Biological Nitrogen Fixation

By Frans J. de Bruijn

Nitrogen is arguably the most important nutrient required by plants. However, the availability of nitrogen is limited in many soils and although the earth's atmosphere consists of 78.1% nitrogen gas (N2) plants are unable to use this form of nitrogen. To compensate , modern agriculture has been highly reliant on industrial nitrogen fertilizers to achieve maximum crop productivity. However, a great deal of fossil fuel is required for the production and delivery of nitrogen fertilizer. Moreover carbon dioxide (CO2) which is released during fossil fuel combustion contributes to the greenhouse effect and run off of nitrate leads to eutrophication of the waterways. Biological nitrogen fixation is an alternative to nitrogen fertilizer. It is carried out by prokaryotes using an enzyme complex called nitrogenase and results in atmospheric N2 being reduced into a form of nitrogen diazotrophic organisms and plants are able to use (ammonia). It is this process and its major players which will be discussed in this book.

Biological Nitrogen Fixation is a comprehensive two volume work bringing together both review and original research articles on key topics in nitrogen fixation. Chapters across both volumes emphasize molecular techniques and advanced biochemical analysis approaches applicable to various aspects of biological nitrogen fixation.

Volume 1 explores the chemistry and biochemistry of nitrogenases, nif gene regulation, the taxonomy, evolution, and genomics of nitrogen fixing organisms, as well as their physiology and metabolism.

Volume 2 covers the symbiotic interaction of nitrogen fixing organisms with their host plants, including nodulation and symbiotic nitrogen fixation, plant and microbial "omics", cyanobacteria, diazotrophs and non-legumes, field studies and inoculum preparation, as well as nitrogen fixation and cereals.

Covering the full breadth of current nitrogen fixation research and expanding it towards future advances in the field, Biological Nitrogen Fixation will be a one-stop reference for microbial ecologists and environmental microbiologists as well as plant and agricultural researchers working on crop sustainability.

• Language: English
• Publisher: Wiley
• Release date: Jun 16, 2015
• ISBN: 9781118637210

Book preview

Cover photo: Courtesy of Embrapa Cerrados, Iêda C. Mendes and Mariangela Hungria. Soybean plants cultivated with and without inoculation in a first-year Cerrado Oxisol, poor on N in Planaltina, Brazil.

The front plot shows small uninoculated soybean plants, light green and yellowish because of the lack of N and the surrounding plots show large dark green plants inoculated with symbiotic nitrogen fixing Bradyrhizobium japonicum bacteria. For further details see Chapter~99 by Hungria and Mendes.

Copyright © 2015 by John Wiley & Sons, Inc. All rights reserved.

Published by John Wiley & Sons, Inc., Hoboken, New Jersey.

Published simultaneously in Canada.

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Set ISBN: 978-1-118-63704-3

Volume 1 ISBN: 978-1-118-63712-8

Volume 2 ISBN: 978-1-118-63707-4

This work is dedicated to my two daughters, Waverly de Bruijn-Klaw and Vanessa de Bruijn, for their support and interest even from a distance and to my wife, Cathy Senta-Loys de Bruijn, for her love and understanding during the editing of this book.

Preface

Nitrogen is arguably the most important nutrient required by plants, being an essential component of all amino acids and nucleic acids. However, the availability of nitrogen is limited in many soils, and although the earth's atmosphere consists of 78.1% nitrogen gas (N2), plants are unable to use this form of nitrogen. To compensate this, modern agriculture has been highly reliant on industrial nitrogen fertilizers to achieve maximum crop productivity (Ferguson et al. 2010).

However, a great deal of fossil fuel is required for the production and delivery of nitrogen fertilizer. Indeed, industrial nitrogen fixation alone accounts for 50% of fossil fuel used in agriculture. This can be exceedingly expensive. In recent years, the price of chemical fertilizers has increased dramatically due to rising fossil fuel costs. Moreover, carbon dioxide (CO2), which is released during fossil fuel combustion, contributes to the greenhouse effect, as does the decomposition of nitrogen fertilizer, which releases nitrous oxide (NOx), itself about 292 times more active as a greenhouse gas than carbon dioxide (Ferguson et al. 2010). In addition, applying chemical fertilizers is largely inefficient, as 30–50% of applied nitrogen fertilizer is lost to leaching, resulting in significant environmental problems, such as the eutrophication of waterways. Thus, there is a strong need to reduce our reliance on chemical nitrogen fertilizers and instead optimize alternative nitrogen inputs (Ferguson et al. 2010).

Biological nitrogen fixation is one alternative to nitrogen fertilizer. It is carried out by prokaryotes using an enzyme complex called nitrogenase and results in atmospheric N2 being reduced into a form of nitrogen diazotrophic organisms, and plants are able to use (ammonia; see Introduction). It is this process and its major players, which will be discussed in this Biological Nitrogen Fixation book.

The research in the field of Biological Nitrogen Fixation is very active at the moment, especially in the subfield of symbiotic nitrogen fixation. Although a number of books and proceedings of the International Congresses on Nitrogen Fixation and North American Symbiotic Nitrogen Fixation Conferences have appeared during the last 10 and more years, a comprehensive book on the field from biochemistry of nitrogenase, through expression and regulation of nitrogen genes, taxonomy, evolution, and comparative genomics of nitrogen-fixing organisms; their physiology and metabolism; their life in the rhizosphere and under stress conditions, rhizobial Omics, plant Omics, nodulation of legumes and nonlegumes, recognition, infection and nodule ontogeny, nitrogen fixation and assimilation, field studies, inoculum preparation and application of Nod factors, endophytic nitrogen fixers, cyanobacteria, and nitrogen fixation and cereals does not presently exist, and this book aims to fill this void.

A number of authors were selected based on the programs of the 21st North American Conference on Symbiotic Nitrogen Fixation in Columbia, Missouri, USA (June 2010); the 17th International Congress on Nitrogen Fixation in Fremantle, Western Australia (December 2011); the 16th Australian Nitrogen Fixation Conference (Manly, June 2012); the programs of the European Nitrogen Fixation Congress (ENFC), held in Munich, Germany, from the September 2, 2012, to September 5, 2012; and the satellite meetings on Genomics of nitrogen fixing bacteria and the Symposium on Biological Nitrogen Fixation with Non-legumes (The latter three were attended by the Editor upon invitation by the Conference Organizer Dr. Anton Hartmann).

The best known and most extensively studied example of biological nitrogen fixation is the symbiotic interaction between nitrogen-fixing rhizobia and legume plants. Here, the rhizobia induce the formation of specialized structures (nodules) on the roots or sometimes stems of the legume plant and fix nitrogen, which is directly assimilated by the host plant; in return, the plant provides the required energy source for the energy-intensive, nitrogen-fixation process. It is this symbiotic interaction, which will be highlighted in this book.

While this book features many chapters on the model system for indeterminate nodule formation, the Sinorhizobium meliloti–Medicago truncatula symbiosis, little information is presented on the Mesorhizobium loti–Lotus japonicus symbiotic model system for determinate nodule formation. The reason for this is the simultaneous publication edited by Dr. S. Tabata and Dr. Jens Stougaard (Springer-Verlag) specifically focused on this topic, and the reader is referred to this book for details on this important model symbiotic system.

While legumes are important as major food and feed crops and are the second group of such crops grown worldwide, the first group (cereals such as wheat, maize, and rice) does not have this symbiotic nitrogen-fixing interaction with rhizobia. It has thus been a focus of a number of studies to transfer the ability to fix nitrogen to cereals, and different timely approaches toward this goal are also included in the book. The case of rice will be discussed in the following section.

Rice is the most important staple food for over 2 billion people in Asia and for hundreds of millions in Africa and Latin America. To feed the ever-increasing population of these regions, the world's annual rice production must increase from the present 460 million to 560 million tons by the year 2000 and to 760 million tons by 2020 (Ladha et al. 1997).

