skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Recovery from temporary endoplasmic reticulum stress in plants relies on the tissue-specific and largely independent roles of bZIP28 and bZIP60, as well as an antagonizing function of BAX-Inhibitor 1 upon the pro-adaptive signaling mediated by bZIP28

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.13768· OSTI ID:1607736

The unfolded protein response (UPR) is an ancient signaling pathway that commits to life-or-death outcomes in response to proteotoxic stress in the endoplasmic reticulum (ER). In plants, the membrane-tethered transcription factor bZIP28 and the ribonuclease-kinase IRE1 along with its splicing target, bZIP60, govern the two cytoprotective UPR signaling pathways known to date. The conserved ER membrane-associated BAX inhibitor 1 (BI1) modulates ER stress-induced programmed cell death through yet-unknown mechanisms. Despite the significance of the UPR for cell homeostasis, in plants the regulatory circuitry underlying ER stress resolution is still largely unmapped. To gain insights into the coordination of plant UPR strategies, we, in this study, analyzed the functional relationship of the UPR modulators through the analysis of single and higher order mutants of IRE1, bZIP60, bZIP28 and BI1 in experimental conditions causing either temporary or chronic ER stress. We established a functional duality of bZIP28 and bZIP60, as they exert partially independent tissue-specific roles in recovery from ER stress, but redundantly actuate survival strategies in chronic ER stress. We also discovered that BI1 attenuates the pro-survival function of bZIP28 in ER stress resolution and, differently to animal cells, it does not temper the ribonuclease activity of inositol-requiring enzyme 1 (IRE1) under temporary ER stress. Together these findings reveal a functional independence of bZIP28 and bZIP60 in plant UPR, and identify an antagonizing role of BI1 in the pro-adaptive signaling mediated by bZIP28, bringing to light the distinctive complexity of the unfolded protein response (UPR) in plants.

Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1607736
Alternate ID(s):
OSTI ID: 1411091
Journal Information:
The Plant Journal, Vol. 93, Issue 1; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 46 works
Citation information provided by
Web of Science

References (42)

Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis journal October 2013
BAX Inhibitor-1 Is a Negative Regulator of the ER Stress Sensor IRE1α journal March 2009
Bax inhibitor 1 regulates ER-stress-induced ROS accumulation through the regulation of cytochrome P450 2E1 journal April 2009
Bax Inhibitor-1, a Mammalian Apoptosis Suppressor Identified by Functional Screening in Yeast journal February 1998
The C Terminus of Bax Inhibitor-1 Forms a Ca 2+ -permeable Channel Pore journal November 2011
XBP1 mRNA Is Induced by ATF6 and Spliced by IRE1 in Response to ER Stress to Produce a Highly Active Transcription Factor journal December 2001
BI-1 Regulates an Apoptosis Pathway Linked to Endoplasmic Reticulum Stress journal August 2004
AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis journal October 2011
BAX inhibitor-1 regulates autophagy by controlling the IRE1α branch of the unfolded protein response: Bax inhibitor-1 controls autophagy journal September 2011
Unfolded protein response in plants: one master, many questions journal October 2015
Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response journal November 2008
A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana journal October 2008
Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor journal July 2011
BAX Inhibitor-1 Modulates Endoplasmic Reticulum Stress-mediated Programmed Cell Death in Arabidopsis journal November 2007
Integrating stress signals at the endoplasmic reticulum: The BCL-2 protein family rheostat journal April 2011
CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses journal February 2017
IRE1/bZIP60-Mediated Unfolded Protein Response Plays Distinct Roles in Plant Immunity and Abiotic Stress Responses journal February 2012
Dissection of Arabidopsis Bax Inhibitor-1 Suppressing Bax–, Hydrogen Peroxide–, and Salicylic Acid–Induced Cell Death journal December 2003
A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants journal April 1992
Conservation between animals and plants of the cis-acting element involved in the unfolded protein response journal January 2003
TMBIM protein family: ancestral regulators of cell death journal February 2014
Cotranslational Targeting of XBP1 Protein to the Membrane Promotes Cytoplasmic Splicing of Its Own mRNA journal April 2009
The unfolded protein response: controlling cell fate decisions under ER stress and beyond journal January 2012
bZIP28 and NF-Y Transcription Factors Are Activated by ER Stress and Assemble into a Transcriptional Complex to Regulate Stress Response Genes in Arabidopsis journal March 2010
The Characteristics of Bax Inhibitor-1 and its Related Diseases journal June 2014
Genomic Analysis of the Unfolded Protein Response in Arabidopsis Shows Its Connection to Important Cellular Processes journal January 2003
Proapoptotic BAX and BAK Modulate the Unfolded Protein Response by a Direct Interaction with IRE1  journal April 2006
Maintaining the factory: the roles of the unfolded protein response in cellular homeostasis in plants journal March 2017
Fine-Tuning of the Unfolded Protein Response: Assembling the IRE1α Interactome journal September 2009
The Lumen-Facing Domain Is Important for the Biological Function and Organelle-to-Organelle Movement of bZIP28 during ER Stress in Arabidopsis journal September 2013
IRE1: ER stress sensor and cell fate executor journal November 2013
An acidic pH environment increases cell death and pro-inflammatory cytokine release in osteoblasts: The involvement of BAX Inhibitor-1 journal September 2011
Role of the unfolded protein response in organ physiology: Lessons from mouse models: Physiological Function of UPR in Organs and Tissues journal November 2013
An Endoplasmic Reticulum Stress Response in Arabidopsis Is Mediated by Proteolytic Processing and Nuclear Relocation of a Membrane-Associated Transcription Factor, bZIP28 journal December 2007
Opposing unfolded-protein-response signals converge on death receptor 5 to control apoptosis journal July 2014
Conserved and plant-unique strategies for overcoming endoplasmic reticulum stress journal January 2014
Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis journal April 2011
pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response journal February 2006
The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis -regulatory element to modulate the unfolded protein response in Arabidopsis journal August 2013
Plant Bax Inhibitor-1 interacts with ATG6 to regulate autophagy and programmed cell death journal July 2017
bZIP17 and bZIP60 Regulate the Expression of BiP3 and Other Salt Stress Responsive Genes in an UPR-Independent Manner in Arabidopsis thaliana : bZIP17 journal June 2015
Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response journal March 2013

Cited By (7)

NADPH oxidase activity is required for ER stress survival in plants journal October 2018
BLISTER-regulated vegetative growth is dependent on the protein kinase domain of ER stress modulator IRE1A in Arabidopsis thaliana text January 2020
BI1 is associated with microvascular protection in cardiac ischemia reperfusion injury via repressing Syk–Nox2–Drp1-mitochondrial fission pathways journal April 2018
Communications Between the Endoplasmic Reticulum and Other Organelles During Abiotic Stress Response in Plants journal June 2019
BLISTER-regulated vegetative growth is dependent on the protein kinase domain of ER stress modulator IRE1A in Arabidopsis thaliana journal December 2019
AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis journal November 2019
BI1 alleviates cardiac microvascular ischemia-reperfusion injury via modifying mitochondrial fission and inhibiting XO/ROS/F-actin pathways: ZHOU et al. journal September 2018