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Title: The Small Ethylene Response Factor ERF96 is Involved in the Regulation of the Abscisic Acid Response in Arabidopsis

Journal Article · · Frontiers in Plant Science
 [1];  [2];  [2];  [2];  [3]
  1. Key Laboratory of Molecular Epigenetics of Ministry of Education and Institute of Genetics and Cytology, Northeast Normal University, Changchun (China); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Key Laboratory of Molecular Epigenetics of Ministry of Education and Institute of Genetics and Cytology, Northeast Normal University, Changchun (China)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

We report that ethylene regulates many aspects of plant growth and development including seed germination, leaf senescence, and fruit ripening, and of plant responses to environmental stimuli including both biotic and abiotic stresses. Ethylene response factors (ERFs) are plant-specific transcription factors and are a subfamily of the AP2 (APETALA2)/ERF transcription factor family. The function of many members in this large gene family remains largely unknown. ERF96, a member of the Group IX ERF family transcription factors, has recently been shown to be a transcriptional activator that is involved in plant defense response in Arabidopsis. Here we provide evidence that ERF96 is a positive regulator of abscisic acid (ABA) responses. Bioinformatics analysis indicated that there are a total four small ERFs in Arabidopsis including ERF95, ERF96, ERF97, and ERF98, and that ERF96 forms a cluster with ERF95 and ERF97. By using quantitative RT-PCR, we found that ERF96 is expressed in all tissues and organs examined except roots, with relatively high expression in flowers and seeds. Results from the protoplast transfection assay indicated that the EDLL motif-containing C-terminal domain is responsible for ERF96’s transcriptional activity. Although loss-of-function mutant of ERF96 was morphologically similar to wild type plants, transgenic plants overexpressing ERF96 had smaller rosette size and were delayed in flowering time. In ABA sensitivity assays, we found that ERF96 overexpression plants were hypersensitive to ABA in terms of ABA inhibition of seed germination, early seedling development and root elongation. Consistent with these observations, elevated transcript levels of some ABA-responsive genes including RD29A, ABI5, ABF3, ABF4, P5CS, and COR15A were observed in the transgenic plants in the presence of ABA. However, in the absence of ABA treatment, the transcript levels of these ABA-responsive genes remained largely unchanged. Our experiments also showed that water loss in ERF96 overexpression plants was slower than that in Col wild type plants. Stomatal closure assays indicated that ERF96 overexpression plants had reduced stomatal aperture in the presence of ABA. In conclusion, taken together, our results suggest that ERF96 positively regulates ABA responses in Arabidopsis.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725; 130014542
OSTI ID:
1311283
Alternate ID(s):
OSTI ID: 1260689
Journal Information:
Frontiers in Plant Science, Vol. 6; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 39 works
Citation information provided by
Web of Science

References (70)

