Genome-Wide Analysis of the TCP Transcription Factor Gene Family in Pepper (Capsicum annuum L.)
Abstract
:1. Introduction
2. Results
2.1. Identification and Characterization of TCP Family Members in Pepper
2.2. Phylogenetic Analysis and Classification of CaTCPs
2.3. Chromosomal Location and Synteny Evaluation of TCP Genes
2.4. Assessment of Gene Structures and Conserved Motifs, and Recognition Sequence of miR319
2.5. Genome-Wide Prediction of miRNA Targeting CaTCPs
2.6. GO Annotation and Enrichment Analysis of CaTCPs
2.7. Expression Profiling of CaTCPs in Different Organs and Development Stages
2.8. Expression Profiling Analysis of CaTCPs under Phytohormones and Abiotic Stress Conditions
2.9. Prediction of Interaction Network of CaTCPs
2.10. Three-Dimensional Structure Prediction of CaTCPs Protein
3. Discussion
3.1. Identification, Expansion, and Evolution of TCP Gene Family in Pepper
3.2. CaTCP Expression Pattern during Various Tissue Growth Stages
3.3. The Essential Role of TCPs in Shoot Branching
3.4. miRNA Participating in the Gene-Regulatory Mechanisms of Stress Response
4. Materials and Methods
4.1. Identification and Characterization Analysis of the TCP Genes in Pepper
4.2. Phylogenetics and Synteny Analysis of CaTCP Proteins
4.3. Gene Structure and Conserved Motif Analysis
4.4. Cis-Elements Analysis in CaTCP Promoters
4.5. Prediction of Putative miRNA Targeting CaTCPs and GO Annotation Analysis
4.6. Transcriptomic Data Analysis of the CaTCPs in Diverse Tissues, Abiotic, and Hormone Conditions
4.7. RNA Isolation and Quantitative RT-PCR
4.8. Prediction of Protein–Protein Interaction Network of CaTCPs
4.9. 3D Structure Prediction, Validation, and Visualization of CaTCP Proteins
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Hoang, X.L.T.; Nhi, D.N.H.; Thu, N.B.A.; Thao, N.P.; Tran, L.P. Transcription factors and their roles in signal transduction in plants under abiotic stresses. Curr. Genom. 2017, 18, 483–497. [Google Scholar] [CrossRef] [PubMed]
- Kosugi, S.; Ohashi, Y. DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J. 2002, 30, 337–348. [Google Scholar] [CrossRef]
- Adryan, B.; Teichmann, S.A. The developmental expression dynamics of Drosophila melanogaster transcription factors. Genome Biol. 2010, 11, R40. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Zeng, B.; Zhao, H.; Zhang, M.; Xie, S.; Lai, J. Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize. J. Integr. Plant Biol. 2012, 54, 616–630. [Google Scholar] [CrossRef]
- Doebley, J.; Stec, A.; Hubbard, L. The evolution of apical dominance in maize. Nature 1997, 386, 485–488. [Google Scholar] [CrossRef] [PubMed]
- Luo, D.; Carpenter, R.; Vincent, C.; Copsey, L.; Coen, E. Origin of floral asymmetry in Antirrhinum. Nature 1996, 383, 794–799. [Google Scholar] [CrossRef] [PubMed]
- Cubas, P.; Lauter, N.; Doebley, J.; Coen, E. The TCP domain: A motif found in proteins regulating plant growth and development. Plant J. 1999, 18, 215–222. [Google Scholar] [CrossRef]
- Kosugi, S.; Ohashi, Y. PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 1997, 9, 1607–1619. [Google Scholar]
- Navaud, O.; Dabos, P.; Carnus, E.; Tremousaygue, D.; Herve, C. TCP transcription factors predate the emergence of land plants. J. Mol. Evol. 2007, 65, 23–33. [Google Scholar] [CrossRef]
- Viola, I.L.; Reinheimer, R.; Ripoll, R.; Manassero, N.G.U.; Gonzalez, D.H. Determinants of the DNA binding specificity of class I and class II TCP transcription factors. J. Biol. Chem. 2012, 287, 347–356. [Google Scholar] [CrossRef]
- Martin-Trillo, M.; Cubas, P. TCP genes: A family snapshot ten years later. Trends Plant Sci. 2010, 15, 31–39. [Google Scholar] [CrossRef] [PubMed]
