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

Rafal Zgadzaj, Ruben Garrido-Oter, Dorthe Bodker Jensen, Anna Koprivova, Paul Schulze-Lefert*, Simona Radutoiu

*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

249 Citations (Scopus)

Abstract

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 (PNAS)
Volume113
Issue49
Pages (from-to)E7996-E8005
Number of pages10
ISSN0027-8424
DOIs
Publication statusPublished - 6 Dec 2016

Keywords

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

Fingerprint

Dive into the research topics of 'Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities'. Together they form a unique fingerprint.

Cite this