ROP GTPase-Dependent Actin Microfilaments Promote PIN1 Polarization by Localized Inhibition of Clathrin-Dependent Endocytosis

TLDR

Cell polarization, essential for diverse cellular functions, remains poorly understood, but in plants the asymmetric distribution of PIN‑FORMED auxin efflux carriers is central to developmental patterning and morphogenesis. ROP2 blocks PIN1 endocytosis by inducing cortical actin microfilament accumulation via its effector RIC4. Auxin activates ROP GTPases, leading to ROP2‑mediated inhibition of PIN1 endocytosis through actin microfilament accumulation, thereby establishing asymmetric PIN1 distribution and promoting cell interdigitation, illustrating a conserved Rho‑GTPase–dependent polarity mechanism.

Abstract

Cell polarization via asymmetrical distribution of structures or molecules is essential for diverse cellular functions and development of organisms, but how polarity is developmentally controlled has been poorly understood. In plants, the asymmetrical distribution of the PIN-FORMED (PIN) proteins involved in the cellular efflux of the quintessential phytohormone auxin plays a central role in developmental patterning, morphogenesis, and differential growth. Recently we showed that auxin promotes cell interdigitation by activating the Rho family ROP GTPases in leaf epidermal pavement cells. Here we found that auxin activation of the ROP2 signaling pathway regulates the asymmetric distribution of PIN1 by inhibiting its endocytosis. ROP2 inhibits PIN1 endocytosis via the accumulation of cortical actin microfilaments induced by the ROP2 effector protein RIC4. Our findings suggest a link between the developmental auxin signal and polar PIN1 distribution via Rho-dependent cytoskeletal reorganization and reveal the conservation of a design principle for cell polarization that is based on Rho GTPase-mediated inhibition of endocytosis.