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Abstract
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Host specialization is considered the strongest driver of pathogen evolution. To successfully infect, colonize and complete the life cycle, plant pathogens are under constant selective pressures imposed by hosts, leading to adaptative genomic evolution and possibly new pathogen species or lineages radiation. Implementing population and comparative genomics approaches, we aim to identify evolutionary and molecular patterns of host specialization in fungal plant pathogens using the fungal pathogen Zymoseptoria tritici (causal agent of Septoria tritici blotch in wheat) as a model of study. Unique collections of Z. tritici were isolated from wild (Aegilops spp.) and domesticated (Triticum aestivum) host grasses in the Middle East, and whole-genome sequencing was performed in a subset of isolates from each collection. We observed distinct population structure between the two host-diverging collections and particular genomic features in the Aegilops-infecting isolates that may have shaped their evolutionary history. Phylogenetic analyses indicated that the Aegilops-infecting population forms a separate Z. tritici cluster when compared to worldwide collections of Z. tritici and to closely-related species. Population genomic analyses and demographic inference allow us to characterize the distinct populations and to detect signatures of recent selection. Moreover we find evidence that divergence of the Z. tritici populations on wild and domesticated hosts likely coincided with wheat domestication. Using infection experiments we show that Z. tritici isolates collected from Aegilops spp. only infect their respective host species and not T. aestivum. Together with other aspects, our findings highlight the interplay between agricultural and wild hosts on the evolution of fungal plant pathogens and illustrate a possible route of crop disease emergence.
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