Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis

Peter Mergaert, Toshiki Uchiumi, Benoît Alunni, Gwénaëlle Evanno, Angélique Cheron, Olivier Catrice, Anne Elisabeth Mausset, Frédérique Barloy-Hubler, Francis Galibert, Adam Kondorosi, Eva Kondorosi

Research output: Contribution to journalArticle

258 Citations (Scopus)

Abstract

Symbiosis between legumes and Rhizobium bacteria leads to the formation of root nodules where bacteria in the infected plant cells are converted into nitrogen-fixing bacteroids. Nodules with a persistent meristem are indeterminate, whereas nodules without meristem are determinate. The symbiotic plant cells in both nodule types are polyploid because of several cycles of endoreduplication (genome replication without mitosis and cytokinesis) and grow consequently to extreme sizes. Here we demonstrate that differentiation of bacteroids in indeterminate nodules of Medicago and related legumes from the galegoid clade shows remarkable similarity to host cell differentiation. During bacteroid maturation, repeated DNA replication without cytokinesis results in extensive amplification of the entire bacterial genome and elongation of bacteria. This finding reveals a positive correlation in prokaryotes between DNA content and cell size, similar to that in eukaryotes, These polyploid bacteroids are metabolically functional but display increased membrane permeability and are nonviable, because they lose their ability to resume growth. In contrast, bacteroids in determinate nodules of the nongalegoid legumes lotus and bean are comparable to free-living bacteria in their genomic DNA content, cell size, and viability. Using recombinant Rhizobium strains nodulating both legume types, we show that bacteroid differentiation is controlled by the host plant. Plant factors present in nodules of galegoid legumes but absent from nodules of nongalegoid legumes block bacterial cell division and trigger endoreduplication cycles, thereby forcing the endosymbionts toward a terminally differentiated state. Hence, Medicago and related legumes have evolved a mechanism to dominate the symbiosis.

Original languageEnglish
Pages (from-to)5230-5235
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume103
Issue number13
DOIs
Publication statusPublished - Mar 28 2006

Keywords

  • Antimicrobial activity
  • Bacteroid
  • Endoreduplication
  • Medicago
  • Nitrogen fixation

ASJC Scopus subject areas

  • General

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    Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A. E., Barloy-Hubler, F., Galibert, F., Kondorosi, A., & Kondorosi, E. (2006). Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 103(13), 5230-5235. https://doi.org/10.1073/pnas.0600912103