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PreprintCited by 10Lipid metabolism and biosynthesisCellular transport and secretionLipid Membrane Structure and Behavior

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Concerted Transport and Phosphorylation of Diacylglycerol at ER-PM Contacts Sites Regulates Phospholipid Dynamics During Stress

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García-Hernández, Selene, Haslam, Richard, Moya-Cuevas, José, Catalá, Rafael, Michaelson, Louise, Amorim-Silva, Vitor, Marković, Vedrana, Salinas, Julio, Napier, Johnathan, Jaillais, Yvon, Ruiz-Lopez, Noemí, Botella, Miguel A.·2024·Proceedings of the National Academy of Sciences
DOI 10.1101/2024.01.16.575708PMC PMC12167946

Preprint — published as 10.1073/pnas.2421334122

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Abstract

A universal response of plants to environmental stresses is the activation of plasma membrane (PM) phospholipase C (PLC) that hydrolyzes phosphatidylinositol phosphate (PIP) to produce soluble inositol phosphate (IP) and diacylglycerol (DAG). DAG produced in this way can be either phosphorylated by PM diacylglycerol kinases (DGKs) to produce the second messenger phosphatidic acid (PA) or transferred to the endoplasmic reticulum (ER) by the Synaptotagmin 1 (SYT1) protein at ER-PM Contact Sites (CS). In Arabidopsis, the clearance of DAG at the PM (avoiding deleterious accumulation) by the transfer activity of SYT is essential to maintain PM stability after stress. In this study we identify that DGK1 and DGK2 form a module with SYT1 at ER-PM CS through interaction of their C1 and C2 domains respectively. Global transcriptomic and metabolomic analyses confirms that SYT1 and DGK1 / DGK2 are functionally related and lipidomic analysis supports the hypothesis that DGK1 and DGK2 function at the ER by phosphorylating DAG transferred by SYT1 from the PM. DGK1 and DGK2 show structural similarity to human DGKε, the DGK isoform that function at ER-PM CS in the phosphoinositide (PI) cycle. Our data indicate that components of the PI cycle are conserved between animals and plants and provide a novel mechanism leading to an increase in the efficiency of the PI cycle by channeling the transport and hydrolysis of DAG at the ER-PM CS.

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Metadata

Authors
García-Hernández, S., Haslam, R., Moya-Cuevas, J., Catalá, R., Michaelson, L., Amorim-Silva, V., Marković, V., Salinas, J., Napier, J., Jaillais, Y., Ruiz-Lopez, N., & Botella, M. A.
Affiliations
  • Rothamsted Research (GB)
  • Consejo Superior de Investigaciones Científicas (ES)
  • École Normale Supérieure de Lyon (FR)
Corresponding author
Botella, Miguel A.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
openRxiv
Published
2024-01-17
Volume
122
Issue
23
Pages
e2421334122-e2421334122
ISSN
0027-8424 (ISSN-L)
DOI
10.1101/2024.01.16.575708
PMC
PMC12167946
OpenAlex
W4410948241
Cited by
10
References
1
Citations by year
2026: 6 · 2025: 4
FWCI
3.21
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Rothamsted Repository (Rothamsted Repository) (acceptedVersion)
  • Rothamsted Repository (Rothamsted Repository) (acceptedVersion, other-oa)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion)
  • HAL (submittedVersion, cc-by-nc-nd)
  • Rothamsted Repository (Rothamsted Repository) (submittedVersion)
  • Repositorio Institucional de la Universidad de Málaga (University of Málaga) (submittedVersion, other-oa)
Funders
  • European Molecular Biology Organization (466-2022)
  • Universidad de Málaga
  • UK Research and Innovation (BB/X010988/1)
  • Consejería de Economía, Conocimiento, Empresas y Universidad, Junta de Andalucía (PAIDI 2020-PY20_00084)
  • European Commission (2014‐2020, 10.13039/501100011033, 13039/501100011033, 501100011033, HORIZON2020, 101001097, /AEI/10.13039/501100011033)
  • Ministerio de Economía y Competitividad (PID2019, 10.13039/501100011033, PID2020, 13039/501100011033, AEI/ 10.13039/501100011033)
  • Ministerio de Ciencia e Innovación (PID2023-147983OB-I00, PID2019-106987RB-I00, PID2021-127649OB-I00, PRE2018-085284, PID2020-114419RB-I00/AEI/10.13039/501100011033)
  • Junta de Andalucía (10.13039/501100011033, PAIDI 2020, 2014-2020)
  • Consejería de Conocimiento, Investigación y Universidad, Junta de Andalucía (PAIDI2020-P20-00222-R, UMA20- FEDERJA-007)
  • Biotechnology and Biological Sciences Research Council (BB/X010988/1, BBS/E/RH/230002B, 10.13039/501100011033)
  • Agencia Estatal de Investigación (AEI//10.13039/501100011033/, 501100011033, 10.13039/501100011033, 13039, .13039/501100011033, 10.13039, AEI/10, I00/AEI/10.13039/501100011033, PID2019)
  • HORIZON EUROPE European Research Council (101001097)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Keywords
diacylglycerol, diacylglycerol kinase, ER-PM contact sites, endoplasmic reticulum, plasma membrane, phospholipase C, phosphoinositide hydrolysis, lipid transport, membrane remodeling, plant stress response, lipid metabolism
MeSH terms
Biological Transport, Cell Membrane, Diglycerides, Endoplasmic Reticulum, Phospholipids, Phosphorylation, Stress, Physiological, Arabidopsis, Diacylglycerol Kinase, Arabidopsis Proteins, Synaptotagmin I

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