Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis

Jon Penterman, Ryan P. Abo, Nicole J. De Nisco, Markus f. F. Arnold, Renato Longhi, Matteo Zanda, Graham C. Walker

Research output: Contribution to journalArticle

66 Citations (Scopus)

Abstract

The α-proteobacterium Sinorhizobium meliloti establishes a chronic intracellular infection during the symbiosis with its legume hosts. Within specialized host cells, S. meliloti differentiates into highly polyploid, enlarged nitrogen-fixing bacteroids. This differentiation is driven by host cells through the production of defensin-like peptides called “nodule-specific cysteine-rich” (NCR) peptides. Recent research has shown that synthesized NCR peptides exhibit antimicrobial activity at high concentrations but cause bacterial endoreduplication at sublethal concentrations. We leveraged synchronized S. meliloti populations to determine how treatment with a sublethal NCR peptide affects the cell cycle and physiology of bacteria at the molecular level. We found that at sublethal levels a representative NCR peptide specifically blocks cell division and antagonizes Z-ring function. Gene-expression profiling revealed that the cell division block was produced, in part, through the substantial transcriptional response elicited by sublethal NCR treatment that affected ∼15% of the genome. Expression of critical cell-cycle regulators, including ctrA, and cell division genes, including genes required for Z-ring function, were greatly attenuated in NCR-treated cells. In addition, our experiments identified important symbiosis functions and stress responses that are induced by sublethal levels of NCR peptides and other antimicrobial peptides. Several of these stress-response pathways also are found in related α-proteobacterial pathogens and might be used by S. meliloti to sense host cues during infection. Our data suggest a model in which, in addition to provoking stress responses, NCR peptides target intracellular regulatory pathways to drive S. meliloti endoreduplication and differentiation during symbiosis.
Original languageEnglish
Pages (from-to)3561-3566
Number of pages6
JournalPNAS
Volume111
Issue number9
Early online date5 Feb 2014
DOIs
Publication statusPublished - 4 Mar 2014

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Ensifer meliloti
symbiosis
cysteine
cell cycle
host plants
peptides
cell division
endopolyploidy
stress response
cell physiology
antimicrobial peptides
Proteobacteria
cells
polyploidy
infection
genes
legumes
anti-infective agents
gene expression
genome

Cite this

Penterman, J., Abo, R. P., De Nisco, N. J., Arnold, M. F. F., Longhi, R., Zanda, M., & Walker, G. C. (2014). Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. PNAS, 111(9), 3561-3566. https://doi.org/10.1073/pnas.1400450111

Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. / Penterman, Jon; Abo, Ryan P.; De Nisco, Nicole J.; Arnold, Markus f. F.; Longhi, Renato; Zanda, Matteo; Walker, Graham C.

In: PNAS, Vol. 111, No. 9, 04.03.2014, p. 3561-3566.

Research output: Contribution to journalArticle

Penterman, J, Abo, RP, De Nisco, NJ, Arnold, MFF, Longhi, R, Zanda, M & Walker, GC 2014, 'Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis', PNAS, vol. 111, no. 9, pp. 3561-3566. https://doi.org/10.1073/pnas.1400450111
Penterman, Jon ; Abo, Ryan P. ; De Nisco, Nicole J. ; Arnold, Markus f. F. ; Longhi, Renato ; Zanda, Matteo ; Walker, Graham C. / Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. In: PNAS. 2014 ; Vol. 111, No. 9. pp. 3561-3566.
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