Molecular Microbial Ecologyof the Rhizosphere

Molecular Microbial Ecologyof the Rhizosphere

Edited by

Frans J. de Bruijn

Cover Photo: Bioluminescence image of a barley root system colonized by Pseudomonas fluorescens strain DF57-40E7 visualized by a Hamamatsuphotonic camera system. Strain DF57-40E7 emits bioluminescence due to an inserted Tn5::luxAB gene cassette. Image courtesy of Lene Kragelund, Fransde Bruijn and Ole Nybroe.

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Library of Congress Cataloging-in-Publication Data:

Molecular microbial ecology of the rhizosphere / edited by Frans J. de Bruijn.p. ; cm.

Includes bibliographical references and index.ISBN 978-1-118-29617-2 (set : cloth : alk. paper) – ISBN 978-1-118-29629-5 (v. 1 : cloth : alk.

paper) – ISBN 978-1-118-29616-5 (v. 2 : cloth : alk. paper)I. Bruijn, F. J. de (Frans J. de)[DNLM: 1. Soil Microbiology. 2. Genetics, Microbial. 3. Microbial Interactions. 4. Rhizosphere.

QW 60]

579′.1757–dc232012032879

Printed in Singapore

10 9 8 7 6 5 4 3 2 1

This work is dedicated to my two daughters Waverly and Vanessa de Bruijn for theirsupport even from a distance and to Marie Lefevre-Fonollosa for her continual

interest in the Book

Contents

Preface xiii

Acknowledgements xv

Contributors xvii

1. Introduction 1

Frans J. de Bruijn

Section 1 Focus Chapters

2. Using Genomics to Unveil Bacterial Determinants of Rhizosphere Life Style 7

Marıa-Isabel Ramos-Gonzalez, Miguel A. Matilla, Jose-Miguel Quesada, Juan L. Ramos,and Manuel Espinosa-Urgel

3. Benefits of Breeding Crops for Yield Response to Soil Organisms 17

Alison E. Bennett, Timothy J. Daniell, and Philip J. White

4. Microbial Interactions in the Rhizosphere 29

Jose-Miguel Barea, Marıa-Jose Pozo, Rosario Azcon, and Concepcion Azcon-Aguilar

5. Culture-Independent Molecular Approaches to Microbial Ecology in Soiland the Rhizosphere 45

Penny R. Hirsch, Tim H. Mauchline, and Ian M. Clark

6. Exploiting New Systems-Based Strategies to Elucidate Plant–Bacterial Interactionsin the Rhizosphere 57

Matthieu Barret, Hao Tan, Frank Egan, John P. Morrissey, Jerry Reen, and Fergal O’Gara

vii

viii Contents

7. Combining Molecular Microbial Ecology with Ecophysiology and Plant Geneticsfor a Better Understanding of Plant–Microbial Communities’ Interactionsin the Rhizosphere 69

Anouk Zancarini, Clementine Lepinay, Judith Burstin, Gerard Duc, Philippe Lemanceau,Delphine Moreau, Nathalie Munier-Jolain, Barbara Pivato, Thierry Rigaud,Christophe Salon, and Christophe Mougel

8. Microbially Mediated Plant Functional Traits 87

Maren L. Friesen

Section 2 Plant-mediated Structuring of Bacterial Communities in the Rhizosphere

9. Unraveling the Shed of Unexplored Rhizosphere Microbial Diversity 105

Puneet S. Chauhan, Vasvi Chaudhry, Sandhya Mishra, Aradhana Mishra,and Chandra S. Nautiyal

10. Advanced Molecular Tools for Analysis of Bacterial Communities and TheirInteractions in the Rhizosphere 115

Jan Dirk van Elsas and Ines Mandic-Mulec

11. Challenges in Assessing Links Between Root Exudates and the Structureand Function of Soil Microbial Communities 125

Shengjing Shi, Alan E. Richardson, Maureen O’Callaghan, Mary Firestone,and Leo Condron

12. Root Secretions: Interrelating Genes and Molecules to Microbial Associations.Is It All That Simple? 137

Meredith L. Biedrzycki and Harsh P. Bais

13. The Use of Stable Isotope Labeling and Compound-Specific Analysis of MicrobialPhospholipid Fatty Acids to Quantify the Influences of Rhizodeposition on MicrobialCommunity Structure and Function 141

Eric Paterson

14. Metarhizium robertsii, a Rhizosphere-Competent Insect Pathogen 149

Monica Pava-Ripoll

15. Shaping of Microbial Community Structure and Function in the Rhizosphereby Four Diverse Plant Species 161

Wafa Achouak and Feteh ElZahar Haichar

16. Exploration of Hitherto-Uncultured Bacteria from the Rhizosphere 169

Leonard S. van Overbeek

17. The Use of Molecular Methods to Assess Chemotactic-Competent BacterialPopulations in the Rhizosphere 179

Alison Buchan and Gladys M Alexandre

Contents ix

18. Assessment of Rice Root-Associated Bacteria 191

Pablo Rodrigo Hardoim and Jan Dirk van Elsas

19. Phylogenetic Analysis of Azospirillum Species Isolated from the Rhizosphereof Field-Grown Wheat Based on Genetic and Phenotypic Features 203

Vezyri Eleni, Venieraki Anastasia, Dimou Maria, Chatzipavlidis Iordanis,Tampakaki Anastasia, and Panagiotis Katinakis

20. Influence of Intercropping and Intercropping plus Rhizobial Inoculationon Microbial Activity and Community Composition in Rhizosphere of Alfalfa(Medicago sativa L.) and Siberian Wildrye (Elymus sibiricus L.) 211

YanMei Sun, NanNan Zhang, En Tao Wang, HongLi Yuan, JinShui Yang, and WenXin Chen

