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.

Septoria leaf blotch is a foliar wheat disease controlled by a combination of plant genetic resistances and fungicides use. R-gene-based qualitative resistance durability is limited due to gene-for-gene interactions with fungal avirulence (Avr) genes. Quantitative resistance is considered more durable but the mechanisms involved are not well documented. We hypothesize that genes involved in quantitative and qualitative plant-pathogen interactions are similar. A bi-parental population of Zymoseptoria tritici was inoculated on wheat cultivar ‘Renan’ and a linkage analysis performed to map QTL. Three pathogenicity QTL, Qzt-I05-1, Qzt-I05-6 and Qzt-I07-13, were mapped on chromosomes 1, 6 and 13 in Z. tritici, and a candidate pathogenicity gene on chromosome 6 was selected based on its effector-like characteristics. The candidate gene was cloned by Agrobacterium tumefaciens-mediated transformation, and a pathology test assessed the effect of the mutant strains on ‘Renan’. This gene was demonstrated to be involved in quantitative pathogenicity. By cloning a newly annotated quantitative-effect gene in Z. tritici that is effector-like, we demonstrated that genes underlying pathogenicity QTL can be similar to Avr genes. This opens up the previously probed possibility that ‘gene-for-gene’ underlies not only qualitative but also quantitative plant-pathogen interactions in this pathosystem.