If future increase in rice production has to come from the same or even reduced land area, rice productivity must be greatly enhanced to meet these goals. Nitrogen is the nutrient that most frequently limits agricultural production of rice and other cereals. As pointed out earlier, global agriculture now relies heavily on N fertilizers derived at the expense of petroleum. Nitrogen fertilizers, therefore, are expensive inputs costing agriculture more than $45 billion (US) per year (Ladha et al. 1997).

In the tropics, lowland rice yields 2–3.5 ton per hectare, utilizing naturally available N derived from biological nitrogen fixation (BNF) by free-living and plant-associated (endophytic) nitrogen-fixing organisms and from mineralization of soil N. Achieving 50% higher rice yield needed by 2020 will require at least double the 10 million ton of N-fertilizer that is currently used each year for rice production. Manufacturing the fertilizer for today's needs requires 544 × 10⁹ MJ of fossil fuel energy annually (Ladha et al. 1997).

Thus, alternatives to chemical fertilizer must be sought.

BNF for rice and other cereals has been the holy grail for decades now and has been explored in laboratories worldwide, mainly looking at free-living, associative, and endophytic nitrogen-fixing organisms. These studies have been presented and discussed at numerous International Nitrogen Fixation Congresses, Nitrogen Fixation with Non-legumes Meetings, and the IRRI funded Working Group Meetings of the Frontier Project on Nitrogen Fixation in Rice and Other Non-Legumes, the latter in the late 1990s (Ladha et al. 1997). Recently, the Bill and Melinda Gates Foundation convened a small meeting on the subject and several projects were funded, including the transfer of the nitrogen-fixation (nitrogenase) genes into cereals and the transfer of the ability to form nitrogen-fixing nodules to cereals. This has greatly stimulated research in this area.

Rice transformation is now routine and since the genome has been sequenced and extensive genetics is available, it should serve as a model species, while for other cereals, a recently developed Brachypodium model system has been established.

The discovery of a common symbiotic pathway in arbuscular mycorrhizal, rhizobial, and actinorhizal symbioses and the identification of conserved pathway genes in legumes and monocots (including rice; Venkateshwaran et al. 2013) have made the extension of the ability to fix nitrogen in nodular associations, with cereals as a more realistic endeavor.

The direct transfer of nitrogen fixation (nif) genes into nonlegumes has also become more feasible especially since it has been shown that six out of the numerous nif genes are absolutely required for FeMo-co biosynthesis and nitrogenase activity, both in vitro and in vivo.

It is likely that the products of some genes that are required for FeMo-co biosynthesis in vivo could be replaced by the activities of plant counterparts.

Thus, we are entering a very promising period of research on BNF, both in more conventional systems and nonlegumes such as rice, based on rapidly advancing basic studies on the chemistry, biochemistry, genetics, physiology, regulation, taxonomy, genomics and metagenomics, and metabolism of nitrogen-fixing organisms (and their hosts). This is the topic of this book, which should be a major resource for scientists in the field, and those wanting to enter it, as well as teachers and agricultural and molecular specialists wanting to apply the technology.

Frans J. de Bruijn

References

Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin Y-H, Reis DE, Gresshoff PM. 2010. J. Int. Plant Biol.52: 61–76.

Ladha JK, de Bruijn FJ, Malik KA. 1997. Plant Soil194: 1–10.

Venkateshwaran, M, Volkening JD, Sussman MR, Ane J-M. 2013. Curr. Opin. Plant Biol. 16: 118–127.

Acknowledgments

I greatly acknowledge Anton Hartmann for inviting me to the European Nitrogen Fixation Congress held in Munich in September 2012 and its two satellite meetings. The programs of these meetings contributed significantly to the list of invited authors. I also thank Jean-Michele Ané for sharing a figure from one of his latest publications for my Chapter 108 of this book and Charles Rosenberg for sharing a figure from his chapter. I thank Julie Cullimore for critically reading my Chapter 108 and making helpful suggestions. I would like to thank the authors for their cooperation and excellent contributions. I would also like to thank Claude Bruand and Marcel Soon for their help with the computer work. The Laboratory for Plant microbe Interaction (LIPM), the Institut National de Recherche Agronomique (INRA), the Centre National de Recherche Scientifique (CNRS) and the Labex Tulip are gratefully acknowledged for their support of my editorial activities.

Contributors

Editor

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

Authors

Josiane Abadie, INRA, UMR Eco&Sols, Montpellier, France

Joaquin Abian, CSIC-UAB Proteomics Laboratory, Instituto de Investigaciones Biomédicas de Barcelona-CSIC, Bellaterra, Spain

Helge K. Abicht, Department of Biology, ETH, Institute of Microbiology, Department of Biology, Zurich, Switzerland

Edit Ábrahám, Biological Research Center of the Hungarian Academy of Sciences, Institute of Biochemistry, Szeged, Hungary

Andriamananjara, LRI-SRA, Laboratoire des Radio-isotopes, Université d'Antananarivo, Antananarivo, Madagascar

O. Sarah Adeyemo, Department of Biological Sciences, University of North Texas, Denton, TX, USA

Christina M. Agapakis, Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, CA, USA

O. Mario Aguilar, Instituto de Biotecnología y Biología Molecular, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas)-Universidad Nacional de La Plata, La Plata, Argentina

Nora Alkama, Faculté des Sciences Biologiques et Agronomiques, Département d'Agronomie, Université Mouloud Mammeri, Tizi Ouzou, Algeria

Nicole Alloisio, Université de Lyon, Centre National de la Recherche Scientifique, UMR 5557, Ecologie Microbienne, Cedex Villeurbanne, France

Nalvo F. Almeida, Faculdade de Computação, Universidade Federal de Mato Grosso do Sul, Grosso do Sul, Brazil

Benoît Alunni, Institute for Integrative Biology of the Cell, Centre National de la Recherche Scientifique UMR9198, Gif-sur-Yvette, France; Département de Biologie, Université Paris Sud, Orsay, France

Laurie Amenc, INRA, UMR Eco&Sols, Montpellier, France

Julie Ardley, Centre for Rhizobium Studies, Murdoch University, Murdoch, WA, Australia

Jean-François Arrighi, IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRA/ UM2 /CIRAD, F-34398, Montpellier, France

Aregu Amsalu Aserse, Department of Environmental Sciences, University of Helsinki, Helsinki, Findland

Mary Atieno, Tropical Soil Biology and Fertility institute of CIAT (TSBF-CIAT), Nairobi, Kenya; Department of Plant and Food Science, Faculty of Agriculture & Environment, The University of Sydney, Sydney, NSW, Australia

Ferhan Ayaydin, Cellular Imaging Laboratory, Biological Research Center, Szeged, Hungary

Rammyani Bagchi, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA

Nadia Bakkou, Microbiology Unit, Department of Botany and Plant Biology, University of Geneva, Geneva, Switzerland; Thermo Scientific, Molecular Biology, St. Leon-Rot, Germany

Eduardo Balsanelli, Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, Curitiba, PR, Brazil

José Ivo Baldani, Embrapa Agrobiologia, Seropédica, Rio de Janeiro, Brazil

Adnane Bargaz, INRA, UMR Eco&Sols, Montpellier, France; Swedish University of Agricultural Sciences, Alnarp, Sweden

David G. Barker, Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de la Recherche Scientifique (UMR 2594), Castanet-Tolosan, France

Bénédicte Bastiat, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR 441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR 2594, Castanet-Tolosan, France

Marco Bazzicalupo, Department of Biology, University of Florence, Sesto Fiorentino, Italy

Perrin H. Beatty, Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada

Nicholas J. Beauchemin, Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA

Manuel Becana, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), Zaragoza, Spain

María Pía Beker, Instituto de Biotecnología y Biología Molecular, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas)-Universidad Nacional de La Plata, La Plata, Argentina

Alphonsus K. Belane, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Vagner A. Benedito, West Virginia University, Morgantown, WV, USA

Anelise Beneduzi, Fundação Estadual de Pesquisa Agropecuária [FEPAGRO], Porto Alegre, RS, Brazil

David R. Benson, Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT, USA

Alison M. Berry, Department of Plant Sciences, University of California, Davis, CA, USA

