Natural Variation in Fruit Color Among Fragaria Species Explained by Independent Mutations in a Single Transcriptional Factor: MYB10

Abstract

Anthocyanins are the pigments responsible for the red color of strawberries. Their biosynthesis is controlled at the transcriptional level by a ternary complex consisting of R2R3-MYB and bHLH transcription factors associated with a WD40-repeat protein. In order to map the genetic factors involved in fruit coloring we generated a mapping population crossing a F. vesca accession bearing white fruits (ESP138.596) with the red-fruited ‘Reine des Vallées’. DNA from white- or red-fruited F2 individuals was pooled to perform a bulk segregant analysis (BSA) linked with high-throughput genome sequencing. This analysis revealed the presence of a gypsy-like retrotransposon inserted in the third exon of FvMYB10. The presence of this retroelement in homozygosis co-segregated with white fruits in the complete F2 population. We further extended this analysis to other white-fruited F. vesca accessions but none of them harbored this retroelement in FvMYB10. Instead we identified two additional polymorphisms affecting FvMYB10, (1) a single nucleotide insertion, which generates a truncated protein, and (2) a large deletion of ~100 Kb spanning a genomic region that contains 7 genes, one of them being FvMYB10. The three newly identified polymorphisms on FvMYB10 differ from the previously described single nucleotide mutation, responsible for the lack of anthocyanins in other F. vesca white/yellow fruited accessions. We next analyzed QTL for fruit color in a segregating population derived from the red-fruited F. x ananassa ‘Senga Sengana’ and a F. chiloensis accession with white flesh. A major QTL controlling 45.7 - 54.7% of variance in internal flesh color was detected on LG I-3. The confidence interval spans the orthologous region where FvMYB10 is located. Furthermore, transient overexpression on FvMYB10 on different F. chiloensis accessions resulted in red sectors both in the epidermis and fruit flesh.