1. Department of Biology, Faculty of Science, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands
2. Department of Plant Systems Biology, VIB, and Department of Molecular Genetics, Ghent University, Technologiepark 927, 9052 Gent, Belgium
3. Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan
4. Department of Plant Molecular Biology (DBMV), University of Lausanne, UNIL-Sorge, Biophore Building, 1015 Lausanne, Switzerland
5. Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, California 92037, USA
6. Molecular Membrane Biology Laboratory, RIKEN Advanced Science Institute, Wako, Saitama 351-0198, Japan
7. These authors contributed equally to this work.

Correspondence to: Pankaj Dhonukshe¹Jií Friml² Correspondence and requests for materials should be addressed to P.D. (Email: P.B.Dhonukshe@uu.nl) or J.F. (Email: jiri.friml@psb.ugent.be).

Abstract

Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication—a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family¹ are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms^{2, 3, 4, 5, 6, 7}. Polar PIN localization determines the direction of intercellular auxin flow⁸, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.

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