Govindaraj Ramakantrao Bhanganagare, Department of Genetics, Indian Agricultural Research Institute, New Delhi, India

Emanuele G. Biondi, Interdisciplinary Research Institute USR3078, CNRS, Lille Nord de France University, Villenenuve d'Ascq, France

Ton Bisseling, Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, Wageningen, The Netherlands; College of Science, King Saud University, Riyadh, Saudi Arabia

Flavio A. Blanco, Instituto de Biotecnología y Biología Molecular, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas)-Universidad Nacional de La Plata, La Plata, Argentina

Didier Bogusz, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France

Deniz Bombar, Department of Ocean Sciences, University of California, Santa Cruz, Santa Cruz, CA, USA

Katia Bonaldi, Section of Cell and Developmental Biology, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA

Jocelyne Bonneau, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France

Jean-Jacques Bono, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France

Nantakorn Boonkerd, School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima, Thailand

Stéphanie Borland, UMR CNRS 5557 Ecologie Microbienne, Université de Lyon, Villeurbanne, France

Kirill Borziak, BioEnergy Science Center and Genome Science and Technology Program, University of Tennessee, Oak Ridge National Laboratory, Oak Ridge, TN, USA

Alexandre Boscari, INRA, Institut Sophia Agrobiotech (ISA), UMR 1355, Sophia Antipolis, France; CNRS, Institut Sophia Agrobiotech (ISA), UMR 7254, Sophia Antipolis cedex, France; Université Nice Sophia Antipolis, Institut Sophia Agrobiotech (ISA), Sophia Antipolis cedex, France

Eric S. Boyd, Department of Chemistry and Biochemistry and Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA

Lambert Brau, School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, Burwood Campus, Melbourne, VIC, Australia

Andrew Breakspear, John Innes Centre, Norwich Research Park, Norwich, UK

Renaud Brouquisse, INRA, Institut Sophia Agrobiotech (ISA), UMR 1355, Sophia Antipolis, France; CNRS, Institut Sophia Agrobiotech (ISA), UMR 7254, Sophia Antipolis cedex, France; Université Nice Sophia Antipolis, Institut Sophia Agrobiotech (ISA), Sophia Antipolis cedex, France

Claude Bruand, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France

Daniel H. Buckley, Department of Crop and Soil Sciences, Cornell University, Ithaca, NY, USA

Saul Burdman, Department of Plant Pathology and Microbiology, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

Mirella Butsch, Victorian Department of Economic Development, Jobs, Transport and Resources, Horsham, VIC, Australia

Priscila A. Calderoli, Instituto de Biotecnología y Biología Molecular, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas)-Universidad Nacional de La Plata, La Plata, Argentina

Georg Carlssonn, Swedish University of Agricultural Sciences, Alnarp, Sweden

Fabienne Cartieaux, IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRA/ UM2 /CIRAD, F-34398 Montpellier, France

Fernanda de Carvalho-Niebel, Laboratory of Plant Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de Recherche Scientifique [UMR 2594], CS 52627, Castanet-Tolosan, Cedex, France

Andrea Casteriano, Faculty of Agriculture and Environment, University of Sydney, Sydney, NSW, Australia

Marion R. Cerri, Laboratory of Plant Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de Recherche Scientifique [UMR 2594], CS 52627, Castanet-Tolosan, Cedex, France

Mireille Chabaud, Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de la Recherche Scientifique (UMR 2594), Castanet-Tolosan, France

Eugenia Chaia, Departamento de Biología General, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue-INIBIOMA, Argentina

Antony Champion, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France; Laboratoire Commun de Microbiologie (IRD/ISRA/UCAD), Centre de Recherche de Bel-Air, Dakar, Sénégal

Bruno Contreras-Moreira, Fundación ARAID, Zaragoza, Spain; Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Cientificas (EEAD-CSIC), Zaragoza, Spain

Devrim Coskun, Department of Biological Sciences & Canadian Centre for World Hunger Research (CCWHR), University of Toronto, Toronto, ON, Canada

Donna R. Cousins, John Innes Centre, Norwich Research Park, Norwich, UK

Jean-Malo Couzigou, Institut of Plant Sciences Paris-Saclay (IPS2), UMR 9213/UMR1403, CNRS, INRA, Université Paris-Sud, Université d'Evry, Université Paris-Diderot, Sorbonne Paris-Cité, Orsay, France

Pedro B. da Costa, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

Xinbin Dai, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Felix D. Dakora, Department of Chemistry, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Basanta Kumar Das, Directorate of Plant Protection, Quarantine and Storage, Department of Agriculture and Cooperation, Ministry of Agriculture, Government of India, Faridabad, Haryana, India

David A. Day, School of Biological Sciences, Flinders University, Adelaide, SA, Australia

Frank B. Dazzo, Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, USA

Rosalind Deaker, Faculty of Agriculture and Environment, University of Sydney, Sydney, NSW, Australia

Frédéric Debellé, INRA, Laboratoire des Interactions Plantes-Micaroorganismes (LIPM), UMR441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France

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

Samanta B. de Campos, Department of Prokaryotic Genetics, Bielefeld University, Bielefeld, Germany

Gabriela de Carvalho Fernandes, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

Sergio Miana de Faria, Embrapa Agrobiologia, Séropédica, Rio de Janeiro, Brazil

Eva E. Deinum, FOM Institute AMOLF, Amsterdam, The Netherlands; Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, Wageningen, The Netherlands

Jakeline Renata Marçon Delamuta, Embrapa Soja, Londrina, PR, Brazil

Alain Desbois, Institut de Biologie Intégrative de la Cellule/UMR 9198 CNRS/CEA-Saclay, Gif-sur-Yvette, France

Nathalie Diagne, Institut Sénégalais de Recherches Agricoles, Bambey, Sénégal et Laboratoire Commun de Microbiologie (IRD/ISRA/UCAD), Centre de Recherche de Bel Air, Dakar, Sénégal

Martin Diaz-Zorita, Novozymes BioAg S.A., Buenos Aires, Argentina, South America

Rebecca Dickstein, Department of Biological Sciences, University of North Texas, Denton, TX, USA

Agota Domonkos, NARIC, Agricultural Biotechnology Institute, Gödöllő, Hungary

Patrick Doumas, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France

Nguyen Van Dong, National Key Laboratory of Plant Cell Biotechnology, Agricultural Genetics Institute, Vietnamese Academy of Agricultural Science, Hanoi, Vietnam

J. Allan Downie, John Innes Centre, Norwich, UK

Jean-Jacques Drevon, INRA, UMR Eco&Sols, Montpellier, France

Benoît Drogue, UMR CNRS 5557 Ecologie Microbienne, Université de Lyon, Villeurbanne, France

Claudine Elmerich, Institut Pasteur, Département de Microbiologie, BMGE, Paris, Cedex, France

Carlos Echavarri-Erasun, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Madrid, Spain

Doreen Fischer, Department of Environmental Sciences, Research Unit Microbe-Plant Interactions, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Neuherberg, Germany

Hans-Martin Fischer, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

Jeffrey J. Fischer, Department of Biological Sciences, University of Calgary, Calgary, AB, Canada

Enrique Flores, Instituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla, Seville, Spain

Karl Forchhammer, Lehrstuhl für Mikrobiologie/Organismische Interaktionen am Interfakultären Institut für Mikrobiologie und Infektionsmedizin, Eberhard-Karls-Universität, Tübingen, Germany

Joëlle Fournier, Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de la Recherche Scientifique (UMR 2594), Castanet-Tolosan, France

Teal Furnholm, Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA

Claudine Franche, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France

Luciano Gabbarini, Laboratorio Bioquímica, Microbiología e Interacciones Biológicas en el Suelo (LBMIBS), Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Buenos Aires, Argentina

John Christian Gaby, Department of Microbiology, Cornell University, Ithaca, NY, USA

Marco Galardini, Department of Biology, University of Florence, Sesto Fiorentino, Italy

