Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants

Jessica Pérez-Sancho; Marija Smokvarska; Gwennogan Dubois; Marie Glavier; Sujith Sritharan; Tatiana S. Moraes; Hortense Moreau; Victor Dietrich; Matthieu P. Platre; Andrea Paterlini; Ziqiang P. Li; Laetitia Fouillen; Magali S. Grison; Pepe Cana-Quijada; Françoise Immel; Valerie Wattelet; Mathieu Ducros; Lysiane Brocard; Clément Chambaud; Yongming Luo; Priya Ramakrishna; Vincent Bayle; Linnka Lefebvre-Legendre; Stéphane Claverol; Matej Zabrady; Pascal G.P. Martin; Wolfgang Busch; Marie Barberon; Jens Tilsner; Yrjö Helariutta; Eugenia Russinova; Antoine Taly; Yvon Jaillais; Emmanuelle M. Bayer

doi:10.1016/j.cell.2024.11.034

Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants

Jessica Pérez-Sancho, Marija Smokvarska, Gwennogan Dubois, Marie Glavier, Sujith Sritharan, Tatiana S. Moraes, Hortense Moreau, Victor Dietrich, Matthieu P. Platre, Andrea Paterlini, Ziqiang P. Li, Laetitia Fouillen, Magali S. Grison, Pepe Cana-Quijada, Françoise Immel, Valerie Wattelet, Mathieu Ducros, Lysiane Brocard, Clément Chambaud, Yongming LuoPriya Ramakrishna, Vincent Bayle, Linnka Lefebvre-Legendre, Stéphane Claverol, Matej Zabrady, Pascal G.P. Martin, Wolfgang Busch, Marie Barberon, Jens Tilsner, Yrjö Helariutta, Eugenia Russinova, Antoine Taly, Yvon Jaillais^*, Emmanuelle M. Bayer^*

^*Corresponding author for this work

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

Abstract

Membrane contact sites (MCSs) are fundamental for intracellular communication, but their role in intercellular communication remains unexplored. We show that in plants, plasmodesmata communication bridges function as atypical endoplasmic reticulum (ER)-plasma membrane (PM) tubular MCSs, operating at cell-cell interfaces. Similar to other MCSs, ER-PM apposition is controlled by a protein-lipid tethering complex, but uniquely, this serves intercellular communication. Combining high-resolution microscopy, molecular dynamics, and pharmacological and genetic approaches, we show that cell-cell trafficking is modulated through the combined action of multiple C2 domains transmembrane domain proteins (MCTPs) 3, 4, and 6 ER-PM tethers and phosphatidylinositol-4-phosphate (PI4P) lipid. Graded PI4P amounts regulate MCTP docking to the PM, their plasmodesmata localization, and cell-cell permeability. SAC7, an ER-localized PI4P-phosphatase, regulates MCTP4 accumulation at plasmodesmata and modulates cell-cell trafficking capacity in a cell-type-specific manner. Our findings expand MCS functions in information transmission from intracellular to intercellular cellular activities.

Original language	English
Pages (from-to)	958-977
Number of pages	20
Journal	Cell
Volume	188
Issue number	4
DOIs	https://doi.org/10.1016/j.cell.2024.11.034
Publication status	Published - 20 Feb 2025

Keywords

Endoplasmic reticulum plasma membrane
Intercellular communication
MCTP
Membrane contact sites
Phosphoinositide
Plant biology
Plasmodesmata

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10.1016/j.cell.2024.11.034

Perez-Sancho_et_al_2025_Plasmodesmata_act_as_Cell_AAM_CCBY
Copyright © 2025 the Authors. This work has been made available online in accordance with the University of St Andrews Open Access policy. This accepted manuscript is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The final published version of this work is available at https://doi.org/10.1016/j.cell.2024.11.034.
Accepted author manuscript, 20.7 MBLicence: CC BY

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Pérez-Sancho, J., Smokvarska, M., Dubois, G., Glavier, M., Sritharan, S., Moraes, T. S., Moreau, H., Dietrich, V., Platre, M. P., Paterlini, A., Li, Z. P., Fouillen, L., Grison, M. S., Cana-Quijada, P., Immel, F., Wattelet, V., Ducros, M., Brocard, L., Chambaud, C., ... Bayer, E. M. (2025). Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants. Cell, 188(4), 958-977. https://doi.org/10.1016/j.cell.2024.11.034

