AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home The Crop Journal Article
PDF (588.6 KB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Review | Open Access

CCT family genes in cereal crops: A current overview

Yipu Li, Mingliang Xu( )
National Maize Improvement Center of China, China Agricultural University, Beijing 100193, China
Show Author Information

Abstract

Control of flowering time is crucial for reproductive success of cereal crops, and has a significant impact on grain yield as well as adaptation to diverse environmental conditions. Plants integrate signals from both environmental cues and endogenous regulatory pathways to fine-tune flowering time. The CCT domain originally described to a 43-amino acid sequence at the C-terminus of three Arabidopsis proteins, namely CONSTANS (CO), CO-LIKE, and TIMING OF CAB1 (TOC1). The CCT domain-containing genes (CCT genes), which encode transcription co-factors, are the major genetic determinants that modulate flowering time, and this in turn enables plants to effectively expand their territory to take advantage of favorable habitats. Moreover, certain CCT genes have pleiotropic effects on morphological traits and confer resistance/tolerance to biotic/abiotic stresses. CCT genes can be classified into three families, namely COL (CONSTANS-like), PRR (Pseudo-response regulator), and CMF (CCT motif family), based on their non-CCT domains. During domestication, natural and artificial selection resulted in reduced nucleotide diversity of CCT genes in modern cultivated cereals than their wild types. Here, we review the features and functions of CCT genes in cereal crops and propose future research to focus on CCT genes and their utilization in crop breeding.

Keywords

PhotoperiodFlowering timeCCT domainPleiotropy

References

[1]

J.S. Jeon, K.H. Jung, H.B. Kim, J.P. Suh, G.S. Khush, Genetic and molecular insights into the enhancement of rice yield potential, J. Plant Biol. 54 (2011) 1-9.
Crossref Google Scholar
[2]

J. Colasanti, V. Coneva, Mechanisms of floral induction in grasses: something borrowed, something new, Plant Physiol. 149 (2009) 56-62.
Crossref Google Scholar
[3]

F. Andrés, G. Coupland, The genetic basis of flowering responses to seasonal cues, Nat. Rev. Genet. 13 (2012) 627-639.
Crossref Google Scholar
[4]

J. Putterill, F. Robson, K. Lee, R. Simon, G. Coupland, The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors, Cell 80 (1995) 847-857.
Crossref Google Scholar
[5]

F. Robson, M.M.R. Costa, S.R. Hepworth, I. Vizir, P.H. Reeves, J. Putterill, G. Coupland, Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants, Plant J. 28 (2001) 619-631.
Crossref Google Scholar
[6]

S. Wenkel, F. Turck, K. Singer, L. Gissot, J. Le Gourrierec, A. Samach, G. Coupland, CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis, Plant Cell 18 (2006) 2971-2984.
Crossref Google Scholar
[7]

W.Y. Xue, Y.Z. Xing, X.Y. Weng, Y. Zhao, W.J. Tang, L. Wang, H.J. Zhou, S.B. Yu, C.G. Xu, X.H. Li, Q.F. Zhang, Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice, Nat. Genet. 40 (2008) 761-767.
Crossref Google Scholar
[8]

Y. Qin, Z. Li, W.Q. Li, L.X. Ku, C. Wang, J.R. Ye, K. Li, N. Yang, Y.P. Li, T. Zhong, J.S. Li, Y.H. Chen, J.B. Yan, X.H. Yang, M.L. Xu, CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize, Proc. Natl. Acad. Sci. U. S. A. 110 (2013) 16969-16974.
Crossref Google Scholar
[9]

J. Cockram, T. Thiel, B. Steuernagel, N. Stein, S. Taudien, P.C. Bailey, D.M. O'Sullivan, Genome dynamics explain the evolution of flowering time CCT domain gene families in the Poaceae, PLoS One 7 (2012) e45307.
Crossref Google Scholar
[10]

S.B. Tiwari, Y. Shen, H.C. Chang, Y. Hou, A. Harris, S.F. Ma, M. McPartland, G.J. Hymus, L. Adam, C. Marion, The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element, New Phytol. 187 (2010) 57-66.
Crossref Google Scholar
[11]

