Arabidopsis has served as a model plant for studying the genetic networks that guide gynoecium development, but less is known about other species. Tomato (Solanum lycopersicum) is a model for fleshy fruit development and ripening. Here we used tomato to study the transcription factor SPATULA (SPT), a bHLH-family member that in Arabidopsis is known to be important for gynoecium development. We analysed the expression of the SlSPT gene during flower and fruit development and the interaction of the SlSPT protein with proteins previously reported as interactors of AtSPT in the gynoecium. We also generated and characterized loss-of-function tomato lines using CRISPR–Cas9. The results showed that SlSPT forms homodimers and partially conserves the interactions reported in Arabidopsis with some HECATE proteins. We conclude that SlSPT has a role in floral organ development, particularly in stamen fusion, style and stigma development, and trichome formation on the carpels. Furthermore, lack of SlSPT caused altered exocarp pigmentation. A metabolomic analysis of the exocarp showed perturbations in several pathways in the slspt mutant, with flavonoid biosynthesis being the most affected, which could potentially impact the nutritional value of the fruit. In summary, our results show conserved functions during gynoecium development and novel roles that enrich knowledge of the SPT gene in fleshy fruits.

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