Herbarium metagenomics reveals the rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine

The oomycete Phytophthora infestans is a plant pathogen of historical dimensions. It is the cause of potato late blight, one of the world’s most destructive crop diseases. Ever since its first global outbreak in the 1840s – which included the Great Famine in Ireland – late blight has been a major threat to potato production. Until a few decades ago, P. infestans genetic diversity outside of its Mexican, center of origin was low, and one scenario held that a single strain had dominated the global P. infestans population for 150 years. This was subsequently challenged, based on the analysis of three SNPs in the mitochondrial DNA of herbarium specimens from the nineteenth century. To resolve this controversy, we have compared the genomes of 11 herbarium samples with 15 modern strains. We conclude that the nineteenth century epidemic was caused by a unique genotype, HERB-1, that persisted for at least 50 years. While HERB-1 is distinct from all examined modern isolates, it is related to the US-1 genotype that replaced it in the global population in the twentieth century. We propose that these two pandemic genotypes emerged from a single metapopulation that was established in the early 1800s either at the margin of the species’ Mexican center of diversity or elsewhere, possibly in North America.