DOE PAGES 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

Abstract

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)more » 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.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1607736
Alternate Identifier(s):
OSTI ID: 1411091
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 93; Journal Issue: 1; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis; unfolded protein response; Bl1; bZIP28; bZIP60; IRE1

Citation Formats

Ruberti, Cristina, Lai, YaShiuan, and Brandizzi, Federica. 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. United States: N. p., 2017. Web. doi:10.1111/tpj.13768.
Ruberti, Cristina, Lai, YaShiuan, & Brandizzi, Federica. 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. United States. https://doi.org/10.1111/tpj.13768
Ruberti, Cristina, Lai, YaShiuan, and Brandizzi, Federica. Fri . "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". United States. https://doi.org/10.1111/tpj.13768. https://www.osti.gov/servlets/purl/1607736.
@article{osti_1607736,
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},
author = {Ruberti, Cristina and Lai, YaShiuan and Brandizzi, Federica},
abstractNote = {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.},
doi = {10.1111/tpj.13768},
journal = {The Plant Journal},
number = 1,
volume = 93,
place = {United States},
year = {Fri Nov 10 00:00:00 EST 2017},
month = {Fri Nov 10 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 46 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis
journal, October 2013

  • Deng, Y.; Srivastava, R.; Howell, S. H.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 48
  • DOI: 10.1073/pnas.1314749110

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

  • Kim, H. -R.; Lee, G. -H.; Yi Cho, E.
  • Journal of Cell Science, Vol. 122, Issue 8
  • DOI: 10.1242/jcs.038430

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

  • Bultynck, Geert; Kiviluoto, Santeri; Henke, Nadine
  • Journal of Biological Chemistry, Vol. 287, Issue 4
  • DOI: 10.1074/jbc.M111.275354

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

  • Castillo, Karen; Rojas-Rivera, Diego; Lisbona, Fernanda
  • The EMBO Journal, Vol. 30, Issue 21
  • DOI: 10.1038/emboj.2011.318

Unfolded protein response in plants: one master, many questions
journal, October 2015

  • Ruberti, Cristina; Kim, Sang-Jin; Stefano, Giovanni
  • Current Opinion in Plant Biology, Vol. 27
  • DOI: 10.1016/j.pbi.2015.05.016

Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response
journal, November 2008

  • Iwata, Yuji; Fedoroff, Nina V.; Koizumi, Nozomu
  • The Plant Cell, Vol. 20, Issue 11
  • DOI: 10.1105/tpc.108.061002

A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana
journal, October 2008

  • Gao, H.; Brandizzi, F.; Benning, C.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 42
  • DOI: 10.1073/pnas.0808463105

Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor
journal, July 2011

  • Nagashima, Yukihiro; Mishiba, Kei-ichiro; Suzuki, Eiji
  • Scientific Reports, Vol. 1, Issue 1
  • DOI: 10.1038/srep00029

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

  • Rodriguez, Diego; Rojas-Rivera, Diego; Hetz, Claudio
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1813, Issue 4
  • DOI: 10.1016/j.bbamcr.2010.11.012

CPR5 modulates salicylic acid and the unfolded protein response to manage tradeoffs between plant growth and stress responses
journal, February 2017

  • Meng, Zhe; Ruberti, Cristina; Gong, Zhizhong
  • The Plant Journal, Vol. 89, Issue 3
  • DOI: 10.1111/tpj.13397

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

  • Kawai-Yamada, Maki; Ohori, Yuri; Uchimiya, Hirofumi
  • The Plant Cell, Vol. 16, Issue 1
  • DOI: 10.1105/tpc.014613

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

  • Oh, Dong-Ha; Kwon, Chang-Seob; Sano, Hiroshi
  • Biochemical and Biophysical Research Communications, Vol. 301, Issue 1
  • DOI: 10.1016/S0006-291X(02)03019-X

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

  • Hetz, Claudio
  • Nature Reviews Molecular Cell Biology, Vol. 13, Issue 2
  • DOI: 10.1038/nrm3270

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

  • Martínez, Immaculada M.; Chrispeels, Maarten J.
  • The Plant Cell, Vol. 15, Issue 2
  • DOI: 10.1105/tpc.007609

Maintaining the factory: the roles of the unfolded protein response in cellular homeostasis in plants
journal, March 2017

  • Angelos, Evan; Ruberti, Cristina; Kim, Sang-Jin
  • The Plant Journal, Vol. 90, Issue 4
  • DOI: 10.1111/tpj.13449

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

  • Sun, Le; Lu, Sun-Jie; Zhang, Shuang-Shuang
  • Molecular Plant, Vol. 6, Issue 5
  • DOI: 10.1093/mp/sst059

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

  • Lee, Geum-Hwa; Hwang, Jung-Doo; Choi, Je-Yong
  • The International Journal of Biochemistry & Cell Biology, Vol. 43, Issue 9
  • DOI: 10.1016/j.biocel.2011.05.004

Role of the unfolded protein response in organ physiology: Lessons from mouse models: Physiological Function of UPR in Organs and Tissues
journal, November 2013

  • Cornejo, Víctor Hugo; Pihán, Philippe; Vidal, René Luis
  • IUBMB Life, Vol. 65, Issue 12
  • DOI: 10.1002/iub.1224

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

  • Deng, Y.; Humbert, S.; Liu, J. -X.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 17
  • DOI: 10.1073/pnas.1102117108

pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response
journal, February 2006

  • Yoshida, Hiderou; Oku, Masaya; Suzuki, Mie
  • The Journal of Cell Biology, Vol. 172, Issue 4
  • DOI: 10.1083/jcb.200508145

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

  • Henriquez-Valencia, Carlos; Moreno, Adrian A.; Sandoval-Ibañez, Omar
  • Journal of Cellular Biochemistry, Vol. 116, Issue 8
  • DOI: 10.1002/jcb.25121

Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response
journal, March 2013

  • Mishiba, K. -i.; Nagashima, Y.; Suzuki, E.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 14
  • DOI: 10.1073/pnas.1219047110

Works referencing / citing this record:

NADPH oxidase activity is required for ER stress survival in plants
journal, October 2018

  • Angelos, Evan; Brandizzi, Federica
  • The Plant Journal, Vol. 96, Issue 6
  • DOI: 10.1111/tpj.14091

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

  • Pu, Yunting; Ruberti, Cristina; Angelos, Evan R.
  • Plant Direct, Vol. 3, Issue 11
  • DOI: 10.1002/pld3.187

BI1 alleviates cardiac microvascular ischemia-reperfusion injury via modifying mitochondrial fission and inhibiting XO/ROS/F-actin pathways: ZHOU et al.
journal, September 2018

  • Zhou, Hao; Wang, Jin; Hu, Shunying
  • Journal of Cellular Physiology, Vol. 234, Issue 4
  • DOI: 10.1002/jcp.27308