The FUL-SHP-AP2 module regulates fruit development in petunia

Abstract

Fruit development is a typical angiosperm feature that greatly facilitates seed dispersal. Despite extensive studies on the gene regulatory network underlying pod shattering in the dry Arabidopsis fruit and the ripening process in the fleshy tomato fruit, it is yet unclear if a conserved regulatory network acts in early fruit development. Here, we investigated the roles of Petunia x hybrida (petunia) FRUITFULL (FUL), SHATTERPROOF (SHP) and APETALA 2 (AP2) homologs, three types of transcription factors repeatedly associated with fruit development and/or ripening. Petunia is closely related to tomato but produces dry dehiscent fruits like Arabidopsis. Our functional analysis revealed that the three petunia FUL-like genes, PETUNIA FLOWERING GENE (PFG), FLORAL BINDING PROTEIN 26 (FBP26) and FBP29, redundantly regulate endocarp development. They promote the formation of regularly shaped inner endocarp cells, probably via auxin/brassinosteroid signalling and cell wall modification. Furthermore, we discovered that the SHP-like gene FLORAL BINDING PROTEIN 6 (FBP6) has an opposite role, promoting more mesocarp-shaped endocarp cells, indicating that the FUL-like and SHP-like genes act antagonistically in early pericarp development. Finally, we show that the AP2-like genes REPRESSOR OF B-FUNCTION 1 (ROB1), ROB2 and ROB3 are crucial factors in petunia fruit development. rob1 rob2 rob3 mutants completely fail to dehisce and show major defects in pericarp patterning. The ROB transcription factors repress the activity of the FUL-like genes, and have, together with FBP6, an opposite effect on auxin and brassinosteroid signalling genes. Our study suggests that a module consisting of antagonistically acting TFs, including co-orthologs of AP2, FUL and SHP, regulates early pericarp patterning, at least partially via auxin and brassinosteroids.