Concerted transport and phosphorylation of diacylglycerol at ER-PM contact sites regulate phospholipid dynamics during stress

• 成果类型: Article
• 署名作者: Garcia-Hernandez, Selene; Morello-Lopez, Jorge; Haslam, Richard; Amorim-Silva, Vitor; Moya-Cuevas, Jose; Catala, Rafael; Michaelson, Louise; Perez-Sancho, Jessica; Markovic, Vedrana; Salinas, Julio; Napier, Johnathan; Jaillais, Yvon; Ruiz-Lopez, Noemi; Botella, Miguel A.
• 署名单位: Consejo Superior de Investigaciones Cientificas (CSIC); Universidad de Malaga; UK Research & Innovation (UKRI); Biotechnology and Biological Sciences Research Council (BBSRC); Rothamsted Research; Consejo Superior de Investigaciones Cientificas (CSIC); CSIC - Centro de Investigaciones Biologicas (CIB); Centre National de la Recherche Scientifique (CNRS); Ecole Normale Superieure de Lyon (ENS de LYON); Universite Claude Bernard Lyon 1; INRAE
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-10340
• DOI: 10.1073/pnas.2421334122
• 发表日期: 2025-06-10
• 关键词: plasma-membrane; endoplasmic-reticulum; arabidopsis-thaliana; synaptotagmin 1; proteins; kinase; binding; phosphatidylinositol; plasmodesmata; metabolism

摘要

A universal response of plants to environmental stresses is the activation of plasma membrane (PM) phospholipase C, which hydrolyzes phosphoinositides to produce soluble inositol phosphate and diacylglycerol (DAG). Because of their conical shape, DAG amounts have to be tightly regulated or they can destabilize membranes. We previously showed that upon stress, Synaptotagmin1 (SYT1) transports DAG from the PM to the endoplasmic reticulum (ER) at ER-PM Contact Sites (CS). Here, we addressed the fate of the incoming DAG in the ER. We show that diacylglycerol kinases (DGKs) DGK1 and DGK2 form a module with SYT1 functionally coupling DAG transport and phosphorylation at ER-PM CS. Although SYT1 and DGK1/DGK2 do not show exclusive ER-PM CS localization, their interaction occurs specifically at ER-PM CS and the removal of ER-PM CS abolishes the interaction. Lipidomic analysis of a dgk-1dgk2 double mutant supports that DGK1 and DGK2 phosphorylate DAG at the ER and transcriptomic and phenotypic analyses indicate that SYT1 and DGK1/DGK2 are functionally related. Taken together, our results highlight a mechanism at ER-PM CS that coordinates the transfer of DAG from the PM to the ER by SYT1 upon stress and the concomitant phosphorylation of DAG by DGK1 and DGK2 at the ER. These findings underscore the critical role of spatial coordination in lipid metabolism during stress-induced membrane remodeling.