Sequential coupling of synaptotagmins and diacylglycerol kinases synergistically regulate diacylglycerol metabolism at ER-PM contact sites
A universal response by plants upon environmental challenge is the activation of phospholipase C (PLC) at the plasma membrane (PM) that hydrolyzes phosphatidylinositol phosphate to produce soluble inositol phosphate (PIP) and diacylglycerol (DAG). Part of this DAG is either phosphorylated by PM diacylglycerol kinases (DGKs) to produce the second messenger phosphatidic acid (PA) or transferred to the endoplasmic reticulum (ER) by Synaptotagmin 1 protein at ER-PM contact sites in Arabidopsis. This clearance of DAG at the PM by the transfer activity of SYT is essential to maintain PM stability after stress by avoiding accumulation of DAG. Here we show that C2 domains of SYT1 interact with the C1 domains of DGK1 and DGK2 at ER-PM CS. Global transcriptomic analysis confirm that SYT1 and DGK1 and DGK2 are functionally related and lipidomic analysis support that DGK1 and DGK2 function at the ER by phosphorylating DAG transferred by SYT1. DGK1 and DGK2 show structural similarity with human DGKE, the DGK isoform that function at ER-PM CS in the phosphoinositide cycle. Our data indicate that some components of the PI cycle are conserved between animals and plants. We also provide a novel mechanism by which the PI cycle increase their efficiency after stress by channeling the transport and hydrolysis of DAG at the ER by the module formed by SYT1 and DGK1 and DGK2.