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

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 <i>dgk1dgk2</i> 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.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2025-06-02
DOI
https://doi.org/10.1073/pnas.2421334122
Citations
3
Primary Topic
Mitochondrial Function and Pathology
Type
article
Field-Weighted Citation Impact
2.42

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article

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

Vítor Amorim‐Silva, Miguel A. Botella, Yvon Jaillais, Richard P. Haslam et al.
3 citations
Proceedings of the National Academy of Sciences
Mitochondrial Function and Pathology
2.42
article

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

Vítor Amorim‐Silva, Miguel A. Botella, Yvon Jaillais, Richard P. Haslam, Selene García‐Hernández, Louise V. Michaelson, Noemí Ruiz‐López, Julio Salinas, Jorge Morello‐López, Johnathan A. Napier, José Moya‐Cuevas, Vedrana Marković, Rafael Catalá, Jessica Pérez‐Sancho
article en
3 citations

Abstract

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 <i>dgk1dgk2</i> 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.

Proceedings of the National Academy of SciencesVol. 122(23)
École Normale Supérieure de Lyon (FR), Centre National de la Recherche Scientifique (FR), Consejo Superior de Investigaciones Científicas (ES), Rothamsted Research (GB), Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora" (ES), Laboratoire Reproduction et Développement des Plantes (FR), Centro de Investigaciones Biológicas Margarita Salas (ES), Universidad de Málaga (ES)
European Molecular Biology Organization, Universidad de Málaga, Consejería de Economía, Conocimiento, Empresas y Universidad, Junta de Andalucía, European Commission, Ministerio de Ciencia e Innovación, Junta de Andalucía, Consejería de Conocimiento, Investigación y Universidad, Junta de Andalucía, Biotechnology and Biological Sciences Research Council, HORIZON EUROPE European Research Council
Life in Land
Openalex Percentile: Top 11%
Mitochondrial Function and Pathology
2.42
DOIOpen Access PDFOpenAlex
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