Abstract
In this study, we cloned flowering-related genes FLOWERING LOCUS T (FT) and TERMINAL FLOWER1 (TFL1) from domesticated octaploid strawberries (Fragaria × ananassa) and analyzed their expression patterns in cultivars Tochiotome and Akihime. The floral meristem generation was induced under the short day and low temperature (SDLT), but not under the long day and high temperature (LDHT). We found that FaFT1, which is an orthologue of the Arabidopsis floral activator FT, was highly expressed in leaves under LDHT but not expressed in leaves under SDLT. On the other hand, the expression of FaTFL2, which belongs to the TFL1 family of flowering repressing genes, decreased in crowns (stem tissue including meristem) under SDLT. These results suggest that FaTFL2, as opposed to FvTFL1 in wild diploid strawberry Fragaria vesca, is related to flowering of the cultivated strawberry. Moreover, the FaTFL2 expression might be regulated by temperature rather than by photoperiod. We demonstrated that a reduction of the FaTFL2 expression is a key signal for flowering in domesticated strawberries.
Similar content being viewed by others
Abbreviations
- AP1:
-
APETALA1
- CO:
-
CONSTANCS
- DTT:
-
dithiothreitol
- EGTA:
-
ethyleneglycoltetraacetic acid
- FD:
-
FLOWERING LOCUS D
- FT:
-
FLOWERING LOCUS T
- LDHT:
-
long day and high temperature
- LDLT:
-
long day and low temperature
- MSI1:
-
multicopy suppressor of IRA1
- PEBP:
-
phosphatidylethanolamine-binding protein
- PVP:
-
polyvinylpyrrolidone
- RT- qPCR:
-
real time quantitative polymerase chain reaction
- SDHT:
-
short day and high temperature
- SDLT:
-
short day and low temperature
- SDS:
-
sodium dodecyl sulfate
- TFL1:
-
TERMINAL FLOWER1
References
Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K., Araki, T.: FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. — Science 309: 1052–1056, 2005.
Abramoff, M.D., Magelhaes, P.J., Ram, S.J.: Image processing with ImageJ. — Biophotonics Int. 11: 36–42, 2004.
Ahn, J.H., Miller, D., Winter, V.J., Banfield, M.J., Lee, J.H., Yoo, S.Y., Henz, S.R., Brady, R.L., Weigel, D.: A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. — EMBO J. 25: 605–614, 2006.
An, H., Roussot, C., Suárez-López, P., Corbesier, L., Vincent, C., Piñeiro, M., Hepworth, S., Mouradov, A., Justin, S., Turnbull, C., Coupland, G.: CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. — Development 131: 3615–3626, 2004.
Bradford, E., Hancock, J.F., Warner, R.M.: Interactions of temperature and photoperiod determine expression of repeat flowering in strawberry. — J. amer. Soc. hort. Sci. 135: 102–107, 2010
Conti, L., Bradley, D.: TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. — Plant Cell 19: 767–778, 2007.
Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C., Coupland, G.: FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. — Science 316: 1030–1033, 2007.
Hanano, S., Goto, K.: Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. — Plant Cell 23: 3172–3184, 2011.
Hanzawa, Y., Money, T., Bradley, D.: A single amino acid converts a repressor to an activator of flowering. — Proc. nat. Acad. Sci. USA 102: 7748–7753, 2005.
Hayama, R., Yokoi, S., Tamaki, S., Yano, M., Shimamoto, K.: Adaptation of photoperiodic control pathways produces short-day flowering in rice. — Nature 422: 719–722, 2003.
Hayama, R., Agashe, B., Luley, E., King, R., Coupland, G.: A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. — Plant Cell 19: 2988–3000, 2007.
Iwata, H., Gaston, A., Remay, A., Thouroude, T., Jeauffre, J., Kawamura, K., Oyant, L.H., Araki, T., Denoyes, B., Foucher, F.: The TFL1 homologue KSN is a regulator of continuous floering in rose and strawberry. — Plant J. 69: 116–125, 2012.
Jaeger, K.E., Wigge, P.A.: FT protein acts as a long-range signal in Arabidopsis. — Curr. Biol. 17: 1050–1054, 2007.
Kong, F., Liu, B., Xia, Z., Sato, S., Kim, B.M., Watanabe, S., Yamada, T., Tabata, S., Kanazawa, A., Harada, K., Abe, J. Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. — Plant Physiol. 154: 1220–1231, 2010.
Koskela, E.A., Mouhu, K., Albani, M.C., Kurokura, T., Rantanen, M., Sargent, D.J., Battey, N.H., Coupland, G., Elomaa, P., Hytönen, T.: Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. — Plant Physiol. 159: 1043–1054, 2012.
Mimida, N., Li, J., Zhang, C., Moriya, S., Moriya-Tanaka, Y., Iwanami, H., Honda, C., Oshino, H., Takagishi, K., Suzuki, A., Komori, S., Wada, M.: Divergence of TERMINAL FLOWER1-like genes in Rosaceae. — Biol. Plant. 56: 465–472, 2012.
