Genomic insights into the evolutionary dynamics of Phytophthora infestans lineages after the Irish Potato Famine

Abstract Background Genomic analysis of infected herbarium specimens provides the opportunity to investigate the evolutionary history of plant pathogens, leading to discoveries such as the identification of FAM-1/HERB-1 as the Phytophthora infestans lineage that caused the nineteenth-century Irish Potato Famine. However, the subsequent evolutionary history of P. infestans in Europe remains unclear. Using herbarium specimens to study genetic changes in plant pathogens such as P. infestans with high spatial and temporal resolution requires an efficient sampling strategy to specifically target the pathogen DNA from herbarium specimens. Results We sampled plant tissue infected with P. infestans from four different locations from each of 23 herbarium specimens collected in Europe between 1850 and 1982. We detected highest pathogen DNA yields in tissue from lesions and tissue adjacent to lesions. The obtained genomic sequencing data allowed the reconstruction of ten mitochondrial and five nuclear P. infestans genomes, which we analyzed together with previously published historical and modern genomes. Our phylogenetic analysis confirmed the persistence of the FAM-1/HERB-1 lineage in Europe until at least 1946, after which FAM-1/HERB-1 appears to have been replaced by the lineage US-1/Ib. In addition, metagenomic analysis revealed historical co-infections between P. infestans and Alternaria solani , supporting the feasibility of our sampling strategy to recover plant pathogens. Conclusions We established an efficient tissue-sampling strategy for plant-pathogen DNA recovery from herbarium samples. Our findings provide important insights into the evolutionary history of P. infestans in Europe including the replacement of FAM-1/HERB-1 by US-1/Ib in the mid-twentieth century as well as historical co-infections with two other plant pathogens.