydrocarbons
pathogen-associated molecular pattern
phenazine-1-carboxylic acid
poly-chlorinated biphenyls
phenazine-1-carboxamide
polymerase chain reaction
plant cell wall degrading enzyme
plant growth-promotion
plant growth-promoting bacteria
plant growth promoting fungi
plant growth promoting microbe
plant growth-promoting rhizobacteria
microarray for the comprehensive identification of microbial
organisms
inorganic phosphate
plant-incorporated protein
protein with internal repeat
pre-infection thread
polyketide synthase

pest management regulatory agency
pre-penetration apparatus
plant protection product
phospho-pantetheinyl-transferase
pyrroloquinoline quinone
pathogenesis related
pattern recognition receptor
phosphate solubilising microorganism
pathogen-triggered immunity
plantazolicin
quantitative real-time PCR (provides copy-number of the target
organism)
quorum-sensing
ribosomal DNA
receptor-like protein
ribonucleic acid interference
radial oxygen loss
reactive oxygen species
rock phosphate


xxiv

SA
SAM
SAR
SIMS
SIP
SL
SRP

SSCP
SWOT
SYM genes
SYM pathway
T1-6SS
T4SS
TAD
TC-DNA
T-RFLP
TTSS
US EPA OCSPP
USDA
VBNC
VOC

Abbreviations

salicylic acid
S-adenosylmethionine
systemic acquired resistance
secondary ion mass spectrometry
stable-isotope probing
strigolactone
signal recognition particle
single strand conformation polymorphism (method to analyze
composition of microbial communities)
strengths, weaknesses, opportunities and threats
common symbiosis genes
symbiosis pathway
type 1-6 secretion system

type 4 secretion system
take-all decline
DNA obtained from the total community present in one sample
terminal restriction fragment length polymorphism (method to
analyze the composition of microbial communities)
type III secretion system
United States Environmental Protection Agency Office of
Chemical Safety and Pollution Prevention
US Department of Agriculture
viable but non-culturable
volatile organic compound


Chapter 1

Introduction to Plant-Microbe Interactions
Ben Lugtenberg

Abstract Pathogenic microbes and pest organisms as well as unfavorable growth
conditions can be a threat for plant growth. Other beneficial microbes and small
organisms can be used to protect plants against these attackers or to assist the plant
to overcome the unfavorable conditions. These plant-beneficial organisms can be
divided into classes which (i) reduce plant diseases, (ii) which regulate plant growth,
(iii) help plants to overcome stresses, and (iv) inactivate soil pollutants which inhibit
plant growth or make (parts of) the plant unsuitable for consumption.
Plant Pathogens and Pest Organisms are a Threat for Plant Growth In this book
we discuss pathogens and pest organisms which are a threat for plant growth. We
highlight the roles which microbes can play in making agriculture and horticulture
more sustainable. Selected microbes are able to (partly) replace most chemicals
which are presently used in agriculture. In addition, microbes can often be used

against diseases for which no chemicals are available. In this book, the following
activities and applications of microbes will be discussed.
Biological Control of Plant Diseases Approximately 25 % of the world’s crop yield
is lost every year, mainly due to diseases caused by fungi, by other pathogens, and by
pests. Plant protection products are on the market to fight these diseases. Presently
these are mainly chemicals. Their use can be threatening the health of people and
polluting the environment. Disease control with beneficial microbes is an alternative
which allows sustainable crop production. The use of microbial plant protection
products is growing and their importance will strongly increase because of political
and public pressure.
Regulation of Plant Growth The world population is growing and the amount of
food needed by 2050 will be the double of what is being produced now, whereas the
area of agricultural land is decreasing. We have to increase crop yield in a sustainable
way, i.e. chemical plant growth regulators have to be replaced by microbiological
B. Lugtenberg ()
Institute of Biology, Sylvius Laboratory, Leiden University,
Sylviusweg 72, 2333 BE Leiden, The Netherlands
Tel.: +31629021472
e-mail:

© Springer International Publishing Switzerland 2015
B. Lugtenberg (ed.), Principles of Plant-Microbe Interactions,
DOI 10.1007/978-3-319-08575-3_1

1


2

B. Lugtenberg


products. Also here, the use of microbial products is growing and their importance
will strongly increase.
Control of Plant Stress by Microbes An increasing area of agricultural land is arid
and/or salinated. Global warming will increase this area. Plant growth is inhibited, or
even made impossible, by drought and salt. It has been proven already that microbes
can be used successfully to alleviate such stresses.
Microbial Cleaning of Polluted Land Chemical pollution of land can make plant
growth difficult or even impossible. But even when crop plants grow on such lands,
their products are often polluted and not suitable for consumption. Selected microbes
have been already been used successfully to detoxify chemical pollutants in soil and
to remove heavy metals, thereby allowing the growth of healthy plants.
The field of Plant-Microbe Interactions has made important progress thanks to
the development of new technologies. Attention to state-of-the-art DNA and visualization techniques is paid in two separate chapters. Moreover, successful examples
of progress are presented under Paradigms of Plant-Microbe Interactions. The book
ends with the presentation of a number of real innovative research projects of which
the future will show whether these are dreams or big steps forwards.


Part I

Introductory Chapters


Chapter 2

The Importance of Microbiology in Sustainable
Agriculture
Thomas Schäfer and Tom Adams


Abstract Deriving from various naturally-occurring microorganisms such as bacteria and fungi, microbial technologies can protect crops from pests and diseases
and enhance plant productivity and fertility. They enable farmers to increase yield
and productivity in a sustainable way and are expected to play a significant role in
agriculture.
As the global population’s rapid growth is set to continue, the need to significantly increase agricultural output without increasing pressure on the environment also grows.
Microbial solutions enable farmers to drive yield and productivity in a sustainable
way. Deriving from various naturally-occurring microorganisms such as bacteria and
fungi, these solutions can protect crops from pests and diseases and enhance plant
productivity and fertility.
Microbial solutions make up approximately two thirds of the agricultural biologicals industry. Representing roughly US$ 2.3 billion in annual sales, agricultural
biologicals have posted double-digit sales growth each of the last several years. There
are numerous biological products currently on the market that contain microorganisms as active ingredients, including seed treatment and foliar applied products.
Microbial technologies can help improve nutrient acquisition, promote growth and
yield, control insects and protect against disease. These emerging agricultural biological technologies complement the integrated systems approach that is necessary
in modern agriculture, bringing together breeding, biotechnology and agronomic
practices to improve and protect crop yields.
There has been significant interest in agricultural biologicals in the past few
years from major crop chemical manufacturers, including Bayer’s acquisition of
Agraquest, BASF’s acquisition of Becker Underwood, and Syngenta’s acquisitions
of Pasteuria and Devgen. Most recently, Novozymes and Monsanto established The
T. Schäfer ()
Novozymes A/S, Brudelysvej 32, 2880 Bagsvaerd, Denmark
Tel.: + 45 44460000
e-mail:
T. Adams
Monsanto Company, 800 N. Lindbergh Blvd., St. Louis, MO 63167, USA
Tel.: + 1 (314) 258-1547
e-mail:
© Springer International Publishing Switzerland 2015
B. Lugtenberg (ed.), Principles of Plant-Microbe Interactions,

DOI 10.1007/978-3-319-08575-3_2

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