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A Peptidoglycan-Remodeling Enzyme Is Critical for Bacteroid Differentiation in Bradyrhizobium spp. During Legume Symbiosis.

Authors
  • Gully, Djamel1
  • Gargani, Daniel2
  • Bonaldi, Katia3
  • Grangeteau, Cédric4
  • Chaintreuil, Clémence1
  • Fardoux, Joël1
  • Nguyen, Phuong1
  • Marchetti, Roberta5
  • Nouwen, Nico1
  • Molinaro, Antonio5
  • Mergaert, Peter6
  • Giraud, Eric1
  • 1 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; , (France)
  • 2 2 CIRAD, UMR BGPI, F-34398 Montpellier, France; , (France)
  • 3 3 Center for Chronobiology, Division of Biological Sciences, 9500 Gilman Drive, University of California San Diego, La Jolla, CA 92093, U.S.A.;
  • 4 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; , (France)
  • 5 5 Dipartimento di Scienze Chimiche, Complesso Universitario Monte Sant'Angelo, Università di Napoli Federico II, Via Cintia 4, I-80126 Napoli, Italy; and. , (Italy)
  • 6 6 Institute for Integrative Biology of the Cell, UMR 9198, CNRS/Université Paris-Sud/CEA, Gif-sur-Yvette, France. , (France)
Type
Published Article
Journal
Molecular Plant-Microbe Interactions
Publisher
Scientific Societies
Publication Date
Jun 01, 2016
Volume
29
Issue
6
Pages
447–457
Identifiers
DOI: 10.1094/MPMI-03-16-0052-R
PMID: 26959836
Source
Medline
Language
English
License
Unknown

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.

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