title: A Peptidoglycan-Remodeling Enzyme Is Critical for Bacteroid Differentiation in Bradyrhizobium spp. During Legume Symbiosis.
abstract: In response to the presence of compatible rhizobium bacteria, legumes form symbiotic organs called nodules on their roots. These nodules house nitrogen-fixing bacteroids that are a differentiated form of the rhizobium bacteria. In some legumes, the bacteroid differentiation comprises a dramatic cell enlargement, polyploidization, and other morphological changes. Here, we demonstrate that a peptidoglycan-modifying enzyme in Bradyrhizobium strains, a DD-carboxypeptidase that contains a peptidoglycan-binding SPOR domain, is essential for normal bacteroid differentiation in Aeschynomene species. The corresponding mutants formed bacteroids that are malformed and hypertrophied. However, in soybean, a plant that does not induce morphological differentiation of its symbiont, the mutation does not affect the bacteroids. Remarkably, the mutation also leads to necrosis in a large fraction of the Aeschynomene nodules, indicating that a normally formed peptidoglycan layer is essential for avoiding the induction of plant immune responses by the invading bacteria. In addition to exopolysaccharides, capsular polysaccharides, and lipopolysaccharides, whose role during symbiosis is well defined, our work demonstrates an essential role in symbiosis for yet another rhizobial envelope component, the peptidoglycan layer.
authors.affiliation: 1 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, 34398 Montpellier Cedex 5, France;
authors.forename: Djamel
authors.initials: D
authors.lastname: Gully
authors.affiliation: 2 CIRAD, UMR BGPI, F-34398 Montpellier, France;
authors.forename: Daniel
authors.initials: D
authors.lastname: Gargani
authors.affiliation: 3 Center for Chronobiology, Division of Biological Sciences, 9500 Gilman Drive, University of California San Diego, La Jolla, CA 92093, U.S.A.;
authors.forename: Katia
authors.initials: K
authors.lastname: Bonaldi
authors.affiliation: 4 UMR Procédés Alimentaires et Microbiologiques, Equipe VAlMiS (Vin, Aliment, Microbiologie, Stress), AgroSup Dijon - Université de Bourgogne Franche-Comté, IUVV, Rue Claude Ladrey, BP 27877, 21000 Dijon, France;
authors.forename: Cédric
authors.initials: C
authors.lastname: Grangeteau
authors.affiliation: 1 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, 34398 Montpellier Cedex 5, France;
authors.forename: Clémence
authors.initials: C
authors.lastname: Chaintreuil
authors.affiliation: 1 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, 34398 Montpellier Cedex 5, France;
authors.forename: Joël
authors.initials: J
authors.lastname: Fardoux
authors.affiliation: 1 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, 34398 Montpellier Cedex 5, France;
authors.forename: Phuong
authors.initials: P
authors.lastname: Nguyen
authors.affiliation: 5 Dipartimento di Scienze Chimiche, Complesso Universitario Monte Sant'Angelo, Università di Napoli Federico II, Via Cintia 4, I-80126 Napoli, Italy; and.
authors.forename: Roberta
authors.initials: R
authors.lastname: Marchetti
authors.affiliation: 1 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, 34398 Montpellier Cedex 5, France;
authors.forename: Nico
authors.initials: N
authors.lastname: Nouwen
authors.affiliation: 5 Dipartimento di Scienze Chimiche, Complesso Universitario Monte Sant'Angelo, Università di Napoli Federico II, Via Cintia 4, I-80126 Napoli, Italy; and.
authors.forename: Antonio
authors.initials: A
authors.lastname: Molinaro
authors.affiliation: 6 Institute for Integrative Biology of the Cell, UMR 9198, CNRS/Université Paris-Sud/CEA, Gif-sur-Yvette, France.
authors.forename: Peter
authors.initials: P
authors.lastname: Mergaert
authors.affiliation: 1 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, 34398 Montpellier Cedex 5, France;
authors.forename: Eric
authors.initials: E
authors.lastname: Giraud
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D001665:Binding Sites; D020369:Bradyrhizobium / Q000502:physiology*; D007887:Fabaceae / Q000382:microbiology*; D015964:Gene Expression Regulation, Bacterial; D009154:Mutation; D010457:Peptidoglycan / Q000378:metabolism*; D010788:Photosynthesis; D013559:Symbiosis / Q000502:physiology*
chemical_list: D001426:Bacterial Proteins; D010457:Peptidoglycan