DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Dynamics of ER stress-induced gene regulation in plants

Journal Article · · Nature Reviews. Genetics
ORCiD logo [1]; ORCiD logo [2]
  1. Michigan State University, East Lansing, MI (United States); Michigan State University Department of Plant Biology
  2. Michigan State University, East Lansing, MI (United States)

Endoplasmic reticulum (ER) stress is a potentially lethal condition that is induced by the abnormal accumulation of unfolded or misfolded secretory proteins in the ER. In eukaryotes, ER stress is managed by the unfolded protein response (UPR) through a tightly regulated, yet highly dynamic, reprogramming of gene transcription. Although the core principles of the UPR are similar across eukaryotes, unique features of the plant UPR reflect the adaptability of plants to their ever-changing environments and the need to balance the demands of growth and development with the response to environmental stressors. Here, the past decades have seen notable progress in understanding the mechanisms underlying ER stress sensing and signaling transduction pathways, implicating the UPR in the effects of physiological and induced ER stress on plant growth and crop yield. Facilitated by sequencing technologies and advances in genetic and genomic resources, recent efforts have driven the discovery of transcriptional regulators and elucidated the mechanisms that mediate the dynamic and precise gene regulation in response to ER stress at the systems level.

Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Michigan State University, East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
Grant/Contract Number:
SC0018409; FG02-91ER20021
OSTI ID:
2370469
Journal Information:
Nature Reviews. Genetics, Journal Name: Nature Reviews. Genetics Vol. 25; ISSN 1471-0056
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (129)

The interplay of GTP-binding protein AGB1 with ER stress sensors IRE1a and IRE1b modulates Arabidopsis unfolded protein response and bacterial immunity journal December 2021
Transcriptomic response of Arabidopsis thaliana to tunicamycin-induced endoplasmic reticulum stress journal January 2010
Unveiling a differential metabolite modulation of sorghum varieties under increasing tunicamycin-induced endoplasmic reticulum stress journal November 2023
IRE1/bZIP60-Mediated Unfolded Protein Response Plays Distinct Roles in Plant Immunity and Abiotic Stress Responses journal February 2012
Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis journal April 2011
Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance journal November 1994
A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana journal October 2008
ZmbZIP60 mRNA is spliced in maize in response to ER stress journal March 2012
The Transcription Factor bZIP60 Links the Unfolded Protein Response to the Heat Stress Response in Maize journal August 2020
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 December 2017
Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana journal June 2005
The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco journal December 2008
Molecular Characterization of Two Arabidopsis Ire1 Homologs, Endoplasmic Reticulum-Located Transmembrane Protein Kinases journal November 2001
An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants journal March 2005
Systemic signaling contributes to the unfolded protein response of the plant endoplasmic reticulum journal September 2018
Endoplasmic Reticulum Stress-Induced Formation of Transcription Factor Complex ERSF Including NF-Y (CBF) and Activating Transcription Factors 6α and 6β That Activates the Mammalian Unfolded Protein Response journal February 2001
Comprehensive Transcriptome Analysis Reveals Genome-Wide Changes Associated with Endoplasmic Reticulum (ER) Stress in Potato (Solanum tuberosum L.) journal November 2022
Functional Diversification of ER Stress Responses in Arabidopsis journal February 2020
The Unfolded Protein Response Is Triggered by a Plant Viral Movement Protein     journal April 2011
A temporal hierarchy underpins the transcription factor–DNA interactome of the maize UPR journal November 2020
Activation of the Arabidopsis membrane-bound transcription factor bZIP28 is mediated by site-2 protease, but not site-1 protease journal May 2017
ArabidopsiseIF2α kinase GCN2 is essential for growth in stress conditions and is activated by wounding journal December 2008
Food Security: The Challenge of Feeding 9 Billion People journal January 2010
BAX Inhibitor-1 Modulates Endoplasmic Reticulum Stress-mediated Programmed Cell Death in Arabidopsis journal November 2007
Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response journal March 2013
Progress, challenges and the future of crop genomes journal April 2015
Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants journal February 2015
Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum journal May 2018
Orchestrated response: a symphony of transcription factors for gene control journal October 2000
Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis journal October 2013
