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Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida

BACKGROUND: The potato cyst nematode Globodera pallida has biotrophic interactions with its host. The nematode induces a feeding structure – the syncytium – which it keeps alive for the duration of the life cycle and on which it depends for all nutrients required to develop to the adult stage. Inter...

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Autores principales: Thorpe, Peter, Mantelin, Sophie, Cock, Peter JA, Blok, Vivian C, Coke, Mirela C, Eves-van den Akker, Sebastian, Guzeeva, Elena, Lilley, Catherine J, Smant, Geert, Reid, Adam J, Wright, Kathryn M, Urwin, Peter E, Jones, John T
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4213498/
https://www.ncbi.nlm.nih.gov/pubmed/25342461
http://dx.doi.org/10.1186/1471-2164-15-923
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author Thorpe, Peter
Mantelin, Sophie
Cock, Peter JA
Blok, Vivian C
Coke, Mirela C
Eves-van den Akker, Sebastian
Guzeeva, Elena
Lilley, Catherine J
Smant, Geert
Reid, Adam J
Wright, Kathryn M
Urwin, Peter E
Jones, John T
author_facet Thorpe, Peter
Mantelin, Sophie
Cock, Peter JA
Blok, Vivian C
Coke, Mirela C
Eves-van den Akker, Sebastian
Guzeeva, Elena
Lilley, Catherine J
Smant, Geert
Reid, Adam J
Wright, Kathryn M
Urwin, Peter E
Jones, John T
author_sort Thorpe, Peter
collection PubMed
description BACKGROUND: The potato cyst nematode Globodera pallida has biotrophic interactions with its host. The nematode induces a feeding structure – the syncytium – which it keeps alive for the duration of the life cycle and on which it depends for all nutrients required to develop to the adult stage. Interactions of G. pallida with the host are mediated by effectors, which are produced in two sets of gland cells. These effectors suppress host defences, facilitate migration and induce the formation of the syncytium. RESULTS: The recent completion of the G. pallida genome sequence has allowed us to identify the effector complement from this species. We identify 128 orthologues of effectors from other nematodes as well as 117 novel effector candidates. We have used in situ hybridisation to confirm gland cell expression of a subset of these effectors, demonstrating the validity of our effector identification approach. We have examined the expression profiles of all effector candidates using RNAseq; this analysis shows that the majority of effectors fall into one of three clusters of sequences showing conserved expression characteristics (invasive stage nematode only, parasitic stage only or invasive stage and adult male only). We demonstrate that further diversity in the effector pool is generated by alternative splicing. In addition, we show that effectors target a diverse range of structures in plant cells, including the peroxisome. This is the first identification of effectors from any plant pathogen that target this structure. CONCLUSION: This is the first genome scale search for effectors, combined to a life-cycle expression analysis, for any plant-parasitic nematode. We show that, like other phylogenetically unrelated plant pathogens, plant parasitic nematodes deploy hundreds of effectors in order to parasitise plants, with different effectors required for different phases of the infection process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-923) contains supplementary material, which is available to authorized users.
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spelling pubmed-42134982014-10-31 Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida Thorpe, Peter Mantelin, Sophie Cock, Peter JA Blok, Vivian C Coke, Mirela C Eves-van den Akker, Sebastian Guzeeva, Elena Lilley, Catherine J Smant, Geert Reid, Adam J Wright, Kathryn M Urwin, Peter E Jones, John T BMC Genomics Research Article BACKGROUND: The potato cyst nematode Globodera pallida has biotrophic interactions with its host. The nematode induces a feeding structure – the syncytium – which it keeps alive for the duration of the life cycle and on which it depends for all nutrients required to develop to the adult stage. Interactions of G. pallida with the host are mediated by effectors, which are produced in two sets of gland cells. These effectors suppress host defences, facilitate migration and induce the formation of the syncytium. RESULTS: The recent completion of the G. pallida genome sequence has allowed us to identify the effector complement from this species. We identify 128 orthologues of effectors from other nematodes as well as 117 novel effector candidates. We have used in situ hybridisation to confirm gland cell expression of a subset of these effectors, demonstrating the validity of our effector identification approach. We have examined the expression profiles of all effector candidates using RNAseq; this analysis shows that the majority of effectors fall into one of three clusters of sequences showing conserved expression characteristics (invasive stage nematode only, parasitic stage only or invasive stage and adult male only). We demonstrate that further diversity in the effector pool is generated by alternative splicing. In addition, we show that effectors target a diverse range of structures in plant cells, including the peroxisome. This is the first identification of effectors from any plant pathogen that target this structure. CONCLUSION: This is the first genome scale search for effectors, combined to a life-cycle expression analysis, for any plant-parasitic nematode. We show that, like other phylogenetically unrelated plant pathogens, plant parasitic nematodes deploy hundreds of effectors in order to parasitise plants, with different effectors required for different phases of the infection process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-923) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-23 /pmc/articles/PMC4213498/ /pubmed/25342461 http://dx.doi.org/10.1186/1471-2164-15-923 Text en © Thorpe 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/4.0), 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
Thorpe, Peter
Mantelin, Sophie
Cock, Peter JA
Blok, Vivian C
Coke, Mirela C
Eves-van den Akker, Sebastian
Guzeeva, Elena
Lilley, Catherine J
Smant, Geert
Reid, Adam J
Wright, Kathryn M
Urwin, Peter E
Jones, John T
Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
title Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
title_full Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
title_fullStr Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
title_full_unstemmed Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
title_short Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida
title_sort genomic characterisation of the effector complement of the potato cyst nematode globodera pallida
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4213498/
https://www.ncbi.nlm.nih.gov/pubmed/25342461
http://dx.doi.org/10.1186/1471-2164-15-923
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