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 ×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 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.
Highlights
The characteristic red color of strawberry fruit is due to the accumulation of anthocyanins, water-soluble pigments synthesized through the flavonoid pathway (Almeida et al, 2007; Tohge et al, 2017)
It is crucial to characterize the genetic control of color variation within the octoploid Fragaria species, and to answer questions such as: how many genes are involved in controlling this trait, are all possible homoeologous copies present in the genome, are they being expressed, and are previously identified mutations in FvMYB10 present in octoploid strawberry? To accomplish this objective, we studied two diverse octoploid populations characterized by a broad variation in fruit skin (University of Florida strawberry breeding population 17.66) and flesh color (Hansabred SS×FcL population)
In this study we demonstrated that anthocyanin biosynthesis is activated predominantly by MYB10-2, the homoeolog lying in the F. iinumae-derived subgenome
Summary
The characteristic red color of strawberry fruit is due to the accumulation of anthocyanins, water-soluble pigments synthesized through the flavonoid pathway (Almeida et al, 2007; Tohge et al, 2017). Gaining insight into the genetic factors affecting natural variation in external (skin) and internal (flesh) fruit color is key for efficient modification of this trait in new cultivars and will facilitate the rapid development of fruits with increased or reduced levels of anthocyanins. The identification of genes or genomic regions governing fruit color variation in cultivated strawberry is crucial for hastening the development of new cultivars with desired characteristics. An 8bp insertion in the coding region of FaMYB10 has been associated with loss of anthocyanins in fruits of ‘Snow Princess’, an octoploid strawberry cultivar with completely white fruits (Wang et al, 2020), but its subgenome location was not described. Two additional DNA markers (one based on PCR and agarose gel and another on Kompetitive allele-specific PCR) were developed that predict strawberry internal fruit color in diverse octoploid germplasm. The described markers represent useful tools for selection of fruit color, when F. chiloensis accessions are used in breeding programs
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