Plasmodesmata act as unconventional membrane contact sites regulating intercellular molecular exchange in plants
Cell. 2025-02-01; 188(4): 958-977.e23
DOI: 10.1016/j.cell.2024.11.034
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https://www.bordeaux-neurocampus.fr/12571
Pérez-Sancho J(1), Smokvarska M(1), Dubois G(2), Glavier M(1), Sritharan S(3),
Moraes TS(1), Moreau H(1), Dietrich V(1), Platre MP(4), Paterlini A(5), Li
ZP(1), Fouillen L(1), Grison MS(1), Cana-Quijada P(1), Immel F(1), Wattelet
V(1), Ducros M(6), Brocard L(6), Chambaud C(7), Luo Y(8), Ramakrishna P(9),
Bayle V(2), Lefebvre-Legendre L(9), Claverol S(10), Zabrady M(11), Martin
PGP(12), Busch W(4), Barberon M(9), Tilsner J(11), Helariutta Y(13), Russinova
E(8), Taly A(3), Jaillais Y(14), Bayer EM(15).
Author information:
(1)Laboratoire de Biogenèse Membranaire, UMR5200, CNRS, Université de Bordeaux,
Villenave-d’Ornon, France.
(2)Laboratoire Reproduction et Développement des Plantes, ENS de Lyon, CNRS,
INRA, 69342 Lyon, France.
(3)Laboratoire de Biochimie Théorique, UPR9080, CNRS, Université Paris Cité,
Paris, France.
(4)Salk Institute for Biological Studies, Plant Molecular and Cellular Biology
Laboratory, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
(5)Laboratoire de Biogenèse Membranaire, UMR5200, CNRS, Université de Bordeaux,
Villenave-d’Ornon, France; The Sainsbury Laboratory, University of Cambridge,
Cambridge, UK.
(6)Bordeaux Imaging Center, Plant Imaging Platform, UAR3420,
CNRS-INSERM-University of Bordeaux-INRAE, Bordeaux, France.
(7)Laboratoire de Biogenèse Membranaire, UMR5200, CNRS, Université de Bordeaux,
Villenave-d’Ornon, France; Bordeaux Imaging Center, Plant Imaging Platform,
UAR3420, CNRS-INSERM-University of Bordeaux-INRAE, Bordeaux, France.
(8)Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052
Ghent, Belgium; Center for Plant Systems Biology, VIB, 9052 Ghent, Belgium.
(9)Department of Plant Sciences, University of Geneva, 1211 Geneva, Switzerland.
(10)University of Bordeaux, Bordeaux Proteome, Bordeaux, France.
(11)Biomedical Sciences Research Complex, University of St Andrews, Fife KY16
9ST, UK; Cell and Molecular Sciences, The James Hutton Institute, Dundee DD2
5DA, UK.
(12)Université de Bordeaux, INRAE, UMR1332 Biologie du Fruit et Pathologie,
33882 Villenave d’Ornon, France.
(13)The Sainsbury Laboratory, University of Cambridge, Cambridge, UK; Institute
of Biotechnology, HiLIFE/Organismal and Evolutionary Biology Research Programme,
Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre,
University of Helsinki, Helsinki, Finland.
(14)Laboratoire Reproduction et Développement des Plantes, ENS de Lyon, CNRS,
INRA, 69342 Lyon, France. Electronic address: .
(15)Laboratoire de Biogenèse Membranaire, UMR5200, CNRS, Université de Bordeaux,
Villenave-d’Ornon, France. Electronic address: .
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.
Copyright © 2024 Elsevier Inc. All rights reserved.
DOI: 10.1016/j.cell.2024.11.034
PMID: 39983675 [Indexed for MEDLINE]
Conflict of interest statement: Declaration of interests The authors declare no
competing interests.