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

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.病虫草害与病原微生物造成的损失严重威胁全球粮食安全，自19世纪爱尔兰饥荒以来，马铃薯晚疫病便一直是这类威胁的典型代表。其致病菌为致病疫霉（Phytophthora infestans），该卵菌病原通过无性谱系的持续出现与迁移，在农业系统中引发种群结构的重大变化。这类选择性扫荡的表型与遗传基础在很大程度上仍不明确，但病害防控策略必须随之调整以适配不断变化的病原种群结构。本研究借助分子标记，证实了欧洲致病疫霉种群中13_A2谱系的出现，并发现其在三年内迅速取代其他谱系，在英国全境的病原种群占比超过75%。研究表明，13_A2谱系的菌株对栽培马铃薯具有极强的致病力，在田间可竞争淘汰其他高致病力谱系，且能突破此前已被证实有效的植物宿主抗病性。对一株13_A2菌株的基因组分析显示，该菌株存在广泛的遗传与表达多态性，尤其是在效应子（effector）基因区域。13_A2菌株中效应子基因的拷贝数变异、基因增减、氨基酸替换以及表达模式改变，可能是其致病力与侵袭能力增强的原因，进而推动了种群取代过程。值得注意的是，13_A2菌株携带完整且在植物体内诱导表达的Avrblb1、Avrblb2与Avrvnt1效应子基因，这些基因可在携带对应免疫受体R基因Rpi-blb1、Rpi-blb2及Rpi-vnt1.1的马铃薯品系中触发抗病性。本研究结果为部署遗传抗性以缓解13_A2谱系的危害提供了可行方向，同时也阐明了病原种群监测结合基因组分析，如何为毁灭性病害流行的防控提供科学依据。