ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites

Renna, Luciana; Stefano, Giovanni; Puggioni, Maria Paola; Kim, Sang-Jin; Lavell, Anastasiya; Froehlich, John E.; Burkart, Graham; Mancuso, Stefano; Benning, Christoph; Brandizzi, Federica

doi:10.1038/s41467-024-50425-7

Title: ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites

Journal Article · 17 July 2024 · Nature Communications

DOI: https://doi.org/10.1038/s41467-024-50425-7 · OSTI ID:2403575

Renna, Luciana;

; Puggioni, Maria Paola;

; Lavell, Anastasiya; Froehlich, John E.; Burkart, Graham; Mancuso, Stefano;

;

Abstract The plant endoplasmic reticulum (ER) contacts heterotypic membranes at membrane contact sites (MCSs) through largely undefined mechanisms. For instance, despite the well-established and essential role of the plant ER-chloroplast interactions for lipid biosynthesis, and the reported existence of physical contacts between these organelles, almost nothing is known about the ER-chloroplast MCS identity. Here we show that the Arabidopsis ER membrane-associated VAP27 proteins and the lipid-binding protein ORP2A define a functional complex at the ER-chloroplast MCSs. Specifically, through in vivo and in vitro association assays, we found that VAP27 proteins interact with the outer envelope membrane (OEM) of chloroplasts, where they bind to ORP2A. Through lipidomic analyses, we established that VAP27 proteins and ORP2A directly interact with the chloroplast OEM monogalactosyldiacylglycerol (MGDG), and we demonstrated that the loss of the VAP27-ORP2A complex is accompanied by subtle changes in the acyl composition of MGDG and PG. We also found that ORP2A interacts with phytosterols and established that the loss of the VAP27-ORP2A complex alters sterol levels in chloroplasts. We propose that, by interacting directly with OEM lipids, the VAP27-ORP2A complex defines plant-unique MCSs that bridge ER and chloroplasts and are involved in chloroplast lipid homeostasis.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: NONE; FG02-91ER20021

OSTI ID:: 2403575

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Endoplasmic Reticulum–Plasma Membrane Contact Sites: Regulators, Mechanisms, and Physiological Functions Li, Chenlu; Qian, Tiantian; He, Ruyue Frontiers in Cell and Developmental Biology, Vol. 9 https://doi.org/10.3389/fcell.2021.627700	journal	February 2021
Functions of Oxysterol-Binding Proteins at Membrane Contact Sites and Their Control by Phosphoinositide Metabolism Nakatsu, Fubito; Kawasaki, Asami Frontiers in Cell and Developmental Biology, Vol. 9 https://doi.org/10.3389/fcell.2021.664788	journal	June 2021
VAP Proteins – From Organelle Tethers to Pathogenic Host Interactors and Their Role in Neuronal Disease Kors, Suzan; Costello, Joseph L.; Schrader, Michael Frontiers in Cell and Developmental Biology, Vol. 10 https://doi.org/10.3389/fcell.2022.895856	journal	June 2022
Manipulating Endoplasmic Reticulum-Plasma Membrane Tethering in Plants Through Fluorescent Protein Complementation Tao, Kai; Waletich, Justin R.; Arredondo, Felipe Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00635	journal	May 2019
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Unbiased proteomic and forward genetic screens reveal that mechanosensitive ion channel MSL10 functions at ER–plasma membrane contact sites in Arabidopsis thaliana Codjoe, Jennette M.; Richardson, Ryan A.; McLoughlin, Fionn eLife, Vol. 11 https://doi.org/10.7554/eLife.80501	journal	October 2022

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