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

Title: A temporal hierarchy underpins the transcription factor–DNA interactome of the maize UPR

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.15044· OSTI ID:1764725

Summary Adverse environmental conditions reduce crop productivity and often increase the load of unfolded or misfolded proteins in the endoplasmic reticulum (ER). This potentially lethal condition, known as ER stress, is buffered by the unfolded protein response (UPR), a set of signaling pathways designed to either recover ER functionality or ignite programmed cell death. Despite the biological significance of the UPR to the life of the organism, the regulatory transcriptional landscape underpinning ER stress management is largely unmapped, especially in crops. To fill this significant knowledge gap, we performed a large‐scale systems‐level analysis of the protein–DNA interaction (PDI) network in maize ( Zea mays ). Using 23 promoter fragments of six UPR marker genes in a high‐throughput enhanced yeast one‐hybrid assay, we identified a highly interconnected network of 262 transcription factors (TFs) associated with significant biological traits and 831 PDIs underlying the UPR. We established a temporal hierarchy of TF binding to gene promoters within the same family as well as across different families of TFs. Cistrome analysis revealed the dynamic activities of a variety of cis ‐regulatory elements (CREs) in ER stress‐responsive gene promoters. By integrating the cistrome results into a TF network analysis, we mapped a subnetwork of TFs associated with a CRE that may contribute to UPR management. Finally, we validated the role of a predicted network hub gene using the Arabidopsis system. The PDIs, TF networks, and CREs identified in our work are foundational resources for understanding transcription‐regulatory mechanisms in the stress responses and crop improvement.

Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Michigan State Univ., East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Michigan State Univ.; National Science Foundation Plant Genome Research Program; USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health
Grant/Contract Number:
SC0018409; FG02-91ER20021; MICL02598; IOS 1444339; R35GM136637
OSTI ID:
1764725
Alternate ID(s):
OSTI ID: 1787366
Journal Information:
The Plant Journal, Vol. 105, Issue 1; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (126)

