SlBZR1 and SlBES1 synergistically regulate internode length and fruit shape in tomato through distinct mechanisms

Abstract Brassinazole-resistant1 (BZR1) and BRI1-EMS-suppressor1 (BES1) are phylogenetically closely related transcription factors that act as key components of brassinosteroid (BR) signaling. Although their individual roles in various plant developmental processes have been extensively reported in model plants such as Arabidopsis, their potential synergistic functions in regulating internode length and fruit shape in tomato, an important crop as well as a model system of fruit development, remain unclear. Here, we demonstrate that SlBZR1 and SlBES1 physically interact and modulate internode length and fruit shape in tomato through distinct mechanisms. Genetic analyses reveal that knockout of SlBZR1 or SlBES1 moderately reduces internode length, whereas the bzr1 bes1 double mutant exhibits severe dwarfism. SlBZR1 and SlBES1 promote internode elongation by directly targeting and repressing the expression of GA metabolic gene SlGA2ox10 while inducing that of gibberellin (GA) receptor gene SlGID1A. During fruit development, elongated fruit resulting from enhanced cell proliferation in the ovary wall was observed specifically in the bzr1 bes1 double mutant, but not in bzr1, bes1, BZR1-OE, BES1-OE, and wild-type plants, in a GA-independent manner. We identify the fruit shape regulator SlFS8.1 as a direct transcriptional target of SlBZR1 and SlBES1. Our work demonstrates that SlBZR1 and SlBES1 synergistically promote internode elongation via crosstalk with the GA pathway, while independently governing fruit shape through direct transcriptional activation of SlFS8.1.