Epigenetic regulation of abiotic stress memory: maintaining the good things while they last journal June 2021
Tissue-Specific Transcriptomics Reveals an Important Role of the Unfolded Protein Response in Maintaining Fertility upon Heat Stress in Arabidopsis journal April 2017
The evolutionary significance of ancient genome duplications journal August 2009
Orosomucoid proteins limit endoplasmic reticulum stress in plants journal August 2023
Endoplasmic Reticulum Stress Responses in Plants journal April 2013
Time-Based Systems Biology Approaches to Capture and Model Dynamic Gene Regulatory Networks journal June 2021
Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor journal July 2011
A New Member of the Leucine Zipper Class of Proteins that Binds to the HLA DRα Promoter journal March 1990
IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA journal January 2002
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
Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana journal June 2003
Stress‐induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis journal November 2008
Empirical Analysis of Transcriptional Activity in the Arabidopsis Genome journal October 2003
AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis journal November 2019
Crosstalk between endoplasmic reticulum and cytosolic unfolded protein response in tomato journal September 2023
RNA-Seq: a revolutionary tool for transcriptomics journal January 2009
The Role and Regulation of ABI5 (ABA-Insensitive 5) in Plant Development, Abiotic Stress Responses and Phytohormone Crosstalk journal December 2016
Unfolded protein response and storage product accumulation in rice grains journal January 2022
Transduction of Calcium Stress through Interaction of the Human Transcription Factor CBF with the Proximal CCAAT Regulatory Element of the grp78/BiP Promoter journal April 1995
SMALLER TRICHOMES WITH VARIABLE BRANCHES (SVB) and its homolog SVBL act downstream of transcription factor NAC089 and function redundantly in Arabidopsis unfolded protein response journal August 2023
Binding of BiP to an assembly‐defective protein in plant cells journal January 1994
A fortunate choice: the history of Arabidopsis as a model plant journal November 2002
A Quantitative Arabidopsis IRE1a Ribonuclease-Dependent in vitro mRNA Cleavage Assay for Functional Studies of Substrate Splicing and Decay Activities journal July 2021
A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis journal July 2014
Exogenous Salicylic Acid Activates Two Signaling Arms of the Unfolded Protein Response in Arabidopsis journal August 2014
The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation journal November 2011
The UPR Branch IRE1-bZIP60 in Plants Plays an Essential Role in Viral Infection and Is Complementary to the Only UPR Pathway in Yeast journal April 2015
IRE1B degrades RNAs encoding proteins that interfere with the induction of autophagy by ER stress in Arabidopsis thaliana journal August 2018
Arabidopsis B‐cell lymphoma2 (Bcl‐2)‐associated athanogene 7 ( BAG 7)‐mediated heat tolerance requires translocation, sumoylation and binding to WRKY 29 journal December 2016
Regulation of the Arabidopsis defense transcriptome journal February 2005
Abiotic stress responses in plants journal September 2021
The Arabidopsis bZIP transcription factor family — an update journal October 2018
Multiple roles of the ER stress sensor IRE1 demonstrated by gene targeting in rice journal December 2012
Mechanisms of substrate processing during ER-associated protein degradation journal August 2023
Isolation and Characterization of a Putative Transducer of Endoplasmic Reticulum Stress in Oryza sativa journal May 2002
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
EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis journal September 2015
Regulation of transcription in plants: mechanisms controlling developmental switches journal November 2010
SPL6 represses signalling outputs of ER stress in control of panicle cell death in rice journal April 2018
Advanced genomics identifies growth effectors for proteotoxic ER stress recovery in Arabidopsis thaliana journal January 2022
Genetic control of a membrane component and zein deposition in maize endosperm journal November 1983
Unfolded Protein Response in Arabidopsis book October 2017
Spatiotemporal signalling in plant development journal August 2013
Identification of the cis-Acting Endoplasmic Reticulum Stress Response Element Responsible for Transcriptional Induction of Mammalian Glucose-regulated Proteins journal December 1998
Nucleosome destabilization in the epigenetic regulation of gene expression journal January 2008
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 UPR regulator IRE1 promotes balanced organ development by restricting TOR‐dependent control of cellular differentiation in Arabidopsis journal December 2021
Transcriptional competition shapes proteotoxic ER stress resolution journal May 2022
Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes journal April 2014
Experimental annotation of the human genome using microarray technology journal February 2001
Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response journal May 2000
