Cell Death Signaling From Endoplasmic Reticulum Stress: Plant-Specific and Conserved Features

Abstract

The endoplasmic reticulum (ER) stress response is triggered by any condition that disrupts protein folding and promotes the accumulation of unfolded proteins in the lumen of the organelle. In eukaryotic cells, the evolutionarily conserved unfolded protein response is activated to clear unfolded proteins and restore ER homeostasis. The recovery from ER stress is accomplished by decreasing protein translation and loading into the organelle, increasing the ER protein processing capacity and ER-associated protein degradation activity. However, if the ER stress persists and cannot be reversed, the chronically prolonged stress leads to cellular dysfunction that activates cell death signaling as an ultimate attempt to survive. Accumulating evidence implicates ER stress-induced cell death signaling pathways as significant contributors for stress adaptation in plants, making modulators of ER stress pathways potentially attractive targets for stress tolerance engineering. Here, we summarize recent advances in understanding plant-specific molecular mechanisms that elicit cell death signaling from ER stress. We also highlight the conserved features of ER stress-induced cell death signaling in plants shared by eukaryotic cells.

Tobacco necrosis virus A overcomes local cell death response in Nicotiana tabacum

“…The unrestricted activity of erUPR, a consequence of viral replication and misfolded protein accumulation, may lead to HR‐associated cell death (Simoni et al, 2022; Verchot & Pajerowska‐Mukhtar, 2021). Two major UPR signalling pathways are activated by viral infection; one is mediated by the interaction of inositol‐requiring enzyme‐1 (IRE1), which mediates unconventional splicing of bZIP60 transcription factor mRNA, and the other by bZIP17 and bZIP28 (Gayral et al, 2020; Herath et al, 2020; Li et al, 2022; Zhang et al, 2015).…”

“…The communication between chloroplast, mitochondria and ER, the main ROS‐producing organelles, triggers specific signalling pathways that may promote cell survival or death. Current evidence shows important roles for ROS in activating and modulating erUPR, but their connection to key UPR players remains unclear (Cao et al, 2022; Depaepe et al, 2021; Simoni et al, 2022; Verchot & Pajerowska‐Mukhtar, 2021). In the present study, TNVA‐associated cell death on the inoculated leaves induced a number of UPR‐related genes including bZIP60s , bZIP28 and CRT , indicating that the two main branches to restore ER‐homoeostasis are activated by TNVA infection.…”

“…Accumulating evidence shows that disease‐associated cell deaths against diverse phytopathogens share similar mechanisms to R‐mediated HR and are referred to as HR‐associated diseases or HR‐like (Arena et al, 2020; El Oirdi & Bouarab, 2007; Govrin & Levine, 2000; Hull, 2013; Komatsu et al, 2010). Recently, it has been reported that the HR‐associated disease response triggered by virus or viral proteins may be a consequence of an excessive activity of the unfolded protein response (UPR) in the endoplasmic reticulum (ER), also called ER stress response or erUPR (Depaepe et al, 2021; Manghwar & Li, 2022; Park & Park, 2019; Simoni et al, 2022). Although the UPR activation is a cytoprotective response to restrict pathogen infection, the virus may manipulate the ER stress to set up its own infection (Simoni et al, 2022; Verchot & Pajerowska‐Mukhtar, 2021).…”

“…Recently, it has been reported that the HR‐associated disease response triggered by virus or viral proteins may be a consequence of an excessive activity of the unfolded protein response (UPR) in the endoplasmic reticulum (ER), also called ER stress response or erUPR (Depaepe et al, 2021; Manghwar & Li, 2022; Park & Park, 2019; Simoni et al, 2022). Although the UPR activation is a cytoprotective response to restrict pathogen infection, the virus may manipulate the ER stress to set up its own infection (Simoni et al, 2022; Verchot & Pajerowska‐Mukhtar, 2021). The HR‐associated disease response and extreme resistance without HR reinforce the idea that plant resistance and HR are uncoupled processes (Balint‐Kurti, 2019; Bendahmane et al, 1999; Cole et al, 2001; Jovel et al, 2007; Komatsu et al, 2010).…”

Tight genetic linkage of genes causing hybrid necrosis and pollinator isolation between young species

“…The high expression of ER stress marker genes in the same background indicates ER stress. Many key pathogenesis-related proteins rely on ER and ER quality control for proper folding and secretion [52][53][54] . We propose that the high and chronic demand for the processing of ChiA1 in the ER exceeds the ER quality control working capacity and causes prolonged ER stress and cell death [55][56][57] .…”