Comparative Transcriptome-Based Mining and Expression Profiling of Transcription Factors Related to Cold Tolerance in Peanut
Abstract
:1. Introduction
2. Results
2.1. Evaluation of Cold Tolerance of the Two Peanut Varieties
2.2. Physiological Responses of the Two Peanut Varieties to Cold Stress
2.3. Transcriptome Sequencing and de Novo Assembly
2.4. Identification of Transcription Factors from Peanut Transcriptome
2.5. Differential Expression Analysis of the Transcription Factors under Cold Stress
2.6. Phylogenetic Analysis of Peanut Transcription Factor Families
2.7. Analysis of Protein Characterization and Conversed Motifs of Peanut Transcription Factor Families
2.8. Temporal Expression Profiles and Gene Ontology Enrichment
2.9. Protein Interactions and Module Analysis
3. Discussion
4. Materials and Methods
4.1. Plant Materials, Growth Conditions, and Treatments
4.2. Morphological Parameters
4.3. Physiological Characteristics
4.4. Total RNA Extraction, Library Construction, and Sequence Analysis
4.5. Quantitative RT-PCR
4.6. Identification of Peanut Transcription Factors
4.7. Multiple Sequence Alignments and Phylogenetic Analysis
4.8. Protein Characterization and Conversed Motif Analysis
4.9. Expression Profile and Functional Enrichment Analyses
4.10. Protein Interactions and Module Analysis
4.11. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
TF | Transcription factor |
PPI | Protein-protein interaction |
JA | Jasmonic acid |
SA | Salicylic acid |
CBFs/DREB1s | C-repeat binding factors |
DREB1s | Dehydration responsive element binding factor1 proteins |
AP2 | APETALA2 |
ERF | ETHYLENE RESPONSIVE FACTOR |
COR | Cold responsive genes |
ICE1 | Inducer of CBF expression 1 |
CAMTA | Calmodulin binding transcription activator |
PIF | Phytochrome-interacting factor |
PH | Plant height |
TLA | Total leaf area |
SFW | Shoot fresh weight |
RFW | Root fresh weight |
SDW | Shoot dry weight |
RDW | Root dry weight |
EL | Electrolyte leakage |
MDA | Malondialdehyde |
FDR | False discovery rate |
GO | Gene Ontology |
KEGG | Kyoto Encyclopedia of Genes and Genomes |
ABA | Abscisic acid |
MAPK | Mitogen-activated protein kinase |
ET | Ethylene |
EIN3 | Ethylene-insensitive 3 |
FPKM | Fragments per kilobase of transcript per million fragments mapped |
bHLH | Basic helix—loop—helix protein |
C2H2 | Cys2/His2 zinc finger protein |
ERF | Ethylene-responsive factor |
MYB | v-myb avian myeloblastosis viral oncogene homolog |
NAC | NAM, ATAF1/2, CUC2 |
References
- Katam, R.; Sakata, K.; Suravajhala, P.; Pechan, T.; Kambiranda, D.M.; Naik, K.S.; Guo, B.; Basha, S.M. Comparative leaf proteomics of drought-tolerant and -susceptible peanut in response to water stress. J. Proteom. 2016, 143, 209–226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, G.H.; Yu, S.T.; Wang, H.; Wang, X.D. Transcriptome profiling of high oleic peanut under low temperatureduring germination. Yi Chuan 2019, 41, 1050–1059. [Google Scholar] [CrossRef] [PubMed]
