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

doi:10.15252/embr.201847182

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 LinsJens Tilsner, Emmanuelle M. Bayer

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Article number	e47182
Number of pages	26
Journal	EMBO Reports
Volume	20
Issue number	8
Early online date	9 Jul 2019
DOIs	https://doi.org/10.15252/embr.201847182
Publication status	Published - 1 Aug 2019

Keywords

Plasmodesmata
Intracellular communication in plants
ER-PM membrane contact sites
Multiple C2 domains transmembrane region proteins

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10.15252/embr.201847182Licence: CC BY

Brault_2019_EMBOR_MultipleC2_CC
Copyright © 2019 The Authors. Published under the terms of the CC BY 4.0 license. This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Cite this

Brault, M. L., Petit, J. D., Immel, F., Nicolas, W. J., Glavier, M., Brocard, L., Gaston, A., Fouché, M., Hawkins, T. J., Crowet, J.-M., Grison, M. S., Germain, V., Rocher, M., Kraner, M., Alva, V., Claverol, S., Paterlini, A., Helariutta, Y., Deleu, M., ... Bayer, E. M. (2019). Multiple C2 domains and Transmembrane region Proteins (MCTPs) tether membranes at plasmodesmata. EMBO Reports, 20(8), Article e47182. https://doi.org/10.15252/embr.201847182

@article{d4917eb8de8b421ab97d4a2674321825,

title = "Multiple C2 domains and Transmembrane region Proteins (MCTPs) tether membranes at plasmodesmata",

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.",

keywords = "Plasmodesmata, Intracellular communication in plants, ER-PM membrane contact sites, Multiple C2 domains transmembrane region proteins",

author = "Brault, {Marie L.} and Petit, {Jules D.} and Fran{\c c}oise Immel and Nicolas, {William J.} and Marie Glavier and Lysiane Brocard and Am{\`e}lia Gaston and Mathieu Fouch{\'e} and Hawkins, {Timothy J.} and Jean-Marc Crowet and Grison, {Magali S.} and V{\'e}ronique Germain and Marion Rocher and Max Kraner and Vikram Alva and St{\'e}phane Claverol and Andrea Paterlini and Yk{\"a} Helariutta and Magali Deleu and Laurence Lins and Jens Tilsner and Bayer, {Emmanuelle M.}",

note = "Funding: Work in J.T, lab 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).",

year = "2019",

month = aug,

day = "1",

doi = "10.15252/embr.201847182",

language = "English",

volume = "20",

journal = "EMBO Reports",

issn = "1469-221X",

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Brault, ML, Petit, JD, Immel, F, Nicolas, WJ, Glavier, M, Brocard, L, Gaston, A, Fouché, M, Hawkins, TJ, Crowet, J-M, Grison, MS, Germain, V, Rocher, M, Kraner, M, Alva, V, Claverol, S, Paterlini, A, Helariutta, Y, Deleu, M, Lins, L, Tilsner, J & Bayer, EM 2019, 'Multiple C2 domains and Transmembrane region Proteins (MCTPs) tether membranes at plasmodesmata', EMBO Reports, vol. 20, no. 8, e47182. https://doi.org/10.15252/embr.201847182

TY - JOUR

T1 - Multiple C2 domains and Transmembrane region Proteins (MCTPs) tether membranes at plasmodesmata

AU - Brault, Marie L.

AU - Petit, Jules D.

AU - Immel, Françoise

AU - Nicolas, William J.

AU - Glavier, Marie

AU - Brocard, Lysiane

AU - Gaston, Amèlia

AU - Fouché, Mathieu

AU - Hawkins, Timothy J.

AU - Crowet, Jean-Marc

AU - Grison, Magali S.

AU - Germain, Véronique

AU - Rocher, Marion

AU - Kraner, Max

AU - Alva, Vikram

AU - Claverol, Stéphane

AU - Paterlini, Andrea

AU - Helariutta, Ykä

AU - Deleu, Magali

AU - Lins, Laurence

AU - Tilsner, Jens

AU - Bayer, Emmanuelle M.

N1 - Funding: Work in J.T, lab 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).

PY - 2019/8/1

Y1 - 2019/8/1

N2 - 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.

AB - 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.

KW - Plasmodesmata

KW - Intracellular communication in plants

KW - ER-PM membrane contact sites

KW - Multiple C2 domains transmembrane region proteins

UR - https://www.embopress.org/doi/10.15252/embr.201847182#support-information-section

U2 - 10.15252/embr.201847182

DO - 10.15252/embr.201847182

M3 - Article

SN - 1469-221X

VL - 20

JO - EMBO Reports

JF - EMBO Reports

IS - 8

M1 - e47182

ER -

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

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

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