Genome-Wide Identification and Characterization of the TCP Gene Family in Cucumber (Cucumis sativus L.) and Their Transcriptional Responses to Different Treatments
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials, Growth Conditions, and Treatment
2.2. Identification of TCP Genes in Cucumber
2.3. Phylogenetic Tree and Cis-Acting Elements Analysis
2.4. Analysis of Chromosomal Location and Collinearity Relationship and Prediction of miR319 Target Genes
2.5. Transcript Expression Analysis of TCP Genes
3. Results
3.1. Identification and Chromosomal Distributions Analysis of Putative TCP Genes in Cucumber
3.2. Phylogenetic Analysis and Classification Putative TCP Genes in Cucumber
3.3. TCP Gene Structures and Conserved Motifs
3.4. Collinearity Analysis of the Relationship among Cucumber, Melon (Cucumis melon) and Arabidopsis Members
3.5. Promotor Cis-Acting Element Analysis of Putative CsTCP Genes
3.6. Expression Profiles of Putative Cucumber TCP Genes in Different Tissues
3.7. Expression Analysis of CsTCPs during Flower Bud Development
3.8. Expression Analysis of CsTCPs Under Hormone Treatments and Environmental Stresses
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Meshi, T.; Iwabuchi, M. Plant Transcription Factors. Plant Cell Physiol. 1995, 36, 1405–1420. [Google Scholar] [PubMed]
- 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]
- 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] [PubMed] [Green Version]
- 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] [PubMed] [Green Version]
- Martin-Trillo, M.; Cubas, P. TCP genes: A family snapshot ten years later. Trends Plant Sci. 2010, 15, 31–39. [Google Scholar] [CrossRef]
- Howarth, D.; Donoghue, M. 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] [Green Version]
- Navaud, O.; Dabos, P.; Carnus, E.; Tremousaygue, D.; Hervé, C. TCP Transcription Factors Predate the Emergence of Land Plants. J. Mol. Evol. 2007, 65, 23–33. [Google Scholar] [CrossRef]
- Yao, X.; Ma, H.; Wang, J.; Zhang, D. 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]
- 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] [Green Version]
- 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] [PubMed] [Green Version]
- Lin, Y.F.; Chen, Y.Y.; Hsiao, Y.Y.; Shen, C.Y.; Hsu, J.L.; Yeh, C.M.; Mitsuda, N.; Ohme-Takagi, M.; Liu, Z.J.; Tsai, W.C. Genome-wide identification and characterization of TCP genes involved in ovule development of Phalaenopsis equestris. J. Exp. Bot. 2016, 67, 5051–5066. [Google Scholar] [CrossRef] [PubMed]
- Bresso, E.G.; Chorostecki, U.; Rodriguez, R.E.; Palatnik, J.F.; Schommer, C. Spatial Control of Gene Expression by miR319-Regulated TCP Transcription Factors in Leaf Development. Plant Physiol. 2018, 176, 1694–1708. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Xu, X.; Mo, X.; Zhong, L.; Zhang, J.; Mo, B.; Kuai, B. Overexpression of TCP8 delays Arabidopsis flowering through a FLOWERING LOCUS C-dependent pathway. BMC Plant Biol. 2019, 19, 534. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koyama, T.; Mitsuda, N.; Seki, M.; Shinozaki, K.; Ohme-Takagi, M. TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 2010, 22, 3574–3588. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, M.Y.; Zhao, P.M.; Cheng, H.Q.; Han, L.B.; Wu, X.M.; Gao, P.; Wang, H.Y.; Yang, C.L.; Zhong, N.Q.; Zuo, J.R.; et al. The cotton transcription factor TCP14 functions in auxin-mediated epidermal cell differentiation and elongation. Plant Physiol. 2013, 162, 1669–1680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ju, Y.; Guo, L.; Cai, Q.; Ma, F.; Zhu, Q.Y.; Zhang, Q.; Sodmergen. Arabidopsis JINGUBANG Is a Negative Regulator of Pollen Germination That Prevents Pollination in Moist Environments. Plant Cell 2016, 28, 2131–2146. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Cochet, F.; Ponnaiah, M.; Lebreton, S.; Matheron, L.; Pionneau, C.; Boudsocq, M.; Resentini, F.; Huguet, S.; Blázquez, M.Á.; et al. The MPK8-TCP14 pathway promotes seed germination in Arabidopsis. Plant J. 2019, 100, 677–692. [Google Scholar] [CrossRef]
- 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]
