Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

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  • Rafal Zgadzaj, Max Planck Inst Plant Breeding Res, Max Planck Society, Dept Plant Microbe Interact, Carbohydrate Recognit & Signaling Ctr
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  • Ruben Garrido-Oter, Heinrich Heine Univ Duesseldorf, Heinrich Heine University Dusseldorf, Dept Algorithm Bioinformat
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  • Dorthe Bodker Jensen
  • Anna Koprivova, Univ Cologne, University of Cologne, Cologne Bioctr, Bot Inst
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  • Paul Schulze-Lefert, Heinrich Heine Univ Duesseldorf, Heinrich Heine University Dusseldorf, Cluster Excellence Plant Sci
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  • Simona Radutoiu

Lotus japonicus has been used for decades as a model legume to study the establishment of binary symbiotic relationships with nitrogen-fixing rhizobia that trigger root nodule organogenesis for bacterial accommodation. Using community profiling of 16S rRNA gene amplicons, we reveal that in Lotus, distinctive noduleand root-inhabiting communities are established by parallel, rather than consecutive, selection of bacteria from the rhizosphere and root compartments. Comparative analyses of wild-type (WT) and symbiotic mutants in Nod factor receptor5 (nfr5), Nodule inception (nin) and Lotus histidine kinase1 (lhk1) genes identified a previously unsuspected role of the nodulation pathway in the establishment of different bacterial assemblages in the root and rhizosphere. We found that the loss of nitrogen-fixing symbiosis dramatically alters community structure in the latter two compartments, affecting at least 14 bacterial orders. The differential plant growth phenotypes seen between WT and the symbiotic mutants in nonsupplemented soil were retained under nitrogen-supplemented conditions that blocked the formation of functional nodules in WT, whereas the symbiosis-impaired mutants maintain an altered community structure in the nitrogen-supplemented soil. This finding provides strong evidence that the root-associated community shift in the symbiotic mutants is a direct consequence of the disabled symbiosis pathway rather than an indirect effect resulting from abolished symbiotic nitrogen fixation. Our findings imply a role of the legume host in selecting a broad taxonomic range of root-associated bacteria that, in addition to rhizobia, likely contribute to plant growth and ecological performance.

Original languageEnglish
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue49
Pages (from-to)E7996-E8005
Number of pages10
ISSN0027-8424
DOIs
Publication statusPublished - 6 Dec 2016

    Research areas

  • Lotus japonicus, microbiota, symbiosis, 16S, nitrogen fixation, RECEPTOR-LIKE KINASE, NITROGEN-FIXATION, SOYBEAN RHIZOSPHERE, RHIZOBIUM-MELILOTI, FUNGAL SYMBIOSIS, MODEL LEGUME, PLANT, MICROBIOTA, NODULATION, EXPRESSION

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