W.X. Wu, X.M. Zheng, G.W. Lu, Z.Z. Zhong, H. Gao, L.P. Chen, C.Y. Wu, H.J. Wang, Q. Wang, K.N. Zhou, J.L. Wang, F.Q. Wu, X. Zhang, X.P. Guo, Z.J. Cheng, C.L. Lei, Q.B. Lin, L. Jiang, H.Y. Wang, S. Ge, J.M. Wan, Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia, Proc. Natl. Acad. Sci. U. S. A. 110 (2013) 2775-2780.
Crossref Google Scholar
[12]

X.Y. Weng, L. Wang, J. Wang, Y. Hu, H. Du, C.G. Xu, Y.Z. Xing, X.H. Li, J.H. Xiao, Q.F. Zhang, Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response, Plant Physiol. 164 (2014) 735-747.
Crossref Google Scholar
[13]

E. Ando, M. Ohnishi, Y. Wang, T. Matsushita, A. Watanabe, Y. Hayashi, M. Fujii, J.F. Ma, S. Inoue, T. Kinoshita, TWIN SISTER OF FT, GIGANTEA, and CONSTANS have a positive but indirect effect on blue light-induced stomatal opening in Arabidopsis, Plant Physiol. 162 (2013) 1529-1538.
Crossref Google Scholar
[14]

L. Corbesier, C. Vincent, S. Jang, F. Fornara, Q.Z. Fan, I. Searle, A. Giakountis, S. Farrona, L. Gissot, C. Turnbull, G. Coupland, FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis, Science 316 (2007) 1030-1033.
Crossref Google Scholar
[15]

S. Tamaki, S. Matsuo, H.L. Wong, S. Yokoi, K. Shimamoto, Hd3a protein is a mobile flowering signal in rice, Science 316 (2007) 1033-1036.
Crossref Google Scholar
[16]

J. Mathieu, N. Warthmann, F. Küttner, M. Schmid, Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis, Curr. Biol. 17 (2007) 1055-1060.
Crossref Google Scholar
[17]

C. Campoli, B. Drosse, I. Searle, G. Coupland, M. von Korff, Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS, Plant J. 69 (2012) 868-880.
Crossref Google Scholar
[18]

S. Fowler, K. Lee, H. Onouchi, A. Samach, K. Richardson, B. Morris, G. Coupland, J. Putterill, GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains, EMBO J. 18 (1999) 4679-4688.
Crossref Google Scholar
[19]

D.H. Park, D.E. Somers, Y.S. Kim, Y.H. Choy, H.K. Lim, M.S. Soh, H.J. Kim, S.A. Kay, H.G. Nam, Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene, Science 285 (1999) 1579-1582.
Crossref Google Scholar
[20]

F. Turck, F. Fornara, G. Coupland, Regulation and identity of florigen, FLOWERING LOCUS T moves center stage, Annu. Rev. Plant Biol. 59 (2008) 573-594.
Crossref Google Scholar
[21]

R. Sibout, S. Plantegenet, C.S. Hardtke, Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root, Curr. Biol. 18 (2008) 458-463.
Crossref Google Scholar
[22]

S. Datta, G. Hettiarachchi, X.W. Deng, M. Holm, Arabidopsis CONSTANS-LIKE3 is a positive regulator of red light signaling and root growth, Plant Cell 18 (2006) 70-84.
Crossref Google Scholar
[23]

X.F. Cheng, Z.Y. Wang, Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana, Plant J. 43 (2005) 758-768.
Crossref Google Scholar
[24]

M. Hassidim, Y. Harir, E. Yakir, I. Kron, R.M. Green, Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis, Planta 230 (2009) 481-491.
Crossref Google Scholar
[25]

H.G. Wang, Z.L. Zhang, H.Y. Li, X.Y. Zhao, X.M. Liu, M. Ortiz, C.T. Lin, B. Liu, CONSTANS-LIKE 7 regulates branching and shade avoidance response in Arabidopsis, J. Exp. Bot. 64 (2013) 1017-1024.
Crossref Google Scholar
[26]

J.H. Min, J.S. Chung, K.H. Lee, C.S. Kim, The CONSTANS-like 4 transcription factor, AtCOL4, positively regulates abiotic stress tolerance through an abscisic acid-dependent manner in Arabidopsis, J. Integr. Plant Biol. 57 (2015) 313-324.
Crossref Google Scholar
[27]