Pascal Gamas, Laboratory of Plant Microbe Interactions, Institut National de Recherche Agronomique [UMR 441], Centre National de Recherche Scientifique [UMR 2594], CS 52627, Castanet-Tolosan, Cedex, France

Greg Gemell, Australian Inoculants Research Group [AIRG], Gosford Primary Industries Institute, NSW Department of Primary Industries, Ourimbah, NSW, Australia

René Geurts, Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, Wageningen, The Netherlands

Hassen Gherbi, Institut de Recherche pour le Développement (IRD), UMR DIADE and LSTM, Montpellier, France

Faten Ghodhbane-Gtari, Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA; Laboratoire Microorganismes et Biomolécules Actives, Université de Tunis El Manar (FST), Tunis, Tunisia

Cherki Ghoulam, Faculté des Sciences et Techniques Guéliz, Marrakech, Morocco

Isaac Gifford, Department of Plant Sciences, University of California, Davis, Davis, CA, USA

Lourdes Girard, Programa de Dinámica Genomica, Centro de Ciencias Genómicas, Universidad Nacional Autónoma at México, Cuernavaca, México

Eric Giraud, IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LTSM), UMR IRD/SupAgro/INRA/M2/CIRAD, Montpellier, France

Alexander N. Glazer, Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA, USA

Rudi Glockshuber, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

Douglas Fabiano Gomes, Embrapa Soja, PR, Brazil; Department of Genetics, Universidade Federal do Paraná, PR, Brazil

Juan E. González, Department of Molecular and Cell Biology, University of Texas at Dallas, Dallas, TX, USA

Victor Gonzáles, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de Mexico, Cuernavaca, México

Manuel González-Guerrero, Centro de Biotecnología y Genómica de Plantas, Madrid, Spain

Allen G. Good, Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada

Clare Gough, INRA, Laboratoire des Interactions Plantes-Microorganismes [LIPM], UMR441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes [LIPM], UMR2594, Castanet-Tolosan, France

Benjamin Gourion, Institut des Sciences du Vegetal, ISV, CNRS – Bat 23, Gif Sur Yvette, France

Dian Guan, John Innes Centre, Norwich Research Park, Norwich, UK

Ibtissem Guefrachi, Institute for Integrative Biology of the Cell, Centre National de la Recherche Scientifique UMR9198, Gif-sur-Yvette, France

Antoine Huyghe, Microbiology Unit, Department of Botany and Plant Biology, University of Geneva, Geneva, Switzerland

Cynthia Gyogluu, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Chien Van Ha, Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan; National Key Laboratory of Plant Cell Biotechnology, Agricultural Genetics Institute, Vietnamese Academy of Agricultural Science, Hanoi, Vietnam

Ahsan Habib, Novozymes Biologicals, Inc., Salem, VA, USA

Elizabeth Hartley, Australian Inoculants Research Group [AIRG], Gosford Primary Industries Institute, NSW Department of Primary Industries, Ourimbah, NSW, Australia

Anton Hartmann, Department of Environmental Sciences, Research Unit Microbe-Plant Interactions, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Neuherberg, Germany

Marijke Hartog, Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, Wageningen, The Netherlands

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

Martin Heil, Departamento de Ingeniería Genética, CINVESTAV-Irapuato, Irapuato, Guanajuato, México

Hauke Hennecke, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

H. M. L. I. Herath, Microbial Biotechnology Unit, Institute of Fundamental Studies, Kandy, Sri Lanka; Department of Agroecology, Faculty of Science and Technology, Aarhus University, Tjele, Denmark

Jose A. Hernandez, Department of Biochemistry, Midwestern University, Glendale, AZ, USA

Antonia Herrero, Instituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla, Seville, Spain

Laetitia Herrmann, Tropical Soil Biology and Fertility institute of CIAT (TSBF-CIAT), United Nation Avenue, Nairobi, Kenya; School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, Burwood Campus, Melbourne, VIC, Australia; CIRAD, UMR Eco&Sols (SupAgro–CIRAD–INRA–IRD), Land Development Department - Office of Science for Land Development, Chatuchak, Bangkok, Thailand

Ann M. Hirsch, Department of Molecular, Cell and Developmental Biology and Molecular Biology Institute, University of California, Los Angeles, Los Angeles, CA, USA

Valérie Hocher, Institut de Recherche pour le Développement, UMR LTSM, Montpellier, France

Zonglie Hong, Department of Plant, Soil, and Entomological Sciences and Program of Microbiology, Molecular Biology and Biochemistry, University of Idaho, Moscow, ID, USA

Beatrix Horvath, NARIC, Agricultural Biotechnology Institute, Gödöllő, Hungary

James B. Howard, Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, Minneapolis, MN, USA

Ying-Sheng Huang, Texas A&M AgriLife Research, Dallas, TX, USA

Luciano F. Huergo, Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, Curitiba, PR, Brazil

Mariangela Hungria, Embrapa Soja, Londrina, PR, Brazil

Jodi L. Humann, Department of Horticulture, Washington State University, Pullman, WA, USA

Michael F. Hynes, Department of Biological Sciences, University of Calgary, Calgary, AB, Canada

A. D. Igalavithana, Microbial Biotechnology Unit, Institute of Fundamental Studies, Kandy, Sri Lanka; Korea Biochar Research Center and Department of Biological Environment, Kangwon National University, Chuncheon, Korea

Leandro Imanishi, Laboratorio Bioquímica, Microbiología e Interacciones Biológicas en el Suelo (LBMIBS), Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Buenos Aires, Argentina

Juan Imperial, Centro de Biotecnología y Genómica de Plantas (UPM-INIA), Universidad Politécnica de Madrid, Campus de Montegancedo, Madrid, Spain; CSIC, Madrid, Spain

Natalia Ivanova, DOE Joint Genome Institute, Walnut Creek, CA, USA

Benoît Jaillard, INRA, UMR Eco&Sols, Montpellier, France

Sanjay Kumar Jaiswal, Department of Chemistry, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Euan K. James, James Hutton Institute, Dundee, UK

Monika Janczarek, Department of Genetics and Microbiology, University of Marie Curie-Skłodowska, Lublin, Poland

Bhavanath Jha, Discipline of Marine Biotechnology and Ecology, CSIR – Central Salt and Marine Chemicals Research Institute, Bhavnagar, Gujarat, India

Emilio Jimenez-Vicente, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Madrid, Spain

José I. Jiménez-Zurdo, Grupo de Ecología Genética de la Rizosfera, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Granada, Spain

Jian Jin, Key Laboratory of Black Soil Ecology, Northeast Institute of Geography and Agro-ecology, Chinese Academy of Sciences, Harbin, PR China

Ryan T. Jones, Department of Microbiology and Immunology, Montana Institute on Ecosystems, Montana State University, Bozeman, MT, USA

Beatriz Jorrín, Centro de Biotecnología y Genómica de Plantas (UPM-INIA), Universidad Politécnica de Madrid, Campus de Montegancedo, Madrid, Spain

Michael L. Kahn, Institute of Biological Chemistry, Washington State University, Pullman, WA, USA

Peter Kalo, NARIC, Agricultural Biotechnology Institute, Gödöllő, Hungary

Yaowei Kang, Novozymes Biologicals, Inc., Salem, VA, USA

Heng Kang, State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China

Ramakrishnan Karunakaran, Molecular Microbiology, John Innes Centre, Norwich, UK

Katerina Kechris, Department of Biostatistics and Informatics, Colorado School of Public Health, University of Colorado, Denver, Aurora, CO, USA

Peter Kennedy, Victorian Department of Economic Development, Jobs, Transport and Resources, Horsham, VIC, Australia

Attila Kereszt, Biological Research Center of the Hungarian Academy of Sciences, Institute of Biochemistry, Szeged, Hungary

Mahipal Singh Kesawat, Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University, Seoul, Republic of Korea

Jitendra Keshri, Discipline of Marine Biotechnology and Ecology, CSIR – Central Salt and Marine Chemicals Research Institute, Bhavnagar, Gujarat, India

