Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 316 (5829): 1307-1312

Copyright © 2007 by the American Association for the Advancement of Science

Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia

Eric Giraud,1*{dagger} Lionel Moulin,1 David Vallenet,2 Valérie Barbe,3 Eddie Cytryn,4 Jean-Christophe Avarre,1 Marianne Jaubert,1 Damien Simon,1 Fabienne Cartieaux,1 Yves Prin,1 Gilles Bena,1 Laure Hannibal,1 Joel Fardoux,1 Mila Kojadinovic,5 Laurie Vuillet,1 Aurélie Lajus,2 Stéphane Cruveiller,2 Zoe Rouy,2 Sophie Mangenot,3 Béatrice Segurens,3 Carole Dossat,3 William L. Franck,6 Woo-Suk Chang,6 Elizabeth Saunders,7 David Bruce,7 Paul Richardson,8 Philippe Normand,9 Bernard Dreyfus,1 David Pignol,5 Gary Stacey,6 David Emerich,6 André Verméglio,5 Claudine Médigue,2 Michael Sadowsky4*{dagger}

Abstract: Leguminous plants (such as peas and soybeans) and rhizobial soil bacteria are symbiotic partners that communicate through molecular signaling pathways, resulting in the formation of nodules on legume roots and occasionally stems that house nitrogen-fixing bacteria. Nodule formation has been assumed to be exclusively initiated by the binding of bacterial, host-specific lipochito-oligosaccharidic Nod factors, encoded by the nodABC genes, to kinase-like receptors of the plant. Here we show by complete genome sequencing of two symbiotic, photosynthetic, Bradyrhizobium strains, BTAi1 and ORS278, that canonical nodABC genes and typical lipochito-oligosaccharidic Nod factors are not required for symbiosis in some legumes. Mutational analyses indicated that these unique rhizobia use an alternative pathway to initiate symbioses, where a purine derivative may play a key role in triggering nodule formation.

1 Laboratoire des Symbioses Tropicales et Méditerranéennes, Unité mixte recherche (UMR) 113, Institut de Recherche pour le Développement, Centre de Coopération International en Recherche Agronomique pour le Développement, AGRO Montpellier, Institut National de la Recherche Agronomique, Université Montpellier 2, TA A-82/J, Campus de Baillarguet, 34398 Montpellier Cedex 5, France.
2 Genoscope, CNRS–UMR 8030, Atelier de Génomique Comparative, 2 rue Gaston Crémieux BP5706, 91057 Evry Cedex, France.
3 Genoscope, Centre National de Séquençage, 2 rue Gaston Crémieux BP5706, 91057 Evry Cedex, France.
4 Department of Soil, Water, and Climate; BioTechnology Institute; and Microbial and Plant Genomics Institute, University of Minnesota, 1991 Upper Buford Circle, 439 BorH, St. Paul, MN, 55108, USA.
5 Commissariat à l'Energie Atomique (CEA) Cadarache, Direction des Sciences du Vivant, Institut de Biologie Environnementale et Biotechnologie, Service de Biologie Végétale et de Microbiologie Environnementale, Laboratoire de Bioénenergétique Cellulaire (DSV/IBEB/SBVME/LBC), UMR 6191 CNRS/CEA/Université Aix-Marseille, Saint-Paul-lez-Durance, F-13108 France.
6 National Center for Soybean Biotechnology, Divisions of Plant Sciences and Biochemistry, Department of Molecular Microbiology and Immunology, University of Missouri, Columbia, MO, 65211, USA.
7 U.S. Department of Energy (DOE) Joint Genome Institute, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.
8 DOE Joint Genome Institute, Walnut Creek, CA 94598, USA.
9 Université Lyon1, CNRS, UMR 5557, Ecologie Microbienne, Lyon, F-69003, France.

{dagger} E.G. and M.S. coordinated the sequence annotation of the Bradyrhizobium ORS278 and BTAi1 genomes, respectively.

