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Arabidopsis D6PK is a lipid domain-dependent mediator of root epidermal planar polarity

Nature Plants volume 1, Article number: 15162 (2015) Cite this article

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Abstract

Development of diverse multicellular organisms relies on coordination of single-cell polarities within the plane of the tissue layer (planar polarity). Cell polarity often involves plasma membrane heterogeneity generated by accumulation of specific lipids and proteins into membrane subdomains. Coordinated hair positioning along Arabidopsis root epidermal cells provides a planar polarity model in plants, but knowledge about the functions of proteo-lipid domains in planar polarity signalling remains limited. Here we show that Rho-of-plant (ROP) 2 and 6, phosphatidylinositol-4-phosphate 5-kinase 3 (PIP5K3), DYNAMIN-RELATED PROTEIN (DRP) 1A and DRP2B accumulate in a sterol-enriched, polar membrane domain during root hair initiation. DRP1A, DRP2B, PIP5K3 and sterols are required for planar polarity and the AGCVIII kinase D6 PROTEIN KINASE (D6PK) is a modulator of this process. D6PK undergoes phosphatidylinositol-4,5-bisphosphate- and sterol-dependent basal-to-planar polarity switching into the polar, lipid-enriched domain just before hair formation, unravelling lipid-dependent D6PK localization during late planar polarity signalling.

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Figure 1: A sterol-enriched polar domain accumulates ROP2, ROP6, PI5K3, DRP1A and DRP2B during hair initiation.
Figure 2: Sterol, PIP5K3 and DRP function is required for polar ROP positioning during planar polarity formation.
Figure 3: D6PK basal-to-planar polarity switching and function in planar polarity.
Figure 4: D6PK polarity requires sterol, DRP1A and PIP5K3 function during early hair bulging.
Figure 5: Direct D6PK interaction with phosphatidylinositol phosphates in vitro.

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Acknowledgements

We are grateful to T. Aoyama, S.Y. Bednarek, D.W. Ehrhardt, N. Geldner, B. Scheres, N. Tsutsumi, R.E. Williamson and Z. Yang for sharing published materials. We thank the Nottingham Arabidopsis Stock Centre for providing seed stocks. A.H. and T.S. were supported by a grant from the Swedish Kempe foundations to M.G., A.H. and A.G. were supported by a ‘ShapeSystems’ project grant number 2012.0050 by the Knut & Alice Wallenberg foundation to M.G., T.S. and M.G. were supported by ERC-2010-STG Green-Lat-Pol, grant number 260699 to M.G.

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Author notes

  1. Thomas Stanislas & Klaus Brackmann

    Present address: †Present addresses: Laboratoire de Reproduction et développement des plantes, INRA, CNRS, ENS Lyon, UCB Lyon 1, Université de Lyon, 46 allée d'Italie, 69364 Lyon, France (T.S.); Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Dr. Bohr-Gasse 3, AT-1030 Vienna, Austria (K.B.),

  2. Thomas Stanislas and Anke Hüser: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, SE-90 187 Umeå, Sweden

    Thomas Stanislas, Anke Hüser, Christian S. Kiefer, Klaus Brackmann, Stefano Pietra, Anna Gustavsson & Markus Grebe

  2. Institute of Biochemistry and Biology, Plant Physiology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Building 20, DE-14476 Potsdam-Golm, Germany

    Thomas Stanislas & Markus Grebe

  3. Technische Universität München, Plant Systems Biology, Emil-Ramann-Str. 4, DE-85354 Freising, Germany

    Inês C. R. Barbosa, Melina Zourelidou & Claus Schwechheimer

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Contributions

M.G. conceived the project. A.H., C.S., I.C.R.B., M.G., T.S. and S.P. designed experiments. A.G., A.H., C.S.K., I.C.R.B., K.B., M.G., M.Z., S.P. and T.S. performed experiments and interpreted the results. I.C.R.B., M.Z. and C.S. provided unpublished materials, discussions on experimental design and interpretation of results. M.G. and T.S. wrote the manuscript. All authors read the manuscript, edited and commented on it before submission.

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Correspondence to Markus Grebe.

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Stanislas, T., Hüser, A., Barbosa, I. et al. Arabidopsis D6PK is a lipid domain-dependent mediator of root epidermal planar polarity. Nature Plants 1, 15162 (2015). https://doi.org/10.1038/nplants.2015.162

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