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In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway

The virulence of numerous Gram-negative bacteria is under the control of a quorum sensing process based on synthesis and perception of N-acyl homoserine lactones. Rhodococcus erythropolis, a Gram-positive bacterium, has recently been proposed as a biocontrol agent for plant protection against soft-r...

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Autores principales: Barbey, Corinne, Crépin, Alexandre, Bergeau, Dorian, Ouchiha, Asma, Mijouin, Lily, Taupin, Laure, Orange, Nicole, Feuilloley, Marc, Dufour, Alain, Burini, Jean-François, Latour, Xavier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3689677/
https://www.ncbi.nlm.nih.gov/pubmed/23805254
http://dx.doi.org/10.1371/journal.pone.0066642
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author Barbey, Corinne
Crépin, Alexandre
Bergeau, Dorian
Ouchiha, Asma
Mijouin, Lily
Taupin, Laure
Orange, Nicole
Feuilloley, Marc
Dufour, Alain
Burini, Jean-François
Latour, Xavier
author_facet Barbey, Corinne
Crépin, Alexandre
Bergeau, Dorian
Ouchiha, Asma
Mijouin, Lily
Taupin, Laure
Orange, Nicole
Feuilloley, Marc
Dufour, Alain
Burini, Jean-François
Latour, Xavier
author_sort Barbey, Corinne
collection PubMed
description The virulence of numerous Gram-negative bacteria is under the control of a quorum sensing process based on synthesis and perception of N-acyl homoserine lactones. Rhodococcus erythropolis, a Gram-positive bacterium, has recently been proposed as a biocontrol agent for plant protection against soft-rot bacteria, including Pectobacterium. Here, we show that the γ-lactone catabolic pathway of R. erythropolis disrupts Pectobacterium communication and prevents plant soft-rot. We report the first characterization and demonstration of N-acyl homoserine lactone quenching in planta. In particular, we describe the transcription of the R. erythropolis lactonase gene, encoding the key enzyme of this pathway, and the subsequent lactone breakdown. The role of this catabolic pathway in biocontrol activity was confirmed by deletion of the lactonase gene from R. erythropolis and also its heterologous expression in Escherichia coli. The γ-lactone catabolic pathway is induced by pathogen communication rather than by pathogen invasion. This is thus a novel and unusual biocontrol pathway, differing from those previously described as protecting plants from phytopathogens. These findings also suggest the existence of an additional pathway contributing to plant protection.
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spelling pubmed-36896772013-06-26 In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway Barbey, Corinne Crépin, Alexandre Bergeau, Dorian Ouchiha, Asma Mijouin, Lily Taupin, Laure Orange, Nicole Feuilloley, Marc Dufour, Alain Burini, Jean-François Latour, Xavier PLoS One Research Article The virulence of numerous Gram-negative bacteria is under the control of a quorum sensing process based on synthesis and perception of N-acyl homoserine lactones. Rhodococcus erythropolis, a Gram-positive bacterium, has recently been proposed as a biocontrol agent for plant protection against soft-rot bacteria, including Pectobacterium. Here, we show that the γ-lactone catabolic pathway of R. erythropolis disrupts Pectobacterium communication and prevents plant soft-rot. We report the first characterization and demonstration of N-acyl homoserine lactone quenching in planta. In particular, we describe the transcription of the R. erythropolis lactonase gene, encoding the key enzyme of this pathway, and the subsequent lactone breakdown. The role of this catabolic pathway in biocontrol activity was confirmed by deletion of the lactonase gene from R. erythropolis and also its heterologous expression in Escherichia coli. The γ-lactone catabolic pathway is induced by pathogen communication rather than by pathogen invasion. This is thus a novel and unusual biocontrol pathway, differing from those previously described as protecting plants from phytopathogens. These findings also suggest the existence of an additional pathway contributing to plant protection. Public Library of Science 2013-06-21 /pmc/articles/PMC3689677/ /pubmed/23805254 http://dx.doi.org/10.1371/journal.pone.0066642 Text en © 2013 Barbey et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Barbey, Corinne
Crépin, Alexandre
Bergeau, Dorian
Ouchiha, Asma
Mijouin, Lily
Taupin, Laure
Orange, Nicole
Feuilloley, Marc
Dufour, Alain
Burini, Jean-François
Latour, Xavier
In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway
title In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway
title_full In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway
title_fullStr In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway
title_full_unstemmed In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway
title_short In Planta Biocontrol of Pectobacterium atrosepticum by Rhodococcus erythropolis Involves Silencing of Pathogen Communication by the Rhodococcal Gamma-Lactone Catabolic Pathway
title_sort in planta biocontrol of pectobacterium atrosepticum by rhodococcus erythropolis involves silencing of pathogen communication by the rhodococcal gamma-lactone catabolic pathway
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3689677/
https://www.ncbi.nlm.nih.gov/pubmed/23805254
http://dx.doi.org/10.1371/journal.pone.0066642
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