TMK-PIN1 drives a short self-organizing circuit for auxin export and signaling in Arabidopsis

Abstract

The versatile and pivotal roles of the phytohormone auxin in regulating plant growth and development are typically linked to its directional transport, relying on the polarized PIN-FORMED (PIN) auxin exporters at the plasma membrane (PM). For decades, auxin has been proposed to promote PIN polarization, generating self-regulatory feedback mediating much of plant development, but mechanistic insight into this regulation is lacking. Here, we uncover an auxin-induced protein complex at the PM, containing auxin co-receptors transmembrane kinases (TMKs) and PIN1 auxin exporter, as the core machinery that underlies this feedback regulation. Auxin promotes PIN1 phosphorylation by TMKs, modulating PIN1 polarization and transport activity. We also provide evidence that PIN1-exported extracellular auxin is crucial for TMK activation and cell elongation, thus forming the simplest two-element self-regulatory feedback circuit. Thus, these findings offer direct mechanistic insights into a potential self-organizing circuit for auxin signaling and transport to ensure proper plant development in Arabidopsis.