Cargando…

The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp

BACKGROUND: The protist Plasmodiophora brassicae is a soil-borne pathogen of cruciferous species and the causal agent of clubroot disease of Brassicas including agriculturally important crops such as canola/rapeseed (Brassica napus). P. brassicae has remained an enigmatic plant pathogen and is a rar...

Descripción completa

Detalles Bibliográficos
Autores principales: Rolfe, Stephen A., Strelkov, Stephen E., Links, Matthew G., Clarke, Wayne E., Robinson, Stephen J., Djavaheri, Mohammad, Malinowski, Robert, Haddadi, Parham, Kagale, Sateesh, Parkin, Isobel A. P., Taheri, Ali, Borhan, M. Hossein
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4815078/
https://www.ncbi.nlm.nih.gov/pubmed/27036196
http://dx.doi.org/10.1186/s12864-016-2597-2
_version_ 1782424535458381824
author Rolfe, Stephen A.
Strelkov, Stephen E.
Links, Matthew G.
Clarke, Wayne E.
Robinson, Stephen J.
Djavaheri, Mohammad
Malinowski, Robert
Haddadi, Parham
Kagale, Sateesh
Parkin, Isobel A. P.
Taheri, Ali
Borhan, M. Hossein
author_facet Rolfe, Stephen A.
Strelkov, Stephen E.
Links, Matthew G.
Clarke, Wayne E.
Robinson, Stephen J.
Djavaheri, Mohammad
Malinowski, Robert
Haddadi, Parham
Kagale, Sateesh
Parkin, Isobel A. P.
Taheri, Ali
Borhan, M. Hossein
author_sort Rolfe, Stephen A.
collection PubMed
description BACKGROUND: The protist Plasmodiophora brassicae is a soil-borne pathogen of cruciferous species and the causal agent of clubroot disease of Brassicas including agriculturally important crops such as canola/rapeseed (Brassica napus). P. brassicae has remained an enigmatic plant pathogen and is a rare example of an obligate biotroph that resides entirely inside the host plant cell. The pathogen is the cause of severe yield losses and can render infested fields unsuitable for Brassica crop growth due to the persistence of resting spores in the soil for up to 20 years. RESULTS: To provide insight into the biology of the pathogen and its interaction with its primary host B. napus, we produced a draft genome of P. brassicae pathotypes 3 and 6 (Pb3 and Pb6) that differ in their host range. Pb3 is highly virulent on B. napus (but also infects other Brassica species) while Pb6 infects only vegetable Brassica crops. Both the Pb3 and Pb6 genomes are highly compact, each with a total size of 24.2 Mb, and contain less than 2 % repetitive DNA. Clustering of genome-wide single nucleotide polymorphisms (SNP) of Pb3, Pb6 and three additional re-sequenced pathotypes (Pb2, Pb5 and Pb8) shows a high degree of correlation of cluster grouping with host range. The Pb3 genome features significant reduction of intergenic space with multiple examples of overlapping untranslated regions (UTRs). Dependency on the host for essential nutrients is evident from the loss of genes for the biosynthesis of thiamine and some amino acids and the presence of a wide range of transport proteins, including some unique to P. brassicae. The annotated genes of Pb3 include those with a potential role in the regulation of the plant growth hormones cytokinin and auxin. The expression profile of Pb3 genes, including putative effectors, during infection and their potential role in manipulation of host defence is discussed. CONCLUSION: The P. brassicae genome sequence reveals a compact genome, a dependency of the pathogen on its host for some essential nutrients and a potential role in the regulation of host plant cytokinin and auxin. Genome annotation supported by RNA sequencing reveals significant reduction in intergenic space which, in addition to low repeat content, has likely contributed to the P. brassicae compact genome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2597-2) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4815078
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-48150782016-04-01 The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp Rolfe, Stephen A. Strelkov, Stephen E. Links, Matthew G. Clarke, Wayne E. Robinson, Stephen J. Djavaheri, Mohammad Malinowski, Robert Haddadi, Parham Kagale, Sateesh Parkin, Isobel A. P. Taheri, Ali Borhan, M. Hossein BMC Genomics Research Article BACKGROUND: The protist Plasmodiophora brassicae is a soil-borne pathogen of cruciferous species and the causal agent of clubroot disease of Brassicas including agriculturally important crops such as canola/rapeseed (Brassica napus). P. brassicae has remained an enigmatic plant pathogen and is a rare example of an obligate biotroph that resides entirely inside the host plant cell. The pathogen is the cause of severe yield losses and can render infested fields unsuitable for Brassica crop growth due to the persistence of resting spores in the soil for up to 20 years. RESULTS: To