Skip to main content
SpringerLink
Log in

Characterization of Chrysanthemum ClSOC1-1 and ClSOC1-2, homologous genes of SOC1

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

The MADS-box gene SOC1/TM3 (SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1/ Tomato MADS-box gene 3) is a main integrator in the Arabidopsis flowering pathway; its structure and function are highly conserved in many plant species. SOC1-like genes have been isolated in chrysanthemum, one of the most well-known ornamental plants, but it has not been well characterized thus far. We isolated and characterized ClSOC1-1 and ClSOC1-2, two putative orthologs of Arabidopsis SOC1, from the wild diploid chrysanthemum, Chrysanthemum lavandulifolium, to investigate the regulatory mechanisms of flowering time control in chrysanthemum. Expression analysis indicated that ClSOC1-1 and ClSOC1-2 were expressed in all examined organs/tissues (leaves, shoot apices, petioles, stems and roots) with different expression levels, and with high expression in the shoot apices and leaves during the early stage of floral transition. The expression levels of ClSOC1-1 and ClSOC1-2 in the shoot apices increased at different developmental stages with the highest expression levels after 7 days of short-day treatment. Overexpression of ClSOC1-1 and ClSOC1-2 in wild-type Arabidopsis resulted in early flowering, which was coupled with the upregulation of one of the flowering promoter genes LEAFY. Our results suggested that the ClSOC1-1 and ClSOC1-2 genes play an evolutionarily conserved role in promoting flowering in Chrysanthemum lavandulifolium and could serve as a vital target for the genetic manipulation of flowering time in the chrysanthemum.

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

Abbreviations

CO :

CONSTANS

FD :

FLOWERING LOCUS D

FLC :

FLOWERING LOCUS C

FT :

FLOWERING LOCUS T

LFY :

LEAFY

LD:

Long day

SD:

Short day

SOC1 :

SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1

TM3:

Tomato MADS-box gene 3

References

  • Anderson NO (2006) Flower breeding and genetics: issues, challenges and opportunities for the 21st century. Springer, Heidelberg

    Book  Google Scholar 

  • Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    Article  CAS  PubMed  Google Scholar 

  • Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489

    Article  CAS  PubMed  Google Scholar 

  • Borner R, Kampmann G, Chandler J, Gleiûner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24:591–599

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116

    Article  CAS  Google Scholar 

  • Chen FH (1957) Origin of Chinese chrysanthemum. Chry Dahlia 7:264–265

    Google Scholar 

  • Chen JY (1984) Studies on the origin of Chinese florist’s chrysanthemum. Acta Hort 167:349–362

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Cseke LJ, Zheng J, Podila GK (2003) Characterization of PTM5 in aspen trees: a MADS-box gene expressed during woody vascular development. Gene 318:55–67

    Article  CAS  PubMed  Google Scholar 

  • Dai SL, Wang WK, Huang JP (2002) Advances of researches on phylogeny of Dendranthema and origin of chrysanthemum. J Beijing For Univ 24:230–234

    Google Scholar 

  • Decroocq V, Zhu X, Kauffman M, Kyozuka J, Peacock WJ, Dennis ES, Llewellyn DJ (1999) A TM3-like MADS-box gene from Eucalyptus expressed in both vegetative and reproductive tissues. Gene 228:155–160

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Fu JX, Dai SL (2012) Characteristics of seed germination and regularities of growth and development of Chrysanthemum lavandulifolium in natural conditions. J Northeast For Univ 40:23–25

    Google Scholar 

  • Ding L, Wang Y, Yu H (2013) Overexpression of DOSOC1, an ortholog of Arabidopsis SOC1, promotes flowering in the Orchid Dendrobium Chao Parya Smile. Plant Cell Physiol 54:595–608

    Article  CAS  PubMed  Google Scholar 

  • Ferrario S, Busscher J, Franken J, Gerats T, Vandenbussche M, Angenent GC, Immink RGH (2004) Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner. Plant Cell 16:1490–1505

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550.e551–550.e552

    Article  Google Scholar 

  • Fu J, Wang Y, Huang H, Zhang C, Dai S (2013) Reference gene selection for RT-qPCR analysis of Chrysanthemum lavandulifolium during its flowering stages. Mol Breed 31(1):205–215

    Article  CAS  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Suh S-S, Park E, Cho E, Ahn JH, Kim S-G, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Gene Dev 14:2366–2376

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li T, Niki T, Nishijima T, Douzono M, Koshioka M, Hisamatsu T (2009) Roles of CmFL, CmAFL1, and CmSOC1 in the transition from vegetative to reproductive growth in Chrysanthemum morifolium Ramat. J Hortic Sci Biotechnol 84:447–453

