Abstract

FLOWERING LOCUS T (FT)-like genes play crucial roles in flowering transition in several plant species. In this study, a homolog of FT, designated as FaFT1, was isolated and characterized from strawberry. The open reading frame of FaFT1 was 531 bp, encoding a protein of 176 amino acids. Phylogenetic and sequence analysis showed that the FaFT1 protein contained the conservation of Tyr84 and Gln139, as well as the highly conserved amino acid sequences LGRQTVYAPGWRQN and LYN and that it was a member of the FT-like genes of dicots. Subcellular localization analysis revealed that the FaFT1 protein mainly localized in the nuclei of the Arabidopsis protoplasts. FaFT1 was highly expressed in strawberry mature leaves and its expression level decreased under floral induction conditions. Additionally, FaFT1 expression exhibited diurnal circadian rhythm both under SD and LD conditions. Over expression of FaFT1 in wild-type Arabidopsis caused early flowering. Taken together, these results indicate that FaFT1 is a putative FT homolog in strawberry, acting as a floral promoter in Arabidopsis.

Keywords:

Arabidopsis, FaFT1, flowering, strawberry,

References

1. Abe, M., Y. Kobayashi, S. Yamamoto, Y. Daimon, A. Yamaguchi, Y. Ikeda, H. Ichinoki, M. Notaguchi, K. Goto and T. Araki, 2005. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science, 309(5737): 1052-1056.
   CrossRef    PMid:16099979    
2. Ahn J.H., D. Miller, V.J. Winter, M.J. Banfield, J.H. Lee, S.Y. Yoo, S.R. Henz, R.L. Brady and D. Weigel, 2006. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J., 25(3): 605-614.
   CrossRef    PMid:16424903 PMCid:PMC1383534    
3. Boss, P.K., R.M. Bastow, J.S. Mylne and C. Dean, 2004. Multiple pathways in the decision to flower: Enabling, promoting and resetting. Plant Cell., 16(Suppl. 1): 18-31.
   CrossRef    PMid:15037730 PMCid:PMC2643402    
4. Castillejo, C. and S. Pelaz, 2008. The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr. Biol., 18(17): 1338-1343.
   CrossRef    PMid:18718758    
5. Chang, S., J. Puryear and J. Cairney, 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep., 11(2): 113-116.
   CrossRef    
6. Clough, S.J. and A.F. Bent, 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16(6): 735-743.
   CrossRef    PMid:10069079    
7. Corbesier, L., C. Vincent, S. Jang, F. Fornara, Q. Fan, I. Searle, A. Giakountis, S. Farrona, L. Gissot, C. Turnbull and G. Coupland, 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 316(5827): 1030-1033.
   CrossRef    PMid:17446353    
8. Fornara, F., A. de Montaigu and G. Coupland, 2010. Snapshot: Control of flowering in arabidopsis. Cell, 141(13): 550-550.e2.
   CrossRef    PMid:20434991    
9. Hanzawa, Y., T. Money and D. Bradley, 2005. A single amino acid converts a repressor to an activator of flowering. P. Natl. Acad. Sci. USA, 102(21): 7748-7753.
   CrossRef    PMid:15894619 PMCid:PMC1140427    
10. Heide, O.M. and A. Sønsteby, 2007. Interactions of temperature and photoperiod in the control of flowering of latitudinal and altitudinal populations of wild strawberry (Fragaria vesca). Physiol. Plant., 130(2): 280-289.
    CrossRef    
11. Hsu, C.Y., J.P. Adams, H. Kim, K. No, C. Ma, S.H. Strauss, J. Drnevich, L. Vandervelde, J.D. Ellis, B.M. Rice, N. Wickett, L.E. Gunter, G.A. Tuskan, A.M. Brunner, G.P. Page, A. Barakat, J.E. Carlson, C.W. DePamphilis, D.S. Luthe and C. Yuceer, 2011. FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. P. Natl. Acad. Sci. USA, 108(26): 10756-10761.
