Inheritance and enzymatic basis of anthocyanin malonylation in Fragaria × ananassa

The cultivated strawberry (Fragaria × ananassa) is highly valued for its attractive color and pleasant taste, which is due to the secondary metabolites it accumulates. To clarify which factors influence the content of secondary metabolites in the fruit, F1 hybrids of the commercial strawberry cultivars “Senga Sengana” and “Candonga,” which are adapted to different climatic zones, were produced. F1 progeny were grown in five European countries, and the content of secondary metabolites was analyzed. The results show that the genetic factor plays a more important role compared with environmental conditions. Cultivar “Senga Sengana” produced significantly more pelargonidin-3-O-(6′-O-malonyl)glucoside than “Candonga,” regardless of the environmental conditions, and the progeny segregated with a ratio of 1:1 in this trait. Twenty-four putative malonyltransferase genes were cloned from F. × ananassa (FaMAT) “Senga Sengana” and “Candonga,” and six FaMATs showed enzymatic activity. Three FaMAT enzymes are promiscuous and malonylate flavonoid glucosides and anthocyanins, whereas the others are specific for quercetin-3-O-glucoside and kaempferol-3-O-glucoside. Expression data indicate that the gene products of FaMAT1 and 4 catalyze the malonylation of anthocyanins in “Senga Sengana” and the related hybrids, while the corresponding functional alleles in “Candonga” and the second group of hybrids are only slightly expressed in the mature fruit. Thus, altered FaMAT transcription genetically determines the different levels of malonylated anthocyanins in the progeny.