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Multiple C2 domains and Transmembrane region Proteins (MCTPs) tether membranes at plasmodesmata

Brault, Marie L. and Petit, Jules D. and Immel, Françoise and Nicolas, William J. and Glavier, Marie and Brocard, Lysiane and Gaston, Amélia and Fouché, Mathieu and Hawkins, Timothy J. and Crowet, Jean-Marc and Grison, Magali S. and Germain, Véronique and Rocher, Marion and Kraner, Max and Alva, Vikram and Claverol, Stéphane and Paterlini, Andrea and Helariutta, Ykä and Deleu, Magali and Lins, Laurence and Tilsner, Jens and Bayer, Emmanuelle E. (2019) Multiple C2 domains and Transmembrane region Proteins (MCTPs) tether membranes at plasmodesmata. EMBO Reports, 20 (8). Art. No. e47182. ISSN 1469-221X. https://resolver.caltech.edu/CaltechAUTHORS:20180927-114225130

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Abstract

In eukaryotes, membrane contact sites (MCS) allow direct communication between organelles. Plants have evolved a unique type of MCS, inside intercellular pores, the plasmodesmata, where endoplasmic reticulum (ER)–plasma membrane (PM) contacts coincide with regulation of cell‐to‐cell signalling. The molecular mechanism and function of membrane tethering within plasmodesmata remain unknown. Here, we show that the multiple C2 domains and transmembrane region protein (MCTP) family, key regulators of cell‐to‐cell signalling in plants, act as ER‐PM tethers specifically at plasmodesmata. We report that MCTPs are plasmodesmata proteins that insert into the ER via their transmembrane region while their C2 domains dock to the PM through interaction with anionic phospholipids. A Atmctp3/Atmctp4 loss of function mutant induces plant developmental defects, impaired plasmodesmata function and composition, while MCTP4 expression in a yeast Δtether mutant partially restores ER‐PM tethering. Our data suggest that MCTPs are unique membrane tethers controlling both ER‐PM contacts and cell‐to‐cell signalling.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.15252/embr.201847182DOIArticle
https://doi.org/10.1101/423905DOIDiscussion Paper
ORCID:
AuthorORCID
Petit, Jules D.0000-0003-4652-2843
Immel, Françoise0000-0002-2028-902X
Nicolas, William J.0000-0001-5970-8626
Glavier, Marie0000-0002-7100-7045
Gaston, Amélia0000-0001-9974-8083
Crowet, Jean-Marc0000-0002-9252-2396
Grison, Magali S.0000-0002-3080-3686
Alva, Vikram0000-0003-1188-473X
Paterlini, Andrea0000-0002-1777-3160
Helariutta, Ykä0000-0002-7287-8459
Deleu, Magali0000-0001-8255-2965
Lins, Laurence0000-0001-7772-6748
Tilsner, Jens0000-0003-3873-0650
Bayer, Emmanuelle E.0000-0001-8642-5293
Additional Information:© 2019 The Authors. Published under the terms of the CC BY 4.0 license. Received 3 October 2018; Revised 28 May 2019; Accepted 6 June 2019; Published online 9 July 2019. Data availability: Proteomic data: PRIDE PXD006800 (http://www.ebi.ac.uk/pride/archive/projects/PXD006800), PRIDE PXD006806 (http://www.ebi.ac.uk/pride/archive/projects/PXD006806) and PRIDE PXD013999 (http://www.ebi.ac.uk/pride/archive/projects/PXD013999). This work was supported by the National Agency for Research (Grant ANR‐14‐CE19‐0006‐01 to E.M.B), “Osez l'interdisciplinarité” OSEZ‐2017‐BRIDGING CNRS programme to E.M.B., the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement No 772103‐BRIDGING) to E.M.B, the EMBO Young Investigator Program to E.M.B., and Fonds National de la Recherche Scientifique (NEAMEMB PDR T.1003.14, BRIDGING CDR J.0114.18 and RHAMEMB CDR J.0086.18) to L. L. and M.D. J.D.P. is funded by a PhD fellowship from the Belgian “Formation à la Recherche dans l'Industrie et l'Agriculture” (FRIA grant no. 1.E.096.18). Work in J.T. laboratory is supported by grant BB/M007200/1 from the U.K. Biotechnology and Biomedical Sciences Research Council (BBSRC) and by the Scottish Government's Rural and Environment Science and Analytical Services Division (RESAS). Fluorescence microscopy analyses were performed at the plant