Skip to main content
SpringerLink
Log in

Identification of a consensus DNA-binding site for the TCP domain transcription factor TCP2 and its important roles in the growth and development of Arabidopsis

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

TEOSINTE BRANCHED 1/CYCLOIDEA/PROLIFERATING CELL FACTOR 1 (TCP) transcription factors control multiple aspects of growth and development in various plant species. However, few genes were reported to be directly targeted and regulated by them through their specific binding sites, and then uncover their functions in plants. A consensus DNA-binding site motif of TCP2 was identified by random binding site selection (RBSS). DNA recognized by TCP2 contained the motif G(G/T)GGNCC(A/C), which showed high consistency with motifs bound by other TCP domain proteins. Consequently, this motif was regarded as the specific DNA-binding sites of TCP2. Circadian clock associated 1 (CCA1) and EARLY FLOWERING 3 (ELF3) were subsequently considered as potential target genes owing to the containing of the similar TCP2 binding sites or core binding sites GGNCC and found to be positively regulated by TCP2 via DNA binding. Phenotype analysis results showed that mutation and over-expression of TCP2 resulted in variations in leaf morphogenesis, especially the double or triple mutations of TCP2, 4 and 10. Mutations in TCPs caused late flowering. Finally, TCP2 was shown to influence hypocotyl elongation by mediating the jasmonate signaling pathway. Overall, these results provide a basis for future studies aimed at distinguishing the target genes of TCP2 and elucidating the important roles of TCP2 in plant growth and development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig.2
Fig. 3
Fig.4
Fig.5

Similar content being viewed by others

Data availability

All data are fully available without restriction.

Abbreviations

TCP2:

Teosinte branched 1, cycloidea and PCF transcription factor 2

RBSS:

Random binding site selection

CCA1 :

Circadian clock associated 1

ELF3 :

Early flowering 3

bHLH:

Basic helix-loop-helix

ECE:

Glutamate-cysteine-glutamate

CYC:

Cycloidea

CRY1 :

Cryptochrome 1

Gly:

Glycine

Asp:

Aspartate

Thr:

Threonine

CDT1a :

Homolog of yeast CDT1 A

CDT1b :

Homolog of yeast CDT1 B

PIF4 :

Phytochrome-interacting factor4

ABAP1:

Armadillo btb protein 1

JA:

Jasmonic acid

BRC1 :

Branched 1

CHE :

CCA1 hiking expedition

TOC1 :

Timing of cab expression 1

ChIP:

Chromatin immunoprecipitation

References

  1. Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30(337):348. https://doi.org/10.1046/j.1365-313X.2002.01294.x

    Article  Google Scholar 

  2. Howarth DG, Donoghue MJ (2006) Phylogenetic analysis of the “ECE” (CYC/TB1) clade reveals duplications predating the core eudicots. Proc Natl Acad Sci USA 103:9101–9106. https://doi.org/10.1073/pnas.0910155107

    Article  PubMed  Google Scholar 

  3. Li S (2015) The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. Plant Signal Behav 10:e1044192. https://doi.org/10.1080/15592324.2015.1044192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Welchen E, Gonzalez DH (2006) Overrepresentation of elements recognized by TCP-domain transcription factors in the upstream regions of nuclear genes encoding components of the mitochondrial oxidative phosphorylation machinery. Plant Physiol 141:540–545. https://doi.org/10.1104/pp.105.075366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Herve C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, Lacout F, Tremousaygue D (2009) In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol 149:1462–1477. https://doi.org/10.2307/40537729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230. https://doi.org/10.1371/journal.pbio.0060230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Aggarwal P, Das Gupta M, Joseph AP, Chatterjee N, Srinivasan N, Nath U (2010) Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell 22:1174–1189. https://doi.org/10.1105/tpc.109.066647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Martin-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15(1):31–39. https://doi.org/10.1016/j.tplants.2009.11.003

    Article  CAS  PubMed  Google Scholar 

  9. Costa MM, Fox S, Hanna AI, Baxter C, Coen E (2005) Evolution of regulatory interactions controlling floral asymmetry. Development 132:5093–5101. https://doi.org/10.1242/dev.02085

