TY - JOUR

T1 - The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence

AU - Eves-van den Akker, Sebastian

AU - Laetsch, Dominik R.

AU - Thorpe, Peter

AU - Lilley, Catherine J.

AU - Danchin, Etienne G. J.

AU - Da Rocha, Martine

AU - Rancurel, Corinne

AU - Holroyd, Nancy E.

AU - Cotton, James A.

AU - Szitenberg, Amir

AU - Grenier, Eric

AU - Montarry, Josselin

AU - Mimee, Benjamin

AU - Duceppe, Marc-Olivier

AU - Boyes, Ian

AU - Marvin, Jessica M. C.

AU - Jones, Laura M.

AU - Yusup, Hazijah B.

AU - Lafond-Lapalme, Joël

AU - Esquibet, Magali

AU - Sabeh, Michael

AU - Rott, Michael

AU - Overmars, Hein

AU - Finkers-Tomczak, Anna

AU - Smant, Geert

AU - Koutsovoulos, Georgios

AU - Blok, Vivian

AU - Mantelin, Sophie

AU - Cock, Peter J. A.

AU - Phillips, Wendy

AU - Henrissat, Bernard

AU - Urwin, Peter E.

AU - Blaxter, Mark

AU - Jones, John T.

N1 - SE-vdA is supported by BBSRC grant BB/M014207/1. Sequencing was funded by BBSRC grant BB/F000642/1 to the University of Leeds and grant BB/F00334X/1 to the Wellcome Trust Sanger Institute). DRL was supported by a fellowship from The James Hutton Institute and the School of Biological Sciences, University of Edinburgh. GK was supported by a BBSRC PhD studentship. The James Hutton Institute receives funding from the Scottish Government. JAC and NEH are supported by the Wellcome Trust through its core funding of the Wellcome Trust Sanger Institute (grant 098051). This work was also supported by funding from the Canadian Safety and Security Program, project number CRTI09_462RD.

PY - 2016/6/10

Y1 - 2016/6/10

N2 - 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.

AB - 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.

KW - Plant-parasitic nematode

KW - Genome sequence

KW - Virulence

KW - Effectors

KW - Horizontal gene transfer

U2 - 10.1186/s13059-016-0985-1

DO - 10.1186/s13059-016-0985-1

M3 - Article

C2 - 27286965

VL - 17

JO - Genome Biology

JF - Genome Biology

SN - 1465-6906

M1 - 124

ER -