Population Genomic Evidence for a Repeated Introduction and Rapid Expansion of the Fungal Maize Pathogen Setosphaeria turcica in Europe

Abstract

Modern agricultural practices, climate change, and globalization foster the rapid spread of plant pathogens, such as the maize fungal pathogen Setosphaeria turcica, which causes Northern corn leaf blight and expanded into Central Europe during the twentieth century. To investigate the rapid expansion of S. turcica, we sequenced 121 isolates from Europe and Kenya. Population genomic inference revealed a single genetically diverse cluster in Kenya and three clonal lineages with low diversity, as well as one cluster of multiple clonal sublineages in Europe. Phylogenetic dating suggests that all European lineages originated through sexual reproduction outside Europe and were subsequently introgressed multiple times. Unlike isolates from Kenya, European isolates did not show sexual recombination, despite the presence of both MAT1-1 and MAT1-2 mating types. For the clonal lineages, coalescent model selection supported a selectively neutral model with strong exponential population growth, rather than models with pervasive positive selection caused by host defense resistance or environmental adaptation. Within clonal lineages, phenotypic variation in virulence to different monogenic resistances, which defines the pathogen races, suggests that these races may originate from repeated mutations in virulence genes. Association testing based on k-mers did not identify genomic regions linked to pathogen races, but it did uncover strongly differentiated genomic regions between clonal lineages, which harbor genes with putative roles in pathogenicity. In conclusion, the expansion and population growth of S. turcica in Europe are mainly driven by an expansion of the maize cultivation area and not by rapid adaptation.