title: Rhizobium-legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS.
abstract: The occurrence of alternative Nod factor (NF)-independent symbiosis between legumes and rhizobia was first demonstrated in some Aeschynomene species that are nodulated by photosynthetic bradyrhizobia lacking the canonical nodABC genes. In this study, we revealed that a large diversity of non-photosynthetic bradyrhizobia, including B. elkanii, was also able to induce nodules on the NF-independent Aeschynomene species, A. indica. Using cytological analysis of the nodules and the nitrogenase enzyme activity as markers, a gradient in the symbiotic interaction between bradyrhizobial strains and A. indica could be distinguished. This ranged from strains that induced nodules that were only infected intercellularly to rhizobial strains that formed nodules in which the host cells were invaded intracellularly and that displayed a weak nitrogenase activity. In all non-photosynthetic bradyrhizobia, the type III secretion system (T3SS) appears required to trigger nodule organogenesis. In contrast, genome sequence analysis revealed that apart from a few exceptions, like the Bradyrhizobium ORS285 strain, photosynthetic bradyrhizobia strains lack a T3SS. Furthermore, analysis of the symbiotic properties of an ORS285 T3SS mutant revealed that the T3SS could have a positive or negative role for the interaction with NF-dependent Aeschynomene species, but that it is dispensable for the interaction with all NF-independent Aeschynomene species tested. Taken together, these data indicate that two NF-independent symbiotic processes are possible between legumes and rhizobia: one dependent on a T3SS and one using a so far unknown mechanism.
authors.affiliation: Department of International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Tokyo, Japan.
authors.forename: Shin
authors.initials: S
authors.lastname: Okazaki
authors.affiliation: Institute of Agricultural Technology, School of Biotechnology, Suranaree University of Technology, Nakhon Ratchasima, Thailand.
authors.forename: Panlada
authors.initials: P
authors.lastname: Tittabutr
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Albin
authors.initials: A
authors.lastname: Teulet
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Julien
authors.initials: J
authors.lastname: Thouin
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Joël
authors.initials: J
authors.lastname: Fardoux
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Clémence
authors.initials: C
authors.lastname: Chaintreuil
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Djamel
authors.initials: D
authors.lastname: Gully
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Arrighi
authors.affiliation: Department of International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Tokyo, Japan.
authors.forename: Noriyuki
authors.initials: N
authors.lastname: Furuta
authors.affiliation: Department of International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Tokyo, Japan.
authors.forename: Hiroki
authors.initials: H
authors.lastname: Miwa
authors.affiliation: Department of International Environmental and Agricultural Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Tokyo, Japan.
authors.forename: Michiko
authors.initials: M
authors.lastname: Yasuda
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Nico
authors.initials: N
authors.lastname: Nouwen
authors.affiliation: Institute of Agricultural Technology, School of Biotechnology, Suranaree University of Technology, Nakhon Ratchasima, Thailand.
authors.forename: Neung
authors.initials: N
authors.lastname: Teaumroong
authors.affiliation: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, Campus International de Baillarguet, TA A-82/J, Montpellier, France.
authors.forename: Eric
authors.initials: E
authors.lastname: Giraud
mesh_terms: D005075:Biological Evolution; D020369:Bradyrhizobium / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D004269:DNA, Bacterial / Q000032:analysis; D007887:Fabaceae / Q000382:microbiology*; D016680:Genome, Bacterial; D009591:Nitrogenase / Q000378:metabolism; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D012336:RNA, Ribosomal, 16S / Q000032:analysis; D017422:Sequence Analysis, DNA; D013559:Symbiosis / Q000235:genetics*
chemical_list: D004269:DNA, Bacterial; D012336:RNA, Ribosomal, 16S; D009591:Nitrogenase