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Title: A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides

Abstract

Homologs of the LuxR acyl-homoserine lactone (AHL) quorum-sensing signal receptor are prevalent in Proteobacteria isolated from roots of the Eastern cottonwood tree, Populus deltoides. Many of these isolates possess an orphan LuxR homolog, closely related to OryR from the rice pathogen Xanthomonas oryzae. OryR does not respond to AHL signals but, instead, responds to an unknown plant compound. We discovered an OryR homolog, PipR, in the cottonwood endophyte Pseudomonas sp. strain GM79. The genes adjacent to pipR encode a predicted ATP-binding cassette (ABC) peptide transporter and peptidases. We purified the putative peptidases, PipA and AapA, and confirmed their predicted activities. A transcriptional pipA-gfp reporter was responsive to PipR in the presence of plant leaf macerates, but it was not influenced by AHLs, similar to findings with OryR. We found that PipR also responded to protein hydrolysates to activate pipA-gfp expression. Among many peptides tested, the tripeptide Ser-His-Ser showed inducer activity but at relatively high concentrations. An ABC peptide transporter mutant failed to respond to leaf macerates, peptone, or Ser-His-Ser, while peptidase mutants expressed higher-than-wild-type levels of pipA-gfp in response to any of these signals. Our studies are consistent with a model where active transport of a peptidelike signal is requiredmore » for the signal to interact with PipR, which then activates peptidase gene expression. As a result, the identification of a peptide ligand for PipR sets the stage to identify plant-derived signals for the OryR family of orphan LuxR proteins.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [3];  [1]; ORCiD logo [1]
  1. Univ. of Washington, Seattle, WA (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. International Centre for Genetic Engineering and Biotechnology, Trieste (Italy)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1324202
Grant/Contract Number:
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 7; Journal Issue: 4; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Schaefer, Amy L., Oda, Yasuhiro, Coutinho, Bruna Goncalves, Pelletier, Dale A., Weiburg, Justin, Venturi, Vittorio, Greenberg, E. Peter, and Harwood, Caroline S. A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides. United States: N. p., 2016. Web. doi:10.1128/mBio.01101-16.
Schaefer, Amy L., Oda, Yasuhiro, Coutinho, Bruna Goncalves, Pelletier, Dale A., Weiburg, Justin, Venturi, Vittorio, Greenberg, E. Peter, & Harwood, Caroline S. A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides. United States. doi:10.1128/mBio.01101-16.
Schaefer, Amy L., Oda, Yasuhiro, Coutinho, Bruna Goncalves, Pelletier, Dale A., Weiburg, Justin, Venturi, Vittorio, Greenberg, E. Peter, and Harwood, Caroline S. 2016. "A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides". United States. doi:10.1128/mBio.01101-16. https://www.osti.gov/servlets/purl/1324202.
@article{osti_1324202,
title = {A LuxR homolog in a cottonwood tree endophyte that activates gene expression in response to a plant signal or specific peptides},
author = {Schaefer, Amy L. and Oda, Yasuhiro and Coutinho, Bruna Goncalves and Pelletier, Dale A. and Weiburg, Justin and Venturi, Vittorio and Greenberg, E. Peter and Harwood, Caroline S.},
abstractNote = {Homologs of the LuxR acyl-homoserine lactone (AHL) quorum-sensing signal receptor are prevalent in Proteobacteria isolated from roots of the Eastern cottonwood tree, Populus deltoides. Many of these isolates possess an orphan LuxR homolog, closely related to OryR from the rice pathogen Xanthomonas oryzae. OryR does not respond to AHL signals but, instead, responds to an unknown plant compound. We discovered an OryR homolog, PipR, in the cottonwood endophyte Pseudomonas sp. strain GM79. The genes adjacent to pipR encode a predicted ATP-binding cassette (ABC) peptide transporter and peptidases. We purified the putative peptidases, PipA and AapA, and confirmed their predicted activities. A transcriptional pipA-gfp reporter was responsive to PipR in the presence of plant leaf macerates, but it was not influenced by AHLs, similar to findings with OryR. We found that PipR also responded to protein hydrolysates to activate pipA-gfp expression. Among many peptides tested, the tripeptide Ser-His-Ser showed inducer activity but at relatively high concentrations. An ABC peptide transporter mutant failed to respond to leaf macerates, peptone, or Ser-His-Ser, while peptidase mutants expressed higher-than-wild-type levels of pipA-gfp in response to any of these signals. Our studies are consistent with a model where active transport of a peptidelike signal is required for the signal to interact with PipR, which then activates peptidase gene expression. As a result, the identification of a peptide ligand for PipR sets the stage to identify plant-derived signals for the OryR family of orphan LuxR proteins.},
doi = {10.1128/mBio.01101-16},
journal = {mBio (Online)},
number = 4,
volume = 7,
place = {United States},
year = 2016,
month = 8
}

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