    Article  CAS  PubMed  Google Scholar 

  10. Viola IL, Reinheimer R, Ripoll R, Manassero NG, Gonzalez DH (2012) Determinants of the DNA binding specificity of class I and class II TCP transcription factors. J Biol Chem 287:347–356. https://doi.org/10.1074/jbc.M111.256271

    Article  CAS  PubMed  Google Scholar 

  11. Viola IL, Manassero NGU, Ripoll R, Gonzalez DH (2011) 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 435:143–155. https://doi.org/10.1042/BJ20101019

    Article  CAS  PubMed  Google Scholar 

  12. Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102:12978–12983. https://doi.org/10.1073/pnas.0504039102

    Article  CAS  PubMed  Google Scholar 

  13. Tremousaygue D, Garnier L, Bardet C, Dabos P, Herve C, Lescure B (2003) Internal telomeric repeats and ‘TCP domain’ protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant J 33:957–966. https://doi.org/10.1046/j.1365-313X.2003.01682.x

    Article  CAS  PubMed  Google Scholar 

  14. Koyama T, Sato F, Ohme-Takagi M (2017) Roles of miR319 and TCP transcription factors in leaf development. Plant Physiol 175:874–885. https://doi.org/10.1104/pp.17.00732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C (2018) Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol 176:1694–1708. https://doi.org/10.1104/pp.17.00823

    Article  CAS  PubMed  Google Scholar 

  16. Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk AD, Muino JM, Cutri L, Dornelas MC, Angenent GC, Immink RG (2012) Arabidopsis class I and class II TCP transcription factors regulate jasmonic acid metabolism and leaf development antagonistically. Plant Physiol 159:1511–1523. https://doi.org/10.1104/pp.112.200303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zhou Y, Xun Q, Zhang D, Lv M, Ou Y, Li J (2019) TCP transcription factors associate with PHYTOCHROME INTERACTING FACTOR 4 and CRYPTOCHROME 1 to regulate thermomorphogenesis in Arabidopsis thaliana. iScience 15:600–610. https://doi.org/10.1016/j.isci.2019.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. He Z, Zhao X, Kong F, Zuo Z, Liu X (2016) TCP2 positively regulates HY5/HYH and photomorphogenesis in Arabidopsis. J Exp Bot 67:775–785. https://doi.org/10.1093/jxb/erv495

    Article  CAS  PubMed  Google Scholar 

  19. Koyama T, Furutani M, Tasaka M, Ohme-Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19:473–484. https://doi.org/10.1105/tpc.106.044792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Masuda HP, Cabral LM, De Veylder L, Tanurdzic M, de AlmeidaEngler J, Geelen D, Inze D, Martienssen RA, Ferreira PC, Hemerly AS (2008) ABAP1 is a novel plant armadillo BTB protein involved in DNA replication and transcription. EMBO J 27:2746–2756. https://doi.org/10.1038/emboj.2008.191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Liu S, Mi X, Zhang R, An Y, Zhou Q, Yang T, Xia X, Guo R, Wang X, Wei C (2019) Integrated analysis of miRNAs and their targets reveals that miR319c/TCP2 regulates apical bud burst in tea plant (Camellia sinensis). Planta 250:1111–1129. https://doi.org/10.1007/s00425-019-03207-1

    Article  CAS  PubMed  Google Scholar 

  22. Hao J, Tu L, Hu H, Tan J, Deng F, Tang W, Nie Y, Zhang X (2012) GbTCP, a cotton TCP transcription factor, confers fibre elongation and root hair development by a complex regulating system. J Exp Bot 63:6267–6281. https://doi.org/10.1093/jxb/ers278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ma J, Liu F, Wang Q, Wang K, Jones DC, Zhang B (2016) Comprehensive analysis of TCP transcription factors and their expression during cotton (Gossypium arboreum) fiber early development. Sci Rep 6:21535. https://doi.org/10.1038/srep21535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wu JF, Tsai HL, Joanito I, Wu YC, Chang CW, Li YH, Wang Y, Hong JC, Chu JW, Hsu CP, Wu SH (2016) LWD-TCP complex activates the morning gene CCA1 in Arabidopsis. Nat Commun 7:13181. https://doi.org/10.1038/ncomms13181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Niwa M, Daimon Y, Kurotani K, Higo A, Pruneda-Paz JL, Breton G, Mitsuda N, Kay SA, Ohme-Takagi M, Endo M, Araki T (2013) BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25:1228–1242. https://doi.org/10.1105/tpc.112.109090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lucero LE, Manavella PA, Gras DE, Ariel FD, Gonzalez DH (2017) Class I and Class II TCP transcription factors modulate SOC1-dependent flowering at multiple levels. Mol Plant 10:1571–1574. https://doi.org/10.1016/j.molp.2017.09.001

