Characterization of quorum sensing-controlled transcriptional regulator MarR and Rieske (2Fe-2S) cluster-containing protein (Orf5), which are involved in resistance to environmental stresses in Pseudomonas syringae pv. tabaci 6605

Fumiko Taguchi, Yuko Inoue, Tomoko Suzuki, Yoshishige Inagaki, Mikihiro Yamamoto, Kazuhiro Toyoda, Yoshiteru Noutoshi, Tomonori Shiraishi, Yuki Ichinose

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Pseudomonas syringae pv. tabaci 6605 (Pta6605) produces acyl homoserine lactones (AHLs), quorum sensing (QS) molecules that are indispensable for virulence in host tobacco infection. Genome-wide transcriptional profiling of several QS-defective mutants revealed that the expression of the genes encoding the MarR family transcriptional regulator (MarR) and a Rieske 2Fe-2S cluster-containing protein (Orf5) located adjacent to psyI, a gene encoding AHL synthetase, are significantly repressed. Exogenous application of AHL recovered the expression of both marR and orf5 genes in the ΔpsyI mutant, indicating that AHL positively regulates the expression of these genes. To investigate the role of these genes in the virulence of Pta6605, ΔmarR and Δorf5 mutants were generated. Both mutants showed decreased swimming and swarming motilities, decreased survival ability under oxidative and nitrosative stresses and, consequently, reduced virulence on host tobacco plants. Transmission electron micrographs showed that the structure of the cell membranes of ΔmarR and Δorf5 mutants was severely damaged. Furthermore, not only the ratio of dead cells, but also the amount of flagella, extracellular DNA and protein released into the culture supernatant, was significantly increased in both mutants, indicating that the disruption of marR and orf5 genes might induce structural changes in the membrane and cell lysis. Because both mutants showed partly similar expression profiles, both gene products might be involved in the same regulatory cascades that are required for QS-dependent survival under environmentally stressed conditions.

Original languageEnglish
Pages (from-to)376-387
Number of pages12
JournalMolecular Plant Pathology
Volume16
Issue number4
DOIs
Publication statusPublished - May 1 2015

Fingerprint

Pseudomonas syringae pv. tabaci
Acyl-Butyrolactones
Pseudomonas syringae
Quorum Sensing
quorum sensing
environmental stress
transcription factors
homoserine
Virulence
mutants
protein
gene
lactones
Genes
bacterial motility
Tobacco
virulence
Proteins
proteins
Cell Membrane Structures

Keywords

  • Extracellular DNA
  • Nitrite
  • Rieske 2Fe-2S cluster
  • Superoxide
  • Surface motility

ASJC Scopus subject areas

  • Plant Science
  • Agronomy and Crop Science
  • Soil Science
  • Molecular Biology

Cite this

@article{8f8f03d600b64ea7b8eb2466766cd1a8,
title = "Characterization of quorum sensing-controlled transcriptional regulator MarR and Rieske (2Fe-2S) cluster-containing protein (Orf5), which are involved in resistance to environmental stresses in Pseudomonas syringae pv. tabaci 6605",
abstract = "Pseudomonas syringae pv. tabaci 6605 (Pta6605) produces acyl homoserine lactones (AHLs), quorum sensing (QS) molecules that are indispensable for virulence in host tobacco infection. Genome-wide transcriptional profiling of several QS-defective mutants revealed that the expression of the genes encoding the MarR family transcriptional regulator (MarR) and a Rieske 2Fe-2S cluster-containing protein (Orf5) located adjacent to psyI, a gene encoding AHL synthetase, are significantly repressed. Exogenous application of AHL recovered the expression of both marR and orf5 genes in the ΔpsyI mutant, indicating that AHL positively regulates the expression of these genes. To investigate the role of these genes in the virulence of Pta6605, ΔmarR and Δorf5 mutants were generated. Both mutants showed decreased swimming and swarming motilities, decreased survival ability under oxidative and nitrosative stresses and, consequently, reduced virulence on host tobacco plants. Transmission electron micrographs showed that the structure of the cell membranes of ΔmarR and Δorf5 mutants was severely damaged. Furthermore, not only the ratio of dead cells, but also the amount of flagella, extracellular DNA and protein released into the culture supernatant, was significantly increased in both mutants, indicating that the disruption of marR and orf5 genes might induce structural changes in the membrane and cell lysis. Because both mutants showed partly similar expression profiles, both gene products might be involved in the same regulatory cascades that are required for QS-dependent survival under environmentally stressed conditions.",
keywords = "Extracellular DNA, Nitrite, Rieske 2Fe-2S cluster, Superoxide, Surface motility",
author = "Fumiko Taguchi and Yuko Inoue and Tomoko Suzuki and Yoshishige Inagaki and Mikihiro Yamamoto and Kazuhiro Toyoda and Yoshiteru Noutoshi and Tomonori Shiraishi and Yuki Ichinose",
year = "2015",
month = "5",
day = "1",
doi = "10.1111/mpp.12187",
language = "English",
volume = "16",
pages = "376--387",
journal = "Molecular Plant Pathology",
issn = "1464-6722",
publisher = "Wiley-Blackwell",
number = "4",