Agnieszka Klonowska, IRD, UMR 113, Laboratory of Mediterranean and Tropical Symbioses, Montpellier, France

Eva Kondorosi, Institute for Integrative Biology of the Cell, Centre National de la Recherche Scientifique UMR9198, Gif-sur-Yvette, France; Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences, Szeged, Hungary

Herbert J. Kronzucker, Department of Biological Sciences & Canadian Centre for World Hunger Research (CCWHR), University of Toronto, Toronto, ON, Canada

Dagmar Krysciak, Biocenter Klein Flottbek, Division of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany

Igor S. Kryvoruchko, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Ken-ichi Kucho, Graduate School of Science and Engineering, Kagoshima University, Kagoshima, Japan

Manu Kumar, Department of Life Science, Sogang University, Seoul, South Korea

Nikos Kyrpides, DOE Joint Genome Institute, Walnut Creek, CA, USA

Carlos Labandera-Gonzales, Department of Soil Microbiology, General Direction of Natural Renewable Resources, Ministry of Livestock, Agriculture and Fisheries, Montevideo, Uruguay

Martin Lage, Lage & Cia. S.A., Montevideo, Uruguay

Pedro Lage, Lage & Cia. S.A., Montevideo, Uruguay

Laurent Laplaze, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France; Laboratoire Commun de Microbiologie (IRD/ISRA/UCAD), Centre de Recherche de Bel-Air, Dakar, Sénégal

Julie LaRoche, Department of Biology, Dalhousie University, Halifax, NS, Canada

Julien Lavenus, Institut de Recherche pour le Développement, UMR DIADE, Montpellier, France

Mohamed Lazali, INRA, UMR Eco&Sols, Montpellier, France

Raphael Ledermann, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

Mary Leggett, Novozymes BioAg Limited, Saskatoon, SK, Canada

Antonio Leonforte, Victorian Department of Economic Development, Jobs, Transport and Resources, Horsham, VIC, Australia

Didier Lesueur, Tropical Soil Biology and Fertility institute of CIAT (TSBF-CIAT), Nairobi, Kenya; School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, Burwood Campus, Melbourne, VIC, Australia; CIRAD, UMR Eco&Sols (SupAgro-CIRAD-INRA-IRD), Land Development Department – Office of Science for Land Development, Chatuchak, Bangkok, Thailand

Jun Li, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Xiao-Dan Li, Laboratory of Biomolecular Research, Paul Scherrer Institut, Villigen, Switzerland

Min Lin, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Crop Biotechnology,Ministry of Agriculture, Beijing, China

Tingsong Liu, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Marc Libault, Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, USA

Kristina Lindström, Department of Environmental Sciences, University of Helsinki, Helsinki, Finland

Chengwu Liu, John Innes Centre, Norwich Research Park, Norwich, UK

Carolin R. Löscher, Institut für Allgemeine Mikrobiologie, Christian-Albrechts-Universität zu Kiel, Kiel, Germany

Antonio López-Lozano, Instituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla, Seville, Spain

Luis Lozano, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de Mexico, Cuernavaca, México

Wei Lu, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Crop Biotechnology, Ministry of Agriculture, Beijing, China

Mikael Lucas, Institut de Recherche pour le Développement (IRD), UMR DIADE, Montpellier, France

Thabo I. Makhubedu, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Pride Makhura, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Iris Maldener, Lehrstuhl für Mikrobiologie/Organismische Interaktionen am Interfakultären Institut für Mikrobiologie und Infektionsmedizin, Eberhard-Karls-Universität, Tübingen, Germany

Manorama, College of Dairy Technology, Indira Gandhi Krishi Vishwa Vidyalaya, Raipur, Chhattisgarh, India

Nyamande Mapope, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Pilar Martínez-Hidalgo, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

Eustoquio Martínez-Molina, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

Bernd Masepohl, Biologie der Mikroorganismen, Ruhr-Universität Bochum, Bochum, Germany

Nadezda Masloboeva, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

Pedro F. Mateos, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

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

Pintu D. Masalkar, Department of Biochemistry & Cellular and Molecular Biology, and Program in Genome Science and Technology, The University of Tennessee, Knoxville, TN, USA

Patrick Mavingui, UMR CNRS 5557 Ecologie Microbienne, Université de Lyon, Villeurbanne, France

Eliane Meilhoc, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France

Iêda Carvalho Mendes, Embrapa Cerrados, Planaltina, DF, Brazil

Esther Menéndez, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

Alessio Mengoni, Department of Biology, University of Florence, Sesto Fiorentino, Italy

K. R. Menikdiwela, Microbial Biotechnology Unit, Institute of Fundamental Studies, Kandy, Sri Lanka; Postgraduate Institute of Agriculture, University of Peradeniya, Peradeniya, Sri Lanka

Pâmela Menna, Embrapa Soja, Londrina, PR, Brazil

Peter Mergaert, Institute for Integrative Biology of the Cell, Centre National de la Recherche Scientifique UMR9198, Gif-sur-Yvette, France

Flora Pule-Meulenberg, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Avinash Mishra, Discipline of Marine Biotechnology and Ecology, CSIR – Central Salt and Marine Chemicals Research Institute, Bhavnagar, Gujarat, India

Keiichi Mochida, Biomass Engineering Program Cooperation Division, RIKEN Center for Sustainable Resource Science, Yokohama, Japan; Kihara Institute for Biological Research, Yokohama City University, Yokohama, Japan

Salmina N. Mogkelhe, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Keletso C. Mohale, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Elisabeth Mohorko, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

Frans Mokobane, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Sjef Moling, Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, Wageningen, The Netherlands

Rose A. Monteiro, Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, Curitiba, PR, Brazil

Daniel Moukouanga, Institut de Recherche pour le Développement (IRD), UMR DIADE, Montpellier, France

Lionel Moulin, IRD, UMR 113, Laboratory of Mediterranean and Tropical Symbioses, Montpellier, France

Seyed Abdollah Mousavi, Department of Environmental Sciences, University of Helsinki, Helsinki, Finland

Douglas G. Muench, Department of Biological Sciences, University of Calgary, Calgary, AB, Canada

Sofia Muhaba, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Bela M. Mulder, FOM Institute AMOLF, Amsterdam, The Netherlands; Laboratory for Cell Biology, Department of Plant Sciences, Wageningen University, Wageningen, The Netherlands

Jeremy D. Murray, John Innes Centre, Norwich Research Park, Norwich, UK

Papri Nag, Department of Life Science and Biotechnology, Jadavpur University, Kolkata, India; (Present address) National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, India

Maki Nagata, Department of Agricultural Sciences, Faculty of Agriculture, Saga University, Saga, Japan

Joaquín Navascués, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), Zaragoza, Spain

William E. Newton, Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA

Liang P. J. Ng, Division of Plant Science, Research School of Biology, The Australian National University, Canberra, ACT, Australia

Siti N. Mohd Noor, School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia

Stefan Nordlund, Department of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden

Philippe Normand, Ecologie Microbienne, Centre National de la Recherche Scientifique, UMR 5557, Université Lyon, Villeurbanne, France

Yaacov Okon, Department of Plant Pathology and Microbiology, Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

Giles E. D. Oldroyd, John Innes Centre, Norwich Research Park, Norwich, UK

Mariita Rodriguez Orbegoso, Biocenter Klein Flottbek, Division of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany

Ernesto Ormeño-Orrillo, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico

Richard Oteng-Frimpong, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Sidi Mohamed Ounane, Département de Phytotechnie, ENSA, El Harrach, Alger, Algeria

Subrata Pal, Department of Life Science and Biotechnology, Jadavpur University, Kolkata, India

Luciane M. P. Passaglia, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

Katharina Pawlowski, Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden

Fabio O. Pedrosa, Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, Curitiba, PR, Brazil

Catherine Pernot, INRA, UMR Eco&Sols, Montpellier, France

Xavier Perret, Department of Botany and Plant Biology, Microbiology Unit, University of Geneva, Geneva, Switzerland

Francine Perrine-Walker, Institut de Recherche pour le Développement (IRD), UMR DIADE, Montpellier, France

