Histological, transcriptomic, and gene functional analyses reveal the regulatory events underlying gibberellin-induced parthenocarpy in tomato

Gibberellin (GA) is one of the major plant hormones that promote parthenocarpy, a highly valuable agronomic trait. Here, we demonstrated that exogenous GA3 application triggered the formation of parthenocarpic fruits with smaller size but unchanged shape in tomato (Solanum lycopersicum). These fruits exhibited a thicker pericarp, undeveloped ovules, and few jelly tissues, leading to smaller locules with empty cavities. Histological investigation showed that GA treatment produced more cell layers with larger cells in the pericarp, suggesting its promotion in both cell division and expansion. Transcriptomic analyses between GA3- and mock-treated unpollinated ovaries/fruits identified a large number of differentially expressed genes related to hormones, cell division, cell expansion, and transcription factors, implying that they coordinately regulated parthenocarpy conferred by GA. In particular, the downregulation of five reported repressors of tomato parthenocarpy, including two auxin signaling components, AUXIN RESPONSE FACTOR5 (SlARF5) and SlARF7, and three MADS-box genes, TOMATO APETALA3 (TAP3), TOMATO PISTILLATA (TPI), and AGAMOUS-LIKE6 (SlAGL6), after GA treatment might play a key role in this process. Furthermore, we found that the knockdown of a GA signaling factor SlMYB33, which was depressed by GA treatment, induced parthenocarpic fruit set in tomato, an effect that might have been achieved by enhancing GA biosynthesis and decreasing the expression of some repressors of tomato parthenocarpy. Thus, our results provide a basis for understanding the regulatory mechanism of GA in tomato parthenocarpy.