C. Strayer, T. Oyama, T.F. Schultz, R. Raman, D.E. Somers, P. Más, S. Panda, J.A. Kreps, S.A. Kay, Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog, Science 289 (2000) 768-771.
Crossref Google Scholar
[28]

D. Alabadı́, T. Oyama, M.J. Yanovsky, F.G. Harmon, P. Más, S.A. Kay, Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock, Science 293 (2001) 880-883.
Crossref Google Scholar
[29]

N. Nakamichi, T. Kiba, R. Henriques, T. Mizuno, N.H. Chua, H. Sakakibara, PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock, Plant Cell 22 (2010) 594-605.
Crossref Google Scholar
[30]

M. Yano, Y. Katayose, M. Ashikari, U. Yamanouchi, L. Monna, T. Fuse, T. Baba, K. Yamamoto, Y. Umehara, Y. Nagamura, Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS, Plant Cell 12 (2000) 2473-2483.
Crossref Google Scholar
[31]

N. Endo-Higashi, T. Izawa, Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice, Plant Cell Physiol. 52 (2011) 1083-1094.
Crossref Google Scholar
[32]

S.K. Kim, C.H. Yun, J.H. Lee, Y.H. Jang, H.Y. Park, J.K. Kim, OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice, Planta 228 (2008) 355-365.
Crossref Google Scholar
[33]

Y.S. Lee, D.H. Jeong, D.Y. Lee, J. Yi, C.H. Ryu, S.L. Kim, H.J. Jeong, S.C. Choi, P. Jin, J. Yang, L.H. Cho, H. Choi, G. An, OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB, Plant J. 63 (2010) 18-30.
Crossref Google Scholar
[34]

J.J. Tan, M.N. Jin, J.C. Wang, F.Q. Wu, P.K. Sheng, Z.J. Cheng, J.L. Wang, X.M. Zheng, L.P. Chen, M. Wang, S.S. Zhu, X.P. Guo, X. Zhang, X.M. Liu, C.M. Wang, H.Y. Wang, C.Y. Wu, J.M. Wan, OsCOL10, a CONSTANS-Like gene, functions as a flowering time repressor downstream of Ghd7 in rice, Plant Cell Physiol. 57 (2016) 798-812.
Crossref Google Scholar
[35]

H. Liu, S.Y. Dong, D.Y. Sun, W. Liu, F.W. Gu, Y.Z. Liu, T. Guo, H. Wang, J.F. Wang, Z.Q. Chen, CONSTANS-like 9 (OsCOL9) interacts with receptor for activated C-kinase 1 (OsRACK1) to regulate blast resistance through salicylic acid and ethylene signaling pathways, PLoS One 11 (2016) e0166249.
Crossref Google Scholar
[36]

J.H. Liu, J.Q. Shen, Y. Xu, X.H. Li, J.H. Xiao, L.Z. Xiong, Ghd2, a CONSTANS-like gene, confers drought sensitivity through regulation of senescence in rice, J. Exp. Bot. 67 (2016) 5785-5798.
Crossref Google Scholar
[37]

J.Q. Shen, J.H. Liu, K.B. Xie, F. Xing, F. Xiong, J.H. Xiao, X.H. Li, L.Z. Xiong, Translational repression by a miniature inverted-repeat transposable element in the 3′ untranslated region, Nat. Commun. 8 (2017) 14651.
Crossref Google Scholar
[38]

H. Gao, M.N. Jin, X.M. Zheng, J. Chen, D.Y. Yuan, Y.Y. Xin, M.Q. Wang, D.Y. Huang, Z. Zhang, K.N. Zhou, P.K. Sheng, J. Ma, W.W. Ma, H.F. Deng, L. Jiang, S.J. Liu, H.Y. Wang, C.Y. Wu, L.P. Yuan, J.M. Wan, Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice, Proc. Natl. Acad. Sci. U. S. A. 111 (2014) 16337-16342.
Crossref Google Scholar
[39]

W.H. Yan, H.Y. Liu, X.C. Zhou, Q.P. Li, J. Zhang, L. Lu, T.M. Liu, H.J. Liu, C.J. Zhang, Z.Y. Zhang, G.J. Shen, W. Yao, H.X. Chen, S.B. Yu, W.B. Xie, Y.Z. Xing, Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice, Cell Res. 23 (2013) 969-971.
Crossref Google Scholar
[40]