John W. Peters, Department of Chemistry and Biochemistry and Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA

Granny P. Phatlane, Department of Crop Sciences, Tshwane University of Technology, Arcadia Campus, Pretoria, South Africa

Francesco Pini, Interdisciplinary Research Institute USR3078, CNRS, Lille Nord de France University, Villenenuve d'Ascq, France

Catalina I. Pislariu, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Jürgen Prell, Soil Ecology, Department of Botany, RWTH Aachen, Aachen, Germany

Claire Prigent-Combaret, UMR CNRS 5557 Ecologie Microbienne, Université de Lyon, Villeurbanne, France

Philip Poole, Molecular Microbiology, John Innes Centre, Norwich, UK

César Poza-Carrión, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Madrid, Spain

Petar Pujic, Ecologie Microbienne, Centre National de la Recherche Scientifique UMR 5557, Université Lyon, Villeurbanne Cedex, France

Joshua P. Ramsay, Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand; School of Biomedical Sciences, CHIRI Biosciences Research Precinct, Curtin University, Perth, Western Australia

Pascal Ratet, Institut of Plant Sciences Paris-Saclay (IPS2), UMR 9213/UMR1403, CNRS, INRA, Université Paris-Sud, Université d'Evry, Université Paris-Diderot, Sorbonne Paris-Cité, Orsay, France

Wayne Reeve, Centre for Rhizobium Studies, Murdoch University, Murdoch, WA, Australia

Veronica Massena Reis, Embrapa Agrobiologia, Seropédica, Rio de Janeiro, Brazil

Eugenia Rigozzi, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

Luciana V. Rinaudi-Marron, Department of Molecular and Cell Biology, University of Texas at Dallas, Dallas, TX, USA

Raúl Rivas, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

Lina Rivera, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

Daniel M. Roberts, Department of Biochemistry & Cellular and Molecular Biology, and Program in Genome Science and Technology, The University of Tennessee, Knoxville, TN, USA

Marta Robledo, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain; LOEWE Research Center for Synthetic Microbiology (SYNMIKRO), Philipps-Universität Marburg, Marburg, Germany

Clive W. Ronson, Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand

Carmen Pérez-Rontomé, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), Zaragoza, Spain

Charles Rosenberg, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, Castanet-Tolosan, France

Pratyush Routray, Department of Biochemistry & Cellular and Molecular Biology, and Program in Genome Science and Technology, The University of Tennessee, Knoxville, TN, USA

Luc Felicianus Marie Rouws, Embrapa Agrobiologia, Seropédica, Rio de Janeiro, Brazil

Sonali Roy, John Innes Centre, Norwich Research Park, Norwich, UK

Luis M. Rubio, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Pozuelo de Alarcón, Madrid, Spain

Mohammad Salehin, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA

Laurent Sauviac, INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR 441, Castanet-Tolosan, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR 2594, Castanet-Tolosan, France

Christel Schmeisser, Biocenter Klein Flottbek, Division of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany

Michael Schmid, Department of Environmental Sciences, Research Unit Microbe-Plant Interactions, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Neuherberg, Germany

Ruth A. Schmitz, Institut für Allgemeine Mikrobiologie, Christian-Albrechts-Universität zu Kiel, Kiel, Germany

G. Seneviratne, Microbial Biotechnology Unit, Institute of Fundamental Studies, Kandy, Sri Lanka

Rodrigo V. Serrato, Setor Litoral, Universidade Federal do Paraná, Matinhos, PR, Brazil

Fabio Serventi, Department of Biology, ETH, Institute of Microbiology, Zurich, Switzerland

João C. Setubal, Departamento de Bioquímica and Instituto de Química, Universidade de São Paulo, São Paulo, Brazil; Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA

Sarah Shailes, John Innes Centre, Norwich Research Park, Norwich, UK

D. Janine Sherrier, Department of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, DE, USA

Björn J. Sieberer, Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de la Recherche Scientifique (UMR 2594), Castanet-Tolosan, France

Bouaziz Sifi, Département des Légumineuses, INRAT, Ariana, Tunisia

Marcelo F. Simon, Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brazil

Penelope M. Smith, School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia

Stewart Smith, Novozymes Biologicals, Inc., Salem, VA, USA

Senjuti Sinharoy, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Patricio Sobrero, Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Buenos Aires, Argentina

Emanuel M. Souza, Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, Curitiba, PR, Brazil

Stijn Spaepen, Department of Microbial and Molecular Systems, Centre of Microbial and Plant Genetics, KU Leuven, Heverlee, Belgium

Gary Stacey, Divisions of Plant Sciences and Biochemistry, National Center for Soybean Biotechnology, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

Wolfgang R. Streit, Biocenter Klein Flottbek, Division of Microbiology and Biotechnology, University of Hamburg, Hamburg, Germany

Saad Sulieman, Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan; Department of Agronomy, Faculty of Agriculture, University of Khartoum, Khartoum North, Sudan

Michael R. Sussman, Department of Biochemistry, University of Wisconsin, Madison, Madison, WI, USA

Akihiro Suzuki, Department of Agricultural Sciences, Faculty of Agriculture, Saga University, Saga, Japan; United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima, Japan

Sergio Svistoonoff, Institut de Recherche pour le Développement, UMR LTSM, Montpellier, France et Laboratoire Commun de Microbiologie (IRD/ISRA/UCAD), Centre de Recherche de Bel-Air, Dakar, Sénégal

Fatma Tajini, INRA, UMR Eco&Sols, Montpellier, France; Département des Légumineuses, INRAT, Ariana, Tunisia

Domancar Orona Tamayo, Departamento de Ingeniería Genética, CINVESTAV-Irapuato, Irapuato, Guanajuato, México

Dinah D. Tambalo, Department of Biology, University of Regina, Regina, SK, Canada

Kiwamu Tanaka, Divisions of Plant Sciences and Biochemistry, National Center for Soybean Biotechnology, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

Neung Teaumroong, School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima, Thailand

Antonius C.J. Timmers, Laboratory of Plant-Microbe Interactions, Institut National de Recherche Agronomique (UMR 441), Centre National de la Recherche Scientifique (UMR 2594), Castanet-Tolosan, France

Louis S. Tisa, Department of Cellular, Molecular and Biomedical Sciences, University of New Hampshire, Durham, NH, USA

Panlada Tittabutr, School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima, Thailand

Mauro Tonolla, Department of Botany and Plant Biology, Microbiology Unit, University of Geneva, Geneva, Switzerland

Omar Torres-Quesada, Grupo de Ecología Genética de la Rizosfera, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Granada, Spain

Katalin Tóth, Divisions of Plant Sciences and Biochemistry, National Center for Soybean Biotechnology, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

Lam-Son Phan Tran, Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan

Alexandre Tromas, Laboratoire Commun de Microbiologie (IRD/ISRA/UCAD), Centre de Recherche de Bel Air, Dakar, Sénégal

Michael K. Udvardi, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Verena Untiet, Soil Ecology, Department of Botany, RWTH Aachen, Aachen, Germany

Virginie Vaissayre, Institut de Recherche pour le Développement (IRD), UMR DIADE, Montpellier, France

Oswaldo Valdés-López, Department of Agronomy, University of Wisconsin, Madison, Madison, WI, USA

Claudio Valverde, Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Buenos Aires, Argentina

Giel E. van Noorden, Division of Plant Science, Research School of Biology, The Australian National University, Canberra, ACT, Australia

Encarna Velázquez, Departamento de Microbiología y Genética and CIALE, Universidad de Salamanca, Salamanca, Spain

Jos Vanderleyden, Department of Microbial and Molecular Systems, Centre of Microbial and Plant Genetics, KU Leuven, Heverlee, Belgium

Alice Vayssières, Institut de Recherche pour le Développement (IRD), UMR DIADE, Montpellier, France

Camille Verly, Institute for Integrative Biology of the Cell, Centre National de la Recherche Scientifique UMR9198, Gif-sur-Yvette, France

