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The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence

BACKGROUND: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote p...

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Autores principales: Eves-van den Akker, Sebastian, Laetsch, Dominik R., Thorpe, Peter, Lilley, Catherine J., Danchin, Etienne G. J., Da Rocha, Martine, Rancurel, Corinne, Holroyd, Nancy E., Cotton, James A., Szitenberg, Amir, Grenier, Eric, Montarry, Josselin, Mimee, Benjamin, Duceppe, Marc-Olivier, Boyes, Ian, Marvin, Jessica M. C., Jones, Laura M., Yusup, Hazijah B., Lafond-Lapalme, Joël, Esquibet, Magali, Sabeh, Michael, Rott, Michael, Overmars, Hein, Finkers-Tomczak, Anna, Smant, Geert, Koutsovoulos, Georgios, Blok, Vivian, Mantelin, Sophie, Cock, Peter J. A., Phillips, Wendy, Henrissat, Bernard, Urwin, Peter E., Blaxter, Mark, Jones, John T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4901422/
https://www.ncbi.nlm.nih.gov/pubmed/27286965
http://dx.doi.org/10.1186/s13059-016-0985-1
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author Eves-van den Akker, Sebastian
Laetsch, Dominik R.
Thorpe, Peter
Lilley, Catherine J.
Danchin, Etienne G. J.
Da Rocha, Martine
Rancurel, Corinne
Holroyd, Nancy E.
Cotton, James A.
Szitenberg, Amir
Grenier, Eric
Montarry, Josselin
Mimee, Benjamin
Duceppe, Marc-Olivier
Boyes, Ian
Marvin, Jessica M. C.
Jones, Laura M.
Yusup, Hazijah B.
Lafond-Lapalme, Joël
Esquibet, Magali
Sabeh, Michael
Rott, Michael
Overmars, Hein
Finkers-Tomczak, Anna
Smant, Geert
Koutsovoulos, Georgios
Blok, Vivian
Mantelin, Sophie
Cock, Peter J. A.
Phillips, Wendy
Henrissat, Bernard
Urwin, Peter E.
Blaxter, Mark
Jones, John T.
author_facet Eves-van den Akker, Sebastian
Laetsch, Dominik R.
Thorpe, Peter
Lilley, Catherine J.
Danchin, Etienne G. J.
Da Rocha, Martine
Rancurel, Corinne
Holroyd, Nancy E.
Cotton, James A.
Szitenberg, Amir
Grenier, Eric
Montarry, Josselin
Mimee, Benjamin
Duceppe, Marc-Olivier
Boyes, Ian
Marvin, Jessica M. C.
Jones, Laura M.
Yusup, Hazijah B.
Lafond-Lapalme, Joël
Esquibet, Magali
Sabeh, Michael
Rott, Michael
Overmars, Hein
Finkers-Tomczak, Anna
Smant, Geert
Koutsovoulos, Georgios
Blok, Vivian
Mantelin, Sophie
Cock, Peter J. A.
Phillips, Wendy
Henrissat, Bernard
Urwin, Peter E.
Blaxter, Mark
Jones, John T.
author_sort Eves-van den Akker, Sebastian
collection PubMed
description BACKGROUND: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes. RESULTS: We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative ‘effector islands’ in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking. CONCLUSIONS: These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-0985-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-49014222016-06-11 The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence Eves-van den Akker, Sebastian Laetsch, Dominik R. Thorpe, Peter Lilley, Catherine J. Danchin, Etienne G. J. Da Rocha, Martine Rancurel, Corinne Holroyd, Nancy E. Cotton, James A. Szitenberg, Amir Grenier, Eric Montarry, Josselin Mimee, Benjamin Duceppe, Marc-Olivier Boyes, Ian Marvin, Jessica M. C. Jones, Laura M. Yusup, Hazijah B. Lafond-Lapalme, Joël Esquibet, Magali Sabeh, Michael Rott, Michael Overmars, Hein Finkers-Tomczak, Anna Smant, Geert Koutsovoulos, Georgios Blok, Vivian Mantelin, Sophie Cock, Peter J. A. Phillips, Wendy Henrissat, Bernard Urwin, Peter E. Blaxter, Mark Jones, John T. Genome Biol Research BACKGROUND: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes. RESULTS: We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative ‘effector islands’ in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking. CONCLUSIONS: These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-0985-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-10 /pmc/articles/PMC4901422/ /pubmed/27286965 http://dx.doi.org/10.1186/s13059-016-0985-1 Text en © The Author(s). 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
Eves-van den Akker, Sebastian
Laetsch, Dominik R.
Thorpe, Peter
Lilley, Catherine J.
Danchin, Etienne G. J.
Da Rocha, Martine
Rancurel, Corinne
Holroyd, Nancy E.
Cotton, James A.
Szitenberg, Amir
Grenier, Eric
Montarry, Josselin
Mimee, Benjamin
Duceppe, Marc-Olivier
Boyes, Ian
Marvin, Jessica M. C.
Jones, Laura M.
Yusup, Hazijah B.
Lafond-Lapalme, Joël
Esquibet, Magali
Sabeh, Michael
Rott, Michael
Overmars, Hein
Finkers-Tomczak, Anna
Smant, Geert
Koutsovoulos, Georgios
Blok, Vivian
Mantelin, Sophie
Cock, Peter J. A.
Phillips, Wendy
Henrissat, Bernard
Urwin, Peter E.
Blaxter, Mark
Jones, John T.
The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
title The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
title_full The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
title_fullStr The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
title_full_unstemmed The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
title_short The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
title_sort genome of the yellow potato cyst nematode, globodera rostochiensis, reveals insights into the basis of parasitism and virulence
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4901422/
https://www.ncbi.nlm.nih.gov/pubmed/27286965
http://dx.doi.org/10.1186/s13059-016-0985-1
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