The miR319‐based repression of SlTCP2/LANCEOLATE activity is required for regulating tomato fruit shape

SUMMARY Fruit morphogenesis is determined by the coordination of cell division and expansion, which are fundamental processes required for the development of all plant organs. Here, we show that the regulation of TEOSINTE BRANCHED1/CYCLOIDEA/PCF (TCP) LANCEOLATE (TCP2/LA) by miR319 is crucial for tomato fruit morphology. The loss of miR319 regulation in the semi‐dominant La mutant led to a premature SlTCP2/LA expression during gynoecium patterning, which results in modified cell division during carpel development. As a consequence, La mutants exhibited elongated ovary and fruit shape, and a reduced number of ovules and seeds. Elongated fruit shape in La may be partially due to the SlTCP2/LA‐mediated repression of OVATE activity in young floral buds. Further analysis showed that the de‐repression of SlTCP2/LA decreases auxin responses in young floral buds by directly repressing SlYUCCA4 expression, but SlTCP2/LA also acts in parallel with ENTIRE (E) to orchestrate fruit morphology and seed production. Our study defines a novel miRNA‐based molecular link between the domestication‐associated OVATE gene and auxin responses. Given the striking variation in fruit morphology among members of the Solanaceae family, fine‐tuning regulation of gene expression by miRNA coupled with modulation of auxin dynamics may be a common driver in the evolution of fruit shape diversity. Significance Statement Although the diversity in fruit morphology is one of the hallmarks of varietal differences among fruit‐bearing crops, the underlying molecular mechanisms are not clear. In this study, we show that miR319‐based regulation of TCP2/LANCEOLATE is crucial for controlling OVATE activity and auxin responses during tomato gynoecium patterning, which impacts final fruit shape.