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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 theZymoseptoria tritici-wheat model to elucidate the genetic architecture of quantitative pathogenicity and mechanisms mediating host adaptation.Z. triticiis 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 expressedin planta. Two of these had large effects and three were shared in more than one cultivar, suggesting thatZ. triticipathogenicity 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.

Zymoseptoria triticiis the fungal pathogen responsible for Septoria tritici blotch on wheat. Disease outcome in this pathosystem is partly determined by isolate-specific resistance, where wheat resistance genes recognize specific fungal factors triggering an immune response. Despite the large number of known wheat resistance genes, fungal molecular determinants involved in such cultivar-specific resistance remain largely unknown. We identified the avirulence factorAvrStb9using association mapping and functional validation approaches. PathotypingAvrStb9transgenic strains onStb9cultivars, near isogenic lines and wheat mapping populations, showed thatAvrStb9interacts withStb9resistance gene, triggering an immune response.AvrStb9encodes an unusually large avirulence gene with a predicted secretion signal and a protease domain. It belongs to a S41 protease family conserved across different filamentous fungi in the Ascomycota class and may constitute a core effector.AvrStb9is also conserved among a globalZ. triticipopulation and carries multiple amino acid substitutions caused by strong positive diversifying selection. These results demonstrate the contribution of an ‘atypical’ conserved effector protein to fungal avirulence and the role of sequence diversification in the escape of host recognition, adding to our understanding of host-pathogen interactions and the evolutionary processes underlying pathogen adaptation.Author SummaryFungal avirulence (Avr) genes are involved in gene-for-gene relationships with host resistance genes.Avrgenes may at the same time target host defenses to allow infection and be recognized by a host resistance gene triggering a defense response. The fungusZymoseptoria triticicauses Septoria tritici blotch, a major disease of wheat worldwide.Z. triticipopulations rapidly adapt to selection pressures such as host resistance, leading to resistance breakdown. We report the identification of the avirulence geneAvrStb9based on genetic mapping, sequence polymorphisms and allele swapping.AvrStb9is involved in the interaction withStb9resistance gene following the gene-for-gene model, and its recognition hinders disease symptoms in hosts carrying the corresponding resistance gene. Unlike other knownZ. tritici Avreffectors,AvrStb9encodes for an unusually large Avr protein with a predicted protease S41 domain conserved among diverse ascomycete lineages. We also highlight several gene mutations likely involved in escapingStb9-mediated recognition.