* To whom correspondence should be addressed. E-mail: giraud{at}mpl.ird.fr; sadowsky{at}umn.edu.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Replicon-Dependent Differentiation of Symbiosis-Related Genes in Sinorhizobium Strains Nodulating Glycine max.
H. J. Guo, E. T. Wang, X. X. Zhang, Q. Q. Li, Y. M. Zhang, C. F. Tian, and W. X. Chen (2014)
Appl. Envir. Microbiol. 80, 1245-1255
   Abstract »    Full Text »    PDF »
From {beta}- to {alpha}-Proteobacteria: The Origin and Evolution of Rhizobial Nodulation Genes nodIJ.
S. Aoki, M. Ito, and W. Iwasaki (2013)
Mol. Biol. Evol. 30, 2494-2508
   Abstract »    Full Text »    PDF »
Ecological Patterns of nifH Genes in Four Terrestrial Climatic Zones Explored with Targeted Metagenomics Using FrameBot, a New Informatics Tool.
Q. Wang, J. F. Quensen III, J. A. Fish, T. Kwon Lee, Y. Sun, J. M. Tiedje, and J. R. Cole (2013)
mBio 4, e00592-13
   Abstract »    Full Text »    PDF »
Life in an Arsenic-Containing Gold Mine: Genome and Physiology of the Autotrophic Arsenite-Oxidizing Bacterium Rhizobium sp. NT-26.
J. Andres, F. Arsene-Ploetze, V. Barbe, C. Brochier-Armanet, J. Cleiss-Arnold, J.-Y. Coppee, M.-A. Dillies, L. Geist, A. Joublin, S. Koechler, et al. (2013)
Genome Biol Evol 5, 934-953
   Abstract »    Full Text »    PDF »
Genome Analysis Suggests that the Soil Oligotrophic Bacterium Agromonas oligotrophica (Bradyrhizobium oligotrophicum) Is a Nitrogen-Fixing Symbiont of Aeschynomene indica.
T. Okubo, S. Fukushima, M. Itakura, K. Oshima, A. Longtonglang, N. Teaumroong, H. Mitsui, M. Hattori, R. Hattori, T. Hattori, et al. (2013)
Appl. Envir. Microbiol. 79, 2542-2551
   Abstract »    Full Text »    PDF »
Photosynthetic Bradyrhizobium sp. Strain ORS285 Is Capable of Forming Nitrogen-Fixing Root Nodules on Soybeans (Glycine max).
E. Giraud, L. Xu, C. Chaintreuil, D. Gargani, D. Gully, and M. J. Sadowsky (2013)
Appl. Envir. Microbiol. 79, 2459-2462
   Abstract »    Full Text »    PDF »
MicroScope--an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data.
D. Vallenet, E. Belda, A. Calteau, S. Cruveiller, S. Engelen, A. Lajus, F. Le Fevre, C. Longin, D. Mornico, D. Roche, et al. (2013)
Nucleic Acids Res. 41, D636-D647
   Abstract »    Full Text »    PDF »
Evolution of Bradyrhizobium-Aeschynomene Mutualism: Living Testimony of the Ancient World or Highly Evolved State?.
T. Okubo, S. Fukushima, and K. Minamisawa (2012)
Plant Cell Physiol. 53, 2000-2007
   Abstract »    Full Text »    PDF »
Genetic Diversity, Symbiotic Evolution, and Proposed Infection Process of Bradyrhizobium Strains Isolated from Root Nodules of Aeschynomene americana L. in Thailand.
R. Noisangiam, K. Teamtisong, P. Tittabutr, N. Boonkerd, U. Toshiki, K. Minamisawa, and N. Teaumroong (2012)
Appl. Envir. Microbiol. 78, 6236-6250
   Abstract »    Full Text »    PDF »
Phylogenetic clustering of Bradyrhizobium symbionts on legumes indigenous to North America.
J. H. Koppell and M. A. Parker (2012)
Microbiology 158, 2050-2059
   Abstract »    Full Text »    PDF »
Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations.
C. F. Tian, Y. J. Zhou, Y. M. Zhang, Q. Q. Li, Y. Z. Zhang, D. F. Li, S. Wang, J. Wang, L. B. Gilbert, Y. R. Li, et al. (2012)
PNAS 109, 8629-8634
   Abstract »    Full Text »    PDF »
New Betaproteobacterial Rhizobium Strains Able To Efficiently Nodulate Parapiptadenia rigida (Benth.) Brenan.
C. Taule, M. Zabaleta, C. Mareque, R. Platero, L. Sanjurjo, M. Sicardi, L. Frioni, F. Battistoni, and E. Fabiano (2012)
Appl. Envir. Microbiol. 78, 1692-1700
   Abstract »    Full Text »    PDF »
International Committee on Systematics of Prokaryotes * Subcommittee on the taxonomy of Agrobacterium and Rhizobium: Minutes of the meeting, 7 September 2010, Geneva, Switzerland.
K. Lindstrom and J. P. W. Young (2011)
Int J Syst Evol Microbiol 61, 3089-3093
   Full Text »    PDF »
Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer.
P. Menna and M. Hungria (2011)
Int J Syst Evol Microbiol 61, 3052-3067
   Abstract »    Full Text »    PDF »
purL gene expression affects biofilm formation and symbiotic persistence of Photorhabdus temperata in the nematode Heterorhabditis bacteriophora.
R. An and P. S. Grewal (2011)
Microbiology 157, 2595-2603
   Abstract »    Full Text »    PDF »
Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia.
N. A. Ahlgren, C. S. Harwood, A. L. Schaefer, E. Giraud, and E. P. Greenberg (2011)
PNAS 108, 7183-7188
