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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}mpl.ird.fr; sadowsky{at}umn.edu.
  • E.G. and M.S. coordinated the sequence annotation of the Bradyrhizobium ORS278 and BTAi1 genomes, respectively.

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.

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

    Citation:

    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).

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