@article{7b83bc4e65d24e23a8bfe237ad5de6b8,

title = "Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants",

abstract = "Membrane contact sites (MCSs) are fundamental for intracellular communication, but their role in intercellular communication remains unexplored. We show that in plants, plasmodesmata communication bridges function as atypical endoplasmic reticulum (ER)-plasma membrane (PM) tubular MCSs, operating at cell-cell interfaces. Similar to other MCSs, ER-PM apposition is controlled by a protein-lipid tethering complex, but uniquely, this serves intercellular communication. Combining high-resolution microscopy, molecular dynamics, and pharmacological and genetic approaches, we show that cell-cell trafficking is modulated through the combined action of multiple C2 domains transmembrane domain proteins (MCTPs) 3, 4, and 6 ER-PM tethers and phosphatidylinositol-4-phosphate (PI4P) lipid. Graded PI4P amounts regulate MCTP docking to the PM, their plasmodesmata localization, and cell-cell permeability. SAC7, an ER-localized PI4P-phosphatase, regulates MCTP4 accumulation at plasmodesmata and modulates cell-cell trafficking capacity in a cell-type-specific manner. Our findings expand MCS functions in information transmission from intracellular to intercellular cellular activities.",

keywords = "Endoplasmic reticulum plasma membrane, Intercellular communication, MCTP, Membrane contact sites, Phosphoinositide, Plant biology, Plasmodesmata",

author = "Jessica P{\'e}rez-Sancho and Marija Smokvarska and Gwennogan Dubois and Marie Glavier and Sujith Sritharan and Moraes, {Tatiana S.} and Hortense Moreau and Victor Dietrich and Platre, {Matthieu P.} and Andrea Paterlini and Li, {Ziqiang P.} and Laetitia Fouillen and Grison, {Magali S.} and Pepe Cana-Quijada and Fran{\c c}oise Immel and Valerie Wattelet and Mathieu Ducros and Lysiane Brocard and Cl{\'e}ment Chambaud and Yongming Luo and Priya Ramakrishna and Vincent Bayle and Linnka Lefebvre-Legendre and St{\'e}phane Claverol and Matej Zabrady and Martin, {Pascal G.P.} and Wolfgang Busch and Marie Barberon and Jens Tilsner and Yrj{\"o} Helariutta and Eugenia Russinova and Antoine Taly and Yvon Jaillais and Bayer, {Emmanuelle M.}",

note = "Funding: This work was supported by the European Research Council (ERC) under the European Union{\textquoteright}s Horizon 2020 research and innovation program (projects 772103-BRIDGING to E.M.B. and 101001097-LIPIDEV to Y.J.), the National Agency for Research (grants ANR-18-CE13-0016 STAYING-TIGHT to E.M.B. and Y.J., ANR-2020-CE20-0002 3C TomFruit Growth to E.M.B., ANR-21-CE13-0016-01 DIVCON to A.T. and E.M.B., and ANR-18-CE13-0025-02 caLIPSO to Y.J.), the Human Frontier Science Program (project RGP0002/2020 to E.M.B.), the French Government in the framework of the IdEX Bordeaux University “Investments for the Future” program/GPR Bordeaux Plant Sciences (E.M.B.), the Swiss National Science Foundation (project 31003A_179159 to M.B.), Research Foundation-Flanders grant G002121N to E.R., the HORIZON-MSCA-2023-PF-01 project 101152141-BRACTION to Y.L., and Projet Emergents FlowValve University of Bordeaux to M.S.",

year = "2025",

month = feb,

day = "20",

doi = "10.1016/j.cell.2024.11.034",

language = "English",

volume = "188",

pages = "958--977",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "4",

}

Pérez-Sancho, J, Smokvarska, M, Dubois, G, Glavier, M, Sritharan, S, Moraes, TS, Moreau, H, Dietrich, V, Platre, MP, Paterlini, A, Li, ZP, Fouillen, L, Grison, MS, Cana-Quijada, P, Immel, F, Wattelet, V, Ducros, M, Brocard, L, Chambaud, C, Luo, Y, Ramakrishna, P, Bayle, V, Lefebvre-Legendre, L, Claverol, S, Zabrady, M, Martin, PGP, Busch, W, Barberon, M, Tilsner, J, Helariutta, Y, Russinova, E, Taly, A, Jaillais, Y & Bayer, EM 2025, 'Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants', Cell, vol. 188, no. 4, pp. 958-977. https://doi.org/10.1016/j.cell.2024.11.034

TY - JOUR

T1 - Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants

AU - Pérez-Sancho, Jessica

AU - Smokvarska, Marija

AU - Dubois, Gwennogan

AU - Glavier, Marie

AU - Sritharan, Sujith

AU - Moraes, Tatiana S.

AU - Moreau, Hortense

AU - Dietrich, Victor

AU - Platre, Matthieu P.

AU - Paterlini, Andrea

AU - Li, Ziqiang P.