21. Root Exudates and Soil: Crucial for Molecular Understanding of Interactionsin the Rhizosphere 221

Nicholas C. Uren

22. Do Root Exudates Exert More Influence on Rhizosphere Bacterial CommunityStructure Than Other Rhizodeposits? 229

Penny R. Hirsch, Anthony J. Miller, and Paul G. Dennis

Section 3 Plant Genetics and Rhizobacterial Communities

23. Arabidopsis thaliana as Model for Studies on the Bacterial Root Microbiota 245

Klaus Schlaeppi, Emiel Ver Loren van Themaat, Davide Bulgarelli, and Paul Schulze-Lefert

24. Genetic and Developmental Control of Rhizosphere Bacterial Communities 257

Shirley Micallef and Adan Colon-Carmona

25. Arabidopsis thaliana: A Useful but Limited Model to Investigate Stress Impactson Rhizosphere Community Composition and Function 265

Kristopher Blee, John Hein, and Gordon V. Wolfe

26. Medicago truncatula Root Proteomics 271

Frank Colditz

Section 4 Hormones and other Signals and Rhizomicrobes

27. Control of the Cooperation Between Plant Growth-Promoting Rhizobacteriaand Crops by Rhizosphere Signals 281

Benoıt Drogue, Emeline Combes-Meynet, Yvan Moenne-Loccoz, Florence Wisniewski-Dye,and Claire Prigent-Combaret

28. Small Molecules Involved in Transkingdom Communication between Plantsand Rhizobacteria 295

Randy Ortiz Castro and Jose Lpopez Bucio

x Contents

29. Bacterial Biosynthesis of Indole-3-Acetic Acid: Signal Messenger Service 309

Mandira Kochar, A Vaishnavi, Anamika Upadhyay, and Sheela Srivastava

30. Fixing and Non-Fixing Rhizobia Affect Arabidopsis Root Architecture by Interferingwith the Auxin Signaling Pathway 327

Guilhem Desbrosses, Nelly Queruel, Arthur Poitout, and Bruno Touraine

31. Terpene Production by Bacteria and its Involvement in Plant Growth Promotion,Stress Alleviation, and Yield Increase 335

Patricia Piccoli and Ruben Bottini

32. Rapid Identification of Plant-Growth-Promoting Rhizobacteria Using an Agar PlateCocultivation System with Arabidopsis 345

Randy Ortiz Castro, Jesus Campos Garcıa, and Jose Lopez Bucio

33. Strigolactone Biosynthesis and Biology 355

Yanxia Zhang, Imran Haider, Carolien Ruyter-Spira, and Harro J. Bouwmeester

34. Chemistry of Strigolactones: Why and How do Plants Produce so ManyStrigolactones? 373

Koichi Yoneyama, Takaya Kisugi, Xiaonan Xie, and Kaori Yoneyama

35. Strigolactones: Crucial Cues in the Rhizosphere 381

Juan A. Lopez-Raez

Section 5 Endophytes

36. Bacterial Endophytes: Who and Where, and What Are They Doing There? 393

Natalia Malfanova, Ben J.J. Lugtenberg, and Gabriele Berg

37. Properties of Bacterial Endophytes Leading to Maximized Host Fitness 405

Pablo R. Hardoim and Jan Dirk van Elsas

38. DNA-Based Stable Isotope Probing for Identifying Active Bacterial Endophytesin Potato 413

Frank Rasche, Michael Schloter, Tillmann Luders, and Angela Sessitsch

39. Visualization of Niches of Colonization of Firmicutes with Bacillus spp. in the Rhizo-sphere, Rhizoplane, and Endorhiza of Grapevine Plants at Flowering Stage of Develop-ment by FISH Microscopy 423

Stephane Compant, Helmut Gangl, and Angela Sessitsch

40. The Poplar Endophyte Pseudomonas putida W619 as a Key to a SuccessfulPhytoremediation of Volatile Organic Contaminants 429