- 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] [Green Version]
- Gastaldi, V.; Lucero, L.E.; Ferrero, L.V.; Ariel, F.D.; Gonzalez, D.H. Class-I TCP Transcription Factors Activate the SAUR63 Gene Subfamily in Gibberellin-Dependent Stamen Filament Elongation. Plant Physiol. 2020, 182, 2096–2110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, Y.; Zhang, D.; Li, J. TCP1 Modulates DWF4 Expression via Directly Interacting with the GGNCCC Motifs in the Promoter Region of DWF4 in Arabidopsis thaliana. J. Genet. Genom. 2015, 42, 383–392. [Google Scholar] [CrossRef] [PubMed]
- Van Es, S.W.; Silveira, S.R.; Rocha, D.I.; Bimbo, A.; Martinelli, A.P.; Dornelas, M.C.; Angenent, G.C.; Immink, R.G.H. Novel functions of the Arabidopsis transcription factor TCP5 in petal development and ethylene biosynthesis. Plant J. 2018, 94, 867–879. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, J.F.; Tsai, H.L.; Joanito, I.; Wu, Y.C.; Chang, C.W.; Li, Y.H.; Wang, Y.; Hong, J.C.; Chu, J.W.; Hsu, C.P.; et al. LWD-TCP complex activates the morning gene CCA1 in Arabidopsis. Nat. Commun. 2016, 7, 13181. [Google Scholar] [CrossRef] [Green Version]
- Mohammadi, A.; Omid, M. Economical analysis and relation between energy inputs and yield of greenhouse cucumber production in Iran. Appl. Energy 2010, 87, 191–196. [Google Scholar] [CrossRef]
- Malepszy, S.; Niemirowicz-Szczytt, K. Sex determination in cucumber (Cucumis sativus) as a model system for molecular biology. Plant Sci. 1991, 80, 39–47. [Google Scholar] [CrossRef]
- Wang, S.; Yang, X.; Xu, M.; Lin, X.; Lin, T.; Qi, J.; Shao, G. A Rare SNP Identified a TCP Transcription Factor Essential for Tendril Development in Cucumber. Mol. Plant 2015, 8, 1795–1808. [Google Scholar] [CrossRef] [Green Version]
- Yang, X.; Yan, J.; Zhang, Z.; Lin, T.; Xin, T.; Wang, B.; Wang, S.; Zhao, J.; Zhang, Z.; Lucas, W.J.; et al. Regulation of plant architecture by a new histone acetyltransferase targeting gene bodies. Nat. Plants 2020, 6, 809–822. [Google Scholar] [CrossRef]
- Shen, J.; Zhang, Y.; Ge, D.; Wang, Z.; Song, W.; Gu, R.; Che, G.; Cheng, Z.; Liu, R.; Zhang, X. CsBRC1 inhibits axillary bud outgrowth by directly repressing the auxin efflux carrierCsPIN3 in cucumber. Proc. Natl. Acad. Sci. USA 2019, 116, 17105–17114. [Google Scholar] [CrossRef] [Green Version]
- Yuan, W.; Gu, Z.; Chu, W.; Ye, L.; Yang, G. Identification and structure analysis of TCP transcription factors in Cucumber. Mol. Plant Breed. 2014, 12, 287–295. (In Chinese) [Google Scholar]
- Chen, C.; Xia, R.; Chen, H.; He, Y. TBtools, a Toolkit for Biologists integrating various HTS-data handling tools with a user-friendly interface. bioRxiv 2018, 289660. [Google Scholar]
- Letunic, I.; Bork, P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2017, 46, D493–D496. [Google Scholar] [CrossRef] [PubMed]
- El-Gebali, S.; Mistry, J.; Bateman, A.; Eddy, S.R.; Luciani, A.; Potter, S.C.; Qureshi, M.; Richardson, L.J.; Salazar, G.A.; Smart, A.; et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2018, 47, D427–D432. [Google Scholar] [CrossRef] [PubMed]
- Subramanian, B.; Gao, S.; Lercher, M.J.; Hu, S.; Chen, W.-H. Evolview v3: A webserver for visualization, annotation, and management of phylogenetic trees. Nucleic Acids Res. 2019, 47, W270–W275. [Google Scholar] [CrossRef] [PubMed]
- Bailey, T.L.; Boden, M.; Buske, F.A.; Frith, M.; Grant, C.E.; Clementi, L.; Ren, J.; Li, W.W.; Noble, W.S. MEME Suite: Tools for motif discovery and searching. Nucleic Acids Res. 2009, 37, W202–W208. [Google Scholar] [CrossRef]
- Wang, Y.; Tang, H.; Debarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.-H.; Jin, H.; Marler, B.; Guo, H.; et al. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012, 40, e49. [Google Scholar] [CrossRef] [Green Version]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Ma, X.; Ma, J.; Fan, D.; Li, C.; Jiang, Y.; Luo, K. Genome-wide Identification of TCP Family Transcription Factors from Populus euphratica and Their Involvement in Leaf Shape Regulation. Sci. Rep. 2016, 6, 32795. [Google Scholar] [CrossRef]