- Zhu, J.K. Abiotic stress signaling and responses in plants. Cell 2016, 167, 313–324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Revilla, P.; Rodriguez, V.M.; Ordas, A.; Rincent, R.; Charcosset, A.; Giauffret, C.; Melchinger, A.E.; Schon, C.C.; Bauer, E.; Altmann, T.; et al. Association mapping for cold tolerance in two large maize inbred panels. BMC Plant Biol. 2016, 16, 127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, J.; Li, J.; Sun, J.; Hu, T.; Wu, A.; Liu, S.; Wang, W.; Ma, D.; Zhao, M. Genome-wide association mapping for cold tolerance in a core collection of rice (Oryza sativa L.) landraces by using high-density single nucleotide polymorphism markers from specific-locus amplified fragment sequencing. Front. Plant Sci. 2018, 9, 875. [Google Scholar] [CrossRef] [PubMed]
- Buti, M.; Pasquariello, M.; Ronga, D.; Milc, J.A.; Pecchioni, N.; Ho, V.T.; Pucciariello, C.; Perata, P.; Francia, E. Transcriptome profiling of short-term response to chilling stress in tolerant and sensitive Oryza sativa ssp. Japonica seedlings. Funct. Integr. Genom. 2018, 18, 627–644. [Google Scholar] [CrossRef]
- Guan, S.; Xu, Q.; Ma, D.; Zhang, W.; Xu, Z.; Zhao, M.; Guo, Z. Transcriptomics profiling in response to cold stress in cultivated rice and weedy rice. Gene 2019, 685, 96–105. [Google Scholar] [CrossRef]
- Ng, D.W.; Abeysinghe, J.K.; Kamali, M. Regulating the regulators: The control of transcription factors in plant defense signaling. Int. J. Mol. Sci. 2018, 19, 3737. [Google Scholar] [CrossRef] [Green Version]
- Nie, J.; Wen, C.; Xi, L.; Lv, S.; Zhao, Q.; Kou, Y.; Ma, N.; Zhao, L.; Zhou, X. The AP2/ERF transcription factor CmERF053 of chrysanthemum positively regulates shoot branching, lateral root, and drought tolerance. Plant Cell Rep. 2018, 37, 1049–1060. [Google Scholar] [CrossRef]
- Zhou, M.; Memelink, J. Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnol. Adv. 2016, 34, 441–449. [Google Scholar] [CrossRef]
- Birkenbihl, R.P.; Kracher, B.; Roccaro, M.; Somssich, I.E. Induced genome-wide binding of three arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell 2017, 29, 20–38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, X.; Wang, Y.; Sui, N. Transcriptional regulation of bHLH during plant response to stress. Biochem. Biophys. Res. Commun. 2018, 503, 397–401. [Google Scholar] [CrossRef] [PubMed]
- Jaglo-Ottosen, K.R.; Gilmour, S.J.; Zarka, D.G.; Schabenberger, O.; Thomashow, M.F. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 1998, 280, 104–106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vogel, J.T.; Zarka, D.G.; Van Buskirk, H.A.; Fowler, S.G.; Thomashow, M.F. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 2005, 41, 195–211. [Google Scholar] [CrossRef]
- Kidokoro, S.; Watanabe, K.; Ohori, T.; Moriwaki, T.; Maruyama, K.; Mizoi, J.; Myint Phyu Sin Htwe, N.; Fujita, Y.; Sekita, S.; Shinozaki, K.; et al. Soybean DREB1/CBF-type transcription factors function in heat and drought as well as cold stress-responsive gene expression. Plant J. 2015, 81, 505–518. [Google Scholar] [CrossRef]
- An, D.; Ma, Q.; Yan, W.; Zhou, W.; Liu, G.; Zhang, P. Divergent regulation of CBF regulon on cold tolerance and plant phenotype in cassava overexpressing arabidopsis CBF3 gene. Front. Plant Sci. 2016, 7, 1866. [Google Scholar] [CrossRef] [Green Version]
- Zhang, T.; Mo, J.; Zhou, K.; Chang, Y.; Liu, Z. Overexpression of Brassica campestris BcICE1 gene increases abiotic stress tolerance in tobacco. Plant Physiol. Biochem. 2018, 132, 515–523. [Google Scholar] [CrossRef]
- Kim, Y.S.; Lee, M.; Lee, J.H.; Lee, H.J.; Park, C.M. The unified ICE-CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant Mol. Biol. 2015, 89, 187–201. [Google Scholar] [CrossRef]