Nele Weyens, Daniel van der Lelie, Safiyh Taghavi, and Jaco Vangronsveld

Contents xi

41. NifH Gene Expression and Nitrogen Fixation by Diazotrophic Endophytesin Sugarcane and Sweet Potatoes 437

Junko Terakado-Tonooka, Shotaro Ando, Yoshinari Ohwaki,and Tadakatsu Yoneyama

42. Surveying Diverse Zea Seed for Populations of Bacterial Endophytes 445

David Johnston-Monje and Manish N. Raizada

Section 6 Symbiotic Plant–Microbe Interactions

43. Molecular Mechanisms Governing Arbuscular Mycorrhiza Developmentand Function 459

Kristina Haage and Martin Parniske

44. Diversity and Evolution of Nitrogen-Fixing Legume Symbionts 467

Delphine Capela, Suhua Guan, and Catherine Masson-Boivin

45. Lipochitooligosaccharide Perception and the Basis of Partner Recognitionin Root Endosymbioses 483

Julie Cullimore and Clare Gough

46. Rhizobial Genetic Repertoire to Inhabit Legume and NonlegumeRhizospheres 495

Martha G. Lopez-Guerrero, Miguel A. Ramırez,and Esperanza Martınez-Romero

47. Who is Controlling Whom within the Ectomycorrhizal Symbiosis: Insightsfrom Genomic and Functional Analyses 501

Claire Veneault-Fourrey, Jonathan M. Plett, and Francis Martin

48. Role of Carotenoid Metabolism in the Arbuscular Mycorrhizal Symbiosis 513

Michael H. Walter

49. Bacterial Colonization of the Arbuscular Mycorrhizal Fungal Hyphosphere 525

Tanja R. Scheublin

50. Role of Quorum Sensing in the Sinorhizobium meliloti–Alfalfa Symbiosis 535

Luciana V. Rinaudi-Marron and Juan E. Gonzalez

51. Roles of Flavonoids in Symbiotic Root–Rhizosphere Interactions 541

Samira Hassan and Ulrike Mathesius

52. Exopolysaccharides and Nodule Invasion in the Sinorhizobium meliloti–AlfalfaSymbiosis 551

Luciana V. Rinaudi-Marron and Juan E. Gonzalez

Contents

Preface xv

Acknowledgements xvii

Contributors xix

Section 7 PGPR, Biocontrol, and Disease-Suppressive Bacteria

53. Plant Growth Promotion by Microbes 561

Ben J.J. Lugtenberg, Natalia Malfanova, Faina Kamilova, and Gabriele Berg

54. Microbial Control of Plant Root Diseases 575

Ben J.J. Lugtenberg, Natalia Malfanova, Faina Kamilova, and Gabriele Berg

55. Biocontrol and Osmoprotection for Plants under Salinated Conditions 587

Gabriele Berg, Mohammadali Alavi, Christoph S. Schmidt, Christin Zachow, DilfuzaEgamberdieva, Faina Kamilova, and Ben J.J. Lugtenberg

56. Genetics and Evolution of 2,4-Diacetylphloroglucinol Synthesis inPseudomonas fluorescens 593

Danielle M. Troppens, Jennifer A. Moynihan, Mathieu Barret, Fergal O’Gara,and John Morrissey

57. Suppression of Crown Gall Disease by Rhizosphere Bacteriaand Agrobacterium-Specific Bacteriophages 607

Leonid Chernin, Natela Toklikishvili, Natalia Dandurishvili, Marina Tediashvili,and Alexander Vainstein

58. Molecular-Based Strategies to Exploit the Inorganic Phosphate-SolubilizationAbility of Pseudomonas in Sustainable Agriculture 615

Patrick Browne, Matthieu Barret, John P. Morrissey, and Fergal O’Gara

vii

viii Contents

59. The Biocontrol Bacterium Pseudomonas Fluorescens Pf29Arp Strain Affects thePathogenesis-Related Gene Expression of the Take-All Fungus GaeumannomycesGraminis Var. Tritici on Wheat Roots 629

Stephanie Daval, Lionel Lebreton, and Alain Sarniguet

60. Marker-Assisted Selection of Novel Bacteria Contributing to Soil-Borne PlantDisease Suppression 637

Jun-Kyung Park, Seung-Hwan Lee, Songhee Han, Jin-Cheol Kim, Young Cheol Kim,and Brian McSpadden Gardener

61. Combined Effects of Wheat Roots and Pathogenic Fungus Gaeumannomyces graminisvar. tritici on Gene Expression of the Biocontrol Bacterium Pseudomonas fluorescensPf29Arp 643

Matthieu Barret, Pascale Frey-Klett, Anne-Yvonne Guillerm-Erckelboudt, Morgane Boutin,Gregory Guernec, Muriel Marchi, Stephanie Daval, and Alain Sarniguet

62. Biocontrol of Tree Root Diseases 655

Clara Pliego and Francisco M. Cazorla

63. Plant Growth Modulation by Bacterial Volatiles—A Focus on Burkholderia Species 665

L Weisskopf and A Bailly

64. Plant Growth Promoting Microorganisms: The Road from an AcademicallyPromising Result to a Commercial Product 677

Faina Kamilova and Roland de Bruyne

65. The Effect of Agricultural Practices on Resident Soil Microbial Communities:Focus on Biocontrol and Biofertilization 687

Natalia Bajsa, Marıa A. Morel, Victoria Brana, and Susana Castro-Sowinski

Section 8 Biofilm Formation and Attachment to Roots

66. Biofilm Formation in the Rhizosphere: Multispecies Interactions and Implicationsfor Plant Growth 703

Annette A. Angus and Ann M. Hirsch

67. Probiotics for Plants: Rhizospheric Microbiome and Plant Fitness 713

Carla Spence and Harsh Bais

68. Motility, Biofilm Formation, and Rhizosphere Colonization byPseudomonas fluorescens F113 723

Rafael Rivilla, Francisco Martınez-Granero, and Marta Martın

69. CMEIAS: An Improved Computing Technology for Quantitative Image Analysisof Root Colonization by Rhizobacteria In Situ At Single-Cell Resolution 733

Frank B. Dazzo and Youssef G. Yanni

Contents ix

Section 9 Quorum Sensing and Signaling

70. Understanding Root–Microbiome Interactions 745

Gaston Zolla, Matthew G Bakker, Dayakar V Badri, Jacqueline M Chaparro,Amy M Sheflin, Daniel K Manter, and Jorge Vivanco

71. An Inter-Kingdom Signaling Mechanism in Rhizosphere Pseudomonas 755

Juan F. Gonzalez, Sujatha Subramoni, and Vittorio Venturi

72. N-Acyl-homoserine-Lactone Quorum-Sensing Signaling in Phenazine and CyclicLipopeptide-Producing Pseudomonas sp. CMR12a from the RedCocoyam Rhizosphere 763

Katrien De Maeyer, Jolien D’aes, Gia K.H. Hua, Nam Phuong Kieu,and Monica Hofte

73. The Response of Plants toward N-Acyl Homoserine Lactonesof Quorum-Sensing-Active Bacteria in the Rhizosphere 775

Anton Hartmann, Sebastian T. Schenk, Tina Riedel, Peter Schroder,and Adam Schikora

74. In Situ Calling Distances and High Population IndependentN-Acylhomoserine Lactone-Mediated Communication on Plant Root Surfaces 785

Frank B. Dazzo and Stephan Gantner

75. Quorum-Sensing Quenching by Volatile Organic CompoundsEmitted by Rhizosphere Bacteria 791

Leonid Chernin, Natela Toklikishvili, Marianna Ovadis,and Inessa Khmel

76. The Biological Significance of the Degradation of N-Acyl HomoserineLactones—Quorum Sensing and Quorum Quenching in Burkholderiaand Agrobacterium 801