    Article  CAS  PubMed  Google Scholar 

  27. Liu J, Cheng X, Liu P, Li D, Chen T, Gu X, Sun J, Lenhard M (2017) MicroRNA319-regulated TCPs interact with FBHs and PFT1 to activate CO transcription and control flowering time in Arabidopsis. PLoS Genet 13:e1006833. https://doi.org/10.1371/journal.pgen.1006833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kubota A, Ito S, Shim JS, Johnson RS, Imaizumi T (2017) TCP4-dependent induction of CONSTANS transcription requires GIGANTEA in photoperiodic flowering in Arabidopsis. PLoS Genet 13:e1006856. https://doi.org/10.1371/journal.pgen.1006856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Van Es SW, van der Auweraert EB, Silveira SR, Angenent GC, van Dijk ADJ, Immink RGH (2019) Comprehensive phenotyping reveals interactions and functions of Arabidopsis thaliana TCP genes in yield determination. Plant J 99:316–328. https://doi.org/10.1111/tpj.14326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Giraud E, Ng S, Carrie C, Duncan O, Low J, Lee CP, Van Aken O, Millar AH, Murcha M, Whelan J (2010) TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. Plant Cell 22:3921–3934. https://doi.org/10.1105/tpc.110.074518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pruneda-Paz JL, Breton G, Para A, Kay SA (2009) A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323:1481–1485. https://doi.org/10.1126/science.1167206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sugio A, MacLean AM, Hogenhout SA (2014) The small phytoplasma virulence effector SAP11 contains distinct domains required for nuclear targeting and CIN-TCP binding and destabilization. New Phytol 202:838–848. https://doi.org/10.1111/nph.12721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:e1003374. https://doi.org/10.1371/journal.pgen.1003374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Liu H, Yu X, Li K, Klejnot J, Yang H, Lisiero D, Lin C (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322:1535–1539. https://doi.org/10.1126/science.1163927

    Article  CAS  PubMed  Google Scholar 

  35. Edward Bruggemann Korie Handwerger Carrie Essex Gisela Storz (1996) Analysis of fast neutron-generated mutants at the Arabidopsis thaliana HY4 locus. Plant J 10:755–760. https://doi.org/10.1046/j.1365-313X.1996.10040755.x

    Article  Google Scholar 

  36. Harmoko R, Fanata WI, Duwi Y, Yong J, Ko KS, Rim YG, Uddin MN, Siswoyo TA, Lee SS, Kim DY, Lee SY (2013) RNA-dependent RNA polymerase 6 is required for efficient hpRNA-induced gene silencing in plants. Mol Cells 35:202–209. https://doi.org/10.1007/s10059-013-2203-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39:776–789. https://doi.org/10.1111/j.1365-313x.2004.02169.x

    Article  CAS  PubMed  Google Scholar 

  38. Kolmos E, Herrero E, Bujdoso N, Millar AJ, Tóth R, Gyula P, Nagy F, Davis SJ (2011) A reduced-function allele reveals that EARLY FLOWERING3 repressive action on the circadian clock is modulated by phytochrome signals in Arabidopsis. Plant Cell 23:3230–3246. https://doi.org/10.1105/tpc.111.088195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Litthauer S, Battle MW, Jones MA (2016) Phototropins do not alter accumulation of evening-phased circadian transcripts under blue light. Plant Signal Behav 11:e1126029. https://doi.org/10.1080/15592324.2015.1126029

    Article  CAS  PubMed  Google Scholar 

  40. Lu SX, Webb CJ, Knowles SM, Kim SH, Wang Z, Tobin EM (2012) CCA1 and ELF3 Interact in the control of hypocotyl length and flowering time in Arabidopsis. Plant Physiol 158:1079–1088. https://doi.org/10.1104/pp.111.189670

