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

David E L Cooke (Corresponding Author), Liliana M Cano, Sylvain Raffaele, Ruairidh A Bain, Louise R Cooke, Graham J Etherington, Kenneth L Deahl, Rhys A Farrer, Eleanor M Gilroy, Erica M Goss, Niklaus J Grünwald, Ingo Hein, Daniel MacLean, James W McNicol, Eva Randall, Ricardo F Oliva, Mathieu A Pel, David S Shaw, Julie N Squires, Moray C Taylor & 4 others Vivianne G A A Vleeshouwers, Paul R. J. Birch, Alison K Lees, Sophien Kamoun

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Abstract

Pest and pathogen losses jeopardise global food security and ever since the 19(th) 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
Article numbere1002940
Number of pages14
JournalPLoS Pathogens
Volume8
Issue number10
DOIs
Publication statusPublished - 4 Oct 2012

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Solanum tuberosum
Starvation
varespladib methyl
Genome
Phytophthora infestans
Population
Genes
Oomycetes
Gene Dosage
Food Supply
Disease Management
Virulence
Amino Acids

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Cooke, D. E. L., Cano, L. M., Raffaele, S., Bain, R. A., Cooke, L. R., Etherington, G. J., ... Kamoun, S. (2012). Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathogens, 8(10), [e1002940]. https://doi.org/10.1371/journal.ppat.1002940

Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. / Cooke, David E L (Corresponding Author); Cano, Liliana M; Raffaele, Sylvain; Bain, Ruairidh A; Cooke, Louise R; Etherington, Graham J; Deahl, Kenneth L; Farrer, Rhys A; Gilroy, Eleanor M; Goss, Erica M; Grünwald, Niklaus J; Hein, Ingo; MacLean, Daniel; McNicol, James W; Randall, Eva; Oliva, Ricardo F; Pel, Mathieu A; Shaw, David S; Squires, Julie N; Taylor, Moray C; Vleeshouwers, Vivianne G A A; Birch, Paul R. J.; Lees, Alison K; Kamoun, Sophien (Corresponding Author).

In: PLoS Pathogens, Vol. 8, No. 10, e1002940, 04.10.2012.

Research output: Contribution to journalArticle

Cooke, DEL, Cano, LM, Raffaele, S, Bain, RA, Cooke, LR, Etherington, GJ, Deahl, KL, Farrer, RA, Gilroy, EM, Goss, EM, Grünwald, 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, no. 10, e1002940. https://doi.org/10.1371/journal.ppat.1002940
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 Oct 4;8(10). e1002940. https://doi.org/10.1371/journal.ppat.1002940
Cooke, David E L ; Cano, Liliana M ; Raffaele, Sylvain ; Bain, Ruairidh A ; Cooke, Louise R ; Etherington, Graham J ; Deahl, Kenneth L ; Farrer, Rhys A ; Gilroy, Eleanor M ; Goss, Erica M ; Grünwald, Niklaus J ; Hein, Ingo ; MacLean, Daniel ; McNicol, James W ; Randall, Eva ; Oliva, Ricardo F ; Pel, Mathieu A ; Shaw, David S ; Squires, Julie N ; Taylor, Moray C ; Vleeshouwers, Vivianne G A A ; Birch, Paul R. J. ; Lees, Alison K ; Kamoun, Sophien. / Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. In: PLoS Pathogens. 2012 ; Vol. 8, No. 10.
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abstract = "Pest and pathogen losses jeopardise global food security and ever since the 19(th) 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.",
author = "Cooke, {David E L} and Cano, {Liliana M} and Sylvain Raffaele and Bain, {Ruairidh A} and Cooke, {Louise R} and Etherington, {Graham J} and Deahl, {Kenneth L} and Farrer, {Rhys A} and Gilroy, {Eleanor M} and Goss, {Erica M} and Gr{\"u}nwald, {Niklaus J} and Ingo Hein and Daniel MacLean and McNicol, {James W} and Eva Randall and Oliva, {Ricardo F} and Pel, {Mathieu A} and Shaw, {David S} and Squires, {Julie N} and Taylor, {Moray C} and Vleeshouwers, {Vivianne G A A} and Birch, {Paul R. J.} and Lees, {Alison K} and Sophien Kamoun",
note = "This work was supported by the Potato Council and The Scottish Government (D.E.L. Cooke, A.K. Lees, I. Hein, E.M. Gilroy, E. Randall, J.N. Squires, P.R.J. Birch & R.A. Bain), the Gatsby Charitable Foundation (S. Kamoun, L.M. Cano, S. Rafaelle, G.J. Etherington & R.A. Farrer), a Marie Curie IEF (contract 255104) to S. Rafaelle, the Dutch Ministry of Agriculture, Nature and Food Quality to V.G.A.A. Vleeshouwers and the FP6 program BioExploit Food-CT-2005-513959 supported M.A. Pel. A BBSRC/RESAS CRF grant also supported D.E.L. Cooke, E. Gilroy, P. Birch, S. Kamoun & I.Hein. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.",
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AU - Cooke, David E L

AU - Cano, Liliana M

AU - Raffaele, Sylvain

AU - Bain, Ruairidh A

AU - Cooke, Louise R

AU - Etherington, Graham J

AU - Deahl, Kenneth L

AU - Farrer, Rhys A

AU - Gilroy, Eleanor M

AU - Goss, Erica M

AU - Grünwald, Niklaus J

AU - Hein, Ingo

AU - MacLean, Daniel

AU - McNicol, James W

AU - Randall, Eva

AU - Oliva, Ricardo F

AU - Pel, Mathieu A

AU - Shaw, David S

AU - Squires, Julie N

AU - Taylor, Moray C

AU - Vleeshouwers, Vivianne G A A

AU - Birch, Paul R. J.

AU - Lees, Alison K

AU - Kamoun, Sophien

N1 - This work was supported by the Potato Council and The Scottish Government (D.E.L. Cooke, A.K. Lees, I. Hein, E.M. Gilroy, E. Randall, J.N. Squires, P.R.J. Birch & R.A. Bain), the Gatsby Charitable Foundation (S. Kamoun, L.M. Cano, S. Rafaelle, G.J. Etherington & R.A. Farrer), a Marie Curie IEF (contract 255104) to S. Rafaelle, the Dutch Ministry of Agriculture, Nature and Food Quality to V.G.A.A. Vleeshouwers and the FP6 program BioExploit Food-CT-2005-513959 supported M.A. Pel. A BBSRC/RESAS CRF grant also supported D.E.L. Cooke, E. Gilroy, P. Birch, S. Kamoun & I.Hein. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

PY - 2012/10/4

Y1 - 2012/10/4

N2 - Pest and pathogen losses jeopardise global food security and ever since the 19(th) 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 19(th) 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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DO - 10.1371/journal.ppat.1002940

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JO - PLoS Pathogens

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