Whole-genome sequencing reveals diverse mechanisms underlying quantitative pathogenicity and host adaptation in a fungal plant pathogen

Knowledge of genetic determinism and evolutionary dynamics mediating host-pathogen interactions is essential to manage fungal plant diseases. However, the genetic architecture of fungal pathogenicity remains poorly understood, and studies often focus on large-effect effector genes triggering strong, qualitative resistance. It is not clear how this translates to predominately quantitative pathogens. Here, we used the Zymoseptoria tritici-wheat model to elucidate the genetic architecture of quantitative pathogenicity and mechanisms mediating host adaptation. Z. tritici is a globally occurring pathogen that causes severe yield losses on wheat. We perform whole-genome sequencing of 103 isolates and quantified pathogenicity traits on 12 cultivars harbouring different resistance genes. We perform a multi-host GWAS and identified 58 candidate genes associated with pathogenicity, of which nineteen are highly expressed and/or differentially expressed in planta. Two of these had large effects and three were shared in more than one cultivar, suggesting that Z. tritici pathogenicity is predominantly quantitative and host-specific. Analysis of genetic diversity revealed that sequence polymorphism is the main evolutionary process mediating differences in quantitative pathogenicity, a process that is likely facilitated by genetic recombination and transposable elements dynamics. We found signatures of positive diversifying selection in ∼68% of the candidate genes acting on specific amino acid substitutions, likely responsible for evasion of host recognition. Finally, we used functional approaches to confirm the role of an effector-like gene and a methyltransferase in quantitative pathogenicity. This study highlights the complex genetic architecture of quantitative pathogenicity, extensive diversifying selection and plausible mechanisms facilitating pathogen adaptation.