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



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.



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.
Division of Plant Sciences, College of Life Sciences, University of Dundee, Dundee, DD1 5EH, UK. s.evesvandenakker@dundee.ac.uk.
Sebastian
S
Eves-van den Akker
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK.
Dominik R
DR
Laetsch
Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK.
Peter
P
Thorpe
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK.
Catherine J
CJ
Lilley
INRA, University Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Etienne G J
EG
Danchin
INRA, University Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Martine
M
Da Rocha
INRA, University Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France.
Corinne
C
Rancurel
Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, CB10 1SA, UK.
Nancy E
NE
Holroyd
Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, CB10 1SA, UK.
James A
JA
Cotton
School of Biological, Biomedical and Environmental Sciences, University of Hull, Hull, HU6 7RX, UK.
Amir
A
Szitenberg
INRA, UMR1349 IGEPP (Institute for Genetics, Environment and Plant Protection), 35653, Le Rheu, France.
Eric
E
Grenier
INRA, UMR1349 IGEPP (Institute for Genetics, Environment and Plant Protection), 35653, Le Rheu, France.
Josselin
J
Montarry
Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada.
Benjamin
B
Mimee
Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada.
Marc-Olivier
MO
Duceppe
Sidney Laboratory, Canadian Food Inspection Agency (CFIA), 8801 East Saanich Rd, Sidney, BC, V8L 1H3, Canada.
Ian
I
Boyes
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK.
Jessica M C
JM
Marvin
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK.
Laura M
LM
Jones
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK.
Hazijah B
HB
Yusup
Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada.
Joël
J
Lafond-Lapalme
INRA, UMR1349 IGEPP (Institute for Genetics, Environment and Plant Protection), 35653, Le Rheu, France.
Magali
M
Esquibet
Agriculture and Agri-food Canada, Horticulture Research and Development Centre, 430 Bboul. Gouin, St-Jean-sur-Richelieu, Quebec, J3B 3E6, Canada.
Michael
M
Sabeh
Sidney Laboratory, Canadian Food Inspection Agency (CFIA), 8801 East Saanich Rd, Sidney, BC, V8L 1H3, Canada.
Michael
M
Rott
Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands.
Hein
H
Overmars
Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands.
Anna
A
Finkers-Tomczak
Laboratory of Nematology, Department of Plant Sciences, Wageningen University, Droevendaalsesteeg 1, 6708, PB, Wageningen, The Netherlands.
Geert
G
Smant
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK.
Georgios
G
Koutsovoulos
Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK.
Vivian
V
Blok
Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK.
Sophie
S
Mantelin
Information and Computational Sciences Group, James Hutton Institute, Dundee, UK.
Peter J A
PJ
Cock
USDA-ARS Horticultural Crops Research Laboratory, Corvallis, OR, USA.
Wendy
W
Phillips
CNRS UMR 7257, INRA, USC 1408, Aix-Marseille University, AFMB, 13288, Marseille, France.|Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
Bernard
B
Henrissat
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK.
Peter E
PE
Urwin
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK.
Mark
M
Blaxter
Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, DD2 5DA, UK.|School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK.
John T
JT
Jones
D000818:Animals; D004742:Enhancer Elements, Genetic; D020869:Gene Expression Profiling; D022761:Gene Transfer, Horizontal; D018503:Genome, Protozoan; D044404:Genomic Islands; D023281:Genomics / Q000379:methods; D059014:High-Throughput Nucleotide Sequencing; D008018:Life Cycle Stages; D059372:Nucleotide Motifs; D010935:Plant Diseases / Q000469:parasitology*; D056510:Position-Specific Scoring Matrices; D022821:RNA Splice Sites; D012326:RNA Splicing; D011198:Solanum tuberosum / Q000469:parasitology*; D059467:Transcriptome; D014431:Tylenchoidea / Q000235:genetics* / Q000254:growth & development / Q000472:pathogenicity*; D014774:Virulence / Q000235:genetics
D022821:RNA Splice Sites
Effectors; Genome sequence; Horizontal gene transfer; Plant-parasitic nematode; Virulence