Cargando…

Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica

BACKGROUND: Oomycetes are a group of filamentous microorganisms that includes both animal and plant pathogens and causes major agricultural losses. Phytophthora species can infect most crops and plants from natural ecosystems. Despite their tremendous economic and ecologic importance, few effective...

Descripción completa

Detalles Bibliográficos
Autores principales: Attard, Agnès, Evangelisti, Edouard, Kebdani-Minet, Naïma, Panabières, Franck, Deleury, Emeline, Maggio, Cindy, Ponchet, Michel, Gourgues, Mathieu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4111850/
https://www.ncbi.nlm.nih.gov/pubmed/24974100
http://dx.doi.org/10.1186/1471-2164-15-538
_version_ 1782328129523548160
author Attard, Agnès
Evangelisti, Edouard
Kebdani-Minet, Naïma
Panabières, Franck
Deleury, Emeline
Maggio, Cindy
Ponchet, Michel
Gourgues, Mathieu
author_facet Attard, Agnès
Evangelisti, Edouard
Kebdani-Minet, Naïma
Panabières, Franck
Deleury, Emeline
Maggio, Cindy
Ponchet, Michel
Gourgues, Mathieu
author_sort Attard, Agnès
collection PubMed
description BACKGROUND: Oomycetes are a group of filamentous microorganisms that includes both animal and plant pathogens and causes major agricultural losses. Phytophthora species can infect most crops and plants from natural ecosystems. Despite their tremendous economic and ecologic importance, few effective methods exist for limiting the damage caused by these species. New solutions are required, and their development will require improvements in our understanding of the molecular events governing infection by these pathogens. In this study, we characterized the genetic program activated during penetration of the plant by the soil-borne pathogen Phytophthora parasitica. RESULTS: Using all the P. parasitica sequences available in public databases, we generated a custom oligo-array and performed a transcriptomic analysis of the early events of Arabidopsis thaliana infection. We characterized biological stages, ranging from the appressorium-mediated penetration of the pathogen into the roots to the occurrence of first dead cells in the plant. We identified a series of sequences that were transiently modulated during host penetration. Surprisingly, we observed an overall down regulation of genes encoding proteins involved in lipid and sugar metabolism, and an upregulation of functions controlling the transport of amino acids. We also showed that different groups of genes were expressed by P. parasitica during host penetration and the subsequent necrotrophic phase. Differential expression patterns were particularly marked for cell wall-degrading enzymes and other proteins involved in pathogenicity, including RXLR effectors. By transforming P. parasitica with a transcriptional fusion with GFP, we showed that an RXLR-ecoding gene was expressed in the appressorium and infectious hyphae during infection of the first plant cell. CONCLUSION: We have characterized the genetic program activated during the initial invasion of plant cells by P. parasitica. We showed that a specific set of proteins, including effectors, was mobilized for penetration and to facilitate infection. Our detection of the expression of an RXLR encoding gene by the appressorium and infection hyphae highlights a role of this structure in the manipulation of the host cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-538) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4111850
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-41118502014-08-05 Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica Attard, Agnès Evangelisti, Edouard Kebdani-Minet, Naïma Panabières, Franck Deleury, Emeline Maggio, Cindy Ponchet, Michel Gourgues, Mathieu BMC Genomics Research Article BACKGROUND: Oomycetes are a group of filamentous microorganisms that includes both animal and plant pathogens and causes major agricultural losses. Phytophthora species can infect most crops and plants from natural ecosystems. Despite their tremendous economic and ecologic importance, few effective methods exist for limiting the damage caused by these species. New solutions are required, and their development will require improvements in our understanding of the molecular events governing infection by these pathogens. In this study, we characterized the genetic program activated during penetration of the plant by the soil-borne pathogen Phytophthora parasitica. RESULTS: Using all the P. parasitica sequences available in public databases, we generated a custom oligo-array and performed a transcriptomic analysis of the early events of Arabidopsis thaliana infection. We characterized biological stages, ranging from the appressorium-mediated penetration of the pathogen into the roots to the occurrence of first dead cells in the plant. We identified a series of sequences that were transiently modulated during host penetration. Surprisingly, we observed an overall down regulation of genes encoding proteins involved in lipid and sugar metabolism, and an upregulation of functions controlling the transport of amino acids. We also showed that different groups of genes were expressed by P. parasitica during host penetration and the subsequent necrotrophic phase. Differential expression patterns were particularly marked for cell wall-degrading enzymes and other proteins involved in pathogenicity, including RXLR effectors. By transforming P. parasitica with a transcriptional fusion with GFP, we showed that an RXLR-ecoding gene was expressed in the appressorium and infectious hyphae during infection of the first plant cell. CONCLUSION: We have characterized the genetic program activated during the initial invasion of plant cells by P. parasitica. We showed that a specific set of proteins, including effectors, was mobilized for penetration and to facilitate infection. Our detection of the expression of an RXLR encoding gene by the appressorium and infection hyphae highlights a role of this structure in the manipulation of the host cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-538) contains supplementary material, which is available to authorized users. BioMed Central 2014-06-29 /pmc/articles/PMC4111850/ /pubmed/24974100 http://dx.doi.org/10.1186/1471-2164-15-538 Text en © Attard et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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 Article
Attard, Agnès
Evangelisti, Edouard
Kebdani-Minet, Naïma
Panabières, Franck
Deleury, Emeline
Maggio, Cindy
Ponchet, Michel
Gourgues, Mathieu
Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
title Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
title_full Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
title_fullStr Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
title_full_unstemmed Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
title_short Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
title_sort transcriptome dynamics of arabidopsis thaliana root penetration by the oomycete pathogen phytophthora parasitica
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4111850/
https://www.ncbi.nlm.nih.gov/pubmed/24974100
http://dx.doi.org/10.1186/1471-2164-15-538
work_keys_str_mv AT attardagnes transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT evangelistiedouard transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT kebdaniminetnaima transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT panabieresfranck transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT deleuryemeline transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT maggiocindy transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT ponchetmichel transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica
AT gourguesmathieu transcriptomedynamicsofarabidopsisthalianarootpenetrationbytheoomycetepathogenphytophthoraparasitica