Diversification, loss, and virulence gains of AvrStb6 during continental expansion of Zymoseptoria tritici
Interactions between plant pathogens and their hosts are highly dynamic and mainly driven by pathogen effectors (Avr) and plant resistance (R) genes. AvrStb6 is the best studied Zymoseptoria tritici effector and it is recognized by Stb6, a widely deployed wheat R gene. AvrStb6 is known to be highly polymorphic across the world, however, how the gene evolved in response to strong selection pressure by the host remains poorly understood. Here, we analyzed a global thousand-genome panel to assess the diversification of AvrStb6 and the genomic context. We detected 59 AvrStb6 protein isoforms in the global collection with the most frequently detected isoform in Europe showing the strongest divergence from the Z. pseudotritici sister species homolog. We found indications that AvrStb6 diversified most strongly in regions with supposedly higher Stb6 deployment rates. AvrStb6 showed also remarkably diversification in transposable element associations near the coding sequence, and we detected complete gene loss in ~3% of all surveyed isolates. Finally, we used genome-wide association mapping data to predict virulence profiles for isoforms present across continents. We found that populations showed marked increases in predicted virulence in Europe and subsequently colonized continents. In conclusion, we show how a rapidly diversifying effector loci can undergo large-scale sequence changes concomitant with gains in virulence on cognizant cultivars.