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.
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
Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664
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
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
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
Chen FH (1957) Origin of Chinese chrysanthemum. Chry Dahlia 7:264–265
Chen JY (1984) Studies on the origin of Chinese florist’s chrysanthemum. Acta Hort 167:349–362
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
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
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
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
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
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
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
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550.e551–550.e552
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
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
Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254
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
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
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
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
Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16:711–722
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
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
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
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
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
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
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
Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1102
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
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
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
Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289
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
Tan F-C, Swain SM (2007) Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol Plant 131:481–495
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
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
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
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
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
Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–312
Yanovsky MJ, Kay SA (2003) Living by the calendar: how plants know when to flower. Nat Rev Mol Cell Biol 4:265–276
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
Zhang LJ, Dai SL (2009) Research advance on germplasm resources of Chrysanthemum × morifolium. Chin Bull Bot 44:526–535
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
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
Corresponding author
Rights 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
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-013-0679-8