A metabolic perspective of selection for fruit quality related to apple domestication and improvement

BackgroundApple is an economically important fruit crop. Changes in metabolism accompanying human-guided evolution can be revealed using a multiomics approach. We perform genome-wide metabolic analysis of apple fruits collected from 292 wild and cultivated accessions representing various consumption types.ResultsWe find decreased amounts of certain metabolites, including tannins, organic acids, phenolic acids, and flavonoids as the wild accessions transition to cultivated apples, while lysolipids increase in the Golden Delicious to Ralls Janet pedigree, suggesting better storage. We identify a total of 222,877 significant single-nucleotide polymorphisms that are associated with 2205 apple metabolites. Investigation of a region from 2.84 to 5.01 Mb on chromosome 16 containing co-mapping regions for tannins, organic acids, phenolic acids, and flavonoids indicates the importance of these metabolites for fruit quality and nutrition during breeding. The tannin and acidity-related genes Myb9-like and PH4 are mapped closely to fruit weight locus fw1 from 3.41 to 3.76 Mb on chromosome 15, a region under selection during domestication. Lysophosphatidylethanolamine (LPE) 18:1, which is suppressed by fatty acid desaturase-2 (FAD2), is positively correlated to fruit firmness. We find the fruit weight is negatively correlated with salicylic acid and abscisic acid levels. Further functional assays demonstrate regulation of these hormone levels by NAC-like activated by Apetala3/Pistillata (NAP) and ATP binding cassette G25 (ABCG25), respectively.ConclusionsThis study provides a metabolic perspective for selection on fruit quality during domestication and improvement, which is a valuable resource for investigating mechanisms controlling apple metabolite content and quality.

Automated summary

This study investigates the metabolic changes in apple fruits during domestication, revealing decreased levels of certain metabolites and increased levels of lysolipids. It also identifies genetic regions associated with fruit quality and nutrition, as well as the regulation of fruit weight and hormone levels. The findings provide valuable insights into the mechanisms controlling apple metabolism and quality.