Diversification, loss, and virulence gains of the major effector AvrStb6 during continental spread of the wheat pathogen Zymoseptoria tritici

Abstract

Interactions between plant pathogens and their hosts are highly dynamic and mainly driven by pathogen effectors and plant receptors. Host-pathogen co-evolution can cause rapid diversification or loss of pathogen genes encoding host-exposed proteins. The molecular mechanisms that underpin such sequence dynamics remains poorly investigated at the scale of entire pathogen species. Here, we focus on AvrStb6, a major effector of the global wheat pathogen Zymoseptoria tritici, evolving in response to the cognate receptor Stb6, a resistance widely deployed in wheat. We comprehensively captured effector gene evolution by analyzing a global thousand-genome panel using reference-free sequence analyses. We found that AvrStb6 has diversified into 59 protein isoforms with a strong association to the pathogen spreading to new continents. Across Europe, we found the strongest differentiation of the effector consistent with high rates of Stb6 deployment. The AvrStb6 locus showed also a remarkable diversification in transposable element content with specific expansion patterns across the globe. We detected the AvrStb6 gene losses and evidence for transposable element-mediated disruptions. We used genome-wide association mapping data to predict virulence emergence and found marked increases in Europe, followed by spread to subsequently colonized continents. Finally, we genotyped French bread wheat cultivars for Stb6 and monitored resistant cultivar deployment concomitant with AvrStb6 evolution. Taken together, our data provides a comprehensive view of how a rapidly diversifying effector locus can undergo large-scale sequence changes concomitant with gains in virulence on resistant cultivars. The analyses highlight also the need for large-scale pathogen sequencing panels to assess the durability of resistance genes and improve the sustainability of deployment strategies. Author summaryInteractions between plants and their specialized pathogens are often mediated by a sophisticated molecular dialogue. Effectors produced by pathogens serve to manipulate the host but may also be used by the host to trigger defence mechanisms upon recognition. Deploying plants carrying a resistance gene against a specific effector could lead to rapid adaptation in the pathogen. Here, we unraveled such dynamics at the scale of the global distribution range of the fungal wheat pathogen Zymoseptoria tritici. The effector is encoded by the gene AvrStb6 located in a polymorphic region of a chromosome near the telomere. We find selfish elements (i.e. transposable elements) repeatedly inserted nearby the gene, which has likely facilitated the rapid sequence evolution. The effector diversified among continents, and we could predict that the sequence changes likely helped escape recognition by the host receptor. Our study provides one of the most comprehensive views how a crop pathogen diversified a major effector in response to host resistance factors. Such studies facilitate devising more durable deployment strategies of host resistance in order to maintain crop yield.