- Ding, Y.; Li, H.; Zhang, X.; Xie, Q.; Gong, Z.; Yang, S. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev. Cell 2015, 32, 278–289. [Google Scholar] [CrossRef] [Green Version]
- Doherty, C.J.; Van Buskirk, H.A.; Myers, S.J.; Thomashow, M.F. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 2009, 21, 972–984. [Google Scholar] [CrossRef] [Green Version]
- Kim, Y.; Park, S.; Gilmour, S.J.; Thomashow, M.F. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 2013, 75, 364–376. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Li, Y.; Cui, L.; Xie, L.; Zheng, C.; Zhou, G.; Zhou, J.; Xie, X. Phytochrome B negatively affects cold tolerance by regulating OsDREB1 gene expression through phytochrome interacting factor-like protein OsPIL16 in rice. Front. Plant Sci. 2016, 7, 1963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lv, Y.; Yang, M.; Hu, D.; Yang, Z.; Ma, S.; Li, X.; Xiong, L. The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing beta-amylase expression. Plant Physiol. 2017, 173, 1475–1491. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Ding, Y.; Li, Z.; Shi, Y.; Wang, J.; Hua, J.; Gong, Z.; Zhou, J.M.; Yang, S. PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Dev. Cell 2019, 51, 222–235. [Google Scholar] [CrossRef] [PubMed]
- Song, H.; Wang, P.; Lin, J.Y.; Zhao, C.; Bi, Y.; Wang, X. Genome-wide identification and characterization of WRKY gene family in peanut. Front. Plant Sci. 2016, 7, 534. [Google Scholar] [CrossRef] [Green Version]
- Gao, C.; Sun, J.; Wang, C.; Dong, Y.; Xiao, S.; Wang, X.; Jiao, Z. Genome-wide analysis of basic/helix-loop-helix gene family in peanut and assessment of its roles in pod development. PLoS ONE 2017, 12, e0181843. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Z.; Yan, L.; Wan, L.; Huai, D.; Kang, Y.; Shi, L.; Jiang, H.; Lei, Y.; Liao, B. Genome-wide systematic characterization of bZIP transcription factors and their expression profiles during seed development and in response to salt stress in peanut. BMC Genom. 2019, 20, 51. [Google Scholar] [CrossRef]
- Li, X.; Duan, X.; Jiang, H.; Sun, Y.; Tang, Y.; Yuan, Z.; Guo, J.; Liang, W.; Chen, L.; Yin, J.; et al. Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol. 2006, 141, 1167–1184. [Google Scholar] [CrossRef] [Green Version]
- Hudson, K.A.; Hudson, M.E. A classification of basic helix-loop-helix transcription factors of soybean. Int. J. Genom. 2015, 2015, 603182. [Google Scholar] [CrossRef] [Green Version]
- Englbrecht, C.C.; Schoof, H.; Bohm, S. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genom. 2004, 5, 39. [Google Scholar] [CrossRef] [Green Version]
- Nakano, T.; Suzuki, K.; Fujimura, T.; Shinshi, H. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 2006, 140, 411–432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, G.; Chen, M.; Chen, X.; Xu, Z.; Guan, S.; Li, L.C.; Li, A.; Guo, J.; Mao, L.; Ma, Y.; et al. Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J. Exp. Bot. 2008, 59, 4095–4107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Du, H.; Yang, S.S.; Liang, Z.; Feng, B.R.; Liu, L.; Huang, Y.B. Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol. 2012, 12, 106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katiyar, A.; Smita, S.; Lenka, S.K.; Rajwanshi, R.; Chinnusamy, V.; Bansal, K.C. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genom. 2012, 13, 544. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ooka, H.; Satoh, K.; Doi, K.; Nagata, T.; Otomo, Y.; Murakami, K.; Matsubara, K.; Osato, N.; Kawai, J.; Carninci, P.; et al. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 2003, 10, 239–247. [Google Scholar] [CrossRef]
