Cargando…

Tomato root microbiota and Phytophthora parasitica-associated disease

BACKGROUND: Interactions between pathogenic oomycetes and microbiota residing on the surface of the host plant root are unknown, despite being critical to inoculum constitution. The nature of these interactions was explored for the polyphagous and telluric species Phytophthora parasitica. RESULTS: C...

Descripción completa

Detalles Bibliográficos
Autores principales: Larousse, Marie, Rancurel, Corinne, Syska, Camille, Palero, Ferran, Etienne, Catherine, Industri, Benoît, Nesme, Xavier, Bardin, Marc, Galiana, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5434524/
https://www.ncbi.nlm.nih.gov/pubmed/28511691
http://dx.doi.org/10.1186/s40168-017-0273-7
_version_ 1783237061711495168
author Larousse, Marie
Rancurel, Corinne
Syska, Camille
Palero, Ferran
Etienne, Catherine
Industri, Benoît
Nesme, Xavier
Bardin, Marc
Galiana, Eric
author_facet Larousse, Marie
Rancurel, Corinne
Syska, Camille
Palero, Ferran
Etienne, Catherine
Industri, Benoît
Nesme, Xavier
Bardin, Marc
Galiana, Eric
author_sort Larousse, Marie
collection PubMed
description BACKGROUND: Interactions between pathogenic oomycetes and microbiota residing on the surface of the host plant root are unknown, despite being critical to inoculum constitution. The nature of these interactions was explored for the polyphagous and telluric species Phytophthora parasitica. RESULTS: Composition of the rhizospheric microbiota of Solanum lycopersicum was characterized using deep re-sequencing of 16S rRNA gene to analyze tomato roots either free of or partly covered with P. parasitica biofilm. Colonization of the host root surface by the oomycete was associated with a shift in microbial community involving a Bacteroidetes/Proteobacteria transition and Flavobacteriaceae as the most abundant family. Identification of members of the P. parasitica-associated microbiota interfering with biology and oomycete infection was carried out by screening for bacteria able to (i) grow on a P. parasitica extract-based medium (ii), exhibit in vitro probiotic or antibiotic activity towards the oomycete (iii), have an impact on the oomycete infection cycle in a tripartite interaction S. lycopersicum-P. parasitica-bacteria. One Pseudomonas phylotype was found to exacerbate disease symptoms in tomato plants. The lack of significant gene expression response of P. parasitica effectors to Pseudomonas suggested that the increase in plant susceptibility was not associated with an increase in virulence. Our results reveal that Pseudomonas spp. establishes commensal interactions with the oomycete. Bacteria preferentially colonize the surface of the biofilm rather than the roots, so that they can infect plant cells without any apparent infection of P. parasitica. CONCLUSIONS: The presence of the pathogenic oomycete P. parasitica in the tomato rhizosphere leads to a shift in the rhizospheric microbiota composition. It contributes to the habitat extension of Pseudomonas species mediated through a physical association between the oomycete and the bacteria. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-017-0273-7) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5434524
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-54345242017-05-17 Tomato root microbiota and Phytophthora parasitica-associated disease Larousse, Marie Rancurel, Corinne Syska, Camille Palero, Ferran Etienne, Catherine Industri, Benoît Nesme, Xavier Bardin, Marc Galiana, Eric Microbiome Research BACKGROUND: Interactions between pathogenic oomycetes and microbiota residing on the surface of the host plant root are unknown, despite being critical to inoculum constitution. The nature of these interactions was explored for the polyphagous and telluric species Phytophthora parasitica. RESULTS: Composition of the rhizospheric microbiota of Solanum lycopersicum was characterized using deep re-sequencing of 16S rRNA gene to analyze tomato roots either free of or partly covered with P. parasitica biofilm. Colonization of the host root surface by the oomycete was associated with a shift in microbial community involving a Bacteroidetes/Proteobacteria transition and Flavobacteriaceae as the most abundant family. Identification of members of the P. parasitica-associated microbiota interfering with biology and oomycete infection was carried out by screening for bacteria able to (i) grow on a P. parasitica extract-based medium (ii), exhibit in vitro probiotic or antibiotic activity towards the oomycete (iii), have an impact on the oomycete infection cycle in a tripartite interaction S. lycopersicum-P. parasitica-bacteria. One Pseudomonas phylotype was found to exacerbate disease symptoms in tomato plants. The lack of significant gene expression response of P. parasitica effectors to Pseudomonas suggested that the increase in plant susceptibility was not associated with an increase in virulence. Our results reveal that Pseudomonas spp. establishes commensal interactions with the oomycete. Bacteria preferentially colonize the surface of the biofilm rather than the roots, so that they can infect plant cells without any apparent infection of P. parasitica. CONCLUSIONS: The presence of the pathogenic oomycete P. parasitica in the tomato rhizosphere leads to a shift in the rhizospheric microbiota composition. It contributes to the habitat extension of Pseudomonas species mediated through a physical association between the oomycete and the bacteria. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-017-0273-7) contains supplementary material, which is available to authorized users. BioMed Central 2017-05-16 /pmc/articles/PMC5434524/ /pubmed/28511691 http://dx.doi.org/10.1186/s40168-017-0273-7 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Larousse, Marie
Rancurel, Corinne
Syska, Camille
Palero, Ferran
Etienne, Catherine
Industri, Benoît
Nesme, Xavier
Bardin, Marc
Galiana, Eric
Tomato root microbiota and Phytophthora parasitica-associated disease
title Tomato root microbiota and Phytophthora parasitica-associated disease
title_full Tomato root microbiota and Phytophthora parasitica-associated disease
title_fullStr Tomato root microbiota and Phytophthora parasitica-associated disease
title_full_unstemmed Tomato root microbiota and Phytophthora parasitica-associated disease
title_short Tomato root microbiota and Phytophthora parasitica-associated disease
title_sort tomato root microbiota and phytophthora parasitica-associated disease
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5434524/
https://www.ncbi.nlm.nih.gov/pubmed/28511691
http://dx.doi.org/10.1186/s40168-017-0273-7
work_keys_str_mv AT laroussemarie tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT rancurelcorinne tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT syskacamille tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT paleroferran tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT etiennecatherine tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT industribenoit tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT nesmexavier tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT bardinmarc tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease
AT galianaeric tomatorootmicrobiotaandphytophthoraparasiticaassociateddisease