Domestication and Improvement Reshaped the Genomic Architecture of Abiotic Stress Tolerance in Sunflower

Abstract

Sunflower (Helianthus annuus) has undergone extensive domestication and modern improvement, yet the extent to which selection has shaped its stress-adaptive variation remains largely unclear. Using genomic data from diverse accessions, including the wild ancestor of sunflower, we identified widespread balancing selection that maintains historical polymorphisms in abiotic-stress-related genes. Additionally, we identified strong positive selection signals associated with domestication and improvement. Using a cutting-edge DNA language model to characterize deleterious alleles, we found that modern cultivars exhibited an elevated deleterious mutation load, particularly within positively selected regions, consistent with patterns observed in other major domesticates. To cross-validate the functional consequences of the selected regions on stress responses, we assessed salt tolerance in an independent association panel and evaluated ancestral allele effects on salt-responsive traits. Although only a small subset of the selected regions reached genome-wide significance, several ancestral alleles within positively selected sweeps tended to enhance salt tolerance. Together, these results indicate that recent selection may have unintentionally eliminated historically beneficial alleles, reshaping the genomic landscape of sunflower stress responses. This study highlights a breeding strategy to recover ancestral beneficial alleles for enhancing abiotic stress tolerance in modern cultivars.