- Hussain, R.M.; Ali, M.; Feng, X.; Li, X. The essence of NAC gene family to the cultivation of drought-resistant soybean (Glycine max L. Merr.) cultivars. BMC Plant Biol. 2017, 17, 55. [Google Scholar] [CrossRef] [Green Version]
- Berri, S.; Abbruscato, P.; Faivre-Rampant, O.; Brasileiro, A.C.; Fumasoni, I.; Satoh, K.; Kikuchi, S.; Mizzi, L.; Morandini, P.; Pe, M.E.; et al. Characterization of WRKY co-regulatory networks in rice and Arabidopsis. BMC Plant Biol. 2009, 9, 120. [Google Scholar] [CrossRef] [Green Version]
- Yu, Y.; Wang, N.; Hu, R.; Xiang, F. Genome-wide identification of soybean WRKY transcription factors in response to salt stress. SpringerPlus 2016, 5, 920. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Dong, J.; Zhao, X.; Zhang, Y.; Ren, J.; Xing, L.; Jiang, C.; Wang, X.; Wang, J.; Zhao, S.; et al. Research progress in membrane lipid metabolism and molecular mechanism in peanut cold tolerance. Front. Plant Sci. 2019, 10, 838. [Google Scholar] [CrossRef]
- Lissarre, M.; Ohta, M.; Sato, A.; Miura, K. Cold-responsive gene regulation during cold acclimation in plants. Plant Signal. Behav. 2010, 5, 948–952. [Google Scholar] [CrossRef] [Green Version]
- Barrero-Gil, J.; Salinas, J. Gene regulatory networks mediating cold acclimation: The CBF pathway. Adv. Exp. Med. Biol. 2018, 1081, 3–22. [Google Scholar] [CrossRef] [PubMed]
- Zhao, C.; Zhang, Z.; Xie, S.; Si, T.; Li, Y.; Zhu, J.K. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol. 2016, 171, 2744–2759. [Google Scholar] [CrossRef] [Green Version]
- Bolt, S.; Zuther, E.; Zintl, S.; Hincha, D.K.; Schmulling, T. ERF105 is a transcription factor gene of Arabidopsis thaliana required for freezing tolerance and cold acclimation. Plant Cell Environ. 2017, 40, 108–120. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.T.; Wang, W.; Mao, B.G.; Chu, C.C. Cold stress tolerance in rice: Physiological changes, molecular mechanism, and future prospects. Yi Chuan 2018, 40, 171–185. [Google Scholar] [CrossRef] [PubMed]
- Pradhan, S.K.; Pandit, E.; Nayak, D.K.; Behera, L.; Mohapatra, T. Genes, pathways and transcription factors involved in seedling stage chilling stress tolerance in indica rice through RNA-Seq analysis. BMC Plant Biol. 2019, 19, 352. [Google Scholar] [CrossRef] [Green Version]
- Ye, K.; Li, H.; Ding, Y.; Shi, Y.; Song, C.; Gong, Z.; Yang, S. BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell 2019, 31, 2682–2696. [Google Scholar] [CrossRef]
- Song, C.; Je, J.; Hong, J.K.; Lim, C.O. Ectopic expression of an Arabidopsis dehydration-responsive element-binding factor DREB2C improves salt stress tolerance in crucifers. Plant Cell Rep. 2014, 33, 1239–1254. [Google Scholar] [CrossRef]
- Lee, S.J.; Kang, J.Y.; Park, H.J.; Kim, M.D.; Bae, M.S.; Choi, H.I.; Kim, S.Y. DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol. 2010, 153, 716–727. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.; Zhao, T.; Sun, X.; Wang, Y.; Du, C.; Zhu, Z.; Gichuki, D.K.; Wang, Q.; Li, S.; Xin, H. Overexpression of VaWRKY12, a transcription factor from Vitis amurensis with increased nuclear localization under low temperature, enhances cold tolerance of plants. Plant Mol. Biol. 2019, 100, 95–110. [Google Scholar] [CrossRef]
