Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen

DEL Cooke, LM Cano, S Raffaele, RA Bain, LR Cooke, GJ Etherington, KL Deahl, RA Farrer, EM Gilroy, EM Goss, NJ Grunwald, I Hein, D MacLean, JW McNicol, E Randall, RF Oliva, MA Pel, DS Shaw, JN Squires, MC TaylorVGAA Vleeshouwers, PRJ Birch, AK Lees, S Kamoun

Research output: Contribution to journalArticle

201 Citations (Scopus)

Abstract

Pest and pathogen losses jeopardise global food security and ever since the 19th century Irish famine, potato late blight has exemplified this threat. The causal oomycete pathogen, Phytophthora infestans, undergoes major population shifts in agricultural systems via the successive emergence and migration of asexual lineages. The phenotypic and genotypic bases of these selective sweeps are largely unknown but management strategies need to adapt to reflect the changing pathogen population. Here, we used molecular markers to document the emergence of a lineage, termed 13_A2, in the European P. infestans population, and its rapid displacement of other lineages to exceed 75% of the pathogen population across Great Britain in less than three years. We show that isolates of the 13_A2 lineage are among the most aggressive on cultivated potatoes, outcompete other aggressive lineages in the field, and overcome previously effective forms of plant host resistance. Genome analyses of a 13_A2 isolate revealed extensive genetic and expression polymorphisms particularly in effector genes. Copy number variations, gene gains and losses, amino-acid replacements and changes in expression patterns of disease effector genes within the 13_A2 isolate likely contribute to enhanced virulence and aggressiveness to drive this population displacement. Importantly, 13_A2 isolates carry intact and in planta induced Avrblb1, Avrblb2 and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding R immune receptor genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. These findings point towards a strategy for deploying genetic resistance to mitigate the impact of the 13_A2 lineage and illustrate how pathogen population monitoring, combined with genome analysis, informs the management of devastating disease epidemics.
Original languageEnglish
Pages (from-to)1 - 14
Number of pages14
JournalPLoS Pathogens
Volume8(10)
Publication statusFirst published - 2012

Fingerprint

genome
pathogens
Phytophthora infestans
genes
food defense
famine
Oomycetes
genetic resistance
plant architecture
Plantae
aggression
virulence
Irish potato famine
genetic polymorphism
pests
potatoes
amino acids
genetic markers
monitoring

Bibliographical note

509331

Keywords

  • Genome analysis
  • Irish potato famine
  • Potato

Cite this

Cooke, DEL., Cano, LM., Raffaele, S., Bain, RA., Cooke, LR., Etherington, GJ., ... Kamoun, S. (2012). Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathogens, 8(10), 1 - 14.
Cooke, DEL ; Cano, LM ; Raffaele, S ; Bain, RA ; Cooke, LR ; Etherington, GJ ; Deahl, KL ; Farrer, RA ; Gilroy, EM ; Goss, EM ; Grunwald, NJ ; Hein, I ; MacLean, D ; McNicol, JW ; Randall, E ; Oliva, RF ; Pel, MA ; Shaw, DS ; Squires, JN ; Taylor, MC ; Vleeshouwers, VGAA ; Birch, PRJ ; Lees, AK ; Kamoun, S. / Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. In: PLoS Pathogens. 2012 ; Vol. 8(10). pp. 1 - 14.
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Cooke, DEL, Cano, LM, Raffaele, S, Bain, RA, Cooke, LR, Etherington, GJ, Deahl, KL, Farrer, RA, Gilroy, EM, Goss, EM, Grunwald, NJ, Hein, I, MacLean, D, McNicol, JW, Randall, E, Oliva, RF, Pel, MA, Shaw, DS, Squires, JN, Taylor, MC, Vleeshouwers, VGAA, Birch, PRJ, Lees, AK & Kamoun, S 2012, 'Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen', PLoS Pathogens, vol. 8(10), pp. 1 - 14.

Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. / Cooke, DEL; Cano, LM; Raffaele, S; Bain, RA; Cooke, LR; Etherington, GJ; Deahl, KL; Farrer, RA; Gilroy, EM; Goss, EM; Grunwald, NJ; Hein, I; MacLean, D; McNicol, JW; Randall, E; Oliva, RF; Pel, MA; Shaw, DS; Squires, JN; Taylor, MC; Vleeshouwers, VGAA; Birch, PRJ; Lees, AK; Kamoun, S.

In: PLoS Pathogens, Vol. 8(10), 2012, p. 1 - 14.

Research output: Contribution to journalArticle

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T1 - Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen

AU - Cooke, DEL

AU - Cano, LM

AU - Raffaele, S

AU - Bain, RA

AU - Cooke, LR

AU - Etherington, GJ

AU - Deahl, KL

AU - Farrer, RA

AU - Gilroy, EM

AU - Goss, EM

AU - Grunwald, NJ

AU - Hein, I

AU - MacLean, D

AU - McNicol, JW

AU - Randall, E

AU - Oliva, RF

AU - Pel, MA

AU - Shaw, DS

AU - Squires, JN

AU - Taylor, MC

AU - Vleeshouwers, VGAA

AU - Birch, PRJ

AU - Lees, AK

AU - Kamoun, S

N1 - 509331

PY - 2012

Y1 - 2012

N2 - Pest and pathogen losses jeopardise global food security and ever since the 19th century Irish famine, potato late blight has exemplified this threat. The causal oomycete pathogen, Phytophthora infestans, undergoes major population shifts in agricultural systems via the successive emergence and migration of asexual lineages. The phenotypic and genotypic bases of these selective sweeps are largely unknown but management strategies need to adapt to reflect the changing pathogen population. Here, we used molecular markers to document the emergence of a lineage, termed 13_A2, in the European P. infestans population, and its rapid displacement of other lineages to exceed 75% of the pathogen population across Great Britain in less than three years. We show that isolates of the 13_A2 lineage are among the most aggressive on cultivated potatoes, outcompete other aggressive lineages in the field, and overcome previously effective forms of plant host resistance. Genome analyses of a 13_A2 isolate revealed extensive genetic and expression polymorphisms particularly in effector genes. Copy number variations, gene gains and losses, amino-acid replacements and changes in expression patterns of disease effector genes within the 13_A2 isolate likely contribute to enhanced virulence and aggressiveness to drive this population displacement. Importantly, 13_A2 isolates carry intact and in planta induced Avrblb1, Avrblb2 and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding R immune receptor genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. These findings point towards a strategy for deploying genetic resistance to mitigate the impact of the 13_A2 lineage and illustrate how pathogen population monitoring, combined with genome analysis, informs the management of devastating disease epidemics.

AB - Pest and pathogen losses jeopardise global food security and ever since the 19th century Irish famine, potato late blight has exemplified this threat. The causal oomycete pathogen, Phytophthora infestans, undergoes major population shifts in agricultural systems via the successive emergence and migration of asexual lineages. The phenotypic and genotypic bases of these selective sweeps are largely unknown but management strategies need to adapt to reflect the changing pathogen population. Here, we used molecular markers to document the emergence of a lineage, termed 13_A2, in the European P. infestans population, and its rapid displacement of other lineages to exceed 75% of the pathogen population across Great Britain in less than three years. We show that isolates of the 13_A2 lineage are among the most aggressive on cultivated potatoes, outcompete other aggressive lineages in the field, and overcome previously effective forms of plant host resistance. Genome analyses of a 13_A2 isolate revealed extensive genetic and expression polymorphisms particularly in effector genes. Copy number variations, gene gains and losses, amino-acid replacements and changes in expression patterns of disease effector genes within the 13_A2 isolate likely contribute to enhanced virulence and aggressiveness to drive this population displacement. Importantly, 13_A2 isolates carry intact and in planta induced Avrblb1, Avrblb2 and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding R immune receptor genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. These findings point towards a strategy for deploying genetic resistance to mitigate the impact of the 13_A2 lineage and illustrate how pathogen population monitoring, combined with genome analysis, informs the management of devastating disease epidemics.

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JO - PLoS Pathogens

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SN - 1553-7366

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Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ et al. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathogens. 2012;8(10):1 - 14.