Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)

Abstract

During natural evolution and artificial selection, the fruit color of many species has been repeatedly gained or lost and is generally associated with mutations in genes encoding <i>R2R3-MYB</i> transcription factors, especially <i>MYB10</i>. In this study, we show that a heterozygous frameshift mutation (<i>FaMYB10^AG-insert/FaMYB10^wild</i> ) is responsible for the loss of anthocyanins in the flesh of cultivated strawberry. Comparative transcriptomic and metabolomic analyses of red- and white-fleshed strawberry indicated that the low expression level of <i>FaUFGT</i> (flavonol-O-glucosyltransferases) was responsible for the loss of anthocyanins and accumulation of proanthocyanidin in the white-fleshed strawberry and was the crucial gene that encodes enzymes of the anthocyanin biosynthesis pathway. Accordingly, overexpression and silencing of <i>FaUFGT</i> altered anthocyanin content and changed the flesh color of strawberry fruits. Furthermore, whole-genome resequencing analyses identified an AG insertion in the <i>FaMYB10</i> coding region (<i>FaMYB10^AG-insert</i> ) of white-fleshed strawberry. Y1H and EMSA assays showed that FaMYB10^wild was able to bind to the promoter of the <i>FaUFGT</i> gene, while the FaMYB10^AG-insert could not. The skin and flesh color were tightly linked to the number of fully functional <i>FaMYB10</i> copies in the selfing progeny of white-fleshed strawberry. Our results suggested that heterozygous frameshift mutation of <i>FaMYB10</i> resulted in the loss of the ability to activate the expression of the <i>FaUFGT</i> gene, was responsible for the natural formation of red and white-fleshed strawberry.