Ludovic Vial, UMR CNRS 5557 Ecologie Microbienne, Université de Lyon, Villeurbanne, France

Pablo Vinuesa, Centro de Ciencias Genómicas, Programa de Ingeniería Genómica, Universidad Nacional Autónoma de México, Cuernavaca, México

J.A.C. Vriezen, Department of Biological Sciences, Smith College, Northampton, MA, USA

F. Ann Walker, Department of Chemistry and Biochemistry, University of Arizona, Tucson, AZ, USA

Robert Walker, School of Biomedical Sciences, Faculty of Health Sciences, Curtin University, Bentley, WA, Australia

Luis Wall, Laboratorio Bioquímica, Microbiología e Interacciones Biológicas en el Suelo (LBMIBS), Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Buenos Aires, Argentina

Anton P. Wasson, Division of Plant Science, Research School of Biology, The Australian National University, Canberra, ACT, Australia; CSIRO Plant Industry, Black Mountain Laboratories, Canberra, ACT, Australia

Elizabeth Watkin, School of Biomedical Sciences, Faculty of Health Sciences, Curtin University, Bentley, WA, Australia

Hairong Wei, School of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, USA

JiangQi Wen, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Meredith A. Wilkes, Faculty of Agriculture and Environment, University of Sydney, Sydney, NSW, Australia

Fritz K. Winkler, Laboratory of Biomolecular Research, Paul Scherrer Institut, Villigen, Switzerland

Florence Wisniewski-Dyé, UMR CNRS 5557 Ecologie Microbienne, Université de Lyon, Villeurbanne, France

Tanja Woyke, DOE Joint Genome Institute, Walnut Creek, CA, USA

Fang Xie, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

Yongliang Yan, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Crop Biotechnology, Ministry of Agriculture, Beijing, China

Youssef G. Yanni, Sakha Agricultural Research Station, Kafr El-Sheikh, Egypt

Zeb A. Youard, Department of Biology, ETH, Institute of Microbiology, Department of Biology, Zurich, Switzerland

Christopher K. Yost, Department of Biology, University of Regina, Regina, SK, Canada

Mainassera Zaman-Allah, INRA, UMR Eco&Sols, Montpellier, France; Département de Physiologie Végétale, Université de Niamey, Niamey, Niger

David Zamorano-Sánchez, Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA, USA

María Eugenia Zanetti, Instituto de Biotecnología y Biología Molecular, CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas)-Universidad Nacional de La Plata, La Plata, Argentina

Jonathan P. Zehr, Department of Ocean Sciences, University of California, Santa Cruz, Santa Cruz, CA, USA

Yuhua Zhan, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Crop Biotechnology, Ministry of Agriculture, Beijing, China

Yunhua Zhang, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Crop Biotechnology, Ministry of Agriculture, Beijing, China

Zhongming Zhang, State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China

Patrick Xuechun Zhao, Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK, USA

Igor B. Zhulin, BioEnergy Science Center and Genome Science and Technology Program, University of Tennessee, Oak Ridge National Laboratory, Oak Ridge, TN, USA

Dominik Ziegler, Department of Botany and Plant Biology, Microbiology Unit, University of Geneva, Geneva, Switzerland

Chapter 1

Introduction

Frans J. de Bruijn

INRA-CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM) UMR441-2594, Castanet-Tolosan, France

Nitrogen fixation is a process by which nitrogen (N2) in the atmosphere is converted into ammonia (NH3) (Postgate, 1998). Atmospheric nitrogen or elemental nitrogen (N2) is relatively inert: it does not easily react with other chemicals to form new compounds. Fixation processes free up the nitrogen atoms from their diatomic form (N2) to be used in other ways. Nitrogen fixation, natural and synthetic, is essential for all forms of life because nitrogen is required to biosynthesize basic building blocks of plants, animals, and other life forms, for example, nucleotides for DNA and RNA and amino acids for proteins. Therefore, nitrogen fixation is essential for agriculture and for the manufacture of fertilizer (Free Wikipedia Encyclopedia, Biological Nitrogen Fixation; Postgate, 1998).

Nitrogen fixation also refers to other biological conversions of nitrogen, such as its conversion to nitrogen dioxide. Microorganisms that fix nitrogen are bacteria called diazotrophs (Postgate, 1998). Some higher plants and some animals (termites) have formed associations (symbioses) with diazotrophs.

The first nitrogen-fixing microbe to be discovered was Clostridium pasteurianum obtained by S. Winogradsky in 1893. The second free-living diazotroph Azotobacter chroococcum was first reported by the Dutch microbiologist M.W. Beijerinck in 1901. Symbiotic nitrogen fixation was discovered by the German agronomists H. Hellriegel and H. Willfarth in 1886–1888 (Postgate, 1998).

Biological nitrogen fixation (BNF) occurs when atmospheric nitrogen is converted to ammonia by an enzyme called nitrogenase (Postgate, 1998). The reaction for BNF is as follows:

equation

The process is coupled to the hydrolysis of 16 equivalents of ATP and is accompanied by the coformation of one molecule of H2. In free-living diazotrophs, the nitrogenase-generated ammonium is assimilated into glutamate through the glutamine synthetase/glutamate synthase pathway (Postgate, 1998). Enzymes responsible for nitrogenase action are very susceptible to destruction by oxygen. Many bacteria cease production of the enzyme in the presence of oxygen. Many nitrogen-fixing organisms exist only in anaerobic conditions, respiring to draw down oxygen levels or binding the oxygen with a protein such as leghemoglobin (Free Wikipedia Encyclopedia, Biological Nitrogen Fixation; Postgate, 1998).

1.1 Free-Living Diazotrophs

Anaerobes: These are obligate anaerobes that cannot tolerate oxygen even if they are not fixing nitrogen. They live in habitats that are low in oxygen, such as soils and decaying vegetable matter. Clostridium is an example. Sulfate-reducing bacteria are important in ocean sediments (e.g., Desulfovibrio); some Archean methanogens fix nitrogen in mud and animal intestines, as well as in the deep ocean.

Facultative anaerobes: These species can grow either with or without oxygen, but they only fix nitrogen anaerobically. Often, they respire oxygen as rapidly as it is supplied, keeping the amount of free oxygen low. Examples include Klebsiella pneumoniae, Bacillus polymyxa, Bacillus macerans, and Escherichia intermedia.

Aerobes: These species require oxygen to grow, yet their nitrogenase is still debilitated if exposed to oxygen. Azotobacter vinelandii is the most studied of these organisms. It uses very high respiration rates and protective compounds to prevent oxygen damage. Many other species also reduce the oxygen levels in this way, but with lower respiration rates and lower oxygen tolerance (Free Wikipedia Encyclopedia, Biological Nitrogen Fixation; Postgate, 1998).

Oxygenic photosynthetic bacteria generate oxygen as a by-product of photosynthesis, yet some are able to fix nitrogen as well. These are colonial bacteria that have specialized cells (heterocysts) that lack the oxygen-generating steps of photosynthesis. Examples are Anabaena cylindrica and Nostoc commune. Other cyanobacteria lack heterocysts and can fix nitrogen only in low light and oxygen levels (e.g., Plectonema), or in a diurnal rhythm.

Anoxygenic photosynthetic bacteria do not generate oxygen during photosynthesis, having only a single photosystem that cannot split water. Nitrogenase is expressed under nitrogen limitation. Usually, the expression is regulated via the negative feedback from the produced ammonium ion, but in the absence of N2, the product is not formed and the by-product H2 continues unabated (biohydrogen). The example species are Rhodobacter sphaeroides, Rhodopseudomonas palustris, and Rhodobacter capsulatus (Free Wikipedia Encyclopedia, Biological Nitrogen Fixation; Postgate, 1998).

1.2 Symbiotic Nitrogen-Fixing Bacteria

Rhizobia are Gram-negative with the ability to establish an N2-fixing symbiosis on legume roots and on the stems of some aquatic legumes. During this interaction, bacteroids, as rhizobia are called in the symbiotic state, are contained in intracellular compartments within a specialized organ, the nodule, where they fix N2. Similarly, Frankia, Gram-positive soil bacteria, induce the formation of nitrogen-fixing nodules in actinorhizal plants (Postgate, 1998).

