Two Alternative Splicing Variants of AtERF73/HRE1, HRE1α and HRE1β, Have Differential Transactivation Activities in Arabidopsis
Abstract
:1. Introduction
2. Results
2.1. Structural Comparison of HRE1α and HRE1β
2.2. Comparison of HRE1α and HRE1β Functions in the Hypoxia Response and Root Development
2.3. N-Terminal and/or C-Terminal Regions of HRE1α and HRE1β Are Responsible for Transactivation Activity
2.4. N-Terminal Region of HRE1β Has One Motif Responsible for Transactivation Activity
2.5. C-Terminal Region of HRE1β Has Two Motifs Responsible for Transactivation Activity
2.6. Four Glutamate Residues and LWS Residues Contribute to Transactivation Activity
2.7. HRE1α and HRE1β Show Transactivation Activity In Vivo
2.8. Both HRE1α and HRE1β Transactivate Downstream Genes via the GCC Box
2.9. Analysis of Downstream Genes Regulated by HRE1α and HRE1β Using RNA-Seq
2.10. Analysis of Genes Downstream of HRE1α and HRE1β in the Hypoxia Response
3. Discussion
4. Materials and Methods
4.1. Plant Materials and Growth Conditions
4.2. Plasmid Construction
4.3. Plant Transformation and Selection of Transgenic Plants
4.4. Stress Treatments
4.5. Root Length Measurement
4.6. Yeast Transformation
4.7. Transactivation Activity Analysis in Yeast
4.8. Protoplast Transformation
4.9. Dual-Luciferase Assay
4.10. RNA Isolation, cDNA Synthesis, Semi-Quantitative RT-PCR, and Quantitative RT-PCR
4.11. Multiple Alignment Analysis
4.12. Phylogenetic Tree
4.13. Library Preparation and Sequencing
4.14. Data Analysis
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
AP2/ERF | APETALA2/ethylene-responsive factor |
BD | DNA-binding domain |
CaMV | Cauliflower mosaic virus |
DAG | Days after germination |
DEG | Differentially expressed gene |
DREB/CBF | Dehydration responsive element-binding factor/C-repeat-binding factor |
GAPc | Glyceraldehyde 3-phosphate dehydrogenase |
GO | Gene ontology |
MS | Murashige and Skoog |
ONPG | 2-nitrophenyl-β-D-galacto-pyranoside |
RAV | Related to ABI3/VP1 |
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GO Term | Description | Number in Input List | p-Value |
---|---|---|---|
GO:0048511 | Rhythmic process | 5 | 1.14 × 10−3 |
GO:0009909 | Regulation of flower development | 5 | 1.85 × 10−3 |
GO:2000241 | Regulation of reproductive process | 6 | 1.90 × 10−3 |
GO:0009628 | Response to abiotic stimulus | 16 | 2.54 × 10−3 |
GO:0009416 | Response to light stimulus | 9 | 3.08 × 10−3 |
GO:0009314 | Response to radiation | 9 | 3.98 × 10−3 |
GO:0048831 | Regulation of shoot system development | 5 | 4.85 × 10−3 |
GO:0009639 | Response to red or far red light | 5 | 6.66 × 10−3 |
GO:0007623 | Circadian rhythm | 4 | 7.67 × 10−3 |
GO:0009719 | Response to endogenous stimulus | 13 | 1.46 × 10−2 |
GO:0009739 | Response to gibberellin | 4 | 1.49 × 10−2 |
GO:0010468 | Regulation of gene expression | 18 | 1.73 × 10−2 |
GO:0048580 | Regulation of postembryonic development | 5 | 2.43 × 10−2 |
GO:0048367 | Shoot system development | 8 | 2.94 × 10−2 |
GO:0010017 | Red or far-red light signaling pathway | 3 | 3.13 × 10−2 |
GO:0051171 | Regulation of nitrogen compound metabolic process | 17 | 3.21 × 10−2 |
GO:0071489 | Cellular response to red or far red light | 3 | 3.27 × 10−2 |
GO:0010605 | Negative regulation of macromolecule metabolic process | 6 | 3.60 × 10−2 |
GO:1901700 | Response to oxygen-containing compound | 11 | 3.64 × 10−2 |
