Out of the blue: family-wide loss of anthocyanin biosynthesis 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, one of the largest fruit and vegetable families, characterised by white and yellow flowers and red, orange and green fruits predominantly pigmented by carotenoids. Using a comprehensive collection of 258 datasets representing 183 unique species across all 15 tribes of Cucurbitaceae, along with 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. Our findings reveal that complete loss of the anthocyanin pathway can occur at the family level and suggest that similar losses may have been overlooked in other lineages. 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.