    CAS  Google Scholar 

  • Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134:1901–1910

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han J-H, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135:1481–1491

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16:711–722

    Article  CAS  PubMed  Google Scholar 

  • Ma YP, Fang XH, Chen F, Dai SL (2008) DFL, a FLORICAULA/LEAFY homologue gene from Dendranthema lavandulifolium is expressed both in the vegetative and reproductive tissues. Plant Cell Rep 27:647–654

    Article  CAS  PubMed  Google Scholar 

  • Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat Genet 40:1489–1492

    Article  CAS  PubMed  Google Scholar 

  • Moon J, Suh S-S, Lee H, Choi K-R, Hong CB, Paek N-C, Kim S-G, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623

    Article  CAS  PubMed  Google Scholar 

  • Na X, Jian B, Yao W, Wu C, Hou W, Jiang B, Bi Y, Han T (2013) Cloning and functional analysis of the flowering gene GmSOC1-like, a putative SUPPRESSOR OF OVEREXPRESSION CO1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in soybean. Plant Cell Rep. doi:10.1007/s00299-00013-01419-00290

    PubMed  Google Scholar 

  • Nakamura T, Song I-J, Fukuda T, Yokoyama J, Maki M, Ochiai T, Kameya T, Kanno A (2005) Characterization of TrcMADS1 gene of Trillium camtschatcense (Trilliaceae) reveals functional evolution of the SOC1/TM3-like gene family. J Plant Res 118:229–234

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Kawashima H, Kinoshita T, Yoshikawa H, Hisamatsu T (2011) Characterization of FLC, SOC1 and FT homologs in Eustoma grandiflorum: effects of vernalization and post-vernalization conditions on flowering and gene expression. Physiol Plant 141:383–393

    Article  CAS  PubMed  Google Scholar 

  • Papaefthimiou D, Kapazoglou A, Tsaftaris AS (2012) Cloning and characterization of SOC1 homologs in barley (Hordeum vulgare) and their expression during seed development and in response to vernalization. Physiol Plant 146:71–85

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1102

    CAS  PubMed  Google Scholar 

  • Ruokolainen S, Ng YP, Albert VA, Elomaa P, Teeri TH (2011) Over-expression of the Gerbera hybrida At-SOC1-like1 gene Gh-SOC1 leads to floral organ identity deterioration. Ann Bot 107:1491–1499

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Gene Dev 20:898–912

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289

    Article  CAS  PubMed  Google Scholar 

  • Sreekantan L, Thomas MR (2006) VvFT and VvMADS8, the grapevine homologues of the floral integrators FT and SOC1, have unique expression patterns in grapevine and hasten flowering in Arabidopsis. Funct Plant Biol 33:1129–1139

    Article  CAS  Google Scholar 

  • Tan F-C, Swain SM (2007) Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol Plant 131:481–495

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Google Scholar 

  • Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006

    Article  CAS  PubMed  Google Scholar 

  • Wang J-W, Czech B, Weigel D (2009a) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Han KT, D SL (2009b) Construction of expression vector and transformation of chrysanthemum with maize Lc gene. Genomics Appl Biol 28:229–236

    CAS  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–312

    Article  CAS  PubMed  Google Scholar 

  • Yanovsky MJ, Kay SA (2003) Living by the calendar: how plants know when to flower. Nat Rev Mol Cell Biol 4:265–276

    Article  CAS  PubMed  Google Scholar 

  • Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH (2005) CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol 139:770–778

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang LJ, Dai SL (2009) Research advance on germplasm resources of Chrysanthemum × morifolium. Chin Bull Bot 44:526–535

    Google Scholar 

  • Zhong X, Dai X, Xv J, Wu H, Liu B, Li H (2012) Cloning and expression analysis of GmGAL1, SOC1 homolog gene in soybean. Mol Biol Rep 39:6967–6974

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Fundamental Research Funds for the Central Universities (grant number BLYJ20133) and Beijing Natural Science Foundation (grant number 6132020). We sincerely thank Dr. Chao Zhang, Beijing Forestry University, China, for the assistance with experimental sampling and valuable suggestions during the writing process.

Author information

Authors and Affiliations

  1. College of Landscape Architecture, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Jianxin Fu, Shuai Qi, Liwen Yang, Yi Dai & Silan Dai

Authors
  1. Jianxin Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuai Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liwen Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yi Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Silan Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Silan Dai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fu, J., Qi, S., Yang, L. et al. Characterization of Chrysanthemum ClSOC1-1 and ClSOC1-2, homologous genes of SOC1 . Plant Mol Biol Rep 32, 740–749 (2014). https://doi.org/10.1007/s11105-013-0679-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-013-0679-8

Keywords

Search

Navigation