Kok G. Chan, Denis Faure, and Yves Dessaux

77. Altering Plant–Microbe Interactions Through Artificially ManipulatingBacterial Quorum Sensing 813

Katalin Kovacs and Rupert Fray

78. Rhizosphere Microbial Communication in Soil Nutrient Acquisition 823

Kristen M. DeAngelis

79. Agony to Harmony—What Decides? Calcium Signaling in Beneficialand Pathogenic Plant–Fungus Interactions—What We Can Learn from theArabidopsis/Piriformospora indica Symbiosis 833

Joy Michal Johnson and Ralf Oelmuller

x Contents

Section 10 Genomic Sequencing and Screening of Genes/Promoters Activatedin the Natural Environment

80. Genome Transcriptome Analysis and Functional Characterizationof a Nitrogen-Fixation Island in Root-Associated Pseudomonas stutzeri 853

Yongliang Yan, Wei Lu, Ming Chen, Jin Wang, Wei Zhang, Yunhua Zhang, Shuzhen Ping,Claudine Elmerich, and Min Lin

81. Genome Analysis, Ecology, and Plant Growth Promotion of the EndophyteBurkholderia phytofirmans Strain PsJN 865

Birgit Mitter, Alexandra Petric, Patrick SG Chain, Friederike Trognitz, Jerzy Nowak,Stephane Compant and Angela Sessitsch

82. Identification and Mutational Activation of Niche-Specific Genes Provide Insightinto Regulatory Networks and Bacterial Function in Complex Environments 875

Robert W. Jackson, Xue-Xian Zhang, and Mark W. Silby

83. Comparative Analysis of the Complete Genome Sequence of the PlantGrowth-Promoting Bacterium Bacillus amyloliquefaciens FZB42 883

Rainer Borriss

84. Genome Sequence of the Plant Growth-Promoting Endophytic BacteriumEnterobacter sp. 638 899

Safiyh Taghavi and Daniel van der Lelie

Section 11 Marker and Reporter Genes For Plant-Host Interaction Studies

85. Approaches for the Design of Genetically Engineered Bacteria for Ecological Studiesand Biotechnological Applications 911

Humberto J.O. Ramos, Marshall Geoffrey Yates, Fabio O. Pedrosa, and Emanuel M. Souza

86. Construction of Signature-Tagged Mutant Libraries and Its Applicationto Plant-Symbiotic Bacteria 921

Anke Becker and Nataliya Pobigaylo

87. Use of DOPE-FISH Tool to Better Visualize Colonization of Plants by BeneficialBacteria? An Example with Saccharothrix algeriensis NRRL B-24137 ColonizingGrapevine Plants 929

Stephane Compant and Florence Mathieu

88. Combining Rhizobox, Reporter Gene Systems, and Molecular Analysesto Assess the Effects of Humic Substances on Plant–Microbes Interactionsin Soil Rhizosphere 933

Edoardo Puglisi and Marco Trevisan

Contents xi

89. Multiparameter Flow Cytometry for Characterization of Physiological Statesin Pseudomonas Fluorescens DR54 Biocontrol Inoculants UnderDry Formulation and Long-Term Storage in Clay Carrier 943

Jan Sørensen and Ole Sjøholm

90. Endophytic Lifestyle of Biocontrol Strains of Pseudomonas spp. in Olive Roots 951

Jesus Mercado-Blanco and Pilar Prieto

Section 12 Phytoremediation and heavy-metal tolerance in the Rhizosphere

91. Improving Phytoremediation through Plant-Associated Bacteria 963

Kieran J. Germaine, Martina McGuinness, and David N. Dowling

92. Ecology of Alkane-Degrading Bacteria and Their Interaction with the Plant 975

Muhammad Afzal, Sohail Yousaf, Thomas G. Reichenauer, and Angela Sessitsch

93. Abiotic Stress Remediation by the Arbuscular Mycorrhizal Symbiosisand Rhizosphere Bacteria/Yeast Interactions 991

Rosario Azcon, Almudena Medina, Ricardo Aroca, and Juan M. Ruiz-Lozano

94. Potential Plant-Growth-Promoting and Nitrogen-Fixing Bacteria Associatedwith Pioneer Plants Growing on Mine Tailings 1003

Yendi E. Navarro-Noya, Esperanza Martınez-Romero, and Cesar Hernandez-Rodrıguez

95. Stimulation of Rhizosphere Microbial Communities During Chemophytostabilizationof a Pb–Zn Mine Soil 1013

Marıa A. Galende, Lur Epelde, M T. Gomez-Sagasti, Oihana Barrutia, Antonio Hernandez,Jose M. Becerril, George A. Kowalchuk, and Carlos Garbisu

96. Arbuscular Mycorrhiza in Glucosinolate-Containing Plants: The Story of the MetalHyperaccumulator Noccaea (Thlaspi) praecox (Brassicaceae) 1023

Paula Pongrac, Katarina Vogel-Mikus, Charlotte Poschenrieder, Juan Barcelo,Roser Tolra, and Marjana Regvar

97. Novel Metal-Resistance Genes from the Rhizosphere of Extreme Environments:A Functional Metagenomics Approach 1033

Salvador Mirete and Jose E. Gonzalez-Pastor

Section 13 Climate Change Effects on Soil/Rhizosphere Microbial Communities

98. Soil Warming Effects on Beneficial Plant–Microbe Interactions 1047

Stephane Compant, Marcel van der Heijden, and Angela Sessitsch

xii Contents

99. Soil Respiration, Climate Change, and the Role of Microbial Communities 1055

O. Roger Anderson

100. Rhizosphere Responses to Elevated CO2 1063

Barbara Drigo and George A. Kowalchuk

101. Applying Stable Isotope Probing of Phospholipid Fatty Acids and Ribosomal RNAin Rice Fields to Study the Composition of the Active MethanotrophicBacterial Community In Situ 1075