    CrossRef    PMid:21653885 PMCid:PMC3127867    
12. Jaeger, K.E. and P.A. Wigge, 2007. FT protein acts as a long-range signal in Arabidopsis. Curr. Biol., 17(12): 1050-1054.
    CrossRef    PMid:17540569    
13. Kim, J.J., J.H. Lee, W. Kim, H.S. Jung, P. Huijser and J.H. Ahn, 2012. The micro RNA 156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol., 159(1): 461-478.
    CrossRef    PMid:22427344 PMCid:PMC3375978    
14. Kobayashi, Y., H. Kaya, K. Goto, M. Iwabuchi and T. Araki, 1999. A pair of related genes with antagonistic roles in mediating flowering signals. Science, 286(5446): 1960-1962.
    CrossRef    PMid:10583960    
15. Kobayashi, Y. and D. Weigel, 2007. Move on up, it's time for change-mobile signals controlling photoperiod-dependent flowering. Genes Dev., 21(19): 2371-2384.
    CrossRef    PMid:17908925    
16. Kong, F., B. Liu, Z. Xia, S. Sato, B.M. Kim, S. Watanabe, T. Yamada, S. Tabata, A. Kanazawa, K. Harada and J. Abe, 2010. Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol., 154(3): 1220-1231.
    CrossRef    PMid:20864544 PMCid:PMC2971601    
17. Koskela, E.A., K. Mouhu, M.C. Albani, T. Kurokura, M. Rantanen, D.J. Sargent, N.H. Battey, G. Coupland, P. Elomaa and T. Hytönen, 2012. Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol., 159(3): 1043-1054.
    CrossRef    PMid:22566495 PMCid:PMC3387692    
18. Kotoda, N., H. Hayashi, M. Suzuki, M. Igarashi, Y. Hatsuyama, S. Kidou, T. Igasaki, M. Nishiguchi, K. Yano, T. Shimizu, S. Takahashi, H. Iwanami, S. Moriya and K. Abe, 2010. Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus×domestica Borkh). Plant Cell Physiol., 51(4): 561-575.
    CrossRef    PMid:20189942    
19. Li, C., L. Luo, Q. Fu, L. Ni and Z. Xu, 2014. Isolation and functional characterization of JcFT: A FLOWERING LOCUS T (FT) homologous gene from the biofuel plant Jatropha curcas. BMC Plant Biol., 14: 125.
    CrossRef    PMid:24886195 PMCid:PMC4036407    
20. Li, D., C. Liu, L. Shen, Y. Wu, H. Chen, M. Robertson, C.A. Helliwell, T. Ito, E. Meyerowitz and H. Yu, 2008. A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell, 15(1): 110-120.
    CrossRef    PMid:18606145    
21. Li, W.M., Y. Tao, Y.X. Yao, Y.J. Hao and C.X. You, 2010. Ectopic over-expression of two apple Flowering Locus T homologues, MdFT1 and MdFT2, reduces juvenile phase in Arabidopsis. Biol. Plantarum, 54(4): 639-646.
    CrossRef    
22. Lifschitz, E., T. Eviatar, A. Rozman, A. Shalit, A. Goldshmidt, Z. Amsellem, J.P. Alvarez and Y, Eshed, 2006. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. P. Natl. Acad. Sci. USA, 103(16): 6398-6403.
    CrossRef    PMid:16606827 PMCid:PMC1458889    
23. Livak, K.J. and T.D. Schmittgen, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-?? Ct method. Methods, 25(4): 402-408.
    CrossRef    PMid:11846609    Direct Link
24. Mathieu, J., N. Warthmann, F. Küttner and M. Schmid, 2007. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol., 17(12): 1055-1060.
    CrossRef    PMid:17540570    
25. Mathieu, J., L.J. Yant, F. Mürdter, F. Küttner and M. Schmid, 2009. Repression of flowering by the miR172 target SMZ. PLoS Biol., 7(7): e1000148.
    CrossRef    PMid:19582143 PMCid:PMC2701598    