- Howarth, D.G.; Donoghue, M.J. Phylogenetic analysis of the “ECE” (CYC/TB1) clade reveals duplications predating the core eudicots. Proc. Natl. Acad. Sci. USA 2006, 103, 9101–9106. [Google Scholar] [CrossRef] [PubMed]
- Crawford, B.C.; Nath, U.; Carpenter, R.; Coen, E.S. CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol. 2004, 135, 244–253. [Google Scholar] [CrossRef] [PubMed]
- Tatematsu, K.; Nakabayashi, K.; Kamiya, Y.; Nambara, E. Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana. Plant J. 2008, 53, 42–52. [Google Scholar] [CrossRef] [PubMed]
- Braun, N.; de Saint Germain, A.; Pillot, J.P.; Boutet-Mercey, S.; Dalmais, M.; Antoniadi, I.; Li, X.; Maia-Grondard, A.; Le Signor, C.; Bouteiller, N.; et al. The pea TCP transcription factor PsBRC1 acts downstream of Strigolactones to control shoot branching. Plant Physiol. 2012, 158, 225–238. [Google Scholar] [CrossRef] [PubMed]
- Li, D.; Zhang, H.; Mou, M.; Chen, Y.; Xiang, S.; Chen, L.; Yu, D. Arabidopsis Class II TCP transcription factors integrate with the FT-FD Module to control flowering. Plant Physiol. 2019, 181, 97–111. [Google Scholar] [CrossRef] [PubMed]
- Kieffer, M.; Master, V.; Waites, R.; Davies, B. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J. 2011, 68, 147–158. [Google Scholar] [CrossRef]
- Palatnik, J.F.; Allen, E.; Wu, X.; Schommer, C.; Schwab, R.; Carrington, J.C.; Weigel, D. Control of leaf morphogenesis by microRNAs. Nature 2003, 425, 257–263. [Google Scholar] [CrossRef]
- Danisman, S.; van Dijk, A.D.; Bimbo, A.; van der Wal, F.; Hennig, L.; de Folter, S.; Angenent, G.C.; Immink, R.G. Analysis of functional redundancies within the Arabidopsis TCP transcription factor family. J. Exp. Bot. 2013, 64, 5673–5685. [Google Scholar] [CrossRef]
- Zhou, M.; Li, D.; Li, Z.; Hu, Q.; Yang, C.; Zhu, L.; Luo, H. Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol. 2013, 161, 1375–1391. [Google Scholar] [CrossRef]
- Lucero, L.E.; Uberti-Manassero, N.G.; Arce, A.L.; Colombatti, F.; Alemano, S.G.; Gonzalez, D.H. TCP15 modulates cytokinin and auxin responses during gynoecium development in Arabidopsis. Plant J. 2015, 84, 267–282. [Google Scholar] [CrossRef]
- Nicolas, M.; Cubas, P. TCP factors: New kids on the signaling block. Curr. Opin. Plant Biol. 2016, 33, 33–41. [Google Scholar] [CrossRef] [PubMed]
- Mukhopadhyay, P.; Tyagi, A.K. OsTCP19 influences developmental and abiotic stress signaling by modulating ABI4-mediated pathways. Sci. Rep. 2015, 5, 9998. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.T.; Sun, X.L.; Hoshino, Y.; Yu, Y.; Jia, B.; Sun, Z.W.; Sun, M.Z.; Duan, X.B.; Zhu, Y.M. MicroRNA319 positively regulates cold tolerance by targeting OsPCF6 and OsTCP21 in rice (Oryza sativa L.). PLoS ONE 2014, 9, e91357. [Google Scholar] [CrossRef] [PubMed]
- Yin, Z.; Li, Y.; Zhu, W.; Fu, X.; Han, X.; Wang, J.; Lin, H.; Ye, W. Identification, characterization, and expression patterns of TCP genes and microRNA319 in cotton. Int. J. Mol. Sci. 2018, 19, 3655. [Google Scholar] [CrossRef] [PubMed]
- Leng, X.; Wei, H.; Xu, X.; Ghuge, S.A.; Jia, D.; Liu, G.; Wang, Y.; Yuan, Y. Genome-wide identification and transcript analysis of TCP transcription factors in grapevine. BMC Genom. 2019, 20, 786. [Google Scholar] [CrossRef] [PubMed]
- Lei, N.; Yu, X.; Li, S.; Zeng, C.; Zou, L.; Liao, W.; Peng, M. Phylogeny and expression pattern analysis of TCP transcription factors in cassava seedlings exposed to cold and/or drought stress. Sci. Rep. 2017, 7, 10016. [Google Scholar] [CrossRef]
- Yao, X.; Ma, H.; Wang, J.; Zhang, D.B. Genome-wide comparative analysis and expression pattern of TCP gene families in Arabidopsis thaliana and Oryza sativa. J. Integr. Plant Biol. 2007, 49, 885–897. [Google Scholar] [CrossRef]
- Ma, J.; Wang, Q.; Sun, R.; Xie, F.; Jones, D.C.; Zhang, B. Genome-wide identification and expression analysis of TCP transcription factors in Gossypium raimondii. Sci. Rep. 2014, 4, 6645. [Google Scholar] [CrossRef]
