Allelic variation of MYB10 is the major force controlling natural variation of skin and flesh color in strawberry (fragaria spp.) fruit

Authors: CASTILLEJO, CRISTINA - Instituto De Investigacion Y Formacion Agraria Y Pesquera; WAURICH, VERONIKA - Hansabred Gmbh & Co Kg; WAGNER, HENNING - Hansabred Gmbh & Co Kg; RAMOS, RUBEN - Instituto De Investigacion Y Formacion Agraria Y Pesquera; OIZA, NICOLAS - Instituto De Investigacion Y Formacion Agraria Y Pesquera; MUNOZ, PILAR - Instituto De Investigacion Y Formacion Agraria Y Pesquera; TRIVINO, JUAN CARLOS - Ascires Genomic Systems; CARUANA, JULIE - University Of Maryland; LIU, ZHONGCHI - University Of Maryland; COBO, NICOLAS - Universidad De La Frontera; Hardigan, Michael; KNAPP, STEVEN - University Of California, Davis; VALLARINO, JOSE - University Of Malaga; OSORIO, SONIA - University Of Malaga; MARTIN-PIZARRO, CARMEN - University Of Malaga

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/25/2020
Publication Date: 9/30/2020
Citation: Castillejo, C., Waurich, V., Wagner, H., Ramos, R., Oiza, N., Munoz, P., Trivino, J., Caruana, J., Liu, Z., Cobo, N., Hardigan, M.A., Knapp, S., Vallarino, J., Osorio, S., Martin-Pizarro, C. 2020. Allelic variation of MYB10 is the major force controlling natural variation of skin and flesh color in strawberry (fragaria spp.) fruit. The Plant Cell. https://doi.org/10.1105/tpc.20.00474.
DOI: https://doi.org/10.1105/tpc.20.00474

Interpretive Summary: The white-fruited strawberry is rare and sought-after due to its unique physical appearance. Breeding for white strawberry fruit has potential economic value, as shown in Chile and Japan, where white-fruited varieties are frequently marketed for holidays and special occasions. The present study employed genetic approaches to identify the mutations underlying this white fruit in cultivated strawberry and in an ancestor species. It was found that there is an insertion in the promoter of MYB10-2, a gene that regulates anthocyanin biosynthesis in developing fruit. The results of this study are important because genetic markers controlling strawberry fruit pigmentation were discovered. This carries significant implications for targeted breeding of white-fruited strawberry cultivars, offering a clear target for future studies to develop this rare fruit trait.

Technical Abstract: Substantial natural variation in color have been observed in fruits of diploid and octoploid strawberry (Fragaria spp.), resulting from distinct accumulation and distribution of anthocyanins. Anthocyanin biosynthesis is controlled by a clade of R2R3 MYB transcription factors, among which MYB10 has been shown as the main activator in strawberry fruit. Here, we show that MYB10 mutations cause most of the anthocyanin variation observed in diploid woodland strawberry (F. vesca) and octoploid cultivated strawberry (F. ×ananassa). Using a mapping-by-sequencing approach, we identified a gypsy-transposon in MYB10 that truncates the protein and knocks out anthocyanin biosynthesis in a white-fruited F. vesca ecotype. Two additional loss-of-function MYB10 mutations were identified among geographically diverse white-fruited F. vesca ecotypes. Genetic and transcriptomic analyses in octoploid Fragaria spp. revealed that FaMYB10-2, one of three MYB10 homoeologs identified, regulates the biosynthesis of anthocyanins 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 required for ectopic MYB10-2 expression and anthocyanin biosynthesis in fruit flesh.