Large-scale Phylogenomics Reveals Systematic Loss of Anthocyanin Biosynthesis Genes at the Family Level in Cucurbitaceae

Plant pigmentation secrets are among the oldest interests of plant scientists, with pigments such as chlorophyll, carotenoids, flavonoids, and betalains contributing to the diversity of hues in higher plants. Anthocyanins, a class of flavonoids responsible for vibrant shades of pink, red, and blue pigmentation, are almost ubiquitous in angiosperms but are replaced by betalains in some families in the order Caryophyllales. We investigated anthocyanin pigmentation in Cucurbitaceae, the second-largest fruit and vegetable family, characterised by white and yellow flowers and red, orange, and green fruits predominantly pigmented by carotenoids. Using a comprehensive collection of 258 datasets representing species across all 15 tribes of Cucurbitaceae and a phylogenomics approach, we observed a systematic absence of genes involved in anthocyanin and proanthocyanidin biosynthesis. Absence of the structural genes DFR, ANS, arGST, LAR, and ANR, along with the anthocyanin-related regulatory MYB genes, was consistently confirmed by synteny and phylogenetic analysis. These results suggest that anthocyanin loss in angiosperms is more common than previously assumed. In light of this new discovery, we propose a stepwise loss of anthocyanin pigmentation in Cucurbitaceae, likely accompanied by a partial functional replacement with carotenoid pigmentation.