pole of the Bordeaux Imaging Centre (http://www.bic.u-bordeaux.fr). For electron microscopy, the Region Aquitaine also supported the acquisition of the electron microscope (grant no. 2011 13 04 007 PFM), and FranceBioImaging Infrastructure supported the acquisition of the AFS2 and ultramicrotome. The proteomic analyses were performed at the Functional Genomic Center of Bordeaux, (https://proteome.cgfb.u-bordeaux.fr). We thank Steffen Vanneste and Abel Rosado for providing the VAP27.1.RFP and SYT1.GFP binary vectors and Yvon Jaillais for providing the 1xPH(FAPP1) Arabidopsis transgenic lines. The plasmid pRBbar‐OCS was kindly provided by Prof. Frederik Börnke (IGZ—Leibniz Institute of Vegetable and Ornamental Crops, Groβbeeren, Germany). We thank Christophe Trehin and Patrice Morel for providing the AtMCT15_C2s construct and Alenka Copic for providing the yeast WT and Δtether strains. We thank Fabrice Cordelières for his help for the fluorescence image quantification and Paul Gouget, Yvon Jaillais, Andrea Paterlini and Yrjo Helariutta for critical review of the article prior to submission. Author contributions: FI, MSG, MF and SC carried out the label‐free proteomic analysis of plasmodesmata fractions isolated from Arabidopsis cell cultures. MLB cloned the MCTPs, produced and phenotyped the Arabidopsis transgenic lines, with the exception of AtMCTP4:GFP‐AtMCTP4 and 35S:GFP‐AtMCTP6 which were generated by MK. MLB and JDP imaged the MCTP reporter lines. WJN carried out the FRAP analysis and image quantification for co‐localisation with the help of LB. MG and JDP performed the CLEM and immunogold labelling approaches. JT, MR and VG performed the plasmodesmata cell‐to‐cell trafficking assay. MK carried out the proteomic comparison and AP the data integration. AG performed the phylogenic analysis. JDP and MLB carried out the PAO experiments. MLB performed the yeast experiments. TJH and JT performed the 3D‐SIM. VA carried out the C2 cluster map analysis. JDP carried out the molecular dynamic analysis with the help of J‐MC, LL and MD. EMB conceived the study and designed experiments with the help of JT and LL. EMB, JDP, JT, MLB and YH wrote the manuscript. All the authors discussed the results and commented on the manuscript. The authors declare that they have no conflict of interest.
Funders:
Funding AgencyGrant Number
Agence Nationale pour la Recherche (ANR)ANR-14-CE19-0006-01
European Research Council (ERC)772103-BRIDGING
European Molecular Biology Organization (EMBO)UNSPECIFIED
Fonds National de la Recherche Scientifique (FNRS)NEAMEMB PDR T.1003.14
Fonds National de la Recherche Scientifique (FNRS)BRIDGING CDR J.0114.18
Fonds National de la Recherche Scientifique (FNRS)RHAMEMB CDR J.0086.18
Formation à la Recherche dans l’Industrie et l’Agriculture1.E.096.18
Biotechnology and Biological Sciences Research Council (BBSRC)BB/M007200/1
Scottish Government Rural and Environment Science and Analytical Services Division (RESAS)UNSPECIFIED
Subject Keywords:ER-PM membrane contact sites; intercellular communication in plants; multiple C2 domains and transmembrane region proteins; plasmodesmata
Issue or Number:8
Record Number:CaltechAUTHORS:20180927-114225130
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180927-114225130
Official Citation:Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. Marie L Brault. Jules D Petit; Françoise Immel; William J Nicolas; Marie Glavier; Lysiane Brocard; Amèlia Gaston; Mathieu Fouché; Timothy J Hawkins; Jean‐Marc Crowet; Magali S Grison; Véronique Germain; Marion Rocher; Max Kraner; Vikram Alva; Stéphane Claverol; Andrea Paterlini; Ykä Helariutta; Magali Deleu; Laurence Lins; Jens Tilsner; Emmanuelle M Bayer. EMBO Reports (2019) 20: e47182https://doi.org/10.15252/embr.201847182
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90012
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:27 Sep 2018 20:37
Last Modified:03 Oct 2019 20:21

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