- Zhou, Y.; Xu, Z.; Zhao, K.; Yang, W.; Cheng, T.; Wang, J.; Zhang, Q. Genome-Wide Identification, Characterization and Expression Analysis of the TCP Gene Family in Prunus mume. Front. Plant Sci. 2016, 7, 1301. [Google Scholar] [CrossRef] [Green Version]
- Huang, S.; Li, R.; Zhang, Z.; Li, L.; Gu, X.; Fan, W.; Lucas, W.J.; Wang, X.; Xie, B.; Ni, P.; et al. The genome of the cucumber, Cucumis sativus L. Nat. Genet. 2009, 41, 1275–1281. [Google Scholar] [CrossRef] [Green Version]
- Bai, S.L.; Peng, Y.B.; Cui, J.X.; Gu, H.T.; Xu, L.Y.; Li, Y.Q.; Xu, Z.H.; Bai, S.N. Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L.). Planta 2004, 220, 230–240. [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, gmr.15027728. [Google Scholar] [CrossRef]
- Murray, J.; Viola, I.L.; Gonzalez, D.H.; Alem, A.L.; Ariel, F.D.; Arce, A.L.; Camoirano, A. Class I TCP transcription factors regulate trichome branching and cuticle development in Arabidopsis. J. Exp. Bot. 2020, 71, 5438–5453. [Google Scholar]
- 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] [PubMed] [Green Version]
- Koyama, T.; Sato, F.; Ohme-Takagi, M. A role of TCP1 in the longitudinal elongation of leaves in Arabidopsis. Biosci. Biotechnol. Biochem. 2010, 74, 2145–2147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, T.; Qu, Y.; Wang, H.; Wang, J.; Song, A.; Hu, Y.; Chen, S.; Jiang, J.; Chen, F. The heterologous expression of a chrysanthemum TCP-P transcription factor CmTCP14 suppresses organ size and delays senescence in Arabidopsis thaliana. Plant Physiol. Biochem. 2017, 115, 239–248. [Google Scholar] [CrossRef]
- Takeda, T.; Amano, K.; Ohto, M.-a.; Nakamura, K.; Sato, S.; Kato, T.; Tabata, S.; Ueguchi, C. RNA interference of the Arabidopsis putative transcription factor TCP16 gene results in abortion of early pollen development. Plant Mol. Biol. 2006, 61, 165–177. [Google Scholar] [CrossRef]
- Viola, I.L.; Manassero, N.G.U.; Ripoll, R.; Gonzalez, D.H. The Arabidopsis class I TCP transcription factor AtTCP11 is a developmental regulator with distinct DNA-binding properties due to the presence of a threonine residue at position 15 of the TCP domain. Biochem. J. 2011, 435, 143–155. [Google Scholar] [CrossRef] [Green Version]
- Katyayini, N.U.; Rinne, P.L.; Tarkowská, D.; Strnad, M.; van der Schoot, C. Dual Role of Gibberellin in Perennial Shoot Branching: Inhibition and Activation. Front. Plant Sci. 2020, 11, 736. [Google Scholar] [CrossRef]
- Wang, D.H.; Li, F.; Duan, Q.H.; Han, T.; Xu, Z.H.; Bai, S.N. Ethylene perception is involved in female cucumber flower development. Plant J. 2010, 61, 862–872. [Google Scholar] [CrossRef]
- Drummond, R.S.; Janssen, B.J.; Luo, Z.; Oplaat, C.; Ledger, S.E.; Wohlers, M.W.; Snowden, K.C. Environmental control of branching in petunia. Plant Physiol. 2015, 168, 735–751. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rameau, C.; Bertheloot, J.; Leduc, N.; Andrieu, B.; Foucher, F.; Sakr, S. Multiple pathways regulate shoot branching. Front. Plant Sci. 2014, 5, 741. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 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
Wen, H.; Chen, Y.; Du, H.; Zhang, L.; Zhang, K.; He, H.; Pan, J.; Cai, R.; Wang, G. Genome-Wide Identification and Characterization of the TCP Gene Family in Cucumber (Cucumis sativus L.) and Their Transcriptional Responses to Different Treatments. Genes 2020, 11, 1379. https://doi.org/10.3390/genes11111379
Wen H, Chen Y, Du H, Zhang L, Zhang K, He H, Pan J, Cai R, Wang G. Genome-Wide Identification and Characterization of the TCP Gene Family in Cucumber (Cucumis sativus L.) and Their Transcriptional Responses to Different Treatments. Genes. 2020; 11(11):1379. https://doi.org/10.3390/genes11111379
Chicago/Turabian StyleWen, Haifan, Yue Chen, Hui Du, Leyu Zhang, Keyan Zhang, Huanle He, Junsong Pan, Run Cai, and Gang Wang. 2020. "Genome-Wide Identification and Characterization of the TCP Gene Family in Cucumber (Cucumis sativus L.) and Their Transcriptional Responses to Different Treatments" Genes 11, no. 11: 1379. https://doi.org/10.3390/genes11111379