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.

病虫害与病原菌造成的产量损失严重威胁全球粮食安全。自19世纪爱尔兰大饥荒以来，马铃薯晚疫病（potato late blight）便始终是这类威胁的典型缩影。其致病卵菌病原体（oomycete pathogen）——致病疫霉（Phytophthora infestans）——在农业生产系统中，通过无性谱系（asexual lineages）的持续出现与迁移发生显著的种群结构更替。这类选择性清除（selective sweeps）事件的表型与基因型基础在很大程度上仍未明确，但病害防控策略必须适配不断演变的病原菌种群。本研究借助分子标记（molecular markers），记录了欧洲致病疫霉种群中13_A2谱系的出现，并证实该谱系可在三年内快速取代其他谱系，使其在大不列颠岛范围内的病原菌种群占比超过75%。研究表明，13_A2谱系的菌株是栽培马铃薯上致病力最强的菌株之一，可在田间竞争中胜出其他强致病谱系，并能突破此前已被证实有效的植物寄主抗性。对一株13_A2菌株的基因组分析显示，其存在广泛的遗传与表达多态性，尤其富集于效应基因（effector genes）区域。13_A2菌株中病害效应基因的拷贝数变异（copy number variations）、基因得失、氨基酸替换（amino-acid replacements）以及表达模式（expression patterns）改变，可能有助于增强其毒力（virulence）与致病力（aggressiveness），进而推动此次种群更替事件。尤为关键的是，13_A2菌株携带完整且在植物体内诱导（in planta induced）表达的Avrblb1、Avrblb2与Avrvnt1效应基因，这些基因可在携带对应R类免疫受体基因（R immune receptor genes）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（genetic resistance）以减轻13_A2谱系的危害提供了可行策略，并阐明了结合基因组分析（genome analysis）的病原菌种群监测（pathogen population monitoring）如何为毁灭性病害流行的防控提供科学支撑。