Molecular Mechanisms Driving the Unusual Pigmentation Shift in Eggplant Fruit Development.

Abstract

Fruit pigmentation is a major signal that attracts frugivores to enable seed dispersal. In most fleshy fruit, green chlorophyll typically accumulates early in development and is replaced in ripening by a range of pigments. Species such as grape and strawberry replace chlorophyll by red anthocyanins generated through the flavonoid biosynthetic pathway. Eggplant (Solanum melongena) is unique as its fruit accumulates anthocyanins starting from fruit set which are later replaced by the yellow flavonoid pathway intermediate naringenin chalcone. To decipher the genetic regulation of such an extraordinary pigmentation shift, we integrated mRNA and microRNA profiling data obtained from developing eggplant fruit. We discovered that while SQUAMOSA PROMOTER BINDING-LIKE (i.e., SPL6a, SPL10, and SPL15), MYB1 and MYB2 transcription factors (TFs) regulate anthocyanin biosynthesis in early fruit development, the MYB12 TF controls late naringenin chalcone accumulation. We further show that microRNA157 and microRNA858 negatively regulate SPLs and MYB12 expression, respectively. Taken together, our model suggests that opposing and complementary expression of microRNAs and TFs controls the pigmentation switch in eggplant fruit skin. Intriguingly, despite the distinctive pigmentation pattern in eggplant, fruit development in other species utilize homologous regulatory factors to control the temporal and spatial production of different pigment classes.