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

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 plasma membrane (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. Additionally, the SYT1-green fluorescent protein (GFP) 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.

The Absence of the AtSYT1 Function Elevates the Adverse Effect of Salt Stress on Photosynthesis in Arabidopsis

“…Additionally, the role of AtSYT1 in delivering the membranes through exocytosis to the plasma membrane in speedily expanded guard cells or membrane removing from the plasma membrane through endocytosis during guard cells shrinkage should be considered. Finally, the participation of AtSYT1 and AtSYT3 in removing toxic DAG from the plasma membrane under salt stress, as suggested recently by Ruiz-Lopez et al [21], could play an important role in very active guard cells.…”

“…However, in the mutant plants, responses to sudden salt stress were much stronger in almost all parameters than in WT plants. Recent studies suggest that some AtSYTs may have a redundant function [20,21]. Perhaps less abundantly expressed AtSYT3 or AtSYT5 may provide a substitute AtSYT1 function when plants grow in a suitable environment.…”

“…Salt stress causes an increase in AtSYT1 abundance at ER-PM CS and their expansion [10]. AtSYT5 [20] and AtSYT3 [21] homologs are also present at ER-PM CS and these three proteins are likely functionally redundant there. The current view is that the N-terminal transmembrane domain of AtSYT1 and other AtSYTs anchor protein to the ER, C2 domains ensure Ca 2+ dependent ER-PM tethering and an SMP domain transfers lipids between the PM and the ER.…”

“…The current view is that the N-terminal transmembrane domain of AtSYT1 and other AtSYTs anchor protein to the ER, C2 domains ensure Ca 2+ dependent ER-PM tethering and an SMP domain transfers lipids between the PM and the ER. Abiotic stress such as salinity causes PM instability by accumulating diacylglycerol (DAG) and SYTs as tethers between the ER, and the PM could help maintain PM homeostasis by transporting DAG to the ER [10,21].…”

Selective Advantages of Synapses in Evolution

“…ER physically and chemically interacts with cellular organelles using vesicular and non-vesicular lipid transport (Holthuis and Menon, 2014) at specialized membrane contact sites (MCS, Levine, 2004;Phillips and Voeltz, 2016;Ruiz-Lopez et al, 2021). MCS support complex interactions with mitochondria (Schlattner et al, 2014;Kannan et al, 2017;Wong et al, 2019) via tethered regions of ER known as mitochondria-associated membranes or MAM (Allen et al, 1989;Helle et al, 2013).…”