N. Nakamichi, Adaptation to local environment by modifications of photoperiod response in crops, Plant Cell Physiol. 56 (2014) 594-604.
Crossref Google Scholar
[41]

Y. Nemoto, Y. Nonoue, M. Yano, T. Izawa, Hd1, a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7, Plant J. 86 (2016) 221-233.
Crossref Google Scholar
[42]

L. Zhang, Q.P. Li, H.J. Dong, Q. He, L.W. Liang, C. Tan, Z.M. Han, W. Yao, G.W. Li, H. Zhao, W.B. Xie, Y.Z. Xing, Three CCT domain-containing genes were identified to regulate heading date by candidate gene-based association mapping and transformation in rice, Sci Rep 5 (2015) 7663.
Crossref Google Scholar
[43]

T.A. Miller, E.H. Muslin, J.E. Dorweiler, A maize CONSTANS-like gene, conz1, exhibits distinct diurnal expression patterns in varied photoperiods, Planta 227 (2008) 1377-1388.
Crossref Google Scholar
[44]

H.Y. Hung, L.M. Shannon, F. Tian, P.J. Bradbury, C. Chen, S.A. Flint-Garcia, M.D. McMullen, D. Ware, E.S. Buckler, J.F. Doebley, J.B. Hollanda, ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 1913-1921.
Crossref Google Scholar
[45]

C. Wang, Q. Yang, W.X. Wang, Y.P. Li, Y.L. Guo, D.F. Zhang, X.N. Ma, W. Song, J.R. Zhao, M.L. Xu, A transposon-directed epigenetic change in ZmCCT underlies quantitative resistance to Gibberella stalk rot in maize, New Phytol. (2017).
Crossref Google Scholar
[46]

G.H. Xu, X.F. Wang, C. Huang, D.Y. Xu, D. Li, J.G. Tian, Q.Y. Chen, C.L. Wang, Y.M. Liang, Y.Y. Wu, X.H. Yang, F. Tian, Complex genetic architecture underlies maize tassel domestication, New Phytol. 214 (2017) 852-864.
Crossref Google Scholar
[47]

J.A.R. Navarro, M. Willcox, J. Burgueño, C. Romay, K. Swarts, S. Trachsel, E. Preciado, A. Terron, H.V. Delgado, V. Vidal, A. Ortega, A.E. Banda, N.O.G. Montiel, I. Ortiz-Monasterio, F.S. Vicente, A.G. Espinoza, G. Atlin, P. Wenzl, S. Hearne, E.S. Buckler, A study of allelic diversity underlying flowering-time adaptation in maize landraces, Nat. Genet. 49 (2017) 476-480.
Crossref Google Scholar
[48]

S.S. Yang, B.D. Weers, D.T. Morishige, J.E. Mullet, CONSTANS is a photoperiod regulated activator of flowering in sorghum, BMC Plant Biol. 14 (2014) 148.
Crossref Google Scholar
[49]

H.H. Liu, H.Q. Liu, L.N. Zhou, Z.H. Zhang, X.X. Zhang, M.L. Wang, H.X. Li, Z.W. Lin, Parallel domestication of the heading date 1 gene in cereals, Mol. Biol. Evol. 32 (2015) 2726-2737.
Crossref Google Scholar
[50]

S.S. Yang, R.L. Murphy, D.T. Morishige, P.E. Klein, W.L. Rooney, J.E. Mullet, Sorghum phytochrome B inhibits flowering in long days by activating expression of SbPRR37 and SbGHD7, repressors of SbEHD1, SbCN8 and SbCN12, PLoS One 9 (2014) e105352.
Crossref Google Scholar
[51]

A. Turner, J. Beales, S. Faure, R.P. Dunford, D.A. Laurie, The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley, Science 310 (2005) 1031-1034.
Crossref Google Scholar
[52]

L. Yan, A. Loukoianov, G. Tranquilli, M. Helguera, T. Fahima, J. Dubcovsky, Positional cloning of the wheat vernalization gene VRN1, Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6263-6268.
Crossref Google Scholar
[53]