Mouhu, K., Hytönen, T., Folta, K., Rantanen, M., Paulin, L., Auvinen, P., Elomaa, P.: Identification of flowering genes in strawberry, a perennial SD plant. — BMC Plant Biol. 9: 122, 2009.
Ratcliffe, O.J., Bradley, D.J., Coen, E.S.: Separation of shoot and floral identity in Arabidopsis. — Development 126: 1109–1120, 1999.
Shulaev, V., Sargent, D.J., Crowhurst, R.N., Mockler, T.C., Folkerts, O., Delcher, A.L., Jaiswal, P., Mockaitis, K., Liston, A., Mane, S.P., Burns, P., Davis, T.M., Slovin, J.P., Bassil, N., Hellens, R.P., Evans, C., Harkins, T., Kodira, C., Desany, B., Crasta, O.R., Jensen, R.V., Allan, A.C., Michael, T.P., Setubal, J.C., Celton, J.-M., Rees, D.J.G., Williams, K.P., Holt, S.H., Rojas, J.J.R., Chatterjee, M., Liu, B., Silva, H., Meisel, L., Adato, A., Filichkin, S.A., Troggio, M., Viola, R., Ashman, T.-L., Wang, H., Dharmawardhana, P., Elser, J., Raja, R., Priest, H.D., Bryant, D.W., Jr., Fox, S.E., Givan, S.A., Wilhelm, L.J., Naithani, S., Christoffels, A., Salama, D.Y., Carter, J., Girona, E.L., Zdepski, A., Wang, W., Kerstetter, R.A., Schwab, W., Korban, S.S., Davik, J., Monfort, A., Denoyes-Rothan, B., Arus, P., Mittler, R., Flinn, B., Aharoni, A., Bennetzen, J.L., Salzberg, S.L., Dickerman, A.W., Velasco, R., Borodovsky, M., Veilleux, R.E., Folta, K.M.: The genome of woodland strawberry (Fragaria vesca). — Nat. Genet. 43: 109–116, 2011.
Sønsteby, A., Nes, A.: Short days and temperature effects on growth and flowering in strawberry (Fragaria × ananassa Duch.). — J. hort. Sci. Biotechnol. 73: 730–736, 1998.
Sønsteby, A., Heide, O.M.: Long-day control of flowering in everbearing strawberries. — J. hort. Sci. Biotechnol. 82: 875–884, 2007.
Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S., Shimamoto, K.: Hd3a protein is a mobile flowering signal in rice. — Science 316: 1033–1036, 2007.
Taoka, K., Ohki, I., Tsuji, H., Furuita, K., Hayashi, K., Yanase, T., Yamaguchi, M., Nakashima, C., Purwestri, Y.A., Tamaki, S., Ogaki, Y., Shimada, C., Nakagawa, A., Kojima, C., Shimamoto, K.: 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. — Nature 476: 332–335, 2011.
Taylor, D.R.: The physiology of flowering in strawberry. — Acta Hort. 567: 245–251, 2002.
Turck, F., Fornara, F., Coupland, G.: Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. — Annu. Rev. Plant Biol. 59: 573–594, 2008.
Turnbull, C.: Long-distance regulation of flowering time. — J. exp. Bot. 62: 4399–4413, 2011.
Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., Coupland, G.: Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. — Science 303: 1003–1006, 2004
Verheul, M.J., Sonsteby, A., Grimstad, S.O.: Interaction of photoperiod, temperature, duration of short-day treatment and plant age on flowering of Fragaria × ananassa Duch. cv. Korona. — Sci. Hort. 107: 164–170, 2006.
Wan, C.-Y., Wilkins, T.A.: A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). — Anal. Biochem. 223: 7–12, 1994.
Weebadde, C.K., Wang, D., Finn, C.E., Lewers, K.S., Luby, J.J., Bushakra, J., Sjulin, T.M., Hancock, J.F.: Using a linkage mapping approach to identify QTL for day-neutrality in the octaploid strawberry. — Plant Breed. 127: 94–101, 2008.
Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U., Weigel, D.: Integration of spatial and temporal information during floral induction in Arabidopsis. — Science 309: 1056–1059, 2005.
Wigge, P.A.: FT, a mobile developmental signal in plants. — Curr. Biol. 21: R374–R378, 2011.
Yeung, K., Seitz, T., Li, S., Janosch, P., McFerran, B., Kaiser, C., Fee, F., Katsanakis, K.D., Rose, D.W., Mischak, H., Sedivy, J.M., Kolch, W.: Suppression of Raf-1 kinase activity and MAP kinase signaling by RKIP. — Nature 401: 173–177, 1999.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: We are indebted to Mrs. S. Niwa and K. Kato for their valuable technical assistance. This research was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (Nos. 17580024 and 23658026).
Rights and permissions
About this article
Cite this article
Nakajima, R., Otagaki, S., Yamada, K. et al. Molecular cloning and expression analyses of FaFT, FaTFL, and FaAP1 genes in cultivated strawberry: their correlation to flower bud formation. Biol Plant 58, 641–648 (2014). https://doi.org/10.1007/s10535-014-0452-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-014-0452-3