Population history of the Northern corn leaf blight fungal pathogen Setosphaeria turcica in Europe

Setosphaeria turcica is a major fungal pathogen of maize and causes the foliar disease Northern corn leaf blight (NCLB). It originates from tropical regions and expanded into Central Europe since the 1980s, simultaneously with a rapid increase of maize cultivation area in this region. To investigate evolutionary processes influencing the rapid expansion of S. turcica we sequenced 121 isolates from Central Europe, Western Europe and Kenya. Population genetic inference revealed five genetically distinct clusters that differ by their geographic distribution and emergence dates. One genetically diverse cluster is restricted to Kenya, and the four European clusters consist of three distinct clonal lineages with low genetic diversity and one genetically diverse cluster with several clonal sublineages. A comparison of two different coalescent models for genetic diversity in the most frequent and geographically widespread clonal lineage in Europe supported a model of neutral, strongly exponential population growth over models accounting for different types of selection. In contrast to Kenyan isolates, European isolates did not show sexual recombination despite the presence of both mating types MAT1-1 and MAT1-2 in Europe. Within clonal lineages phenotypic variation in virulence to different monogenic resistances likely originated from repeated de novo mutations in virulence genes of S. turcica. k-mer based association mapping between genetic clusters did not identify genomic regions associated with pathogen races but few genomic regions that are significantly differentiated between two clonal lineages and contain putative effector genes. Our results suggest that the rapid colonization of Europe by different clonal lineages of S. turcica was not driven by selection of virulent races but reflects a neutral demographic process of fast pathogen population growth fostered by a rapid expansion of the maize cultivation area in this region.