The 5?-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression journal March 1994
ETHYLENE RESPONSE FACTOR 96 positively regulates A rabidopsis resistance to necrotrophic pathogens by direct binding to GCC elements of jasmonate - and ethylene-responsive defence genes : ERF96 in journal July 2015
Genome-Wide Analysis and Expression Profiling of the ERF Transcription Factor Family in Potato (Solanum tuberosum L.) journal December 2014
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana journal December 1998
Genome-Wide Analysis of the AP2/ERF Gene Family in Prunus mume journal November 2012
Arabidopsis Ethylene-Responsive Element Binding Factors Act as Transcriptional Activators or Repressors of GCC Box–Mediated Gene Expression journal March 2000
Comparative genomic analysis and expression of the APETALA2-like genes from barley, wheat, and barley-wheat amphiploids journal January 2009
An auxin responsive CLE gene regulates shoot apical meristem development in Arabidopsis journal May 2015
Regulation of disease resistance pathways by AP2/ERF transcription factors journal August 2004
The small, versatilepPZP family ofAgrobacterium binary vectors for plant transformation journal September 1994
Overexpression of the poplar NF-YB7 transcription factor confers drought tolerance and improves water-use efficiency in Arabidopsis journal September 2013
Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant journal December 2002
Molecular cloning, expression profile and promoter analysis of a novel ethylene responsive transcription factor gene GhERF4 from cotton (Gossypium hirstum) journal January 2008
Arabidopsis Basic Leucine Zipper Proteins That Mediate Stress-Responsive Abscisic Acid Signaling journal February 2002
Functional characterization of NtCEF1, an AP2/EREBP-type transcriptional activator highly expressed in tobacco callus journal May 2005
AtERF15 is a positive regulator of ABA response journal September 2014
ABA Signaling in Guard Cells Entails a Dynamic Protein–Protein Interaction Relay from the PYL-RCAR Family Receptors to Ion Channels journal March 2013
Isolation and functional characterization of CE1 binding proteins journal January 2010
Genome-wide Analysis of the Distribution of AP2/ERF Transcription Factors Reveals Duplication and Elucidates their Potential Function in Chinese Cabbage (Brassica rapa ssp. pekinensis) journal February 2013
Overexpression of an AP2/ERF-type Transcription Factor CRF5 Confers Pathogen Resistance to Arabidopsis Plants journal April 2010
APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs journal May 2013
Expression analysis and functional characterization of a cold-responsive gene COR15A from Arabidopsis thaliana journal July 2014
Abscisic Acid Increases Arabidopsis ABI5 Transcription Factor Levels by Promoting KEG E3 Ligase Self-Ubiquitination and Proteasomal Degradation journal August 2010
Expression of wild-type PtrIAA14.1, a poplar Aux/IAA gene causes morphological changes in Arabidopsis journal June 2015
ABI1 regulates carbon/nitrogen-nutrient signal transduction independent of ABA biosynthesis and canonical ABA signalling pathways in Arabidopsis journal March 2015
Repressor- and Activator-Type Ethylene Response Factors Functioning in Jasmonate Signaling and Disease Resistance Identified via a Genome-Wide Screen of Arabidopsis Transcription Factor Gene Expression journal September 2005
GmDREB2A;2, a Canonical DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN2-Type Transcription Factor in Soybean, Is Posttranslationally Regulated and Mediates Dehydration-Responsive Element-Dependent Gene Expression journal November 2012
Ethylene Response Factors: A Key Regulatory Hub in Hormone and Stress Signaling journal June 2015
Genome-Wide Analysis of the ERF Gene Family in Arabidopsis and Rice journal January 2006
Transcriptional Regulation of ABI3- and ABA-responsive Genes Including RD29B and RD29A in Seeds, Germinating Embryos, and Seedlings of Arabidopsis journal January 2006
High-throughput in planta expression screening identifies a class II ethylene-responsive element binding factor-like protein that regulates plant cell death and non-host resistance: Overexpression of a class II ERF causes plant cell death journal July 2005
AtERF14, a Member of the ERF Family of Transcription Factors, Plays a Nonredundant Role in Plant Defense journal November 2006
ABR1, an APETALA2-Domain Transcription Factor That Functions as a Repressor of ABA Response in Arabidopsis journal October 2005
Arabidopsis Transcription Factors: Genome-Wide Comparative Analysis Among Eukaryotes journal December 2000
DNA-Binding Specificity of the ERF/AP2 Domain of Arabidopsis DREBs, Transcription Factors Involved in Dehydration- and Cold-Inducible Gene Expression journal January 2002
Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato journal October 2010
Gene Structures, Classification and Expression Models of the AP2/EREBP Transcription Factor Family in Rice journal December 2010
Role of an Arabidopsis AP2/EREBP-Type Transcriptional Repressor in Abscisic Acid and Drought Stress Responses journal July 2005
Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis) journal January 2013
Differential expression of two P5CS genes controlling proline accumulation during salt‐stress requires ABA and is regulated by ABA1 , ABI1 and AXR2 in Arabidopsis journal September 1997
Effect of hydroxylated carotenoid deficiency on ABA accumulation in Arabidopsis journal November 2004
The EDLL motif: a potent plant transcriptional activation domain from AP2/ERF transcription factors: Strong plant transcriptional activation domain journal March 2012
Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance journal May 2004
TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis journal October 2007
Regulation of secondary cell wall biosynthesis by poplar R2R3 MYB transcription factor PtrMYB152 in Arabidopsis journal May 2014
AUXIN RESPONSE FACTOR7 Restores the Expression of Auxin-Responsive Genes in Mutant Arabidopsis Leaf Mesophyll Protoplasts journal May 2005
Characterization of an activation-tagged mutant uncovers a role of GLABRA2 in anthocyanin biosynthesis in Arabidopsis journal June 2015
Genome-wide survey and expression profiles of the AP2/ERF family in castor bean (Ricinus communis L.) journal January 2013
Functions of the ERF transcription factor family in plants journal September 2008
Functions and Application of the AP2/ERF Transcription Factor Family in Crop ImprovementF: Functions of the AP2/EREBP Family journal July 2011
Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses journal July 2005
Differential expression of kiwifruit ERF genes in response to postharvest abiotic stress journal April 2012
Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.) journal October 2008
The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis: Regulation of AtERF98 in ascorbic acid biosynthesis journal June 2012
Transcriptional activator TSRF1 reversely regulates pathogen resistance and osmotic stress tolerance in tobacco journal October 2006
The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco journal August 2004
An AP2 Domain-Containing Gene, ESE1 , Targeted by the Ethylene Signaling Component EIN3 Is Important for the Salt Response in Arabidopsis journal August 2011
Control of trichome formation in Arabidopsis by poplar single-repeat R3 MYB transcription factors journal June 2014
TRANSLUCENT GREEN, an ERF Family Transcription Factor, Controls Water Balance in Arabidopsis by Activating the Expression of Aquaporin Genes journal April 2014
Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa journal July 2008
Discovery and expression profile analysis of AP2/ERF family genes from Triticum aestivum journal April 2010
Discovery, phylogeny and expression patterns of AP2-like genes in maize journal May 2010
Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera journal December 2009
A celery transcriptional repressor AgERF8 negatively modulates abscisic acid and salt tolerance journal November 2020
Transcriptomic analysis reveals the mechanism of the alleviation of salt stress by salicylic acid in pepper (Capsicum annuum L.) journal November 2022
Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers journal January 2011
AP2/ERF Transcription Factor in Rice: Genome-Wide Canvas and Syntenic Relationships between Monocots and Eudicots journal January 2012
Genome-wide analysis of the AP2/ERF superfamily in peach (Prunus persica) journal January 2012
A genome-wide analysis of the ERF gene family in sorghum journal January 2013
Genome-wide identification and phylogenetic analysis of the AP2/ERF gene superfamily in sweet orange (Citrus sinensis) journal January 2014

