The genetic architecture of fruit colour in strawberry (Fragaria x ananassa) uncovers the predominant contribution of the F. vesca subgenome to anthocyanins and reveals underlying genetic variations

Fruit colour, which is central to the sensorial and nutritional quality of the fruit, is a major breeding target in cultivated strawberry (Fragaria x ananassa). Red fruit colour is caused by the accumulation of anthocyanins, which are water-soluble flavonoids. Here, using pseudo F1 progeny derived from the cv. Capitola and the advanced line CF1116 and taking advantage of the available high density SNP array, we delineated fruit flavonoids mQTLs (13 compounds: anthocyanin, flavonols and flavan-3-ols) and colour-related QTLs (total anthocyanins and fruit colour) to narrow genomic regions corresponding to specific subgenomes of the cultivated strawberry. Findings showed that the overwhelming majority of the anthocyanin mQTLs and other colour-related QTLs are specific to F. vesca subgenome but that other subgenomes also contribute to colour variations. We then focused on two major homoeo-mQTLs for pelargonidin-3-glucoside (PgGs) localized on both male and female maps on linkage group LG3a (F. vesca subgenome). Combined high-resolution mapping of PgGs mQTLs and colour QTLs, transcriptome analysis of selected progeny individuals and whole genome sequencing of the parents led to the identification of several INDELS in the cis-regulatory region of a MYB102-like ODORANT gene and of the deletion of a putative MADS box binding motif in the 5UTR upstream region of an anthocyanidin reductase (ANR) gene, which likely underlie significant colour variations in strawberry fruit. The implications of these findings are important for the functional analysis and genetic engineering of colour-related genes and for the breeding by Marker-Assisted-Selection of new strawberry varieties with improved colour and health-benefits.