- Parapunova, V.; Busscher, M.; Busscher-Lange, J.; Lammers, M.; Karlova, R.; Bovy, A.G.; Angenent, G.C.; de Maagd, R.A. Identification, cloning and characterization of the tomato TCP transcription factor family. BMC Plant Biol. 2014, 14, 157. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, N.; Li, T.; Yang, J.; Zhu, X.; Fang, C.; Li, S.; Si, H. Genome-wide identification and expression analysis of StTCP transcription factors of potato (Solanum tuberosum L.). Comput. Biol. Chem. 2019, 78, 53–63. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.; Park, M.; Yeom, S.I.; Kim, Y.M.; Lee, J.M.; Lee, H.A.; Seo, E.; Choi, J.; Cheong, K.; Kim, K.T.; et al. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 2014, 46, 270–278. [Google Scholar] [CrossRef] [PubMed]
- Ali, M.; Luo, D.X.; Khan, A.; Haq, S.U.; Gai, W.X.; Zhang, H.X.; Cheng, G.X.; Muhammad, I.; Gong, Z.H. Classification and genome-wide analysis of Chitin-Binding Proteins gene family in pepper (Capsicum annuum L.) and transcriptional regulation to phytophthora capsici, abiotic stresses and hormonal applications. Int. J. Mol. Sci. 2018, 19, 2216. [Google Scholar] [CrossRef] [PubMed]
- Diao, W.; Snyder, J.C.; Wang, S.; Liu, J.; Pan, B.; Guo, G.; Ge, W.; Dawood, M. Genome-wide analyses of the NAC transcription factor gene family in pepper (Capsicum annuum L.): Chromosome location, phylogeny, structure, expression patterns, cis-elements in the promoter, and interaction network. Int. J. Mol. Sci. 2018, 19, 1028. [Google Scholar] [CrossRef] [PubMed]
- Qin, C.; Yu, C.; Shen, Y.; Fang, X.; Chen, L.; Min, J.; Cheng, J.; Zhao, S.; Xu, M.; Luo, Y.; et al. Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc. Natl. Acad. Sci. USA 2014, 111, 5135–5140. [Google Scholar] [CrossRef] [PubMed]
- Bailey, T.L.; Johnson, J.; Grant, C.E.; Noble, W.S. The MEME Suite. Nucleic Acids Res. 2015, 43, W39–W49. [Google Scholar] [CrossRef] [PubMed]
- Seeliger, D.; de Groot, B.L. Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J. Comput. Aided Mol. Des. 2010, 24, 417–422. [Google Scholar] [CrossRef] [PubMed]
- Aguilar-Martinez, J.A.; Poza-Carrion, C.; Cubas, P. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 2007, 19, 458–472. [Google Scholar] [CrossRef]
- Nicolas, M.; Torres-Perez, R.; Wahl, V.; Cruz-Oro, E.; Rodriguez-Buey, M.L.; Zamarreno, A.M.; Martin-Jouve, B.; Garcia-Mina, J.M.; Oliveros, J.C.; Prat, S.; et al. Spatial control of potato tuberization by the TCP transcription factor BRANCHED1b. Nat. Plants 2022, 8, 281–294. [Google Scholar] [CrossRef]
- Liu, M.M.; Wang, M.M.; Yang, J.; Wen, J.; Guo, P.C.; Wu, Y.W.; Ke, Y.Z.; Li, P.F.; Li, J.N.; Du, H. Evolutionary and comparative expression analyses of TCP transcription factor gene family in land plants. Int. J. Mol. Sci. 2019, 20, 3591. [Google Scholar] [CrossRef]
- Cusack, B.P.; Wolfe, K.H. Not born equal: Increased rate asymmetry in relocated and retrotransposed rodent gene duplicates. Mol. Biol. Evol. 2007, 24, 679–686. [Google Scholar] [CrossRef] [PubMed]
- Freeling, M. Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 2009, 60, 433–453. [Google Scholar] [CrossRef] [PubMed]
- Tomato Genome, C. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485, 635–641. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wang, X.; Paterson, A.H. Genome and gene duplications and gene expression divergence: A view from plants. Ann. N. Y. Acad. Sci. 2012, 1256, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Jeifetz, D.; David-Schwartz, R.; Borovsky, Y.; Paran, I. CaBLIND regulates axillary meristem initiation and transition to flowering in pepper. Planta 2011, 234, 1227–1236. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Chen, Y.Q.; Ding, A.M.; Chen, H.; Xia, F.; Wang, W.F.; Sun, Y.H. Genome-wide analysis of TCP family in tobacco. Genet. Mol. Res. 2016, 15, 10–4238. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Guan, X.; Liu, S.; Yang, M.; Ren, J.; Guo, M.; Huang, Z.; Zhang, Y. Genome-wide identification and analysis of TCP transcription factors involved in the formation of leafy head in Chinese cabbage. Int. J. Mol. Sci. 2018, 19, 847. [Google Scholar] [CrossRef]
