The coordination of cell proliferation and cell-division orientation controls Arabidopsis radial style development

The biological mechanisms responsible for correct shape acquisition at the apex of the female reproductive organ—the gynoecium— remain poorly understood, despite its fundamental importance for successful plant reproduction and seed production. This process involves a rare bilateral-to-radial symmetry transition in Arabidopsis thaliana, orchestrated in part by the transcription factor SPATULA (SPT). Here, we show that SPT negatively controls cell proliferation, promoted by the hormone cytokinin, to enhance the robustness of cell-division orientation by orchestrating a coherent feed-forward loop that converges on the cell-cycle regulators CYCLIN-P3;1 (CYCP3;1) and CYCP3;2. While cytokinin induces both P-type cyclins, SPT represses their expression. Overexpression of CYCP3s disrupts style radial symmetry, causing the split-style phenotype and hypersensitivity to cytokinin observed in the spt mutant. Finally, we demonstrate a genetic link connecting the machinery of cell-division orientation, controlled by auxin, with the cell-proliferation input induced by cytokinin. Thus, our work reveals how the antagonistic auxin-cytokinin interaction scales up symmetry from the cellular to the organ level.