MicroRNA­-Regulated Pathways Coordinate Auxin Responses to Regulate Fruit Shape and Fruit Set

MicroRNAs (miRNAs) and phytohormones are fundamental regulatory elements of plant development; however, their interactions during fruit development remain poorly exploited. Here we show that two closely related miRNAs (miR159 and miR319) regulate tomato (Solanum lycopersicum L.) fruit set and fruit shape by modulating auxin responses. Overexpression of the SlMIR159 precursor in tomato cultivar Micro-Tom (MT) downregulates SlGAMYB genes in developing ovaries, leading to earlier fruit set and parthenocarpy. Misregulation of SlARF8 in ovaries by overexpressing SlMIR159 or de-repressing GAMYBgenes (MIM159 plants) led to altered auxin responsiveness in early ovary growth, and consequently, to parthenocarpy.

We also provide evidences that miR319-regulated TCP LANCEOLATE (LA) gene is a key regulator of tomato fruit shape. La/+ mutant plants contain a miR319-insensitive version of LA, and their fruits display an elongated shape, resembling those from Capsicum annuum. LA is expressed earlier in La/+ floral meristems, likely leading to precocious cell differentiation. Auxin biosynthesis is higher in the base of developing ovaries of La/+, suggesting that LA regulates auxin responses during gynoecium development. Altered auxin responses may be also responsible for the rudimental placenta and absence of septum observed in La/+ fruits, which led to facultative parthenocarpy . Our results unveil new functions for miR159/GAMYB and miR319/LA modules and show that molecular circuits involving miRNA-controlled modules and phytormones are essential for fruit development.