Genome-wide analysis of the AP2/ERF gene family in maize waterlogging stress response journal March 2014
Identification of ERSE-II, a New cis-Acting Element Responsible for the ATF6-dependent Mammalian Unfolded Protein Response journal March 2001
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
Clustering and Differential Alignment Algorithm: Identification of Early Stage Regulators in the Arabidopsis thaliana Iron Deficiency Response journal August 2015
Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants journal February 2015
A Gateway-Compatible Yeast One-Hybrid System journal October 2004
Integrated transcriptome, small RNA, and degradome analysis reveals the complex network regulating starch biosynthesis in maize journal July 2019
Exogenous Salicylic Acid Activates Two Signaling Arms of the Unfolded Protein Response in Arabidopsis journal August 2014
A stele‐enriched gene regulatory network in the Arabidopsis root journal January 2011
Comparative expression profiles of maize genes from a water stress-specific cDNA macroarray in response to high-salinity, cold or abscisic acid journal June 2006
Genome-wide analysis of maize NLP transcription factor family revealed the roles in nitrogen response journal September 2017
Endoplasmic Reticulum Stress Responses in Plants journal April 2013
Circadian- and UPR-dependent control of CPEB4 mediates a translational response to counteract hepatic steatosis under ER stress journal January 2017
Transcriptome Analysis of Flowering Time Genes under Drought Stress in Maize Leaves journal March 2017
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation journal May 2010
Toward the identification of genes underlying maize QTLs for lignin content, focusing on colocalizations with lignin biosynthetic genes and their regulatory MYB and NAC transcription factors journal February 2015
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions journal January 2013
Tissue-Specific Transcriptomics Reveals an Important Role of the Unfolded Protein Response in Maintaining Fertility upon Heat Stress in Arabidopsis journal April 2017
AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis journal October 2011
A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. journal December 1989
ZmMADS47 Regulates Zein Gene Transcription through Interaction with Opaque2 journal April 2016
PPIM: A Protein-Protein Interaction Database for Maize journal November 2015
Arabidopsis bZIP60 Is a Proteolysis-Activated Transcription Factor Involved in the Endoplasmic Reticulum Stress Response journal November 2008
Crop losses to pests journal December 2005
Yield Trends Are Insufficient to Double Global Crop Production by 2050 journal June 2013
Maize Global Transcriptomics Reveals Pervasive Leaf Diurnal Rhythms but Rhythms in Developing Ears Are Largely Limited to the Core Oscillator journal September 2010
Comparative transcriptome analysis of transcription factors in different maize varieties under salt stress conditions journal July 2016
Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation journal December 2014
Profiling of Accessible Chromatin Regions across Multiple Plant Species and Cell Types Reveals Common Gene Regulatory Principles and New Control Modules journal December 2017
Functional and Genomic Analyses Reveal an Essential Coordination between the Unfolded Protein Response and ER-Associated Degradation journal April 2000
SPL6 represses signalling outputs of ER stress in control of panicle cell death in rice journal April 2018
Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana journal January 2014
Genomewide analysis of LATERAL ORGAN BOUNDARIES Domain gene family in Zea mays journal April 2014
Expression analysis of genes encoding double B-box zinc finger proteins in maize journal May 2017
The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants journal March 1999
Identification of the cis-Acting Endoplasmic Reticulum Stress Response Element Responsible for Transcriptional Induction of Mammalian Glucose-regulated Proteins journal December 1998
Specific functions of individual class III peroxidase genes journal January 2009
Long-Lasting Primed State in Maize Plants: Salicylic Acid and Steroid Signaling Pathways as Key Players in the Early Activation of Immune Responses in Silks journal January 2019
Genomic Analysis of the Unfolded Protein Response in Arabidopsis Shows Its Connection to Important Cellular Processes journal January 2003
Diverging importance of drought stress for maize and winter wheat in Europe journal October 2018
Phosphorylation of a NAC Transcription Factor by a Calcium/Calmodulin-Dependent Protein Kinase Regulates Abscisic Acid-Induced Antioxidant Defense in Maize journal May 2016
Identification of a cis -element that mediates multiple pathways of the endoplasmic reticulum stress response in rice journal March 2013
A Novel Maize Homeodomain–Leucine Zipper (HD-Zip) I Gene, Zmhdz10, Positively Regulates Drought and Salt Tolerance in Both Rice and Arabidopsis journal June 2014
A Gene Regulatory Network for Cellular Reprogramming in Plant Regeneration journal February 2018
Response to Persistent ER Stress in Plants: A Multiphasic Process That Transitions Cells from Prosurvival Activities to Cell Death journal May 2018
A PERK–miR-211 axis suppresses circadian regulators and protein synthesis to promote cancer cell survival journal December 2017
Conservation of IRE1-Regulated bZIP74 mRNA Unconventional Splicing in Rice (Oryza sativa L.) Involved in ER Stress Responses journal March 2012
Transcriptome profiling of two maize inbreds with distinct responses to Gibberella ear rot disease to identify candidate resistance genes journal February 2018
Genome-wide association analysis for nine agronomic traits in maize under well-watered and water-stressed conditions journal July 2013
The Maize (Zea mays L.) AUXIN/INDOLE-3-ACETIC ACID Gene Family: Phylogeny, Synteny, and Unique Root-Type and Tissue-Specific Expression Patterns during Development journal November 2013
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis journal January 2007
A Genome-Scale Resource for the Functional Characterization of Arabidopsis Transcription Factors journal July 2014
Preservation of circadian rhythms by the protein folding chaperone, BiP journal March 2019
An Arabidopsis gene regulatory network for secondary cell wall synthesis journal December 2014
The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation journal November 2011
The interaction landscape between transcription factors and the nucleosome journal September 2018
A Maize Gene Regulatory Network for Phenolic Metabolism journal March 2017
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape journal May 2016
Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis journal October 2013
ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death journal April 2013