Ralf Conrad and Yahai Lu

Section 14 Metagenomics and the Soil/Rhizosphere

102. Impact of Mangrove Roots on Bacterial Composition 1083

Newton C.M. Gomes and Daniel F.R. Cleary

103. Prediction of an Ectomycorrhizal Metabolome from Transcriptomic Data 1089

Peter E. Larsen, Leland J. Cseke, and Frank R. Collart

104. Metagenomic Analysis of the Rhizosphere Soil Microbial Community 1099

Yusuke Unno and Takuro Shinano

105. Bacterial Diversity in Rhizosphere Soil from Antarctic Vascular Plantsof Admiralty Bay in Maritime Antarctica 1105

Lia C. R. S. Teixeira, Raquel S. Peixoto, and Alexandre S. Rosado

106. Arbuscular Mycorrhizal Fungi throughout the Year: Using MassivelyParallel Pyrosequencing to Quantify Spatiotemporal Seasonal Dynamics 1113

Alex J. Dumbrell

107. Transcriptomics and Metatranscriptomic Analysis of the Response of RhizosphereBacteria to Environmental Change 1123

Thomas Turner and Philip Poole

108. Unraveling the Rhizosphere Using the cpn60 Genomic Marker and Pyrosequencing 1129

George Lazarovits, Amy L. Turnbull, Brenda Haug, Matthew G. Links, Janet E. Hill,and Sean M. Hemmingsen

109. Rhizosphere Metatranscriptomics: Challenges and Opportunities 1137

Lilia C. Carvalhais, Paul G. Dennis, Gene W. Tyson, and Peer M. Schenk

Section 15 Engineering the Rhizosphere: The “Biased Rhizosphere” Concept

110. The “Biased Rhizosphere” Concept and Advances in the OmicsEra to Study Bacterial Competitiveness and Persistence in the Phytosphere 1147

Michael A. Savka, Yves Dessaux, Brian B. McSpadden Gardener, Samuel Mondy,Petra R.A. Kohler, Frans J. de Bruijn, and Silvia Rossbach

Contents xiii

111. Bacterial Inositol Catabolism—A Sweet Ride into the Host 1163

Petra R. A. Kohler and Silvia Rossbach

112. Exogenous Glucosinolate Produced by Transgenic Arabidopsis thalianahas an Impact on Microbes in the Rhizosphere and Plant Roots 1173

Melanie Bressan, Wafa Achouak, and Odile Berge

113. Reciprocal Interactions between Plants and Fluorescent Pseudomonadsin Relation to Iron in the Rhizosphere 1181

Philippe Lemanceau, Sylvie Mazurier, Laure Avoscan, Agnes Robin,and Jean-Francois Briat

114. Enhancement of Plant–Microbe Interactions using RhizosphereMetabolomics-Driven Approach and its Application in the Removalof Polychlorinated Biphenyls 1191

Yong J. Lee, Kothandaraman Narasimhan, and Sanjay Swarup

Section 16 Concluding Chapters

115. Rhizophagy—A New Dimension of Plant–Microbe Interactions 1201

Chanyarat Paungfoo-Lonhienne, Susanne Schmidt, Richard I. Webb,and Thierry G. A. Lonhienne

116. The Rhizosphere as a Reservoir for Opportunistic Human Pathogenic Bacteria 1209

Gabriele Berg, Mohammadali Alavi, Michael Schmid, and Anton Hartmann

117. Mechanisms of Plant Colonization by Human Pathogenic Bacteria: An Emphasison the Roots and Rhizosphere 1217

Nicola J. Holden, Leighton Pritchard, Kathryn Wright, and Ian K. Toth

118. Perspectives for Rhizosphere Research 1227

Jos M. Raaijmakers and Ben J.J. Lugtenberg

Index 1233

Preface

Having worked on symbiotic plant-microbe interactionsand molecular microbial ecology for nearly 30 years,I have become very cognizant and appreciative of the“Black Box” of the plant Rhizosphere, the below groundzone of soil immediately adjacent to plant roots (“rhiza”)and influenced by these roots (“sphere”). The Rhizospheresupports high levels of microbial activity, as comparedto the bulk soil, although microbial diversity in theRhizosphere may be reduced. The plant roots secrete amagnitude of compounds into the Rhizosphere, includingsugars (up to 20% of the available photosynthate),amino acids, organic acids, fatty acids, sterols, vitamins,enzymes, flavonones, nucleotides, and other inorganicmolecules. These root exudates differ from plant to plant,ecotype to ecotype, and depend on the growth stageof the plant, but the exudates benefit the growth andaction of the Rhizosphere microbial communities. Infact, one may speculate that plants structure microbialcommunities through the root exudates, selecting forbeneficial microbes and warding off pathogens.

In addition, in the Rhizosphere, multiple signalsgo back and forth between plants and microorganisms,which are responsible for recognition of microorganisms;plant growth and development, (Plant Growth PromotingBacteria; PGPR); plant protection from pathogenic attack(Biocontrol); nodulation and symbiotic nitrogen fixation(primarily in legumes); mycorrhization (increased P andN uptake); and resistance to stresses, such as drought,salinity, extreme temperatures, and nutrient deficiencies.Pathogens and stresses cause an average yield loss of50% for most crops worldwide. Yield losses due to stressmay increase with global warming and the expansion ofagriculture into marginal lands. While pest control is stillmostly managed by pesticide application and nutrientdeficiencies by applying nitrogen and phosphorus, thelatter are not only expensive, but lead to runoff, resultingin environmental problems, such as euthrophication ofrivers and lakes and pollution of the drinking water.Since the world’s population is still growing, the pro-duction of food should be increased, without further

