Experimental evolution reveals genomic signatures of variety-specific selection of Cercospora beticola in Germany

Cercospora leaf spot, caused by Cercospora beticola, is the most destructive foliar disease of sugar beet. Management has relied heavily on fungicides, but widespread fungicide resistance emphasized the need for resistant varieties. To assess how varietal resistance shapes C. beticola populations, we conducted a 3-year field experiment at four locations in Germany using sugar beet varieties ranging from susceptible to highly resistant. Infected leaves were collected separately per variety and location to serve as inoculum for the following year, maintaining variety- and location-specific pathogen populations under controlled selective conditions. A total of 900 isolates were subjected to whole-genome sequencing and population genetic analyses. Isolates collected in 2022 showed extensive admixture among locations. Equal mating-type ratios were observed in some populations but skewed in others, suggesting that sexual reproduction may occur locally. Location-specific re-inoculation preserved population continuity but did not produce detectable local adaptation. By contrast, the population was affected to some extent by variety-specific re-inoculation. Populations from one highly resistant variety formed two divergent lineages with reduced diversity and altered allele frequency spectra, consistent with host-driven selection. Genome scans identified 26 candidate genes, including two putative effectors, associated with adaptation to the highly resistant variety. These findings demonstrate rapid C. beticola adaptation to resistant varieties, highlighting the role of host-driven selection in resistance management.