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Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia

Science, 1 June 2007
Vol. 316, Issue 5829, p. 1307-1312
DOI: 10.1126/science.1139548

Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia

  1. Eric Giraud1,*,,
  2. Lionel Moulin1,
  3. David Vallenet2,
  4. Valérie Barbe3,
  5. Eddie Cytryn4,
  6. Jean-Christophe Avarre1,
  7. Marianne Jaubert1,
  8. Damien Simon1,
  9. Fabienne Cartieaux1,
  10. Yves Prin1,
  11. Gilles Bena1,
  12. Laure Hannibal1,
  13. Joel Fardoux1,
  14. Mila Kojadinovic5,
  15. Laurie Vuillet1,
  16. Aurélie Lajus2,
  17. Stéphane Cruveiller2,
  18. Zoe Rouy2,
  19. Sophie Mangenot3,
  20. Béatrice Segurens3,
  21. Carole Dossat3,
  22. William L. Franck6,
  23. Woo-Suk Chang6,
  24. Elizabeth Saunders7,
  25. David Bruce7,
  26. Paul Richardson8,
  27. Philippe Normand9,
  28. Bernard Dreyfus1,
  29. David Pignol5,
  30. Gary Stacey6,
  31. David Emerich6,
  32. André Verméglio5,
  33. Claudine Médigue2,
  34. Michael Sadowsky4,*,
  1. 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. 2 Genoscope, CNRS–UMR 8030, Atelier de Génomique Comparative, 2 rue Gaston Crémieux BP5706, 91057 Evry Cedex, France.
  3. 3 Genoscope, Centre National de Séquençage, 2 rue Gaston Crémieux BP5706, 91057 Evry Cedex, France.
  4. 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. 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. 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. 7 U.S. Department of Energy (DOE) Joint Genome Institute, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.
  8. 8 DOE Joint Genome Institute, Walnut Creek, CA 94598, USA.
  9. 9 Université Lyon1, CNRS, UMR 5557, Ecologie Microbienne, Lyon, F-69003, France.
  1. * To whom correspondence should be addressed. E-mail: giraud{at}; sadowsky{at}
  • E.G. and M.S. coordinated the sequence annotation of the Bradyrhizobium ORS278 and BTAi1 genomes, respectively.


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.

    • Received for publication 4 January 2007.
    • Accepted for publication 12 April 2007.


    E. Giraud, L. Moulin, D. Vallenet, V. Barbe, E. Cytryn, J.-C. Avarre, M. Jaubert, D. Simon, F. Cartieaux, Y. Prin, G. Bena, L. Hannibal, J. Fardoux, M. Kojadinovic, L. Vuillet, A. Lajus, S. Cruveiller, Z. Rouy, S. Mangenot, B. Segurens, C. Dossat, W. L. Franck, W.-S. Chang, E. Saunders, D. Bruce, P. Richardson, P. Normand, B. Dreyfus, D. Pignol, G. Stacey, D. Emerich, A. Verméglio, C. Médigue, and M. Sadowsky, Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia. Science 316, 1307-1312 (2007).

    Symbiosis Island Shuffling with Abundant Insertion Sequences in the Genomes of Extra-Slow-Growing Strains of Soybean Bradyrhizobia
    T. Iida, M. Itakura, M. Anda, M. Sugawara, T. Isawa, T. Okubo, S. Sato, K. Chiba-Kakizaki, and K. Minamisawa
    Appl. Environ. Microbiol. 81, 4143-4154 (15 June 2015)

    A novel family of integrases associated with prophages and genomic islands integrated within the tRNA-dihydrouridine synthase A (dusA) gene
    D. N. Farrugia, L. D. H. Elbourne, B. C. Mabbutt, and I. T. Paulsen
    Nucleic Acids Res 43, 4547-4557 (19 May 2015)

    Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa)
    L. D. H. Elbourne, B. C. Mabbutt, and I. T. Paulsen
    FEMS Microbiol Ecol 91, 1-17 (1 February 2015)

    Characterization of p-Hydroxycinnamate Catabolism in a Soil Actinobacterium
    H. Otani, Y.-E. Lee, I. Casabon, and L. D. Eltis
    J. Bacteriol. 196, 4293-4303 (15 December 2014)

    Genetic Diversity and Evolution of Bradyrhizobium Populations Nodulating Erythrophleum fordii, an Evergreen Tree Indigenous to the Southern Subtropical Region of China
    Y. Yao, R. Wang, J. K. Lu, X. H. Sui, E. T. Wang, and W. X. Chen
    Appl. Environ. Microbiol. 80, 6184-6194 (1 October 2014)

    Genetic Divergence of Bradyrhizobium Strains Nodulating Soybeans as Revealed by Multilocus Sequence Analysis of Genes Inside and Outside the Symbiosis Island
    X. X. Zhang, H. J. Guo, R. Wang, X. H. Sui, Y. M. Zhang, E. T. Wang, C. F. Tian, and W. X. Chen
    Appl. Environ. Microbiol. 80, 3181-3190 (15 May 2014)

    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
    Appl. Environ. Microbiol. 80, 1245-1255 (15 February 2014)

    From {beta}- to {alpha}-Proteobacteria: The Origin and Evolution of Rhizobial Nodulation Genes nodIJ
    S. Aoki, M. Ito, and W. Iwasaki
    Mol Biol Evol 30, 2494-2508 (1 November 2013)