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A novel AP2/ERF family transcription factor from Glycine soja, GsERF71, is a DNA binding protein that positively regulates alkaline stress tolerance in Arabidopsis journal July 2017
Toward a Molecular Understanding of Abscisic Acid Actions in Floral Transition journal January 2018
APETALA 2-domain-containing transcription factors: focusing on abscisic acid and gibberellins antagonism journal October 2017
A novel family of transcription factors conserved in angiosperms is required for ABA signalling journal September 2017
A genome-wide association study of 23 agronomic traits in Chinese wheat landraces journal July 2017
Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte journal February 2019
The differential expression patterns of paralogs in response to stresses indicate expression and sequence divergences journal June 2020
Regulation of Apetala2/Ethylene Response Factors in Plants journal February 2017
Impact of Alternatively Polyadenylated Isoforms of ETHYLENE RESPONSE FACTOR4 with Activator and Repressor Function on Senescence in Arabidopsis thaliana L. journal January 2019
Ethylene Response of Plum ACC Synthase 1 (ACS1) Promoter is Mediated through the Binding Site of Abscisic Acid Insensitive 5 (ABI5)   journal May 2019
The differential expression patterns of paralogs in response to stresses indicate expression and sequence divergences posted_content June 2020
The differential expression patterns of paralogs in response to stresses indicate expression and sequence divergences posted_content June 2020
Functional Analysis of the Pepper Ethylene-Responsive Transcription Factor, CaAIEF1, in Enhanced ABA Sensitivity and Drought Tolerance journal August 2017
GhVTC1, the Key Gene for Ascorbate Biosynthesis in Gossypium hirsutum, Involves in Cell Elongation Under Control of Ethylene journal September 2019
Ethylene Responsive Factor MeERF72 Negatively Regulates Sucrose synthase 1 Gene in Cassava journal April 2018