damaging the environment and with a decreased inputof chemical hormones and fertilizers. These realizationshave led to an increased interest in the use of beneficialmicrobes as sustainable and inexpensive alternatives foragrochemicals, especially for the production of cerealssuch as wheat, maize, and rice, accounting for onehalf of the human calorie intake. In addition to foodproblems, anthropogenic activities such as mining, oilcollection and refining, as well as the production ofother hazardous chemicals have led to large areas ofheavy metals and organics-polluted sites, which can onlybe decontaminated at high costs, if at all. Against thisbackdrop, the interest in microbial biofertilizers andthe combination of certain plants together with specificmicrobes for phytoremediation purposes is steadilyincreasing. Strategies are being developed to use benefi-cial microbes and these constitute a substantial portionof this two-volume book on the Molecular MicrobialEcology of the Rhizosphere. However, the design ofthese strategies must be based on solid knowledge aboutthe soil, the Rhizosphere, and the plant and its associatedmicroorganisms. This knowledge gathering is the mainpurpose of this book. The development of moleculartechniques, especially high throughput DNA and RNAsequencing to investigate microbes, the microbiome, plantroots, plant-microbe interactions and the Rhizospherehave allowed an increased knowledge base, which cannow be used to design better strategies for the use ofspecific microorganisms and plants for applied purposes,some of which are described in the book. This bookis aimed at soil microbiologists, molecular microbialecologists, plant biologists, and scientists studying plant-microbe interactions, as well as students in these fields.The combination of basic and applied studies is a specialfeature of the book, as is the mixture of reviews andoriginal research papers. I hope that it will be as enlight-ening for you as it has been for me putting these volumestogether.

Frans J. de Bruijn

xiii

Acknowledgements

I greatfully acknowledge Ben Lugtenberg for his mutlti-ple inputs into the Book and Hans Lambers for providingthe Program of the Rhizosphere 3 Conference in advanceof the Meeting. I would like to thank Claude Bruandand Marcel Soon for their help with the computer work.

The Laboratory for Plant Microbe Interactions (LIPM),the Institut National de Recherche Agronomique (INRA);the Centre National de Recherche Scientifique (CNRS)and the Labex TULIP are acknowledged for their supportof the Project.

xv

Contributors

Editor

Frans J. de Bruijn, INRA-CNRS Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441-2594BP52627, F-31320 Castanet-Tolosan, France

Authors

Wafa Achouak, Laboratoire d’Ecologie Microbienne de la Rhizosphere et Environnements extremes, CEA, DSV,IBEB, 13108 Saint-Paul-lez-Durance, France; CNRS, UMR 7265, 13108 Saint-Paul-lez-Durance, France; Univer-site Aix-Marseille, 13108 Saint-Paul-lez-Durance, France; CNRS, UMR 6191, 13115 Saint-Paul-lez-Durance, France;Universite Aix-Marseille, 13115 Saint-Paul-lez-Durance, France

Gladys M. Alexandre, Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville,TN, USA

Tampakaki Anastasia, Department of Agricultural Biotechnology, Laboratory of General and Agricultural Microbiology,Agricultural University of Athens, Iera Odos 75, Votanikos 11855, Athens, Greece

Venieraki Anastasia, Department of Agricultural Biotechnology, Laboratory of General and Agricultural Microbiology,Agricultural University of Athens, Iera Odos 75, Votanikos 11855, Athens, Greece

Shotaro Ando, Japan International Research Center for Agricultural Sciences, Tropical Agriculture Research Front,Maezato-Kawarabaru 1091-1, Ishigaki, Okinawa 907-0002, Japan

Rosario Azcon, Departamento de Microbiologıa del Suelo y Sistemas Simbioticos, Estacion Experimental del Zaidın,CSIC, Profesor Albareda 1, 18008 Granada, Spain

Concepcion Azcon-Aguilar, Departamento de Microbiologıa del Suelo y Sistemas Simbioticos, Estacion Experimentaldel Zaidın, CSIC, Profesor Albareda 1, 18008 Granada, Spain

Harsh P. Bais, Plant and Soil Sciences Department, 531 South College Avenue, Newark, DE 19716, USA; DelawareBiotechnology Institute, 15 Innovation Way, Newark, DE 19711.

Jose-Miguel Barea, Departamento de Microbiologıa del Suelo y Sistemas Simbioticos, Estacion Experimental del Zaidın,CSIC, Profesor Albareda 1, 18008 Granada, Spain

Matthieu Barret, Department of Microbiology, BIOMERIT Research Centre, University College Cork, Cork, Ireland

Alison E. Bennett, Ecological Sciences Group, The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK

Gabriele Berg, Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria

Meredith L. Biedrzycki, Department of Plant and Soil Sciences, 531 South College Avenue, Newark, DE 19716, USA;Delaware Biotechnology Institute, 15 Innovation Way, Newark, DE 19711, USA

Kristopher Blee, Department of Biological Sciences, California State University, Chico, Chico, CA 95929-0515, USA

xvii

xviii Contributors

Ruben Bottini, Laboratorio de Bioquımica Vegetal, Instituto de Biologıa Agrıcola de Mendoza, Facultad de CienciasAgrarias, Universidad Nacional de Cuyo-Consejo Nacional de Investigaciones Cientıficas y Tecnicas, Almirante Brown500, M5528AHB Chacras de Coria, Argentina

Harro J. Bouwmeester, Laboratory of Plant Physiology, Wageningen University, Droevendaalsesteeg 1, 6708 PBWageningen, The Netherlands; Centre for Biosystems Genomics, Wageningen, The Netherlands

Alison Buchan, Department of Microbiology, University of Tennessee, Knoxville, TN, USA

Davide Bulgarelli, Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne,Germany

Judith Burstin, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17, rue Sully, B.P. 86510,21065 Dijon Cedex, France

Jesus Campos Garcıa, Instituto de Investigaciones Quımico-Biologicas, Universidad Michoacana de San Nicolas deHidalgo, Edificio B3, Ciudad Universitaria, C. P. 58030 Morelia, Michoacan, Mexico