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 2011
Salicylic acid-independent role of NPR1 is required for protection from proteotoxic stress in the plant endoplasmic reticulum journal May 2018
The Cysteine Protease CEP1, a Key Executor Involved in Tapetal Programmed Cell Death, Regulates Pollen Development in Arabidopsis journal July 2014
ZmCOL3 , a CCT gene represses flowering in maize by interfering with the circadian clock and activating expression of ZmCCT: Maize CCT genes and flowering time journal March 2018
OsDER1 Is an ER-Associated Protein Degradation Factor That Responds to ER Stress journal July 2018
Whole Transcriptome Profiling of Maize during Early Somatic Embryogenesis Reveals Altered Expression of Stress Factors and Embryogenesis-Related Genes journal October 2014
The Unfolded Protein Response Supports Plant Development and Defense as well as Responses to Abiotic Stress journal March 2017
Dual functions of ZmNF-YA3 in photoperiod-dependent flowering and abiotic stress responses in maize journal August 2018
HY5, a positive regulator of light signaling, negatively controls the unfolded protein response in Arabidopsis journal February 2017
ZmNF-YB16 Overexpression Improves Drought Resistance and Yield by Enhancing Photosynthesis and the Antioxidant Capacity of Maize Plants journal May 2018
Systematic Analysis of the Maize PHD-Finger Gene Family Reveals a Subfamily Involved in Abiotic Stress Response journal September 2015
DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis journal July 2006
Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves journal January 2015
Corn Yield Loss Estimates Due to Diseases in the United States and Ontario, Canada from 2012 to 2015 journal January 2016
Enhanced yeast one-hybrid assays for high-throughput gene-centered regulatory network mapping journal October 2011
The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition journal January 2012
Control of translation during the unfolded protein response in maize seedlings: Life without PERKs journal July 2020
Network-Guided Discovery of Extensive Epistasis between Transcription Factors Involved in Aliphatic Glucosinolate Biosynthesis journal January 2018
Bulked Segregant RNA-seq Reveals Differential Expression and SNPs of Candidate Genes Associated with Waterlogging Tolerance in Maize journal June 2017
Transcriptional regulation of nitrogen-associated metabolism and growth journal October 2018
FASCIATED EAR4 Encodes a bZIP Transcription Factor That Regulates Shoot Meristem Size in Maize journal January 2015
Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors journal April 2015
Characterization of a maize G-box binding factor that is induced by hypoxia journal April 1995
Modified expression of ZmMYB167 in Brachypodium distachyon and Zea mays leads to increased cell wall lignin and phenolic content journal June 2019
Orchestrated response: a symphony of transcription factors for gene control journal October 2000
Enhanced Y1H assays for Arabidopsis journal October 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
Differential manipulation of leaf angle throughout the canopy: current status and prospects journal November 2017
Temporal Shift of Circadian-Mediated Gene Expression and Carbon Fixation Contributes to Biomass Heterosis in Maize Hybrids journal July 2016
The Maize TFome - development of a transcription factor open reading frame collection for functional genomics journal August 2014
Conservation between animals and plants of the cis-acting element involved in the unfolded protein response journal January 2003
Establishment of Expression in the SHORTROOT-SCARECROW Transcriptional Cascade through Opposing Activities of Both Activators and Repressors journal December 2016
Analysis of ER stress in developing rice endosperm accumulating β-amyloid peptide: ER stress in maturing rice seed by accumulation of Aβ journal March 2010
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
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
Shared and genetically distinct Zea mays transcriptome responses to ongoing and past low temperature exposure journal October 2018
ZmbZIP4 Contributes to Stress Resistance in Maize by Regulating ABA Synthesis and Root Development journal August 2018
Fast gapped-read alignment with Bowtie 2 journal March 2012
BEDTools: a flexible suite of utilities for comparing genomic features journal January 2010
Functional Diversification of ER Stress Responses in Arabidopsis journal February 2020
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Dolichol Biosynthesis and Its Effects on the Unfolded Protein Response and Abiotic Stress Resistance in Arabidopsis journal July 2008
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
Quantifying similarity between motifs journal January 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
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
A PXY-Mediated Transcriptional Network Integrates Signaling Mechanisms to Control Vascular Development in Arabidopsis journal December 2019
Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response journal July 2015
The chromatin remodeler ZmCHB101 impacts expression of osmotic stress-responsive genes in maize journal June 2018
XBP1-KLF9 Axis Acts as a Molecular Rheostat to Control the Transition from Adaptive to Cytotoxic Unfolded Protein Response journal October 2018
Effects of maize organ-specific drought stress response on yields from transcriptome analysis journal August 2019
Maize Sep15 ‐like functions in endoplasmic reticulum and reactive oxygen species homeostasis to promote salt and osmotic stress resistance journal January 2019
The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family journal October 2018
Influence of extreme weather disasters on global crop production journal January 2016
ZmbZIP60 mRNA is spliced in maize in response to ER stress journal March 2012
Assigning roles to DNA regulatory motifs using comparative genomics journal February 2010
Spatiotemporal signalling in plant development journal August 2013
Interaction between abscisic acid receptor PYL3 and protein phosphatase type 2C in response to ABA signaling in maize journal October 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
Maize ZmRAV1 contributes to salt and osmotic stress tolerance in transgenic arabidopsis journal January 2014
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
Food Security: The Challenge of Feeding 9 Billion People journal January 2010
Yeast Bax Inhibitor, Bxi1p, Is an ER-Localized Protein That Links the Unfolded Protein Response and Programmed Cell Death in Saccharomyces cerevisiae journal June 2011
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Identification and expression profiling analysis of calmodulin-binding transcription activator genes in maize (Zea mays L.) under abiotic and biotic stresses journal July 2015