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Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

BACKGROUND: Fungal plant pathogens belonging to the genus Venturia cause damaging scab diseases of members of the Rosaceae. In terms of economic impact, the most important of these are V. inaequalis, which infects apple, and V. pirina, which is a pathogen of European pear. Given that Venturia fungi...

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Autores principales: Deng, Cecilia H., Plummer, Kim M., Jones, Darcy A. B., Mesarich, Carl H., Shiller, Jason, Taranto, Adam P., Robinson, Andrew J., Kastner, Patrick, Hall, Nathan E., Templeton, Matthew D., Bowen, Joanna K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5412055/
https://www.ncbi.nlm.nih.gov/pubmed/28464870
http://dx.doi.org/10.1186/s12864-017-3699-1
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author Deng, Cecilia H.
Plummer, Kim M.
Jones, Darcy A. B.
Mesarich, Carl H.
Shiller, Jason
Taranto, Adam P.
Robinson, Andrew J.
Kastner, Patrick
Hall, Nathan E.
Templeton, Matthew D.
Bowen, Joanna K.
author_facet Deng, Cecilia H.
Plummer, Kim M.
Jones, Darcy A. B.
Mesarich, Carl H.
Shiller, Jason
Taranto, Adam P.
Robinson, Andrew J.
Kastner, Patrick
Hall, Nathan E.
Templeton, Matthew D.
Bowen, Joanna K.
author_sort Deng, Cecilia H.
collection PubMed
description BACKGROUND: Fungal plant pathogens belonging to the genus Venturia cause damaging scab diseases of members of the Rosaceae. In terms of economic impact, the most important of these are V. inaequalis, which infects apple, and V. pirina, which is a pathogen of European pear. Given that Venturia fungi colonise the sub-cuticular space without penetrating plant cells, it is assumed that effectors that contribute to virulence and determination of host range will be secreted into this plant-pathogen interface. Thus the predicted secretomes of a range of isolates of Venturia with distinct host-ranges were interrogated to reveal putative proteins involved in virulence and pathogenicity. RESULTS: Genomes of Venturia pirina (one European pear scab isolate) and Venturia inaequalis (three apple scab, and one loquat scab, isolates) were sequenced and the predicted secretomes of each isolate identified. RNA-Seq was conducted on the apple-specific V. inaequalis isolate Vi1 (in vitro and infected apple leaves) to highlight virulence and pathogenicity components of the secretome. Genes encoding over 600 small secreted proteins (candidate effectors) were identified, most of which are novel to Venturia, with expansion of putative effector families a feature of the genus. Numerous genes with similarity to Leptosphaeria maculans AvrLm6 and the Verticillium spp. Ave1 were identified. Candidates for avirulence effectors with cognate resistance genes involved in race-cultivar specificity were identified, as were putative proteins involved in host-species determination. Candidate effectors were found, on average, to be in regions of relatively low gene-density and in closer proximity to repeats (e.g. transposable elements), compared with core eukaryotic genes. CONCLUSIONS: Comparative secretomics has revealed candidate effectors from Venturia fungal plant pathogens that attack pome fruit. Effectors that are putative determinants of host range were identified; both those that may be involved in race-cultivar and host-species specificity. Since many of the effector candidates are in close proximity to repetitive sequences this may point to a possible mechanism for the effector gene family expansion observed and a route to diversification via transposition and repeat-induced point mutation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3699-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-54120552017-05-03 Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range Deng, Cecilia H. Plummer, Kim M. Jones, Darcy A. B. Mesarich, Carl H. Shiller, Jason Taranto, Adam P. Robinson, Andrew J. Kastner, Patrick Hall, Nathan E. Templeton, Matthew D. Bowen, Joanna K. BMC Genomics Research Article BACKGROUND: Fungal plant pathogens belonging to the genus Venturia cause damaging scab diseases of members of the Rosaceae. In terms of economic impact, the most important of these are V. inaequalis, which infects apple, and V. pirina, which is a pathogen of European pear. Given that Venturia fungi colonise the sub-cuticular space without penetrating plant cells, it is assumed that effectors that contribute to virulence and determination of host range will be secreted into this plant-pathogen interface. Thus the predicted secretomes of a range of isolates of Venturia with distinct host-ranges were interrogated to reveal putative proteins involved in virulence and pathogenicity. RESULTS: Genomes of Venturia pirina (one European pear scab isolate) and Venturia inaequalis (three apple scab, and one loquat scab, isolates) were sequenced and the predicted secretomes of each isolate identified. RNA-Seq was conducted on the apple-specific V. inaequalis isolate Vi1 (in vitro and infected apple leaves) to highlight virulence and pathogenicity components of the secretome. Genes encoding over 600 small secreted proteins (candidate effectors) were identified, most of which are novel to Venturia, with expansion of putative effector families a feature of the genus. Numerous genes with similarity to Leptosphaeria maculans AvrLm6 and the Verticillium spp. Ave1 were identified. Candidates for avirulence effectors with cognate resistance genes involved in race-cultivar specificity were identified, as were putative proteins involved in host-species determination. Candidate effectors were found, on average, to be in regions of relatively low gene-density and in closer proximity to repeats (e.g. transposable elements), compared with core eukaryotic genes. CONCLUSIONS: Comparative secretomics has revealed candidate effectors from Venturia fungal plant pathogens that attack pome fruit. Effectors that are putative determinants of host range were identified; both those that may be involved in race-cultivar and host-species specificity. Since many of the effector candidates are in close proximity to repetitive sequences this may point to a possible mechanism for the effector gene family expansion observed and a route to diversification via transposition and repeat-induced point mutation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3699-1) contains supplementary material, which is available to authorized users. BioMed Central 2017-05-02 /pmc/articles/PMC5412055/ /pubmed/28464870 http://dx.doi.org/10.1186/s12864-017-3699-1 Text en © The New Zealand Institute for Plant and Food Research Limited. 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 Article
Deng, Cecilia H.
Plummer, Kim M.
Jones, Darcy A. B.
Mesarich, Carl H.
Shiller, Jason
Taranto, Adam P.
Robinson, Andrew J.
Kastner, Patrick
Hall, Nathan E.
Templeton, Matthew D.
Bowen, Joanna K.
Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range
title Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range
title_full Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range
title_fullStr Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range
title_full_unstemmed Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range
title_short Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range
title_sort comparative analysis of the predicted secretomes of rosaceae scab pathogens venturia inaequalis and v. pirina reveals expanded effector families and putative determinants of host range
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5412055/
https://www.ncbi.nlm.nih.gov/pubmed/28464870
http://dx.doi.org/10.1186/s12864-017-3699-1
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