AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells

• DOI: 10.1016/j.cub.2021.02.028
• Publication Date: 2021-03-11T05:09:31Z
• Authors: Matouš Glanc; Kasper Van Gelderen; Lukas Hoermayer; Shutang Tan; Satoshi Naramoto; Xixi Zhang; David Domjan; Ludmila Včelařová; Robert Hauschild; Alexander Johnson; Edward de Koning; Maritza van Dop; Eike Rademacher; Stef Janson; Xiaoyu Wei; Gergely Molnár; Matyáš Fendrych; Bert De Rybel; Remko Offringa; Jiří Friml
• Keywords: POLARIZATION; ENDOCYTOSIS; General Biochemistry,Genetics and Molecular Biology; Arabidopsis; DEPENDENT AUXIN TRANSPORT; GRADIENTS; Plant Roots; Article; SYMMETRY-BREAKING; Gene Expression Regulation, Plant; Plant Cells; lateral diffusion; TRAFFICKING; PHOSPHORYLATION; PHOTOTROPISM; ORGANOGENESIS; Indoleacetic Acids; polar auxin transport; Arabidopsis Proteins; General Neuroscience; Biology and Life Sciences; positive feedback; Cell Polarity; Membrane Transport Proteins; Biological Transport; ARABIDOPSIS; protein phosphorylation; cell polarity; plant development; General Agricultural and Biological Sciences

Polar subcellular localization of the PIN exporters of the phytohormone auxin is a key determinant of directional, intercellular auxin transport and thus a central topic of both plant cell and developmental biology. Arabidopsis mutants lacking PID, a kinase that phosphorylates PINs, or the MAB4/MEL proteins of unknown molecular function display PIN polarity defects and phenocopy pin mutants, but mechanistic insights into how these factors convey PIN polarity are missing. Here, by combining protein biochemistry with quantitative live-cell imaging, we demonstrate that PINs, MAB4/MELs, and AGC kinases interact in the same complex at the plasma membrane. MAB4/MELs are recruited to the plasma membrane by the PINs and in concert with the AGC kinases maintain PIN polarity through limiting lateral diffusion-based escape of PINs from the polar domain. The PIN-MAB4/MEL-PID protein complex has self-reinforcing properties thanks to positive feedback between AGC kinase-mediated PIN phosphorylation and MAB4/MEL recruitment. We thus uncover the molecular mechanism by which AGC kinases and MAB4/MEL proteins regulate PIN localization and plant development.