A Pair of microRNAs Controls the Unique Pigmentation Shift in Developing Eggplant Fruit Skin

Abstract

Pigments are specialized (secondary) metabolites present in fruit, fulfil a dual role by offering protection against diverse pathogens and attracting agents for seed dispersal. In most fleshy fruit, green chlorophyll accumulates early in development and is replaced by a range of pigments during fruit ripening. In blueberries, grapes, and strawberries, chlorophyll is replaced by red anthocyanins generated downstream of the flavonoid biosynthetic pathway. Eggplant (Solanum melongena) fruit is unique in terms of pigmentation, as, according to our knowledge, is among the rare fruits where anthocyanin is present from fruit set and is exchanged through maturation by a yellow pigment . We found that this colour results from naringenin chalcone, a flavonoid pathway intermediate that accumulates in tomatoes starting from the breaker stage of fruit development. To understand the genetic regulation of such an unusual shift, we integrated microRNA (miRNA) and mRNA sequencing data obtained from eggplant fruit during development. We discovered that while Squamosa Promoter Binding-Like (SPL6a, SPL10, and SPL15), MYB1 and MYB2 transcription factors (TFs) regulate anthocyanin biosynthesis, the MYB12 TF controls naringenin chalcone. We prove that miRNA157 and miRNA858 negatively regulate SPLs and MYB12, respectively. Interestingly, in contrast to other plants, in eggplant SPLs positively regulate anthocyanin biosynthesis by transcriptional regulation of MYB1 and MYB2 TFs. Taken together, our model suggests that the opposing and complementary expression of miRNA157 and miRNA858 control various parts of the flavonoid pathway in developing eggplant fruit skin. This results in an unusual shift in eggplant fruit pigmentation in which anthocyanins are replaced through ripening by yellow intermediates of the flavonoid pathway.