provide insight into the biology of the pathogen and its interaction with its primary host B. napus, we produced a draft genome of P. brassicae pathotypes 3 and 6 (Pb3 and Pb6) that differ in their host range. Pb3 is highly virulent on B. napus (but also infects other Brassica species) while Pb6 infects only vegetable Brassica crops. Both the Pb3 and Pb6 genomes are highly compact, each with a total size of 24.2 Mb, and contain less than 2 % repetitive DNA. Clustering of genome-wide single nucleotide polymorphisms (SNP) of Pb3, Pb6 and three additional re-sequenced pathotypes (Pb2, Pb5 and Pb8) shows a high degree of correlation of cluster grouping with host range. The Pb3 genome features significant reduction of intergenic space with multiple examples of overlapping untranslated regions (UTRs). Dependency on the host for essential nutrients is evident from the loss of genes for the biosynthesis of thiamine and some amino acids and the presence of a wide range of transport proteins, including some unique to P. brassicae. The annotated genes of Pb3 include those with a potential role in the regulation of the plant growth hormones cytokinin and auxin. The expression profile of Pb3 genes, including putative effectors, during infection and their potential role in manipulation of host defence is discussed. CONCLUSION: The P. brassicae genome sequence reveals a compact genome, a dependency of the pathogen on its host for some essential nutrients and a potential role in the regulation of host plant cytokinin and auxin. Genome annotation supported by RNA sequencing reveals significant reduction in intergenic space which, in addition to low repeat content, has likely contributed to the P. brassicae compact genome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-2597-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-03-31 /pmc/articles/PMC4815078/ /pubmed/27036196 http://dx.doi.org/10.1186/s12864-016-2597-2 Text en © Rolfe et al. 2016 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 Article
Rolfe, Stephen A.
Strelkov, Stephen E.
Links, Matthew G.
Clarke, Wayne E.
Robinson, Stephen J.
Djavaheri, Mohammad
Malinowski, Robert
Haddadi, Parham
Kagale, Sateesh
Parkin, Isobel A. P.
Taheri, Ali
Borhan, M. Hossein
The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp
title The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp
title_full The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp
title_fullStr The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp
title_full_unstemmed The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp
title_short The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp
title_sort compact genome of the plant pathogen plasmodiophora brassicae is adapted to intracellular interactions with host brassica spp
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4815078/
https://www.ncbi.nlm.nih.gov/pubmed/27036196
http://dx.doi.org/10.1186/s12864-016-2597-2
work_keys_str_mv AT rolfestephena thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT strelkovstephene thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT linksmatthewg thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT clarkewaynee thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT robinsonstephenj thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT djavaherimohammad thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT malinowskirobert thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT haddadiparham thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT kagalesateesh thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT parkinisobelap thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT taheriali thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT borhanmhossein thecompactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT rolfestephena compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT strelkovstephene compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT linksmatthewg compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT clarkewaynee compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT robinsonstephenj compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT djavaherimohammad compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT malinowskirobert compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT haddadiparham compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT kagalesateesh compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT parkinisobelap compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT taheriali compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp
AT borhanmhossein compactgenomeoftheplantpathogenplasmodiophorabrassicaeisadaptedtointracellularinteractionswithhostbrassicaspp