GO:0010033 | Response to organic substance | 13 | 4.12 × 10−2 |
GO:0019438 | Aromatic compound biosynthetic process | 18 | 4.27 × 10−2 |
GO:0033993 | Response to lipid | 7 | 4.52 × 10−2 |
GO:0009892 | Negative regulation of metabolic process | 6 | 4.75 × 10−2 |
GO:2000112 | Regulation of cellular macromolecule biosynthetic process | 16 | 4.86 × 10−2 |
GO:0010556 | Regulation of macromolecule biosynthetic process | 16 | 4.99 × 10−2 |
GO Term | Description | Number in Input List | p-Value |
---|---|---|---|
GO:0009636 | Response to toxic substance | 17 | 2.52 × 10−11 |
GO:1901700 | Response to oxygen-containing compound | 60 | 8.75 × 10−9 |
GO:0019748 | Secondary metabolic process | 29 | 2.76 × 10−7 |
GO:0009404 | Toxin metabolic process | 10 | 6.78 × 10−7 |
GO:0009407 | Toxin catabolic process | 9 | 1.16 × 10−6 |
GO:0090487 | Secondary metabolite catabolic process | 9 | 1.16 × 10−6 |
GO:0001101 | Response to acid chemical | 43 | 6.89 × 10−6 |
GO:0051707 | Response to another organism | 44 | 9.27 × 10−6 |
GO:0043207 | Response to external biotic stimulus | 44 | 9.59 × 10−6 |
GO:0009607 | Response to biotic stimulus | 45 | 1.29 × 10−5 |
GO:0009605 | Response to external stimulus | 53 | 1.49 × 10−5 |
GO:0006749 | Glutathione metabolic process | 9 | 2.63 × 10−5 |
GO:0034614 | Cellular response to reactive oxygen species | 8 | 2.78 × 10−5 |
GO:0071555 | Cell wall organization | 25 | 4.92 × 10−5 |
GO:1901698 | Response to nitrogen compound | 17 | 5.02 × 10−5 |
GO:0006952 | Defense response | 50 | 8.59 × 10−5 |
GO:0045229 | External encapsulating structure organization | 25 | 1.29 × 10−4 |
GO:0002213 | Defense response to insect | 5 | 2.30 × 10−4 |
GO:0071554 | Cell wall organization or biogenesis | 28 | 2.71 × 10−4 |
GO:0010039 | Response to iron ion | 7 | 3.12 × 10−4 |
GO:0071732 | Cellular response to nitric oxide | 5 | 3.55 × 10−4 |
GO:0006790 | Sulfur compound metabolic process | 19 | 3.91 × 10−4 |
GO:0010033 | Response to organic substance | 57 | 3.93 × 10−4 |
GO:0006575 | Cellular modified amino acid metabolic process | 10 | 3.94 × 10−4 |
GO:0010035 | Response to inorganic substance | 32 | 4.05 × 10−4 |
GO Term | Description | Number in Input List | p-Value |
---|---|---|---|
GO:0010033 | Response to organic substance | 14 | 1.57 × 10−4 |
GO:0009719 | Response to endogenous stimulus | 13 | 1.61 × 10−4 |
GO:1901700 | Response to oxygen-containing compound | 12 | 2.36 × 10−4 |
GO:0009725 | Response to hormone | 11 | 1.59 × 10−3 |
GO:0001101 | Response to acid chemical | 9 | 2.49 × 10−3 |
GO:0014070 | Response to organic cyclic compound | 5 | 7.19 × 10−3 |
GO:0009751 | Response to salicylic acid | 4 | 9.32 × 10−3 |
GO:0009753 | Response to jasmonic acid | 4 | 9.81 × 10−3 |
GO:0006355 | Regulation of transcription, DNA-template | 12 | 1.29 × 10−2 |
GO:2001141 | Regulation of RNA biosynthetic process | 12 | 1.30 × 10−2 |
GO:1903506 | Regulation of nucleic acid-templated transcription | 12 | 1.30 × 10−2 |
GO:0051252 | Regulation of RNA metabolic process | 12 | 1.46 × 10−2 |
GO:0071229 | Cellular response to acid chemical | 5 | 1.61 × 10−2 |
GO:0019219 | Regulation of nucleobase-containing compound metabolic process | 12 | 1.70 × 10−2 |
GO:0043161 | Proteasome-mediated ubiquitin-dependent protein catabolic process | 5 | 1.90 × 10−2 |
