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Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions

Nature volume 456, pages 962–966 (2008)Cite this article

A Retraction to this article was published on 16 July 2014

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 tropisms2,3,4,5,6,7. 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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Figure 1: Endocytic recycling-based two-step mechanism generates PIN polarity.
Figure 2: Rab5-mediated endocytosis is required for PIN polarization.
Figure 3: Manipulation of the Rab5 pathway during embryogenesis leads to defects in PIN polarity, auxin response distribution and embryo development.
Figure 4: Manipulation of Rab5 pathway leads to homeotic leaf-to-root transformation.

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Acknowledgements

We thank M. Bennett, T. Gaude, L. Jiang, G. Jürgens, C. Luschnig, E. Meywerowitz, W. Michalke, R. Offringa, D. Robinson, K. Schumacher, J. Wiedenmann and D. Weijers for sharing published material and RIKEN, SALK and NASC Arabidopsis stock centres for providing mutant lines and the RNAi construct. We thank W. Muller for assistance with SEM and F. Kindt and R. Leito for photography. We acknowledge the Center for Plant Molecular Biology (ZMBP), University of Tübingen, Germany for the facilities during the initial phase of the project. This work was supported by VolkswagenStiftung (P.D. and J.F.), EMBO Long Term Fellowship and Netherlands Organization for Scientific Research (NWO)-VENI grant (P.D.), EMBO Young Investigator Program and Odysseus program of FWO (J.F.), HFSP fellowship (H.T.), EMBO Long Term Fellowship and HFSP fellowship (A.P.M.), EMBO Long Term Fellowship (K.P.), NWO-VIDI grant (I.B.), HFSP fellowship and Swiss National Science Foundation (N.G.), HHMI, USDA and NIH (J.C.), NWO-Spinoza award (B.S.) and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (T.U. and A.N.).

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Author notes

  1. Hirokazu Tanaka, Tatsuaki Goh, Kazuo Ebine and Ari Pekka Mähönen: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands,

    Pankaj Dhonukshe, Ari Pekka Mähönen, Kalika Prasad, Ikram Blilou, Jian Xu & Ben Scheres

  2. Department of Plant Systems Biology, and Department of Molecular Genetics, VIB, Ghent University, Technologiepark 927, 9052 Gent, Belgium,

    Hirokazu Tanaka & Jiří Friml

  3. Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan,

    Tatsuaki Goh, Kazuo Ebine, Tomohiro Uemura, Takashi Ueda & Akihiko Nakano

  4. Department of Plant Molecular Biology (DBMV), University of Lausanne, UNIL-Sorge, Biophore Building, 1015 Lausanne, Switzerland,

    Niko Geldner

  5. Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, California 92037, USA ,

    Niko Geldner & Joanne Chory

  6. Molecular Membrane Biology Laboratory, RIKEN Advanced Science Institute, Wako, Saitama 351-0198, Japan ,

    Akihiko Nakano

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Correspondence to Pankaj Dhonukshe or Jiří Friml.

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Dhonukshe, P., Tanaka, H., Goh, T. et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456, 962–966 (2008). https://doi.org/10.1038/nature07409

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