- Liu, Z.; Yang, J.; Li, S.; Liu, L.; Qanmber, G.; Chen, G.; Duan, Z.; Zhao, N.; Wang, G. Systematic characterization of TCP gene family in four cotton species revealed that GhTCP62 regulates branching in Arabidopsis. Biology 2021, 10, 1104. [Google Scholar] [CrossRef]
- Martin-Trillo, M.; Grandio, E.G.; Serra, F.; Marcel, F.; Rodriguez-Buey, M.L.; Schmitz, G.; Theres, K.; Bendahmane, A.; Dopazo, H.; Cubas, P. Role of tomato BRANCHED1-like genes in the control of shoot branching. Plant J. 2011, 67, 701–714. [Google Scholar] [CrossRef]
- Jones-Rhoades, M.W.; Bartel, D.P.; Bartel, B. MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 2006, 57, 19–53. [Google Scholar] [CrossRef]
- Kozomara, A.; Griffiths-Jones, S. miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014, 42, D68–D73. [Google Scholar] [CrossRef] [PubMed]
- Shriram, V.; Kumar, V.; Devarumath, R.M.; Khare, T.S.; Wani, S.H. MicroRNAs as potential targets for abiotic stress tolerance in plants. Front. Plant Sci. 2016, 7, 817. [Google Scholar] [CrossRef] [PubMed]
- Michlewski, G.; Caceres, J.F. Post-transcriptional control of miRNA biogenesis. RNA 2019, 25, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Hwang, D.G.; Park, J.H.; Lim, J.Y.; Kim, D.; Choi, Y.; Kim, S.; Reeves, G.; Yeom, S.I.; Lee, J.S.; Park, M.; et al. The hot pepper (Capsicum annuum) microRNA transcriptome reveals novel and conserved targets: A foundation for understanding MicroRNA functional roles in hot pepper. PLoS ONE 2013, 8, e64238. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.S.; Lee, D.Y.; Cho, L.H.; An, G. Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice 2014, 7, 31. [Google Scholar] [CrossRef] [PubMed]
- Huo, H.; Wei, S.; Bradford, K.J. DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc. Natl. Acad. Sci. USA 2016, 113, E2199–E2206. [Google Scholar] [CrossRef] [PubMed]
- Sarvepalli, K.; Nath, U. Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J. 2011, 67, 595–607. [Google Scholar] [CrossRef] [PubMed]
- Koyama, T.; Sato, F.; Ohme-Takagi, M. Roles of miR319 and TCP transcription factors in leaf development. Plant Physiol. 2017, 175, 874–885. [Google Scholar] [CrossRef]
- Guo, C.; Xu, Y.; Shi, M.; Lai, Y.; Wu, X.; Wang, H.; Zhu, Z.; Poethig, R.S.; Wu, G. Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in Arabidopsis. Plant Cell 2017, 29, 1293–1304. [Google Scholar] [CrossRef]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant. 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dong, Z.; Hao, Y.; Zhao, Y.; Tang, W.; Wang, X.; Li, J.; Wang, L.; Hu, Y.; Guan, X.; Gu, F.; et al. Genome-Wide Analysis of the TCP Transcription Factor Gene Family in Pepper (Capsicum annuum L.). Plants 2024, 13, 641. https://doi.org/10.3390/plants13050641
Dong Z, Hao Y, Zhao Y, Tang W, Wang X, Li J, Wang L, Hu Y, Guan X, Gu F, et al. Genome-Wide Analysis of the TCP Transcription Factor Gene Family in Pepper (Capsicum annuum L.). Plants. 2024; 13(5):641. https://doi.org/10.3390/plants13050641
Chicago/Turabian StyleDong, Zeyu, Yupeng Hao, Yongyan Zhao, Wenchen Tang, Xueqiang Wang, Jun Li, Luyao Wang, Yan Hu, Xueying Guan, Fenglin Gu, and et al. 2024. "Genome-Wide Analysis of the TCP Transcription Factor Gene Family in Pepper (Capsicum annuum L.)" Plants 13, no. 5: 641. https://doi.org/10.3390/plants13050641