Host specialization defines the emergence of new fungal plant pathogen populations

Host-driven selection can be considered a strong driver of pathogen evolution. To successfully infect, colonize and complete their life cycle, plant pathogens are under constant selective pressures imposed by hosts, leading to genetic adaptation and possibly lineage radiation or speciation. Population and comparative genomics approaches are powerful tools to identify signatures of selection associated with host specialization in pathogen genomes and further allow recapturing population histories. Implementing such approaches, we identified evolutionary signatures of divergent host specialisation in distinct lineages of the fungal pathogen Zymoseptoria tritici, a major disease causing-agent of wheat. 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 selected subset of isolates from each collection. We observed distinct population structure between the two host-diverging pathogens and identified particular genomic features in the Aegilops-infecting isolates that may have shaped their evolutionary history. Phylogenomic analyses revealed that A. cylindrica and A. tauchii -infecting populations of Z. tritici form separate clusters, possibly reflecting incipient speciation driven by divergent host specialization. Using infection experiments, we confirm that Z. tritici isolates collected from Aegilops spp. only infect their respective host species and not T. aestivum. Population genomics analyses and demographic inference furthermore allowed us to detect signatures of recent selection and show that divergence of the wheat-infecting lineage likely coincided with wheat domestication. At last, we confirm a virulence-related role for one candidate effector located in a selective sweep region of the A. cylindrica-infecting pathogen. Taken together, our findings highlight the interplay between agricultural and wild hosts on the evolution of fungal plant pathogens and illustrate host specialization as a possible route of rapid pathogen emergence.