AU - Fouillen, Laetitia

AU - Grison, Magali S.

AU - Cana-Quijada, Pepe

AU - Immel, Françoise

AU - Wattelet, Valerie

AU - Ducros, Mathieu

AU - Brocard, Lysiane

AU - Chambaud, Clément

AU - Luo, Yongming

AU - Ramakrishna, Priya

AU - Bayle, Vincent

AU - Lefebvre-Legendre, Linnka

AU - Claverol, Stéphane

AU - Zabrady, Matej

AU - Martin, Pascal G.P.

AU - Busch, Wolfgang

AU - Barberon, Marie

AU - Tilsner, Jens

AU - Helariutta, Yrjö

AU - Russinova, Eugenia

AU - Taly, Antoine

AU - Jaillais, Yvon

AU - Bayer, Emmanuelle M.

N1 - Funding: This work was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (projects 772103-BRIDGING to E.M.B. and 101001097-LIPIDEV to Y.J.), the National Agency for Research (grants ANR-18-CE13-0016 STAYING-TIGHT to E.M.B. and Y.J., ANR-2020-CE20-0002 3C TomFruit Growth to E.M.B., ANR-21-CE13-0016-01 DIVCON to A.T. and E.M.B., and ANR-18-CE13-0025-02 caLIPSO to Y.J.), the Human Frontier Science Program (project RGP0002/2020 to E.M.B.), the French Government in the framework of the IdEX Bordeaux University “Investments for the Future” program/GPR Bordeaux Plant Sciences (E.M.B.), the Swiss National Science Foundation (project 31003A_179159 to M.B.), Research Foundation-Flanders grant G002121N to E.R., the HORIZON-MSCA-2023-PF-01 project 101152141-BRACTION to Y.L., and Projet Emergents FlowValve University of Bordeaux to M.S.

PY - 2025/2/20

Y1 - 2025/2/20

N2 - Membrane contact sites (MCSs) are fundamental for intracellular communication, but their role in intercellular communication remains unexplored. We show that in plants, plasmodesmata communication bridges function as atypical endoplasmic reticulum (ER)-plasma membrane (PM) tubular MCSs, operating at cell-cell interfaces. Similar to other MCSs, ER-PM apposition is controlled by a protein-lipid tethering complex, but uniquely, this serves intercellular communication. Combining high-resolution microscopy, molecular dynamics, and pharmacological and genetic approaches, we show that cell-cell trafficking is modulated through the combined action of multiple C2 domains transmembrane domain proteins (MCTPs) 3, 4, and 6 ER-PM tethers and phosphatidylinositol-4-phosphate (PI4P) lipid. Graded PI4P amounts regulate MCTP docking to the PM, their plasmodesmata localization, and cell-cell permeability. SAC7, an ER-localized PI4P-phosphatase, regulates MCTP4 accumulation at plasmodesmata and modulates cell-cell trafficking capacity in a cell-type-specific manner. Our findings expand MCS functions in information transmission from intracellular to intercellular cellular activities.

AB - Membrane contact sites (MCSs) are fundamental for intracellular communication, but their role in intercellular communication remains unexplored. We show that in plants, plasmodesmata communication bridges function as atypical endoplasmic reticulum (ER)-plasma membrane (PM) tubular MCSs, operating at cell-cell interfaces. Similar to other MCSs, ER-PM apposition is controlled by a protein-lipid tethering complex, but uniquely, this serves intercellular communication. Combining high-resolution microscopy, molecular dynamics, and pharmacological and genetic approaches, we show that cell-cell trafficking is modulated through the combined action of multiple C2 domains transmembrane domain proteins (MCTPs) 3, 4, and 6 ER-PM tethers and phosphatidylinositol-4-phosphate (PI4P) lipid. Graded PI4P amounts regulate MCTP docking to the PM, their plasmodesmata localization, and cell-cell permeability. SAC7, an ER-localized PI4P-phosphatase, regulates MCTP4 accumulation at plasmodesmata and modulates cell-cell trafficking capacity in a cell-type-specific manner. Our findings expand MCS functions in information transmission from intracellular to intercellular cellular activities.

KW - Endoplasmic reticulum plasma membrane

KW - Intercellular communication

KW - MCTP

KW - Membrane contact sites

KW - Phosphoinositide

KW - Plant biology

KW - Plasmodesmata

U2 - 10.1016/j.cell.2024.11.034

DO - 10.1016/j.cell.2024.11.034

M3 - Article

AN - SCOPUS:85217978333

SN - 0092-8674

VL - 188

SP - 958

EP - 977

JO - Cell

JF - Cell

IS - 4

ER -

Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants

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Keywords

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