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

Sebastian Eves-van den Akker*, Dominik R. Laetsch, Peter Thorpe, Catherine J. Lilley, Etienne G.J. Danchin, Martine Da Rocha, Corinne Rancurel, Nancy E. Holroyd, James A. Cotton, Amir Szitenberg, Eric Grenier, Josselin Montarry, Benjamin Mimee, Marc Olivier Duceppe, Ian Boyes, Jessica M.C. Marvin, Laura M. Jones, Hazijah B. Yusup, Joël Lafond-Lapalme, Magali EsquibetMichael Sabeh, Michael Rott, Hein Overmars, Anna Finkers-Tomczak, Geert Smant, Georgios Koutsovoulos, Vivian Blok, Sophie Mantelin, Peter J.A. Cock, Wendy Phillips, Bernard Henrissat, Peter E. Urwin, Mark Blaxter, John T. Jones

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

66 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article number124
JournalGenome Biology
Volume17
Issue number1
DOIs
Publication statusPublished - 2016

Keywords

  • Effectors
  • Genome sequence
  • Horizontal gene transfer
  • Plant-parasitic nematode
  • Virulence

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

    Eves-van den Akker, S. (Creator), Laetsch, D. R. (Creator), Thorpe, P. (Creator), Lilley, C. J. (Creator), Danchin, E. G. J. (Creator), Da Rocha, M. (Creator), Rancurel, C. (Creator), Holroyd, N. E. (Creator), Cotton, J. A. (Creator), Szitenberg, A. (Creator), Grenier, E. (Creator), Montarry, J. (Creator), Mimee, B. (Creator), Duceppe, M. O. (Creator), Boyes, I. (Creator), Marvin, J. M. C. (Creator), Jones, L. M. (Creator), Yusup, H. B. (Creator), Lafond-Lapalme, J. (Creator), Esquibet, M. (Creator), Sabeh, M. (Creator), Rott, M. (Creator), Overmars, H. (Creator), Finkers-Tomczak, A. M. (Creator) & Smant, G. (Creator), Wageningen University & Research, 2016

    Dataset

    Globodera rostochiensis Raw sequence reads

    Eves-van den Akker, S. (Creator), Laetsch, D. R. (Creator), Thorpe, P. (Creator), Lilley, C. J. (Creator), Danchin, E. G. J. (Creator), Da Rocha, M. (Creator), Rancurel, C. (Creator), Holroyd, N. E. (Creator), Cotton, J. A. (Creator), Szitenberg, A. (Creator), Overmars, H. (Creator), Finkers-Tomczak, A. M. (Creator) & Smant, G. (Creator), Agriculture and Agri-Food Canada, 12 Dec 2015

    Dataset

    Cite this

    Eves-van den Akker, S., Laetsch, D. R., Thorpe, P., Lilley, C. J., Danchin, E. G. J., Da Rocha, M., Rancurel, C., Holroyd, N. E., Cotton, J. A., Szitenberg, A., Grenier, E., Montarry, J., Mimee, B., Duceppe, M. O., Boyes, I., Marvin, J. M. C., Jones, L. M., Yusup, H. B., Lafond-Lapalme, J., ... Jones, J. T. (2016). The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome Biology, 17(1), [124]. https://doi.org/10.1186/s13059-016-0985-1