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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}; sadowsky{at}

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