Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum

Abstract

The unfolded protein response (UPR) is an ancient signaling pathway designed to protect cells from the accumulation of unfolded and misfolded proteins in the endoplasmic reticulum (ER). Because misregulation of the UPR is potentially lethal, a stringent surveillance signaling system must be in place to modulate the UPR. The major signaling arms of the plant UPR have been discovered and rely on the transcriptional activity of the transcription factors bZIP60 and bZIP28 and on the kinase and ribonuclease activity of IRE1, which splices mRNA to activate bZIP60. Both bZIP28 and bZIP60 modulate UPR gene expression to overcome ER stress. In this study, we demonstrate at a genetic level that the transcriptional role of bZIP28 and bZIP60 in ER-stress responses is antagonized by nonexpressor of PR1 genes 1 (NPR1), a critical redox-regulated master regulator of salicylic acid (SA)-dependent responses to pathogens, independently of its role in SA defense. We also establish that the function of NPR1 in the UPR is concomitant with ER stress-induced reduction of the cytosol and translocation of NPR1 to the nucleus where it interacts with bZIP28 and bZIP60. Our results support a cellular role for NPR1 as well as a model for plant UPR regulation whereby SA-independent ER stress-induced redox activation of NPR1 suppresses the transcriptional role of bZIP28 and bZIP60 in the UPR.

Systemic signaling contributes to the unfolded protein response of the plant endoplasmic reticulum

“…The role of these inducers in long-distance ER stress signaling is yet to be evaluated and it is conceivable that long-distance ER stress signaling may overlay a bZIP60-mediated signaling with the action of other stress transducers. Nonetheless, it has been shown in seedlings that ER stress responses are independent from endogenous SA and that Tm does not induce accumulation of SA 52 . Therefore, long-distance ER stress signaling is likely independent from SA.…”

A Novel Protein Elicitor PeBL2, from Brevibacillus laterosporus A60, Induces Systemic Resistance against Botrytis cinerea in Tobacco Plant

“…Signal transduction mechanisms of ISR remain poorly understood. It has been confirmed that salicylic acid pathway (SA), ethylene pathway (ET) and the jasmonic acid (JA) are different regulatory pathways, and act as core candidates in the signaling system, as well as in the defense response ( Lai et al, 2018 ; Pieterse and van Loon, 1999 ; Zhang et al, 2018a ). SA is considered to be the most prominent signaling molecule having a key role in system resistance as well as local defense reactions ( Glazebrook, 2001 ).…”

Cysteine and Methionine Biosynthetic Enzymes Have Distinct Effects on Seed Nutritional Quality and on Molecular Phenotypes Associated With Accumulation of a Methionine-Rich Seed Storage Protein in Rice

“…Furthermore, some level of oxidative stress due to H 2 O 2 production is intrinsic to disulfide bond formation in the ER (Harding et al, 2003). An overloaded ER that is not able to sufficiently correct and resolve misfolded proteins can result in H 2 O 2 production significant enough to alter the glutathione redox state (Ozgur et al, 2014;Dietz et al, 2016) and to influence the cytosolic redox potential (Lai et al, 2018). Therefore, in the context of an overloaded ER protein folding machinery, it might be adaptive to specifically downregulate expression of SSPs with very high S-AA density, such as S-rich 10kDa prolamin (Hagan et al, 2003), so that cysteine could then be repurposed for GSH synthesis.…”