Interspecific gene exchange introduces high genetic variability in crop pathogen

Genome analyses have revealed a profound role of hybridization and introgression in the evolution of many eukaryote lineages, including fungi. The impact of recurrent introgression on fungal evolution however remains elusive. Here, we analyzed signatures of introgression along the genome of the fungal wheat pathogen Zymoseptoria tritici. We applied a comparative population genomics approach, including genome data from five Zymoseptoria species, to characterize the distribution and composition of introgressed regions representing segments with an exceptional haplotype pattern. These regions are found throughout the genome, comprising five percent of the total genome and overlapping with > 1000 predicted genes. We performed window-based phylogenetic analyses along the genome to distinguish regions which have a monophyletic or non-monophyletic origin with Z. tritici sequences. A majority of non-monophyletic windows overlap with the highly variable regions suggesting that these originate from introgression. We verified that incongruent gene genealogies do not result from incomplete lineage sorting (ILS) by comparing the observed and expected length distribution of haplotype blocks resulting from ILS. Although protein-coding genes are not enriched in these regions, we identify 18 that encode putative virulence determinants. Moreover, we find an enrichment of transposable elements (TEs) in these regions implying that hybridization may contribute to the horizontal spread of TEs. We detected a similar pattern in the closely related species Zymoseptoria ardabiliae, suggesting that hybridization is widespread among these closely related grass pathogens. Overall, our results demonstrate a significant impact of recurrent hybridization on overall genome evolution of this important wheat pathogen