Allelic Variation of MYB10 Is the Major Force Controlling Natural Variation in Skin and Flesh Color in Strawberry (Fragaria spp.) Fruit

Abstract

The fruits of diploid and octoploid strawberry (Fragaria spp) show substantial natural variation in color due to distinct anthocyanin accumulation and distribution patterns. Anthocyanin biosynthesis is controlled by a clade of R2R3 MYB transcription factors, among which MYB10 is the main activator in strawberry fruit. Here, we show that mutations in MYB10 cause most of the variation in anthocyanin accumulation and distribution observed in diploid woodland strawberry (F. vesca) and octoploid cultivated strawberry (F. 3ananassa). Using a mapping-by-sequencing approach, we identified a gypsytransposon in MYB10 that truncates the protein and knocks out anthocyanin biosynthesis in a white-fruited F. vesca ecotype. Two additional loss-of-function mutations in MYB10 were identified among geographically diverse white-fruited F. vesca ecotypes. Genetic and transcriptomic analyses of octoploid Fragaria spp revealed that FaMYB10-2, one of three MYB10 homoeologs identified, regulates anthocyanin biosynthesis in developing fruit. Furthermore, independent mutations in MYB10-2 are the underlying cause of natural variation in fruit skin and flesh color in octoploid strawberry. We identified a CACTA-like transposon (FaEnSpm-2) insertion in the MYB10-2 promoter of red-fleshed accessions that was associated with enhanced expression. Our findings suggest that cis-regulatory elements in FaEnSpm-2 are responsible for enhanced MYB10-2 expression and anthocyanin biosynthesis in strawberry fruit flesh.

Genome-Wide Identification and Expression Analysis of MYB Transcription Factors and Their Responses to Abiotic Stresses in Woodland Strawberry (Fragaria vesca)

“…This indicates that FveMYB10 may regulate anthocyanin biosynthesis during the ripening of woodland strawberry fruit, whereas FveMYB75 may have a different function. This function of FveMYB10 has been reported by Chen and Castillejo C et al [73,74], corroborating our results. During the fruit ripening of octoploid strawberry (Fragaria × ananassa), FaMYB10 promotes the biosynthesis of anthocyanins through the independent regulation of light and ABA [75].…”

Chromosome Level Assembly of Homozygous Inbred Line ‘Wongyo 3115’ Facilitates the Construction of a High-Density Linkage Map and Identification of QTLs Associated With Fruit Firmness in Octoploid Strawberry (Fragaria × ananassa)

“…Due to the low density of markers in multiple chromosomal regions, 28 pseudomolecules were divided into 44 linkage groups with the total genetic map size of 3,861 cM (Supplementary Dataset 3; Supplementary Figure 7). In addition, to validate the genetic map, QTL mapping for fruit core color was performed, and the MYB10 gene controlling fruit and flesh color of strawberry reported by Castillejo et al (2020) was mapped on the QTL region (Manivannan et al, unpublished).…”

Chromosome-Scale Genome for a Red-Fruited, Perpetual Flowering and Runnerless Woodland Strawberry (Fragaria vesca)

“…Here we present a high quality genome of an F. vesca accession, CFRA 2339 (PI 698244), which phenotypically differs from Hawaii-4 in two important traits: fruit color and runner production (Figures 1A,B). Hawaii-4 has yellow fruit and produces runners while CFRA 2339 produces red fruit and is runnerless (Hawkins et al, 2016;Tenreira et al, 2017;Caruana et al, 2018;Castillejo et al, 2020). Both accessions are perpetual flowering instead of the seasonal flowering displayed by other accessions (Iwata et al, 2012).…”

“…Both accessions are perpetual flowering instead of the seasonal flowering displayed by other accessions (Iwata et al, 2012). This genome will serve as a valuable new resource for the strawberry and the larger Rosaceae community, allowing for the identification of the genetics controlling runner production as well as fruit color in a diploid model organism (Caruana et al, 2018;Castillejo et al, 2020).…”