GO:0097659 | Nucleic acid-templated transcription | 12 | 1.92 × 10−2 |
GO:0010498 | Proteasomal protein catabolic process | 5 | 1.93 × 10−2 |
GO:0032774 | RNA biosynthetic process | 12 | 1.95 × 10−2 |
GO:0071310 | Cellular response to organic substance | 7 | 1.96 × 10−2 |
GO:0033993 | Response to lipid | 6 | 2.05 × 10−2 |
GO:1901698 | Response to nitrogen compound | 4 | 2.22 × 10−2 |
GO:2000112 | Regulation of cellular macromolecule biosynthetic process | 12 | 2.57 × 10−2 |
GO:0010556 | Regulation of macromolecule biosynthetic process | 12 | 2.63 × 10−2 |
GO:0051171 | Regulation of nitrogen compound metabolic process | 12 | 3.19 × 10−2 |
GO:0032870 | Cellular response to hormone stimulus | 6 | 3.36 × 10−2 |
GO Term | Description | Number in Input List | p-Value |
---|---|---|---|
GO:0009628 | Response to abiotic stimulus | 37 | 3.49 × 10−5 |
GO:0009719 | Response to endogenous stimulus | 33 | 8.07 × 10−5 |
GO:0010033 | Response to organic substance | 35 | 2.57 × 10−4 |
GO:0009725 | Response to hormone | 30 | 3.11 × 10−4 |
GO:0009061 | Anaerobic respiration | 4 | 3.65 × 10−4 |
GO:1901700 | Response to oxygen-containing compound | 27 | 1.42 × 10−3 |
GO:0009664 | Plant-type cell wall organization | 7 | 2.97 × 10−3 |
GO:0001101 | Response to acid chemical | 21 | 4.14 × 10−3 |
GO:0006979 | Response to oxidative stress | 12 | 4.59 × 10−3 |
GO:0032870 | Cellular response to hormone stimulus | 17 | 5.09 × 10−3 |
GO:0009416 | Response to light stimulus | 15 | 5.70 × 10−3 |
GO:0071495 | Cellular response to endogenous stimulus | 17 | 6.31 × 10−3 |
GO:0000160 | Phosphorelay signal transduction system | 8 | 6.31 × 10−3 |
GO:0009314 | Response to radiation | 15 | 8.13 × 10−3 |
GO:0009741 | Response to brassinosteroid | 5 | 8.15 × 10−3 |
GO:0042744 | Hydrogen peroxide catabolic process | 5 | 8.48 × 10−3 |
GO:0071669 | Plant-type cell wall organization or biogenesis | 8 | 9.75 × 10−3 |
GO:0071369 | Cellular response to ethylene stimulus | 7 | 1.16 × 10−2 |
GO:0071555 | Cell wall organization | 12 | 1.21 × 10−2 |
GO:0010411 | Xyloglucan metabolic process | 4 | 1.33 × 10−2 |
GO:0072593 | Reactive oxygen species metabolic process | 6 | 1.34 × 10−2 |
GO:0042743 | Hydrogen peroxide metabolic process | 5 | 1.35 × 10−2 |
GO:0031328 | Positive regulation of cellular biosynthetic process | 10 | 1.38 × 10−2 |
GO:0009755 | Hormone-mediated signaling pathway | 15 | 1.42 × 10−2 |
GO:0009891 | Positive regulation of biosynthetic process | 10 | 1.58 × 10−2 |
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Seok, H.-Y.; Ha, J.; Lee, S.-Y.; Bae, H.; Moon, Y.-H. Two Alternative Splicing Variants of AtERF73/HRE1, HRE1α and HRE1β, Have Differential Transactivation Activities in Arabidopsis. Int. J. Mol. Sci. 2020, 21, 6984. https://doi.org/10.3390/ijms21196984
Seok H-Y, Ha J, Lee S-Y, Bae H, Moon Y-H. Two Alternative Splicing Variants of AtERF73/HRE1, HRE1α and HRE1β, Have Differential Transactivation Activities in Arabidopsis. International Journal of Molecular Sciences. 2020; 21(19):6984. https://doi.org/10.3390/ijms21196984
Chicago/Turabian StyleSeok, Hye-Yeon, Jimin Ha, Sun-Young Lee, Hyoungjoon Bae, and Yong-Hwan Moon. 2020. "Two Alternative Splicing Variants of AtERF73/HRE1, HRE1α and HRE1β, Have Differential Transactivation Activities in Arabidopsis" International Journal of Molecular Sciences 21, no. 19: 6984. https://doi.org/10.3390/ijms21196984