- Sun, X.; Zhang, L.; Wong, D.C.J.; Wang, Y.; Zhu, Z.; Xu, G.; Wang, Q.; Li, S.; Liang, Z.; Xin, H. The ethylene response factor VaERF092 from Amur grape regulates the transcription factor VaWRKY33, improving cold tolerance. Plant J. 2019, 99, 988–1002. [Google Scholar] [CrossRef]
- Birkenbihl, R.P.; Diezel, C.; Somssich, I.E. Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol. 2012, 159, 266–285. [Google Scholar] [CrossRef] [Green Version]
- Xu, J.; Meng, J.; Meng, X.; Zhao, Y.; Liu, J.; Sun, T.; Liu, Y.; Wang, Q.; Zhang, S. Pathogen-responsive MPK3 and MPK6 reprogram the biosynthesis of indole glucosinolates and their derivatives in Arabidopsis immunity. Plant Cell 2016, 28, 1144–1162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chakraborty, J.; Ghosh, P.; Sen, S.; Das, S. Epigenetic and transcriptional control of chickpea WRKY40 promoter activity under Fusarium stress and its heterologous expression in Arabidopsis leads to enhanced resistance against bacterial pathogen. Plant Sci. 2018, 276, 250–267. [Google Scholar] [CrossRef]
- Sreenivasulu, N.; Harshavardhan, V.T.; Govind, G.; Seiler, C.; Kohli, A. Contrapuntal role of ABA: Does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 2012, 506, 265–273. [Google Scholar] [CrossRef] [PubMed]
- Verma, V.; Ravindran, P.; Kumar, P.P. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016, 16, 86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, Y.; Jiang, L.; Wang, F.; Yu, D. Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 2013, 25, 2907–2924. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Min, D.; Li, F.; Zhang, X.; Cui, X.; Shu, P.; Dong, L.; Ren, C. SlMYC2 involved in methyl Jasmonate-induced tomato fruit chilling tolerance. J. Agric. Food Chem. 2018, 66, 3110–3117. [Google Scholar] [CrossRef]
- Zhao, M.; Liu, W.; Xia, X.; Wang, T.; Zhang, W.H. Cold acclimation-induced freezing tolerance of Medicago truncatula seedlings is negatively regulated by ethylene. Physiol. Plant 2014, 152, 115–129. [Google Scholar] [CrossRef]
- Shi, Y.; Tian, S.; Hou, L.; Huang, X.; Zhang, X.; Guo, H.; Yang, S. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 2012, 24, 2578–2595. [Google Scholar] [CrossRef] [Green Version]
- Jiang, B.; Shi, Y.; Zhang, X.; Xin, X.; Qi, L.; Guo, H.; Li, J.; Yang, S. PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA 2017, 114, 6695–6702. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Huang, R. Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol. Biol. 2010, 73, 241–249. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Y.; Jiao, C.; Sun, H.; Rosli, H.G.; Pombo, M.A.; Zhang, P.; Banf, M.; Dai, X.; Martin, G.B.; Giovannoni, J.J. iTAK: A Program for Genome-wide Prediction and Classification of Plant Transcription Factors, Transcriptional Regulators, and Protein Kinases. Mol. Plant 2016, 9, 1667–1670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, C.S.; Chen, Y.C.; Lu, C.H.; Hwang, J.K. Prediction of protein subcellular localization. Proteins 2006, 64, 643–651. [Google Scholar] [CrossRef] [PubMed]
- Florea, L.; Song, L.; Salzberg, S.L. Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues. F1000Research 2013, 2, 188. [Google Scholar] [CrossRef]
- Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M.; Davis, A.P.; Dolinski, K.; Dwight, S.S.; Eppig, J.T.; et al. Gene ontology: Tool for the unification of biology. The gene ontology consortium. Nat. Genet. 2000, 25, 25–29. [Google Scholar] [CrossRef] [Green Version]
- Szklarczyk, D.; Gable, A.L.; Lyon, D.; Junge, A.; Wyder, S.; Huerta-Cepas, J.; Simonovic, M.; Doncheva, N.T.; Morris, J.H.; Bork, P.; et al. STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019, 47, 607–613. [Google Scholar] [CrossRef] [Green Version]
- Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498–2504. [Google Scholar] [CrossRef]
Serial Number | TF Family | Number of Genes | Serial Number | TF Family | Number of Genes | Serial Number | TF Family | Number of Genes |
---|---|---|---|---|---|---|---|---|
1 | bHLH | 144 | 30 | MIKC_MADS | 29 | 59 | PLATZ | 9 |
2 | C2H2 | 129 | 31 | TCP | 23 | 60 | SRS | 9 |
3 | MYB-related | 95 | 32 | IWS1 | 22 | 61 | LSD | 8 |
4 | WRKY | 95 | 33 | Tify | 22 | 62 | SWI3 | 8 |
5 | MYB | 92 | 34 | LOB | 21 | 63 | WOX | 8 |
6 | C3H | 86 | 35 | BAF60b | 20 | 64 | AP2 | 6 |
7 | ERF | 79 | 36 | ARID | 18 | 65 | Coactivator p15 | 6 |
8 | bZIP | 74 | 37 | RWP-RK | 18 | 66 | DBB | 6 |
9 | NAC | 73 | 38 | HB-other | 17 | 67 | GeBP | 6 |
10 | SET | 73 | 39 | CO-like | 16 | 68 | LIM | 6 |
11 | SNF2 | 72 | 40 | NF-YA | 16 | 69 | ZF-HD | 6 |
12 | HD-ZIP | 67 | 41 | TUB | 16 | 70 | MBF1 | 5 |
13 | G2-like | 58 | 42 | NF-YC | 15 | 71 | DBP | 4 |
14 | GNAT | 53 | 43 | HMG | 13 | 72 | EIL | 4 |
15 | PHD | 53 | 44 | M-type MADS | 13 | 73 | MED7 | 4 |
16 | FAR1 | 47 | 45 | Alfin-like | 12 | 74 | NF-X1 | 4 |
17 | ARF | 43 | 46 | CAMTA | 12 | 75 | Rcd1-like | 4 |
18 | B3 | 42 | 47 | E2F/DP | 12 | 76 | S1Fa-like | 4 |
19 | Trihelix | 42 | 48 | Pseudo ARR-B | 12 | 77 | VOZ | 4 |
20 | GRAS | 38 | 49 | ARR-B | 11 | 78 | Whirly | 4 |
21 | mTERF | 38 | 50 | BES1 | 11 | 79 | CSD | 3 |
22 | AUX/IAA | 37 | 51 | GRF | 11 | 80 | HB-PHD | 3 |
23 | Dof | 35 | 52 | LUG | 11 | 81 | OFP | 3 |
24 | HSF | 34 | 53 | TAZ | 11 | 82 | RAV | 3 |
25 | SBP | 33 | 54 | BBR-BPC | 10 | 83 | ULT | 3 |
26 | TALE | 33 | 55 | CPP | 10 | 84 | MED6 | 2 |
27 | TRAF | 33 | 56 | DDT | 10 | 85 | RB | 2 |
28 | GATA | 32 | 57 | YABBY | 10 | 86 | SOH1 | 2 |
29 | Jumonji | 29 | 58 | NF-YB | 9 | 87 | STAT | 2 |
Total | 2328 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Jiang, C.; Zhang, H.; Ren, J.; Dong, J.; Zhao, X.; Wang, X.; Wang, J.; Zhong, C.; Zhao, S.; Liu, X.; et al. Comparative Transcriptome-Based Mining and Expression Profiling of Transcription Factors Related to Cold Tolerance in Peanut. Int. J. Mol. Sci. 2020, 21, 1921. https://doi.org/10.3390/ijms21061921
Jiang C, Zhang H, Ren J, Dong J, Zhao X, Wang X, Wang J, Zhong C, Zhao S, Liu X, et al. Comparative Transcriptome-Based Mining and Expression Profiling of Transcription Factors Related to Cold Tolerance in Peanut. International Journal of Molecular Sciences. 2020; 21(6):1921. https://doi.org/10.3390/ijms21061921
Chicago/Turabian StyleJiang, Chunji, He Zhang, Jingyao Ren, Jiale Dong, Xinhua Zhao, Xiaoguang Wang, Jing Wang, Chao Zhong, Shuli Zhao, Xibo Liu, and et al. 2020. "Comparative Transcriptome-Based Mining and Expression Profiling of Transcription Factors Related to Cold Tolerance in Peanut" International Journal of Molecular Sciences 21, no. 6: 1921. https://doi.org/10.3390/ijms21061921