Force-responsive symmetric cell divisions orient stomata along global tissue axes

Abstract

Stomata, microscopic pores that regulate gas exchange in plants, are patterned according to conserved pathways that regulate their physiology. Here, we identify a new mode of stomatal patterning that depends on previously unrecognized regulation of the final symmetric cell division that creates paired guard cells. Symmetric cell divisions are aligned by tensile stress at both the subcellular and supracellular scales, creating a globally polarized stomatal field that tracks the major axes of tissue growth. By identifying KATANIN as a critical regulator of symmetric division orientation, we show that stress-based division orientation is required to prepattern stomatal morphology and pore creation. We find that expansion of neighboring cells non-autonomously controls symmetric division orientation, linking stomatal alignment to overall leaf shape. Finally, we show that polarized stomatal fields are widespread across plant genera and their species-specific alignment patterns are consistent with the force-based mechanism we identify in Arabidopsis. This force-responsive pathway provides a unifying model that explains long-standing observations of stomatal organization across species.