The JAW-TCP-FUL genetic axis triggers an early reorientation of cell anisotropy to initiate and drive fertilization-dependent fruit elongation in Arabidopsis

In angiosperms, the ovary grows and develops into a fruit after fertilization, and the seeds are formed within to ensure reproductive success. Although genetic regulators suppressing fertilization-independent fruit growth or parthenocarpy have been identified in the Brassicaceae model Arabidopsis thaliana, the fertilization-dependent activator of fruit growth has not been elucidated. Here, we show that the miR319-regulated TCP transcription factors (JAW-TCPs) directly activate the transcription of the FRUITFULL (FUL) gene and promote fruit morphogenesis. By activating FUL, JAW-TCPs indirectly repress the four valve-margin specifying genes SHATTERPROOF1, SHATTERPROOF2, INDEHISCENT and ALCATRAZ in the valves. Mutating these genes suppresses defects caused by the combined loss of JAW-TCPs and FUL. Through extensive confocal imaging studies, we deciphered the cellular basis of JAW-TCP function revealing that JAW-TCPs promote fruit elongation by triggering the reorientation of cell anisotropy along the length axis at an early growth stage after fertilization. Our study uncovers a fertilization-dependent genetic module driving fruit elongation and sets the stage to identify other genetic regulators in this pathway.