Y. Nemoto, M. Kisaka, T. Fuse, M. Yano, Y. Ogihara, Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice, Plant J. 36 (2003) 82-93.
Crossref Google Scholar
[54]

L.L. Yan, A. Loukoianov, A. Blechl, G. Tranquilli, W. Ramakrishna, P. SanMiguel, J.L. Bennetzen, V. Echenique, J. Dubcovsky, The wheat VRN2 gene is a flowering repressor down-regulated by vernalization, Science 303 (2004) 1640-1644.
Crossref Google Scholar
[55]

J. Dubcovsky, A. Loukoianov, D.L. Fu, M. Valarik, A. Sanchez, L.L. Yan, Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2, Plant Mol. Biol. 60 (2006) 469-480.
Crossref Google Scholar
[56]

J. Beales, A. Turner, S. Griffiths, J.W. Snape, D.A. Laurie, A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.), Theor. Appl. Genet. 115 (2007) 721-733.
Crossref Google Scholar
[57]

E.P. Wilhelm, A.S. Turner, D.A. Laurie, Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.), Theor. Appl. Genet. 118 (2009) 285-294.
Crossref Google Scholar
[58]

H. Nishida, T. Yoshida, K. Kawakami, M. Fujita, B. Long, Y. Akashi, D.A. Laurie, K. Kato, Structural variation in the 5′ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time, Mol. Breed. 31 (2013) 27-37.
Crossref Google Scholar
[59]

A. Díaz, M. Zikhali, A.S. Turner, P. Isaac, D.A. Laurie, Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum), PLoS One 7 (2012) e33234.
Crossref Google Scholar
[60]

H. Sun, Z.A. Guo, L.F. Gao, G.Y. Zhao, W.P. Zhang, R.H. Zhou, Y.Z. Wu, H.Y. Wang, H.L. An, J.Z. Jia, DNA methylation pattern of Photoperiod-B1 is associated with photoperiod insensitivity in wheat (Triticum aestivum), New Phytol. 204 (2014) 682-692.
Crossref Google Scholar
[61]

N.D. González-Schain, M. Díaz-Mendoza, M. Żurczak, P. Suárez-López, Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner, Plant J. 70 (2012) 678-690.
Crossref Google Scholar
[62]

T. Izawa, Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice, J. Exp. Bot. 58 (2007) 3091-3097.
Crossref Google Scholar
[63]

R.S. Meyer, M.D. Purugganan, Evolution of crop species: genetics of domestication and diversification, Nat. Rev. Genet. 14 (2013) 840-852.
Crossref Google Scholar
[64]

M.D. Purugganan, D.Q. Fuller, The nature of selection during plant domestication, Nature 457 (2009) 843-848.
Crossref Google Scholar
[65]

J. Zhang, X.C. Zhou, W.H. Yan, Z.Y. Zhang, L. Lu, Z.M. Han, H. Zhao, H.Y. Liu, P. Song, Y. Hu, G.J. Shen, Q. He, S.B. Guo, G.Q. Gao, G.W. Wang, Y.Z. Xing, Combinations of the Ghd7, Ghd8 and Hd1 genes largely define the ecogeographical adaptation and yield potential of cultivated rice, New Phytol. 208 (2015) 1056-1066.
Crossref Google Scholar
[66]

Y.J. Yang, C. Ma, Y.J. Xu, Q. Wei, M. Imtiaz, H.B. Lan, S. Gao, L.N. Cheng, M.Y. Wang, Z.J. Fei, B. Hong, J.P. Gao, A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis, Plant Cell 26 (2014) 2038-2054.
Crossref Google Scholar
The Crop Journal
Volume 5 Issue 6,
December 2017
Pages 449-458
DOI: 10.1016/j.cj.2017.07.001
Cite this article:
Li Y, Xu M. CCT family genes in cereal crops: A current overview. The Crop Journal, 2017, 5(6): 449-458. https://doi.org/10.1016/j.cj.2017.07.001

278

Views

4

Downloads

40

Crossref

N/A

Web of Science

41

Scopus

3

CSCD

Altmetrics
Received: 26 April 2017
Revised: 11 July 2017
Accepted: 01 August 2017
Published: 25 September 2017
© 2017 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return