Genome Analyses of an Aggressive and Invasive Lineage of the Irish Potato Famine Pathogen

D E L Cooke ,Mathieu A Pel,Eva Randall,Graham J Etherington,Kenneth L Deahl,Eleanor M Gilroy,Rhys A Farrer,Sophien Kamoun,Sylvain Raffaele,Vivianne G A A Vleeshouwers,Niklaus J Grünwald,Paul R J Birch,Erica M Goss,James W Mcnicol,Ingo Hein,Julie Squires ,Ricardo Oliva ,A K Lees ,R A Bain ,Moray Taylor ,Liliana Cano ,David Shaw ,Dan Maclean ,L R Cooke

doi:10.1371/journal.ppat.1002940

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.

Highlights

As the cause of potato late blight, Phytophthora infestans is one of the most destructive plant pathogens within this genus of funguslike oomycetes and widely known as the Irish potato famine pathogen [1,2]
We investigated changes in the population of the late blight pathogen P. infestans in Great Britain (GB) and identified a major new lineage of P. infestans that first emerged in mainland Europe in 2004
Late blight caused by this lineage has proved challenging to manage and its migration to other potato growing regions of the world poses a threat to sustainable crop production

Summary

Introduction

As the cause of potato late blight, Phytophthora infestans is one of the most destructive plant pathogens within this genus of funguslike oomycetes and widely known as the Irish potato famine pathogen [1,2]. P. infestans has migrated from Central or South America [3,4], where it infects many native solanaceous hosts, and remains responsible for significant losses to key staple crops (potato, tomato and other solanaceous plants) worldwide [5,6]. Potato late blight management relies on regular applications of a range of anti-oomycete ‘fungicides’. Under optimal weather conditions the pathogen may complete several infection cycles a week on a susceptible host, with control failure leading to rapid epidemics and crop loss. P. infestans is normally diploid with a heterothallic (i.e. outbreeding) mating system that

Author Summary

Conclusions

Findings

Materials and Methods