}

TY - JOUR

T1 - Characterization of quorum sensing-controlled transcriptional regulator MarR and Rieske (2Fe-2S) cluster-containing protein (Orf5), which are involved in resistance to environmental stresses in Pseudomonas syringae pv. tabaci 6605

AU - Taguchi, Fumiko

AU - Inoue, Yuko

AU - Suzuki, Tomoko

AU - Inagaki, Yoshishige

AU - Yamamoto, Mikihiro

AU - Toyoda, Kazuhiro

AU - Noutoshi, Yoshiteru

AU - Shiraishi, Tomonori

AU - Ichinose, Yuki

PY - 2015/5/1

Y1 - 2015/5/1

N2 - Pseudomonas syringae pv. tabaci 6605 (Pta6605) produces acyl homoserine lactones (AHLs), quorum sensing (QS) molecules that are indispensable for virulence in host tobacco infection. Genome-wide transcriptional profiling of several QS-defective mutants revealed that the expression of the genes encoding the MarR family transcriptional regulator (MarR) and a Rieske 2Fe-2S cluster-containing protein (Orf5) located adjacent to psyI, a gene encoding AHL synthetase, are significantly repressed. Exogenous application of AHL recovered the expression of both marR and orf5 genes in the ΔpsyI mutant, indicating that AHL positively regulates the expression of these genes. To investigate the role of these genes in the virulence of Pta6605, ΔmarR and Δorf5 mutants were generated. Both mutants showed decreased swimming and swarming motilities, decreased survival ability under oxidative and nitrosative stresses and, consequently, reduced virulence on host tobacco plants. Transmission electron micrographs showed that the structure of the cell membranes of ΔmarR and Δorf5 mutants was severely damaged. Furthermore, not only the ratio of dead cells, but also the amount of flagella, extracellular DNA and protein released into the culture supernatant, was significantly increased in both mutants, indicating that the disruption of marR and orf5 genes might induce structural changes in the membrane and cell lysis. Because both mutants showed partly similar expression profiles, both gene products might be involved in the same regulatory cascades that are required for QS-dependent survival under environmentally stressed conditions.

AB - Pseudomonas syringae pv. tabaci 6605 (Pta6605) produces acyl homoserine lactones (AHLs), quorum sensing (QS) molecules that are indispensable for virulence in host tobacco infection. Genome-wide transcriptional profiling of several QS-defective mutants revealed that the expression of the genes encoding the MarR family transcriptional regulator (MarR) and a Rieske 2Fe-2S cluster-containing protein (Orf5) located adjacent to psyI, a gene encoding AHL synthetase, are significantly repressed. Exogenous application of AHL recovered the expression of both marR and orf5 genes in the ΔpsyI mutant, indicating that AHL positively regulates the expression of these genes. To investigate the role of these genes in the virulence of Pta6605, ΔmarR and Δorf5 mutants were generated. Both mutants showed decreased swimming and swarming motilities, decreased survival ability under oxidative and nitrosative stresses and, consequently, reduced virulence on host tobacco plants. Transmission electron micrographs showed that the structure of the cell membranes of ΔmarR and Δorf5 mutants was severely damaged. Furthermore, not only the ratio of dead cells, but also the amount of flagella, extracellular DNA and protein released into the culture supernatant, was significantly increased in both mutants, indicating that the disruption of marR and orf5 genes might induce structural changes in the membrane and cell lysis. Because both mutants showed partly similar expression profiles, both gene products might be involved in the same regulatory cascades that are required for QS-dependent survival under environmentally stressed conditions.

KW - Extracellular DNA

KW - Nitrite

KW - Rieske 2Fe-2S cluster

KW - Superoxide

KW - Surface motility

UR - http://www.scopus.com/inward/record.url?scp=84928205161&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84928205161&partnerID=8YFLogxK

U2 - 10.1111/mpp.12187

DO - 10.1111/mpp.12187

M3 - Article

VL - 16

SP - 376

EP - 387

JO - Molecular Plant Pathology

JF - Molecular Plant Pathology

SN - 1464-6722

IS - 4

ER -