    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, J. A. Fish, T. Kwon Lee, Y. Sun, J. M. Tiedje, and J. R. Cole
    mBio 4, e00592-13-e00592-13 (17 September 2013)

    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.
    Genome Biol Evol 5, 934-953 (10 May 2013)

    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.
    Appl. Environ. Microbiol. 79, 2542-2551 (15 April 2013)

    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
    Appl. Environ. Microbiol. 79, 2459-2462 (1 April 2013)

    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.
    Nucleic Acids Res 41, D636-D647 (1 January 2013)

    Evolution of Bradyrhizobium-Aeschynomene Mutualism: Living Testimony of the Ancient World or Highly Evolved State?
    T. Okubo, S. Fukushima, and K. Minamisawa
    Plant Cell Physiol 53, 2000-2007 (1 December 2012)

    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
    Appl. Environ. Microbiol. 78, 6236-6250 (1 September 2012)

    Phylogenetic clustering of Bradyrhizobium symbionts on legumes indigenous to North America
    J. H. Koppell, and M. A. Parker
    Microbiology 158, 2050-2059 (1 August 2012)

    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.
    Proc. Natl. Acad. Sci. USA 109, 8629-8634 (29 May 2012)

    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
    Appl. Environ. Microbiol. 78, 1692-1700 (15 March 2012)

    Phylogenetic relationship of Lotus uliginosus symbionts with bradyrhizobia nodulating genistoid legumes
    M. J. Lorite, I. Videira e Castro, S. Munoz, and J. Sanjuan
    FEMS Microbiol Ecol 79, 454-564 (1 February 2012)

    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
    Int. J. Syst. Evol. Microbiol. 61, 3052-3067 (1 December 2011)

    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
    Int. J. Syst. Evol. Microbiol. 61, 3089-3093 (1 December 2011)

    purL gene expression affects biofilm formation and symbiotic persistence of Photorhabdus temperata in the nematode Heterorhabditis bacteriophora
    R. An, and P. S. Grewal
    Microbiology 157, 2595-2603 (1 September 2011)

    The purL gene of Bacillus subtilis is associated with nematicidal activity
    Y. Xia, S. Xie, X. Ma, H. Wu, X. Wang, and X. Gao
    FEMS Microbiol Lett 322, 99-107 (1 September 2011)

    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
    Proc. Natl. Acad. Sci. USA 108, 7183-7188 (26 April 2011)

    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
    Appl. Environ. Microbiol. 76, 4185-4193 (1 July 2010)

    Thiosulfate-Dependent Chemolithoautotrophic Growth of Bradyrhizobium japonicum
    S. Masuda, S. Eda, S. Ikeda, H. Mitsui, and K. Minamisawa
    Appl. Environ. Microbiol. 76, 2402-2409 (15 April 2010)

    The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots
    J. A. Downie, S. Eda, S. Ikeda, H. Mitsui, and K. Minamisawa
    FEMS Microbiol Rev 34, 150-170 (1 March 2010)

    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.
    Int. J. Syst. Evol. Microbiol. 60, 664-674 (1 March 2010)

    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.
    DNA Res 17, 37-50 (1 February 2010)

    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
    Appl. Environ. Microbiol. 75, 5012-5017 (1 August 2009)

    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.
    Appl. Environ. Microbiol. 75, 4035-4045 (15 June 2009)

    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
    J. Bacteriol. 191, 2133-2143 (1 April 2009)

    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
    Appl. Environ. Microbiol. 75, 1088-1098 (15 February 2009)

    De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis
    M. Crespi, and F. Frugier
    Sci Signal 1, re11-re11 (9 December 2008)

    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
    J. Bacteriol. 190, 6568-6579 (15 October 2008)

    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.
    DNA Res 15, 297-308 (1 October 2008)

    Root-Microbe Communication through Protein Secretion
    C. De-la-Pena, Z. Lei, B. S. Watson, L. W. Sumner, and J. M. Vivanco
    J Biol Chem 283, 25247-25255 (12 September 2008)

    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.
    Genome Res 18, 1472-1483 (1 September 2008)

    60Ma of legume nodulation. What's new? What's changing?
    J. I. Sprent, G. Pascal, S. Mangenot, M. Glew, C. Bontemps, D. Capela, S. Carrere, S. Cruveiller, C. Dossat, A. Lajus et al.
    J Exp Bot 59, 1081-1084 (1 March 2008)

    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
    DNA Res 15, 13-23 (1 February 2008)

    Advances in environmental genomics: towards an integrated view of micro-organisms and ecosystems
    P. N. Bertin, C. Medigue, and P. Normand
    Microbiology 154, 347-359 (1 February 2008)

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    S. Radutoiu, L. H. Madsen, E. B. Madsen, A. Jurkiewicz, E. Fukai, E. M. Quistgaard, A. S. Albrektsen, E. K. James, S. Thirup, J. Stougaard et al.
    EMBO J. 26, 3923-3935 (5 September 2007)

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    J. A. Downie, L. H. Madsen, E. B. Madsen, A. Jurkiewicz, E. Fukai, E. M. Quistgaard, A. S. Albrektsen, E. K. James, S. Thirup, J. Stougaard et al.
    Science 316, 1296-1297 (1 June 2007)

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