   Abstract »    Full Text »    PDF »
Disruption of the Glycine Cleavage System Enables Sinorhizobium fredii USDA257 To Form Nitrogen-Fixing Nodules on Agronomically Improved North American Soybean Cultivars.
J. C. Lorio, W.-S. Kim, A. H. Krishnan, and H. B. Krishnan (2010)
Appl. Envir. Microbiol. 76, 4185-4193
   Abstract »    Full Text »    PDF »
Thiosulfate-Dependent Chemolithoautotrophic Growth of Bradyrhizobium japonicum.
S. Masuda, S. Eda, S. Ikeda, H. Mitsui, and K. Minamisawa (2010)
Appl. Envir. Microbiol. 76, 2402-2409
   Abstract »    Full Text »    PDF »
Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov..
C. Merabet, M. Martens, M. Mahdhi, F. Zakhia, A. Sy, C. Le Roux, O. Domergue, R. Coopman, A. Bekki, M. Mars, et al. (2010)
Int J Syst Evol Microbiol 60, 664-674
   Abstract »    Full Text »    PDF »
Complete Genomic Structure of the Cultivated Rice Endophyte Azospirillum sp. B510.
T. Kaneko, K. Minamisawa, T. Isawa, H. Nakatsukasa, H. Mitsui, Y. Kawaharada, Y. Nakamura, A. Watanabe, K. Kawashima, A. Ono, et al. (2010)
DNA Res 17, 37-50
   Abstract »    Full Text »    PDF »
Aerobic Vanillate Degradation and C1 Compound Metabolism in Bradyrhizobium japonicum.
N. Sudtachat, N. Ito, M. Itakura, S. Masuda, S. Eda, H. Mitsui, Y. Kawaharada, and K. Minamisawa (2009)
Appl. Envir. Microbiol. 75, 5012-5017
   Abstract »    Full Text »    PDF »
Rhizobium sp. Strain NGR234 Possesses a Remarkable Number of Secretion Systems.
C. Schmeisser, H. Liesegang, D. Krysciak, N. Bakkou, A. Le Quere, A. Wollherr, I. Heinemeyer, B. Morgenstern, A. Pommerening-Roser, M. Flores, et al. (2009)
Appl. Envir. Microbiol. 75, 4035-4045
   Abstract »    Full Text »    PDF »
Role of Potassium Uptake Systems in Sinorhizobium meliloti Osmoadaptation and Symbiotic Performance.
A. Dominguez-Ferreras, S. Munoz, J. Olivares, M. J. Soto, and J. Sanjuan (2009)
J. Bacteriol. 191, 2133-2143
   Abstract »    Full Text »    PDF »
Genetic Diversity and Host Range of Rhizobia Nodulating Lotus tenuis in Typical Soils of the Salado River Basin (Argentina).
M. J. Estrella, S. Munoz, M. J. Soto, O. Ruiz, and J. Sanjuan (2009)
Appl. Envir. Microbiol. 75, 1088-1098
   Abstract »    Full Text »    PDF »
De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis.
M. Crespi and F. Frugier (2008)
Science Signaling 1, re11
   Abstract »    Full Text »    PDF »
Comprehensive Assessment of the Regulons Controlled by the FixLJ-FixK2-FixK1 Cascade in Bradyrhizobium japonicum.
S. Mesa, F. Hauser, M. Friberg, E. Malaguti, H.-M. Fischer, and H. Hennecke (2008)
J. Bacteriol. 190, 6568-6579
   Abstract »    Full Text »    PDF »
Construction of Signature-tagged Mutant Library in Mesorhizobium loti as a Powerful Tool for Functional Genomics.
Y. Shimoda, H. Mitsui, H. Kamimatsuse, K. Minamisawa, E. Nishiyama, Y. Ohtsubo, Y. Nagata, M. Tsuda, S. Shinpo, A. Watanabe, et al. (2008)
DNA Res 15, 297-308
   Abstract »    Full Text »    PDF »
Root-Microbe Communication through Protein Secretion.
C. De-la-Pena, Z. Lei, B. S. Watson, L. W. Sumner, and J. M. Vivanco (2008)
J. Biol. Chem. 283, 25247-25255
   Abstract »    Full Text »    PDF »
Genome sequence of the {beta}-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia.
C. Amadou, G. Pascal, S. Mangenot, M. Glew, C. Bontemps, D. Capela, S. Carrere, S. Cruveiller, C. Dossat, A. Lajus, et al. (2008)
Genome Res. 18, 1472-1483
   Abstract »    Full Text »    PDF »
60Ma of legume nodulation. What's new? What's changing?.
J. I. Sprent (2008)
J. Exp. Bot. 59, 1081-1084
   Abstract »    Full Text »    PDF »
Advances in environmental genomics: towards an integrated view of micro-organisms and ecosystems.
P. N. Bertin, C. Medigue, and P. Normand (2008)
Microbiology 154, 347-359
   Abstract »    Full Text »    PDF »
A Large Scale Analysis of Protein-Protein Interactions in the Nitrogen-fixing Bacterium Mesorhizobium loti.
Y. Shimoda, S. Shinpo, M. Kohara, Y. Nakamura, S. Tabata, and S. Sato (2008)
DNA Res 15, 13-23
   Abstract »    Full Text »    PDF »
LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range.
S. Radutoiu, L. H. Madsen, E. B. Madsen, A. Jurkiewicz, E. Fukai, E. M. Quistgaard, A. S. Albrektsen, E. K. James, S. Thirup, and J. Stougaard (2007)
EMBO J. 26, 3923-3935
   Abstract »    Full Text »    PDF »
PLANT SCIENCE: Infectious Heresy.
J. A. Downie (2007)
Science 316, 1296-1297
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882