Vasvi Chaudhry, Division of Plant Microbe Interactions, CSIR-National Botanical Research Institute, Rana Pratap Marg,Lucknow 226001, India

Puneet S. Chauhan, Division of Plant Microbe Interactions, CSIR-National Botanical Research Institute, Rana PratapMarg, Lucknow 226001, India

WenXin Chen, State Key Laboratory for Agrobiotechnology, College of Biological Sciences and Center for BiomassEngineering, China Agricultural University, Beijing 100193, China

Ian M. Clark, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK

Frank Colditz, Department of Plant Molecular Biology III, Institute for Plant Genetics, Leibniz University of Hannover,Herrenhauser Straße 2, 30419 Hannover, Germany

Adan Colon-Carmona, Department of Biology, University of Massachusetts Boston, Boston, MA, USA

Emeline Combes-Meynet, Universite de Lyon, F-69622 Lyon, France; Universite Lyon 1, Villeurbanne, France; CNRS,UMR5557, Ecologie Microbienne, Villeurbanne, France

Stephane Compant, Dept Bioprocedes et Systemes Microbiens, ENSAT-INP de Toulouse, Universite de Toulouse, LGCUMR 5503 (CNRS/INPT/UPS), 1 Avenue de l’Agrobiopole, B.P. 32607, F-31326 Castanet-Tolosan Cedex 1, France

Leo Condron, Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 84, Lincoln 7647, Christchurch,New Zealand; Bio-Protection Research Centre, Lincoln University, PO Box 84, Lincoln 7647, Christchurch, NewZealand

Julie Cullimore, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326 Castanet-Tolosan, France

Timothy J. Daniell, Ecological Sciences Group, The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK

Paul G. Dennis, Australian Centre for Ecogenomics, The University of Queensland, Brisbane, Queensland 4072, Aus-tralia; Advanced Water Management Centre, The University of Queensland, Brisbane, Queensland 4072, Australia

Guilhem Desbrosses, Laboratoire des Symbioses Tropicales et Mediterraneennes (UM2/IRD/Cirad/SupAgro/INRA), Uni-versite Montpellier 2, CC 002, Place Eugene Bataillon, 34095 Montpellier Cedex 05, France

Jan Dirk van Elsas, Department of Microbial Ecology, Centre for Ecological and Evolutionary Studies, University ofGroningen, Linneausborg, Nijenborgh 7, 9747 AG Groningen, The Netherlands

Benoıt Drogue, Universite de Lyon, F-69622 Lyon, France; Universite Lyon 1, Villeurbanne, France; CNRS, UMR5557,Ecologie Microbienne, Villeurbanne, France

Gerard Duc, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17 rue Sully, B.V.86510,21065 Dijon Cedex, France

Feteh Elzachar Haichar, Laboratoire d’Ecologie Microbienne de la Rhizosphere et Environnements Extremes, CEA,DSV, IBEB, 13108 Saint-Paul-lez-Durance, France; CNRS, UMR 7265, 13108 Saint-Paul-lez-Durance, France; Uni-versite Aix-Marseille, 13108 Saint-Paul-lez-Durance, France

Frank Egan, Department of Microbiology, BIOMERIT Research Centre, University College Cork, Cork, Ireland

Vezyri Eleni, Department of Agricultural Biotechnology, Laboratory of General and Agricultural Microbiology, Agri-cultural University of Athens, Iera Odos 75, Votanikos 11855, Athens, Greece

Contributors xix

Manuel Espinosa-Urgel, Department of Environmental Protection, Estacion Experimental del Zaidın, Consejo Superiorde Investigaciones Cientıficas (CSIC), Profesor Albareda 1, 18008 Granada, Spain

Mary Firestone, Department of Environmental Science, Policy and Management, University of California, Berkeley,CA, USA

Maren L. Friesen, Section of Molecular and Computational Biology, Department of Biology, University of SouthernCalifornia, Los Angeles, CA 90089, USA; Department of Plant Bilogy, Michigan State University, USA

Helmut Gangl, Bundesamt fur Weinbau, Golbeszeile 1, A-7000 Eisenstadt, Austria

Juan E. Gonzalez, Department of Molecular and Cell Biology, RL11, 800 W. Campbell Rd., University of Texas atDallas, Richardson, TX 75080, USA

Clare Gough, CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326 Castanet-Tolosan, France

Suhua Guan, INRA/CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441-UMR2594,F-31326 Castanet-Tolosan, France

Kristina Haage, Institute of Genetics, Biocenter University of Munich (LMU), Großhaderner Str. 2-4, Martinsried 82152,Germany

Imran Haider, Laboratory of Plant Physiology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen,The Netherlands

Samira Hassan, Division of Plant Science, Research School of Biology, Australian National University, Linnaeus Way,Canberra ACT 0200, Australia

John Hein, Whitman College, Walla Walla, WA 99362, USA; Department of Biological Sciences, California StateUniversity, Chico, Chico, CA 95929-0515, USA

Penny R. Hirsch, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK

Chatzipavlidis Iordanis, Department of Agricultural Biotechnology, Laboratory of General and Agricultural Microbiol-ogy, Agricultural University of Athens, Iera Odos 75, Votanikos 11855, Athens, Greece

David Johnston-Monje, Department of Plant Agriculture, University of Guelph, Guelph, Ontario, N1G 2W1 Canada

Faina Kamilova, Koppert Biological Systems, Veilingweg 14, PO Box 155, 2650 AD Berkel en Rodenrijs, The Nether-lands

Panagiotis Katinakis, Department of Agricultural Biotechnology, Laboratory of General and Agricultural Microbiology,Agricultural University of Athens, Iera Odos 75, Votanikos 11855, Athens, Greece

Takaya Kisugi, Weed Science Center, Utsunomiya University, 350 Mine-machi, Utsunomiya 321-8505, Japan

