Genetic architecture of angular leaf spot resistance in cultivated strawberry shaped by epistasis and...

Angular leaf spot (ALS), caused by Xanthomonas fragariae, is a bacterial disease that limits strawberry (Fragaria × ananassa) productivity worldwide. Although major resistance loci have been identified in wild Fragaria species, their introgression into elite germplasm remains constrained by linkage drag and inconsistent inheritance. To dissect the genetic architecture of ALS resistance, we evaluated a diverse panel of n = 241 greenhouse-tested and n = 468 field-tested strawberry accessions representing elite cultivars, breeding materials, and heirloom varieties of cultivated strawberry (F. × ananassa). Plants were evaluated under controlled inoculations and natural field infection using a standardized phenotypic scale and genotyped with 50K single nucleotide polymorphism array. Broad-sense heritability was moderate (H² = 0.45), whereas narrow-sense heritability was low (h² = 0.10), reflecting the contribution of nonadditive genetic effects such as epistasis. Genome-wide association studies (GWAS) identified two loci on chromosomes 1D and 2D, explaining 4%-5% of phenotypic variance, respectively. A segregating F1 population validated the 2D locus, confirmed by co-localization with the GWAS signal explaining 11.3% of the phenotypic variance. Two-dimensional genome wide scan in this F1 population revealed a significant epistatic interaction between locus on chromosome 2D and an additional locus on chromosome 6B, collectively explaining 27% of the phenotypic variance. Together, these results demonstrate that nonadditive effects in these populations control ALS resistance. Understanding this complexity provides a foundation for developing elite cultivars with durable resistance, such as UCD Royal Royce. Our findings underscore the need for predictive breeding strategies that capture epistatic and environmental variance to accelerate genetic gain for ALS resistance in strawberry.