Genomic Analysis of the Unfolded Protein Response in Arabidopsis Shows Its Connection to Important Cellular Processes journal January 2003
A transcription factor hierarchy defines an environmental stress response network journal November 2016
Protein folding in the cell journal January 1992
AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis journal October 2011
A defective signal peptide in the maize high-lysine mutant floury 2. journal July 1995
BAX Inhibitor-1 Is a Negative Regulator of the ER Stress Sensor IRE1α journal March 2009
ER-Anchored Transcription Factors bZIP17 and bZIP28 Regulate Root Elongation journal January 2018
The plant endoplasmic reticulum UPRome: A repository and pathway browser for genes involved in signaling networks linked to the endoplasmic reticulum journal July 2022
CRISPR/Cas9-Mediated HY5 Gene Editing Reduces Growth Inhibition in Chinese Cabbage (Brassica rapa) under ER Stress journal August 2023
Identification of a cis -element that mediates multiple pathways of the endoplasmic reticulum stress response in rice journal March 2013
The G-Box Transcriptional Regulatory Code in Arabidopsis journal September 2017
Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response journal November 2008
Arabidopsis enhanced ethylene response 4 encodes an EIN3-interacting TFIID transcription factor required for proper ethylene response, including ERF1 induction journal June 2007
Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice: ER stress response in rice journal December 2011
Endoplasmic Reticulum Plays a Critical Role in Integrating Signals Generated by Both Biotic and Abiotic Stress in Plants journal April 2019
ER-Phagy: A New Regulator of ER Homeostasis journal July 2021
Conservation of IRE1-Regulated bZIP74 mRNA Unconventional Splicing in Rice (Oryza sativa L.) Involved in ER Stress Responses journal March 2012
Stress response proteins NRP1 and NRP2 are pro-survival factors that inhibit cell death during ER stress journal July 2021
Bax inhibitor-1: a highly conserved endoplasmic reticulum-resident cell death suppressor journal May 2011
The Dynamic of the Splicing of bZIP60 and the Proteins Encoded by the Spliced and Unspliced mRNAs Reveals Some Unique Features during the Activation of UPR in Arabidopsis thaliana journal April 2015
Arabidopsis TBP-ASSOCIATED FACTOR 12 ortholog NOBIRO6 controls root elongation with unfolded protein response cofactor activity journal February 2022
Road to Ruin: Targeting Proteins for Degradation in the Endoplasmic Reticulum journal November 2011
The Membrane-Associated Transcription Factor NAC089 Controls ER-Stress-Induced Programmed Cell Death in Plants journal March 2014
Linking genotype to phenotype using the Arabidopsis unimutant collection journal March 2010
Ufmylation reconciles salt stress-induced unfolded protein responses via ER-phagy in Arabidopsis journal January 2023
Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana journal July 2009
An IRE1-proteasome system signalling cohort controls cell fate determination in unresolved proteotoxic stress of the plant endoplasmic reticulum journal August 2023
Advances and Opportunities in Single-Cell Transcriptomics for Plant Research journal June 2021
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
Response to Persistent ER Stress in Plants: A Multiphasic Process That Transitions Cells from Prosurvival Activities to Cell Death journal May 2018
Targeted destabilization of HY5 during light-regulated development of Arabidopsis journal May 2000
The art and design of genetic screens: Arabidopsis thaliana journal February 2002
Genetic Evidence for a Role of BiP/Kar2 That Regulates Ire1 in Response to Accumulation of Unfolded Proteins journal June 2003
The Endoplasmic Reticulum Role in the Plant Response to Abiotic Stress journal November 2021
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana journal December 2000
A Functional Unfolded Protein Response Is Required for Normal Vegetative Development journal February 2019
Molecular and genetic control of plant thermomorphogenesis journal January 2016
Enhanced Y1H assays for Arabidopsis journal October 2011
Tunicamycin and brefeldin a induce in plant cells a programmed cell death showing apoptotic features journal March 2001
Endoplasmic reticulum stress-induced programmed cell death in soybean cells journal May 2004
Network‐based approaches for understanding gene regulation and function in plants journal August 2020
Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling: Salt stress elicits ER stress response journal July 2007
The Tobacco Luminal Binding Protein Is Encoded by a Multigene Family journal November 1991
Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants journal June 2017
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
Update on the Basic Helix-Loop-Helix Transcription Factor Gene Family in Arabidopsis thaliana journal November 2003
HY5, a positive regulator of light signaling, negatively controls the unfolded protein response in Arabidopsis journal February 2017
Identification of ERSE-II, a New cis-Acting Element Responsible for the ATF6-dependent Mammalian Unfolded Protein Response journal March 2001