26. Mouhu, K., T. Hytönen, K. Folta, M. Rantanen, L. Paulin, P. Auvinen and P. Elomaa, 2009. Identi?cation of flowering genes in strawberry, a perennial SD plant. BMC Plant Biol., 9: 122.
    CrossRef    PMid:19785732 PMCid:PMC2761920    
27. Mouhu, K., T. Kurokura, E.A. Koskela, V.A. Albert, P. Elomaa and T. Hytönen, 2013. The Fragaria vesca homolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 represses flowering and promotes vegetative growth. Plant Cell, 25(9): 3296-3310.
    CrossRef    PMid:24038650 PMCid:PMC3809533    
28. Oda, A., T. Narumi, T. Li, T. Kando, Y. Higuchi, K. Sumitomo, S. Fukai and T. Hisamatsu, 2012. CsFTL3: A chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums. J. Exp. Bot., 63(3): 1461-1477.
    CrossRef    PMid:22140240 PMCid:PMC3276106    
29. Parcy, F., 2005. Flowering: A time for integration. Int. J. Dev. Biol., 49: 585-593.
    CrossRef    PMid:16096967    
30. Pin, P. and O. Nilsson, 2012. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ., 35(10): 1742-1755.
    CrossRef    PMid:22697796    
31. Saitou, N. and M. Nei, 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4(4): 406-425.
    PMid:3447015    
32. Sawa, M. and S.A. Kay, 2011. GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. P. Natl. Acad. Sci. USA, 108(28): 11698-11703.
    CrossRef    PMid:21709243 PMCid:PMC3136272    
33. Suárez-López, P., K. Wheatley, F. Robson, H. Onouchi, F. Valverde and G. Coupland, 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature, 410(6832): 1116-1120.
    CrossRef    PMid:11323677    
34. Tamaki, S., S. Matsuo, H.L. Wong, S. Yokoi and K. Shimamoto, 2007. Hd3a protein is a mobile flowering signal in rice. Science, 316 (5827): 1033-1036.
    CrossRef    PMid:17446351    
35. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei and S. Kumar, 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol. Biol. Evol., 28(10): 2731-2739.
    CrossRef    PMid:21546353 PMCid:PMC3203626    
36. Teper-Bamnolker, P. and A. Samach, 2005. The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell, 17(10): 2661-2675.
    CrossRef    PMid:16155177 PMCid:PMC1242264    
37. Thompson, J.D., D.G. Higgins and T.J. Gibson, 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(22): 4673-4680.
    CrossRef    PMid:7984417 PMCid:PMC308517    Direct Link
38. Wenkel, S., F. Turck, K. Singer, L. Gissot, J. Le Gourrierec, A. Samach and G. Coupland, 2006. CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell, 18(11): 2971-2984.
    CrossRef    PMid:17138697 PMCid:PMC1693937    
39. Wigge, P.A., M.C. Kim, K.E. Jaeger, W. Busch, M. Schmid, J.U. Lohmann and D. Weigel, 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309(5737): 1056-1059.
    CrossRef    PMid:16099980    
40. Xiang, L., X. Li, D. Qin, F. Guo, C. Wu, L. Miao and C. Sun, 2012. Functional analysis of FLOWERING LOCUS T orthologs from spring orchid (Cymbidium goeringii Rchb. f.) that regulates the vegetative to reproductive transition. Plant Physiol. Biochem., 58: 98-105.
    CrossRef    PMid:22796899    
41. Yoo, S.D., Y.H. Cho and J. Sheen, 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc., 2(7): 1565-1572.
    CrossRef    PMid:17585298    

Competing interests

The authors have no competing interests.

Open Access Policy

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Copyright

The authors have no competing interests.