Genomics Reveals the Past and Informs the Future of Apple Improvement

Apple (Malus domestica) is one of the world’s most valuable fruit crops and a promising candidate for marker-assisted selection (MAS) due to its lengthy juvenile phase. To examine the genetic structure of apples and discover genotype-phenotype associations, we generated over 8,000 SNP genotypes from 689 M. domestica accessions from the USDA germplasm collection using genotyping-by-sequencing (GBS). The primary axes of genetic differentiation in apples separate Old World from New World cultivars, and early from late harvested cultivars. We confirm that apples used for making alcoholic cider derive part of their ancestry from M. sylvestris, the wild European crab apple. We also find a complex pedigree network among cultivars that suggests extensive use of elite cultivars in recent apple breeding. The extremely rapid linkage disequilibrium (LD) decay in apple suggests that whole genome sequencing will be required for well-powered genome wide association (GWA). Despite this, we conducted GWA using over 24,000 phenotypic data points from the USDA-GRIN database and found significant hits for skin colour and fruit firmness, both of which show the genetic signature of improvement through breeding. Most notably, we found an amino acid substitution in the transcription factor NAC18.1 that is a strong functional candidate for fruit firmness. We demonstrate that GWA in the USDA apple germplasm collection results in extremely high resolution mapping of causal variants, which holds great potential for continued improvement of apples through MAS.