Cargando…

Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors

BACKGROUND: The fungus Cronartium ribicola (Cri) is an economically and ecologically important forest pathogen that causes white pine blister rust (WPBR) disease on five-needle pines. To cause stem cankers and kill white pine trees the fungus elaborates a life cycle with five stages of spore develop...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Jun-Jun, Sturrock, Rona N., Sniezko, Richard A., Williams, Holly, Benton, Ross, Zamany, Arezoo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4559923/
https://www.ncbi.nlm.nih.gov/pubmed/26338692
http://dx.doi.org/10.1186/s12864-015-1861-1
_version_ 1782388858251378688
author Liu, Jun-Jun
Sturrock, Rona N.
Sniezko, Richard A.
Williams, Holly
Benton, Ross
Zamany, Arezoo
author_facet Liu, Jun-Jun
Sturrock, Rona N.
Sniezko, Richard A.
Williams, Holly
Benton, Ross
Zamany, Arezoo
author_sort Liu, Jun-Jun
collection PubMed
description BACKGROUND: The fungus Cronartium ribicola (Cri) is an economically and ecologically important forest pathogen that causes white pine blister rust (WPBR) disease on five-needle pines. To cause stem cankers and kill white pine trees the fungus elaborates a life cycle with five stages of spore development on five-needle pines and the alternate host Ribes plants. To increase our understanding of molecular WP-BR interactions, here we report genome-wide transcriptional profile analysis of C. ribicola using RNA-seq. RESULTS: cDNA libraries were constructed from aeciospore, urediniospore, and western white pine (Pinus monticola) tissues post Cri infection. Over 200 million RNA-seq 100-bp paired-end (PE) reads from rust fungal spores were de novo assembled and a reference transcriptome was generated with 17,880 transcripts that were expressed from 13,629 unigenes. A total of 734 unique proteins were predicted as a part of the Cri secretome from complete open reading frames (ORFs), and 41 % of them were Cronartium-specific. This study further identified a repertoire of candidate effectors and other pathogenicity determinants. Differentially expressed genes (DEGs) were identified to gain an understanding of molecular events important during the WPBR fungus life cycle by comparing Cri transcriptomes at different infection stages. Large-scale changes of in planta gene expression profiles were observed, revealing that multiple fungal biosynthetic pathways were enhanced during mycelium growth inside infected pine stem tissues. Conversely, many fungal genes that were up-regulated at the urediniospore stage appeared to be signalling components and transporters. The secreted fungal protein genes that were up-regulated in pine needle tissues during early infection were primarily associated with cell wall modifications, possibly to mask the rust pathogen from plant defenses. CONCLUSION: This comprehensive transcriptome profiling substantially improves our current understanding of molecular WP-BR interactions. The repertoire of candidate effectors and other putative pathogenicity determinants identified here are valuable for future functional analysis of Cri virulence and pathogenicity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1861-1) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4559923
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-45599232015-09-05 Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors Liu, Jun-Jun Sturrock, Rona N. Sniezko, Richard A. Williams, Holly Benton, Ross Zamany, Arezoo BMC Genomics Research Article BACKGROUND: The fungus Cronartium ribicola (Cri) is an economically and ecologically important forest pathogen that causes white pine blister rust (WPBR) disease on five-needle pines. To cause stem cankers and kill white pine trees the fungus elaborates a life cycle with five stages of spore development on five-needle pines and the alternate host Ribes plants. To increase our understanding of molecular WP-BR interactions, here we report genome-wide transcriptional profile analysis of C. ribicola using RNA-seq. RESULTS: cDNA libraries were constructed from aeciospore, urediniospore, and western white pine (Pinus monticola) tissues post Cri infection. Over 200 million RNA-seq 100-bp paired-end (PE) reads from rust fungal spores were de novo assembled and a reference transcriptome was generated with 17,880 transcripts that were expressed from 13,629 unigenes. A total of 734 unique proteins were predicted as a part of the Cri secretome from complete open reading frames (ORFs), and 41 % of them were Cronartium-specific. This study further identified a repertoire of candidate effectors and other pathogenicity determinants. Differentially expressed genes (DEGs) were identified to gain an understanding of molecular events important during the WPBR fungus life cycle by comparing Cri transcriptomes at different infection stages. Large-scale changes of in planta gene expression profiles were observed, revealing that multiple fungal biosynthetic pathways were enhanced during mycelium growth inside infected pine stem tissues. Conversely, many fungal genes that were up-regulated at the urediniospore stage appeared to be signalling components and transporters. The secreted fungal protein genes that were up-regulated in pine needle tissues during early infection were primarily associated with cell wall modifications, possibly to mask the rust pathogen from plant defenses. CONCLUSION: This comprehensive transcriptome profiling substantially improves our current understanding of molecular WP-BR interactions. The repertoire of candidate effectors and other putative pathogenicity determinants identified here are valuable for future functional analysis of Cri virulence and pathogenicity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1861-1) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-04 /pmc/articles/PMC4559923/ /pubmed/26338692 http://dx.doi.org/10.1186/s12864-015-1861-1 Text en © Liu et al. 2015 Open Access This 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
Liu, Jun-Jun
Sturrock, Rona N.
Sniezko, Richard A.
Williams, Holly
Benton, Ross
Zamany, Arezoo
Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
title Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
title_full Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
title_fullStr Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
title_full_unstemmed Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
title_short Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
title_sort transcriptome analysis of the white pine blister rust pathogen cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4559923/
https://www.ncbi.nlm.nih.gov/pubmed/26338692
http://dx.doi.org/10.1186/s12864-015-1861-1
work_keys_str_mv AT liujunjun transcriptomeanalysisofthewhitepineblisterrustpathogencronartiumribicoladenovoassemblyexpressionprofilingandidentificationofcandidateeffectors
AT sturrockronan transcriptomeanalysisofthewhitepineblisterrustpathogencronartiumribicoladenovoassemblyexpressionprofilingandidentificationofcandidateeffectors
AT sniezkoricharda transcriptomeanalysisofthewhitepineblisterrustpathogencronartiumribicoladenovoassemblyexpressionprofilingandidentificationofcandidateeffectors
AT williamsholly transcriptomeanalysisofthewhitepineblisterrustpathogencronartiumribicoladenovoassemblyexpressionprofilingandidentificationofcandidateeffectors
AT bentonross transcriptomeanalysisofthewhitepineblisterrustpathogencronartiumribicoladenovoassemblyexpressionprofilingandidentificationofcandidateeffectors
AT zamanyarezoo transcriptomeanalysisofthewhitepineblisterrustpathogencronartiumribicoladenovoassemblyexpressionprofilingandidentificationofcandidateeffectors