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A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants

Nature Plants volume 2, Article number: 16089 (2016) Cite this article

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Abstract

Many signalling proteins permanently or transiently localize to specific organelles. It is well established that certain lipids act as biochemical landmarks to specify compartment identity. However, they also influence membrane biophysical properties, which emerge as important features in specifying cellular territories. Such parameters include the membrane inner surface potential, which varies according to the lipid composition of each organelle. Here, we found that the plant plasma membrane (PM) and the cell plate of dividing cells have a unique electrostatic signature controlled by phosphatidylinositol-4-phosphate (PtdIns(4)P). Our results further reveal that, contrarily to other eukaryotes, PtdIns(4)P massively accumulates at the PM, establishing it as a critical hallmark of this membrane in plants. Membrane surface charges control the PM localization and function of the polar auxin transport regulator PINOID as well as proteins from the BRI1 KINASE INHIBITOR1 (BKI1)/MEMBRANE ASSOCIATED KINASE REGULATOR (MAKR) family, which are involved in brassinosteroid and receptor-like kinase signalling. We anticipate that this PtdIns(4)P-driven physical membrane property will control the localization and function of many proteins involved in development, reproduction, immunity and nutrition.

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Figure 1: The plant PM and the cell plate are highly electronegative.
Figure 2: PI(4)K activity is required to maintain the PM electrostatic signature.
Figure 3: PtdIns(4)P is a hallmark of the plant PM.
Figure 4: PM PtdIns(4)P drives the electrostatic field of the cell membrane.
Figure 5: PINOID and BKI1/MAKRs are effectors of the PM electrostatic field.
Figure 6: PM targeting by PID cationic membrane hook is required for function.

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Acknowledgements

We thank M. Dreux, O. Hamant, G. Vert, T. Vernoux, S. Mongrand, A. Martiniere-Delaunay and the SiCE group for discussions and comments, J. Chory for initial support and discussions, S. Grinstein, M. Lemmon, G. Hammond, J. Friml, J. Goedhart, B. Scheres for reagents, A. Lacroix and J. Berger for plant care and PLATIM for help with imaging. Y.J. is funded by ERC no. 3363360-APPL and Marie Curie Action, no. PCIG-GA-2011-303601, under FP/2007-2013. This work was initially supported by grants from the US National Institutes of Health (GM094428) and the Howard Hughes Medical Institute to Joanne Chory and a fellowship from the H.M. Kirby foundation to Y.J. M.S. is funded by a PhD fellowship from the French Ministry of Education. T.S is supported by ERC grant no. 615739-MechanoDevo to O. Hamant.

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  1. Mathilde Laetitia Audrey Simon and Matthieu Pierre Platre: These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratoire Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, F-69342 Lyon, France

    Mathilde Laetitia Audrey Simon, Matthieu Pierre Platre, Maria Mar Marquès-Bueno, Laia Armengot, Thomas Stanislas, Vincent Bayle, Marie-Cécile Caillaud & Yvon Jaillais

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Contributions

M.S., M.P. and M.C.C. produced and imaged the lipid and MSC reporter lines; M.S., M.P., M.C.C. and T.S. imaged the KA1MARK1 reporter in various tissues and plant systems; and M.S. and M.P. carried out the PAO and Wortmannin experiments. V.B. performed the FRAP experiments and helped with image quantification and acquisition; M.C.C. performed cytokinesis and N. benthamiana experiments; M.S., M.M.M.B. and L.A. performed yeast and lipid overlay experiments; M.M.M.B. and L.A. produced and imaged the MAKRs–cYFP lines; M.S. produced and phenotyped the EXP7::PID lines; M.S., M.P., M.C.C. and Y.J. conceived the study and designed experiments; and M.S., M.P., M.C.C. and Y.J. wrote the manuscript.

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Correspondence to Marie-Cécile Caillaud or Yvon Jaillais.

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Simon, M., Platre, M., Marquès-Bueno, M. et al. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nature Plants 2, 16089 (2016). https://doi.org/10.1038/nplants.2016.89

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