Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress

Ruiz-Lopez N, Pérez-Sancho J, Esteban Del Valle A, Haslam R, Vanneste S, Catalá R, Perea-Resa C, Van Damme D, García-Hernández S, Albert A, Vallarino J, Lin J, Friml J, Macho A, Salinas J, Rosado A, Napier J, Amorim-Silva V, Botella M. 2021. Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. Plant Cell.

Download
OA 2021_PlantCell_Ruiz-Lopez.pdf 2.97 MB

Journal Article | Epub ahead of print | English
Author
Ruiz-Lopez, N; Pérez-Sancho, J; Esteban Del Valle, A; Haslam, RP; Vanneste, S; Catalá, R; Perea-Resa, C; Van Damme, D; García-Hernández, S; Albert, A; Vallarino, J; Lin, J
All
Abstract
Endoplasmic reticulum–plasma membrane contact sites (ER–PM CS) play fundamental roles in all eukaryotic cells. Arabidopsis thaliana mutants lacking the ER–PM protein tether synaptotagmin1 (SYT1) exhibit decreased PM integrity under multiple abiotic stresses, such as freezing, high salt, osmotic stress, and mechanical damage. Here, we show that, together with SYT1, the stress-induced SYT3 is an ER–PM tether that also functions in maintaining PM integrity. The ER–PM CS localization of SYT1 and SYT3 is dependent on PM phosphatidylinositol-4-phosphate and is regulated by abiotic stress. Lipidomic analysis revealed that cold stress increased the accumulation of diacylglycerol at the PM in a syt1/3 double mutant relative to wild-type while the levels of most glycerolipid species remain unchanged. In addition, the SYT1-green fluorescent protein fusion preferentially binds diacylglycerol in vivo with little affinity for polar glycerolipids. Our work uncovers a SYT-dependent mechanism of stress adaptation counteracting the detrimental accumulation of diacylglycerol at the PM produced during episodes of abiotic stress.
Publishing Year
Date Published
2021-01-01
Journal Title
Plant Cell
Acknowledgement
We would also like to thank Lothar Willmitzer for the lipidomic analysis at the Max Planck Institute of Molecular Plant Physiology (Potsdam, Germany). We thank Manuela Vega from SCI for her technical assistance in image analysis. We thank John R. Pearson and the Bionand Nanoimaging Unit, F. David Navas Fernández and the SCAI Imaging Facility and The Plant Cell Biology facility at the Shanghai Center for Plant Stress Biology for assistance with confocal microscopy. The FaFAH1 clone was a gift from Iraida Amaya Saavedra (IFAPA-Centro de Churriana, Málaga, Spain). The AHA3 antibody against the H+-ATPase was a gift from Ramón Serrano Salom (Instituto de Biología Molecular y Celular de Plantas, Valencia, Spain). The MAP-mTU2-SAC1 construct was provided by Yvon Jaillais (Laboratoire Reproduction et Développement des Plantes, Univ Lyon, France). The pGWB5 from the pGWB vector series, was provided by Tsuyoshi Nakagawa (Department of Molecular and Functional Genomics, Shimane University). We thank Plan Propio from the University of Málaga for financial support. Funding
IST-REx-ID

Cite this

Ruiz-Lopez N, Pérez-Sancho J, Esteban Del Valle A, et al. Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. Plant Cell. 2021. doi:10.1093/plcell/koab122
Ruiz-Lopez, N., Pérez-Sancho, J., Esteban Del Valle, A., Haslam, R., Vanneste, S., Catalá, R., … Botella, M. (2021). Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. Plant Cell. American Society of Plant Biologists. https://doi.org/10.1093/plcell/koab122
Ruiz-Lopez, N, J Pérez-Sancho, A Esteban Del Valle, RP Haslam, S Vanneste, R Catalá, C Perea-Resa, et al. “Synaptotagmins at the Endoplasmic Reticulum-Plasma Membrane Contact Sites Maintain Diacylglycerol Homeostasis during Abiotic Stress.” Plant Cell. American Society of Plant Biologists, 2021. https://doi.org/10.1093/plcell/koab122.
N. Ruiz-Lopez et al., “Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress,” Plant Cell. American Society of Plant Biologists, 2021.
Ruiz-Lopez N, Pérez-Sancho J, Esteban Del Valle A, Haslam R, Vanneste S, Catalá R, Perea-Resa C, Van Damme D, García-Hernández S, Albert A, Vallarino J, Lin J, Friml J, Macho A, Salinas J, Rosado A, Napier J, Amorim-Silva V, Botella M. 2021. Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. Plant Cell.
Ruiz-Lopez, N., et al. “Synaptotagmins at the Endoplasmic Reticulum-Plasma Membrane Contact Sites Maintain Diacylglycerol Homeostasis during Abiotic Stress.” Plant Cell, American Society of Plant Biologists, 2021, doi:10.1093/plcell/koab122.
All files available under the following license(s):
Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0):
Main File(s)
Access Level
OA Open Access
Date Uploaded
2021-06-09
MD5 Checksum
524f85f0e626966ac721f036ffa6fc7a


Export

Marked Publications

Open Data IST Research Explorer

Sources

PMID: 33944955
PubMed | Europe PMC

Search this title in

Google Scholar