Mandira Kochar, Centre for Mycorrhizal Research, The Energy and Resources Institute [TERI], India Habitat Centre,Lodhi Road, New Delhi 110003, India

Daniel van der Lelie, Center for Agriculture and Environmental Biotechnology, Research Triangle Institute (RTI) Inter-national, 3040 Cornwallis Road, PO Box 12194, Research Triangle Park, NC 27709-2194, USA

Philippe Lemanceau, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17 Rue Sully,B.V.86510, 21065 Dijon Cedex, France

Clementine Lepinay, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17 Rue Sully,B.V.86510, 21065 Dijon Cedex, France

Jose Lopez Bucio, Instituto de Investigaciones Quımico-Biologicas, Universidad Michoacana de San Nicolas de Hidalgo,Edificio B3, Ciudad Universitaria, C. P. 58030 Morelia, Michoacan, Mexico

Martha G. Lopez-Guerrero, Centro de Ciencias Genomicas, UNAM, Av. Universidad SN, Chamilpa, Cuernavaca,Morelos, Mexico

Juan A. Lopez-Raez, Department of Soil Microbiology and Symbiotic Systems, Estacion Experimental del Zaidın(CSIC), Profesor Albareda 1, 18008 Granada, Spain

Tillmann Luders, Helmholtz Center Munich, Institute of Groundwater Ecology, 85764 Neuherberg, Germany

Ben J.J. Lugtenberg, Institute of Biology, Sylvius Laboratory, Leiden University, Sylviusweg 72, PO Box 9505, 2300RA Leiden, The Netherlands

xx Contributors

Natalia Malfanova, Institute of Biology, Sylvius Laboratory, Leiden University, Sylviusweg 72, PO Box 9505, 2300 RALeiden, The Netherlands; All-Russian Research Institute for Agricultural Microbiology (ARRIAM), Saint-Petersburg-Pushkin, Russia; Koppert Biological Systems, Veilingweg 14, PO Box 155, 2650 AD Berkel en Rodenrijs, TheNetherlands

Ines Mandic-Mulec, Department of Food Science and Technology, Biotechnical Faculty, University of Ljubljana, Vecnapot 111, 1000 Ljubljana, Slovenia

Dimou Maria, Department of Agricultural Biotechnology, Laboratory of General and Agricultural Microbiology, Agri-cultural University of Athens, Iera Odos 75, Votanikos 11855, Athens, Greece

Francis Martin, Interactions Arbres-Microorganismes, UMR 1136, INRA-Universite de Lorraine, INRA Nancy 54280,Champenoux, France; Faculte des Sciences et Techniques, BP 239 54 506 Vandoeuvre, les Nancy Cedex, France

Esperanza Martınez-Romero, Centro de Ciencias Genomicas, Universidad Nacional Autonoma de Mexico, Av. Uni-versidad SN, Chamilpa, Cuernavaca, Morelos, Mexico

Catherine Masson-Boivin, INRA/CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441-UMR2594, F-31326 Castanet-Tolosan, France

Ulrike Mathesius, Division of Plant Science, Research School of Biology, Australian National University, LinnaeusWay, Canberra, ACT 0200, Australia

Miguel A. Matilla, Department of Environmental Protection, Estacion Experimental del Zaidın, Consejo Superior deInvestigaciones Cientıficas (CSIC), Profesor Albareda 1, 18008 Granada, Spain; Department of Biochemistry, Univer-sity of Cambridge, Tennis Court Road, Cambridge CB2 1QW, UK

Tim H. Mauchline, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK

Shirley Micallef, Department of Plant Science and Landscape Architecture, Center for Food Safety and Security Systems,University of Maryland, College Park, MD, USA

Anthony J. Miller, John Innes Centre, Norwich, Norfolk NR4 7UH, UK

Aradhana Mishra, Division of Plant Microbe Interactions, CSIR-National Botanical Research Institute, Rana PratapMarg, Lucknow 226001, India

Sandhya Mishra, Division of Plant Microbe Interactions, CSIR-National Botanical Research Institute, Rana Pratap Marg,Lucknow 226001, India

Yvan Moenne-Loccoz, Universite de Lyon, F-69622 Lyon, France; Universite Lyon 1, Villeurbanne, France; CNRS,UMR5557, Ecologie Microbienne, Villeurbanne, France

Delphine Moreau, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17 Rue Sully, B.V.86510,21065 Dijon Cedex, France

John P. Morrissey, Department of Microbiology, BIOMERIT Research Centre, University College Cork, Cork, Ireland;Environmental Research Institute, University College Cork, Cork, Ireland

Christophe Mougel, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17 Rue Sully, B.V.86510, 21065 Dijon Cedex, France

Nathalie Munier-Jolain, INRA, UMR 1347 Agroecologie, Universite de Bourgogne, AgroSup Dijon, 17 Rue Sully,B.V. 86510, 21065 Dijon Cedex, France

Chandra S. Nautiyal, Division of Plant Microbe Interactions, CSIR-National Botanical Research Institute, Rana PratapMarg, Lucknow 226001, India

Maureen O’Callaghan, AgResearch, Private Bag 4749, Christchurch 8140, New Zealand

Fergal O’Gara, Department of Microbiology, BIOMERIT Research Centre, University College Cork, Cork, Ireland;Environmental Research Institute, University College Cork, Cork, Ireland

Randy Ortiz Castro, Instituto de Investigaciones Quımico-Biologicas, Universidad Michoacana de San Nicolas deHidalgo, Edificio B3, Ciudad Universitaria, C. P. 58030 Morelia, Michoacan, Mexico

Leonard S. van Overbeek, Plant Research International, Wageningen University and Research Centre, Wageningen, TheNetherlands

Martin Parniske, Institute of Genetics, Biocenter University of Munich (LMU), Großhaderner Str. 2-4, Martinsried82152, Germany