The Multifaceted Roles of Plant Hormone Salicylic Acid in Endoplasmic Reticulum Stress and Unfolded Protein Response

Abstract

Different abiotic and biotic stresses lead to the accumulation of unfolded and misfolded proteins in the endoplasmic reticulum (ER), resulting in ER stress. In response to ER stress, cells activate various cytoprotective responses, enhancing chaperon synthesis, protein folding capacity, and degradation of misfolded proteins. These responses of plants are called the unfolded protein response (UPR). ER stress signaling and UPR can be regulated by salicylic acid (SA), but the mode of its action is not known in full detail. In this review, the current knowledge on the multifaceted role of SA in ER stress and UPR is summarized in model plants and crops to gain a better understanding of SA-regulated processes at the physiological, biochemical, and molecular levels.

Keywords: binding protein; cell death; pathogenesis-related genes; systemic acquired resistance; tunicamycin.

Figure 1

A schematic illustration of unfolded protein response (UPR) and the effects of salicylic acid (SA) under stress condition in plants. The accumulation of unfolded proteins in the ER leads to the conformational changes and activated RNAse function of IRE1 (inositol-requiring enzyme 1), which mediates an unconventional splicing bZIP60 transcription factor mRNA. Spliced bZIP60 mRNA is translated to an active transcription factor and translocated to the nucleus and upregulates UPR genes containing unfolded protein response element (UPRE) and ER stress element (ERSE) in their promoters. bZIP28 and bZIP17 are activated by Golgi proteases (S2P and S1P). Then, the cleaved forms of bZIPs translocate into the nucleus and binds to ERSE to activate the UPR gene expression. NAC062 and NAC089 also undergo proteolytic cleavage and translocate to the nucleus to promote the transcription of UPR or cell death genes. SA has multifaceted roles in the regulation of defense or cell death processes in plants. SA is synthesized by phenylalanine ammonia-lyase (PAL) from L-phenylalanine (Phe) or in the isochorismate (IC) pathway by isochorismate synthase (ICS). Then through the activity of isochorismate pyruvate lyase (IPL) in the chloroplast, it is translocated to the cytosol by EDS5. SA induces high production of reactive oxygen (ROS) and nitrogen species (RNS) in chloroplast and mitochondria and activates NADPH oxidase, respectively. Simultaneously, SA activates various antioxidant enzymes, such as superoxide dismutases (SOD). SA induces cytochrome c (Cyt c) release from the mitochondrial inner membrane by the permeability transition pore (PTP), decreases the transcript levels of Bax inhibitor-1 (BI-1), and increases the expression of vacuolar processing enzymes (VPEs) inducing cell death. Moreover, SA has a significant effect on polyamine levels (e.g. that of spermine), influencing ER stress in plants. SA changes the redox homeostasis and induces the reduction and monomerization of NPR1, which is translocated to the nucleus where it binds to specific TGA transcriptions factors, inducing the expression of SA-induced defensive response genes (PRs). SA can be inactivated and stored as SA O-β-glucoside (SAG) in the vacuole. Detailed description and references are in the text.