Exogenous Salicylic Acid Activates Two Signaling Arms of the Unfolded Protein Response in Arabidopsis

Abstract

The unfolded protein response (UPR) is a highly conserved cellular response that prevents abnormal maturation of proteins in the endoplasmic reticulum (ER). The expression of genes encoding ER chaperones is induced during the UPR. In the Arabidopsis UPR, two membrane-bound transcription factors, bZIP60 and bZIP28, activate the expression of those genes. bZIP60 is regulated by unconventional cytoplasmic splicing catalyzed by inositol requiring enzyme 1 (IRE1), which is located in the ER membrane. bZIP28 is regulated by intramembrane proteolysis. Pathogen infection and salicylic acid (SA) have been reported to induce the expression of some UPR genes. Here, we show that UPR genes including BiP3, a marker gene of the Arabidopsis UPR, are induced by exogenous SA treatment and activation of bZIP60 in an IRE1-dependent manner. The induction of gene expression and activation of bZIP60 were independent of NPR1 and HsfB1 under these experimental conditions. We generated antibodies to detect the proteolytic products of bZIP28 after SA treatment. An assay using these antibodies showed that SA activated bZIP28, as well as activating bZIP60 through IRE1. Together, these results show that exogenous SA treatment activates two signaling arms of the Arabidopsis UPR. We propose a possible mechanism of activation of the UPR machinery by SA.

Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum

“…Next, we examined whether the activation of the UPR in ceh1 is due to: (i) the specific signaling activity of MEcPP; (ii) the high levels of SA in the ceh1 mutant; (iii) or a general response to perturbations of the MEP pathway. Recent reports of SA involvement in the UPR (16,17), led us to examine not only ceh1 2. UPR transcripts are induced in a MEcPP-specific manner.…”

Quantitative Proteomic Profiling of Early and Late Responses to Salicylic Acid in Cucumber Leaves

“…SA down-regulated the proteins that are involved in protein processing but up-regulated the proteins that are related to proteolysis (S1 Text, “Proteolysis, protein folding and modification”). Pathogen infection or exogenous SA treatment can induce the expression of genes that are involved in intracellular proteolysis [60]. Additionally, SA-induced ROS might function as the second signal for the proteolysis [61].…”

Unfolded protein response in plants: one master, many questions

“…Understanding the mechanisms of the plant UPR is important to define conserved and unique strategies for ER stress responses, and it offers exciting perspectives to improve plant productivity. While we are beginning to understand how the UPR intersects with hormone-regulated growth [37••,38], defense [5,24,39], and resistance to hostile environments [4,40], further insights into the temporal and spatial complexity of the UPR regulation will support biotechnological applications. For example, overexpression of rice IRE1 may lead to suppression of endogenous IRE1 expression, which may compromise endogenous defense [41]; on the other hand, overexpression of BiP proteins renders them more resistant to stress [42,43].…”

“…This is further reinforced by the observations that while AtIRE1b has a preponderant role in AtbZIP60 splicing upon tunicamycin-induced ER-stress, AtIRE1a seems preferentially required for AtbZIP60 splicing upon pathogen and salicylic acid (SA) infection [5]. Although functional diversification of the SA response has been recently questioned [24], the evidence that AtIRE1b but not AtIRE1a is required for AtbZIP60 splicing [4] supports that AtIRE1 proteins may have undergone functional specialization. These observations raise the question how the multiple IRE1-functions may be executed in species with one IRE1 isoform.…”