Plants that contribute to nitrogen fixation include the legume family – Fabaceae – with taxa such as kudzu, clovers, soybeans, alfalfa, lupines, and peanuts. They contain symbiotic bacteria called Rhizobia within nodules in their root systems, producing nitrogen compounds that help the plant to grow and compete with other plants. When the plant dies, the fixed nitrogen is released, making it available to other plants and this helps to fertilize the soil. The great majority of legumes have this association, but a few genera (e.g., Styphnolobium) do not. In many traditional and organic farming practices, fields are rotated through various types of crops, which usually includes one consisting mainly or entirely of clover, alfalfa, or buckwheat (nonlegume family Polygonaceae), which are often referred to as green manure (Free Wikipedia Encyclopedia, Biological Nitrogen Fixation).

Legumes also include major food and feed crop species, such as soybean, pea, clover, chickpea, alfalfa, and mung bean. They represent the third largest group of angiosperms and are the second largest group of food and feed crops grown globally. They are cultivated on 12–15% of the available arable land and are responsible for more than 25% of the world's primary crop production with 247 million tons of grain legumes produced annually (European Association for Grain Legume Research, 2007). In addition to food and feed crops, legumes such as soybeans and Pongamia pinnata have gathered a great deal of attention as future sustainable biofuel sources because of their high seed oil content (Ferguson et al., 2010).

Although by far the majority of plants able to form nitrogen-fixing root nodules are in the legume family Fabaceae, there are a few exceptions: Parasponia, a tropical Celtidaceae, is also able to interact with rhizobia and form nitrogen-fixing nodules. Actinorhizal plants, such as alder and bayberry, can also form nitrogen-fixing nodules, thanks to a symbiotic association with Frankia bacteria. These plants belong to 25 genera distributed among 8 plant families. The ability to fix nitrogen is far from universally present in these families. For instance, of 122 genera in the Rosaceae, only 4 genera are capable of fixing nitrogen. All these families belong to the orders Cucurbitales, Fagales, and Rosales, which together with the Fabales form a clade of eurosids. In this clade, Fabales were the first lineage to branch off; thus, the ability to fix nitrogen may be plesiomorphic and subsequently lost in most descendants of the original nitrogen-fixing plant; however, it may be that the basic genetic and physiological requirements were present in an incipient state in the last common ancestors of all these plants, but only evolved to full function in some of them (Free Wikipedia Encyclopedia, Biological Nitrogen Fixation).

1.3 Associative Nitrogen-Fixing Bacteria

Associative nitrogen fixers form a group of mutualist systems in which there is some interdependence between the partners though both can grow satisfactorily apart (Postgate, 1998). They involve grasses (Gramineae) principally. The prospect of finding bacteria that would form associative relationships with rice, other cereals, or graminaceous crops has provoked considerable interest in those diazotrophic bacteria that inhabit the rhizosphere of such plants (Postgate, 1998). In recent years, several types have been reported, for example, species of the new genera Herbaspirillum, Gluconobacter, Azoarcus, and Burkholderia, as well as diazotrophic species of Acetobacter called Acetobacter diazotrophicus (Postgate, 1998).

1.4 Outline of This Book

In this book, the most recent findings about a variety of free-living, associative, or symbiotic diazotrophs are covered, nitrogenase(s) and their mechanism of action and regulation are reviewed, and the use of diazotrophs in agriculture is summarized.

The flow of the chapters is as follows: This chapter is an introduction to the book by the editor, giving the background to the field, describing the flow of sections and chapters and highlighting sections, individual contributions, and some future trends. Section 1 contains a number of focus chapters (reviews) introducing the main topics of the book, including nitrogenases and how they work, evolution and taxonomy of nitrogen-fixing organisms, the evolution of Rhizobium nodulation, and bioengineering nitrogen acquisition in rice. Section 2 covers selected recent advances in the biochemistry of nitrogenases, including the biosynthesis of the FeMo-cofactor (FeMo-co) subunit of nitrogenase, and conserved amino acid sequence features in MoFe, VFe, and FeFe nitrogenases. Section 3 covers the regulation of nitrogen-fixation genes and nitrogenase itself. The chapters in this section will describe regulatory aspects of several different nitrogen-fixing systems, such as A. vinelandii, R. capsulatus, Rhodospirillum rubrum, Pseudomonas stutzeri, and Rhizobium etli. Section 4 covers taxonomic and evolutionary features of nitrogen-fixing organisms, including chapters on taxonomy as well as the origin and diversity of Burkholderia and other beta-rhizobia; the phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium; and a global census of nitrogenases and nitrogen-fixation genes. Section 5 covers the genomics of selected nitrogen-fixing organisms and the comparative analysis of their genomes. Also included are a chapter on the transfer of the symbiotic island of Mesorhizobium loti and a chapter on software program for pan-genomic analysis. Section 6 covers aspects of the physiology and metabolism of nitrogen-fixing organisms and a chapter on the need for photosynthesis for efficient nitrogen fixation in a rhizobial strain, as well as chapters on cytochrome oxidases, the role of BacA in rhizobia, and the analysis of flagellins in Rhizobium leguminosarum. Section 7 contains a number of chapters on the rhizobial life in the rhizosphere of plants, including the effect of plant root exudates, role of quorum sensing and quenching, exopolysaccharides, flavonoids, luminochrome, and the response to various stresses. Section 8 deals with the physiology and regulation of nodulation. Chapters include the root hair as a single cell model for systems biology, two chapters on the conserved genetic program among arbuscular mycorrhizal, actinorhizal, and legume–rhizobial symbiosis, the molecular determinants of nodulation in the Frankia/Discaria symbiosis and the physiology of nitrogen assimilation in the Datisca–Frankia root nodule symbiosis, as well as chapters on the Nod-independent symbiosis in Aeschynomene, the role of phosphorus efficiency, the regulation of nodule development by auxin transport, and the NOOT mutant of Medicago truncatula. Section 9 then initiates a series of chapters on nodulation. This section covers the very early events in nodulation, including putative Nod-factor receptors and signal transduction, early signaling in Frankia, the role of ectopyrases and cellulose CelC2 in nodulation, and calcium spiking. Section 10 addresses the infection and nodule ontogeny topics. A multitude of aspects are covered in this section, which are as follows: Ca²+ signaling and infection thread formation; the role of hormones in nodulation; the role of a transporter in integrating nutrient and hormone signaling with lateral root growth and nodule development; the role of genes encoding MYB coiled-coil and ERF transcription factors; the dissection of the roles in outer and inner root cell layers of plant genes that control rhizobial infection and nodule ontogeny; the multifaceted role of nitric oxide in nodulation; the role of pectate lyase in root infection; the identification of novel M. truncatula genes required for rhizobial invasion and bacteroid differentiation, as well as novel approaches such as RNA-seq; and cortical auxin modeling for nodulation. Section 11 covers the next stage in nodule biology, namely, the development of bacteroids required for nitrogen fixation and the proteomic profile of the soybean symbiosome membrane. Section 12 addresses briefly N-assimilation (ammonium transport) in nodules and nodule senescence. In Section 13, several Omics applications in rhizobia and Frankia (metagenomics, transcriptomics, proteomics, genomics) are discussed, such as the metagenomic analysis of microsymbiont selection by the legume host plant, proteomic profiling of Rhizobium tropici, the Frankia alni symbiotic transcriptome, a comprehensive survey of the Rhizobiales using high-throughput DNA sequencing and gene-targeted metagenomics of diazotrophs in coastal saline soil. Section 14 does the same with (host) plant genomics, proteomics, and transcriptomics, including chapters on the M. truncatula genome, retrotransposon Tnt1 mutagenesis, leveraging large-scale approaches to dissect legume genomics and the Rhizobium–legume symbiosis, databases, and functional genomics of symbiotic nitrogen fixation in legumes. In