    Article  CAS  PubMed  Google Scholar 

  41. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM, Froehlich JE, Johnson BF, Kramer DM, Jander G, Sharkey TD, Howe GA (2016) Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570. https://doi.org/10.1038/ncomms12570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Guo Q, Major IT, Howe GA (2018) Resolution of growth-defense conflict: mechanistic insights from jasmonate signaling. Curr Opin Plant Biol 44:72–81. https://doi.org/10.1016/j.pbi.2018.02.009

    Article  CAS  PubMed  Google Scholar 

  43. Lucero LE, Uberti-Manassero NG, Arce AL, Colombatti F, Alemano SG, Gonzalez DH (2015) TCP15 modulates cytokinin and auxin responses during gynoecium development in Arabidopsis. Plant J 84:267–282. https://doi.org/10.1111/tpj.12992

    Article  CAS  PubMed  Google Scholar 

  44. Resentini F, Felipo-Benavent A, Colombo L, Blazquez MA, Alabadi D, Masiero S (2015) TCP14 and TCP15 mediate the promotion of seed germination by gibberellins in Arabidopsis thaliana. Mol Plant 8:482–485. https://doi.org/10.1016/j.molp.2014.11.018

    Article  CAS  PubMed  Google Scholar 

  45. Daviere JM, Wild M, Regnault T, Baumberger N, Eisler H, Genschik P, Achard P (2014) Class I TCP-DELLA interactions in inflorescence shoot apex determine plant height. Curr Biol 24:1923–1928. https://doi.org/10.1016/j.cub.2014.07.012

    Article  CAS  PubMed  Google Scholar 

  46. Challa KR, Rath M, Nath U (2019) The CIN-TCP transcription factors promote commitment to differentiation in Arabidopsis leaf pavement cells via both auxin-dependent and independent pathways. PLoS Genet 15:e1007988. https://doi.org/10.1371/journal.pgen.1007988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263. https://doi.org/10.1038/nature01958

    Article  CAS  Google Scholar 

  48. Tao Q, Guo D, Wei B, Zhang F, Pang C, Jiang H, Zhang J, Wei T, Gu H, Qu LJ, Qin G (2013) The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS- RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell 25:421–437. https://doi.org/10.1105/tpc.113.109223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Broholm SK, Tahtiharju S, Laitinen RA, Albert VA, Teeri TH, Elomaa P (2008) A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proc Natl Acad Sci USA 105:9117–9122. https://doi.org/10.1073/pnas.0801359105

    Article  PubMed  Google Scholar 

  50. Li D, Zhang H, Mou M, Chen Y, Xiang S, Chen L, Yu D (2019) Arabidopsis Class II TCP transcription factors integrate with the FT-FD module to control flowering. Plant Physiol 181:97–111. https://doi.org/10.1104/pp.19.00252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Detlef Weigel for tcp2, tcp2tcp4, and tcp2tcp4tcp10 seeds. The authors acknowledge the financial support was provided by Hunan Provincial Natural Science Foundation of China (Grant No. 2019JJ50692) and the National Natural Science Foundation of China (Grant No. 31902345).

Funding

This study was funded by grants from Hunan Provincial Natural Science Foundation of China (Grant No.2019JJ50692) and the National Natural Science Foundation of China (Grant No. 31902345).

Author information

Authors and Affiliations

  1. College of Biological and Environmental Engineering, Changsha University, Changsha, 410003, Hunan, China

    Zhimin He, Xiaomei Zhou, Jiamin Chen, Lingting Yin, Zihao Zeng & Jing Xiang

  2. College of Food Science and Technology, Hunan Agricultural University, Changsha, 410128, Hunan, China

    Suchun Liu

Authors
  1. Zhimin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaomei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiamin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lingting Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zihao Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jing Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Suchun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SL conceived the study and commented on the manuscript. ZH performed laboratory and data analyses. The first draft of the manuscript was written by ZH. XZ, JC, LY and ZZ participated in the data supplement and reviewing of the revised manuscript. JX commented on the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Zhimin He.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 518 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, Z., Zhou, X., Chen, J. et al. Identification of a consensus DNA-binding site for the TCP domain transcription factor TCP2 and its important roles in the growth and development of Arabidopsis. Mol Biol Rep 48, 2223–2233 (2021). https://doi.org/10.1007/s11033-021-06233-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06233-z

Keywords

Search

Navigation