The FLOWERING LOCUS T/TERMINAL FLOWER 1 Gene Family: Functional Evolution and Molecular Mechanisms

Molecular Plant

Volumn 8, Issue 7, 2015, Pages 983-997

  Wickland, Daniel P ^a   Hanzawa, Yoshie ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

evolution; flowering; FT; inflorescence architecture; PEBP; TFL1

Indexed keywords

ARABIDOPSIS PROTEIN; FT PROTEIN, ARABIDOPSIS; TFL1 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMISTRY; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FLOWERS;

EID: 84935876214     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2015.01.007     Document Type: Review

References (172)

1. M. Abe, Y. Kobayashi, S. Yamamoto, Y. Daimon, A. Yamaguchi, Y. Ikeda, H. Ichinoki, M. Notaguchi, K. Goto, and T. Araki FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex Science 309 2005 1052 1056
2. J. Adrian, S. Farrona, J.J. Reimer, M.C. Albani, G. Coupland, and F. Turck cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis Plant Cell 22 2010 1425 1440
3. J.A. Aguilar-Martínez, C. Poza-Carrión, and P. Cubas Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds Plant Cell 19 2007 458 472
4. J.H. Ahn, D. Miller, V.J. Winter, M.J. Banfield, J.H. Lee, S.Y. Yoo, S.R. Henz, R.L. Brady, and D. Weigel A divergent external loop confers antagonistic activity on floral regulators FT and TFL1 EMBO J. 25 2006 605 614
5. R. Amasino Seasonal and developmental timing of flowering Plant J. 61 2010 1001 1013
6. I. Amaya, O.J. Ratcliffe, and D.J. Bradley Expression of CENTRORADIALIS (CEN) and CEN-like genes in tobacco reveals a conserved mechanism controlling phase change in diverse species Plant Cell 11 1999 1405 1418
7. E. Ando, M. Ohnishi, Y. Wang, T. Matsushita, A. Watanabe, Y. Hayashi, M. Fujii, J.F. Ma, S. Inoue, and 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
8. F. Andrés, and G. Coupland The genetic basis of flowering responses to seasonal cues Nat. Rev. Genet. 13 2012 627 639
9. R.L. Bernard Two genes affecting stem termination in soybeans Crop Sci. 12 1972 235 239
10. B.K. Blackman, J.L. Strasburg, A.R. Raduski, S.D. Michaels, and L.H. Rieseberg The role of recently derived FT paralogs in sunflower domestication Curr. Biol. 20 2010 629 635
11. M.A. Blázquez, J.H. Ahn, and D. Weigel A thermosensory pathway controlling flowering time in Arabidopsis thaliana Nat. Genet. 33 2003 168 171
12. H. Böhlenius, T. Huang, L. Charbonnel-Campaa, A.M. Brunner, S. Jansson, S.H. Strauss, and O. Nilsson CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees Science 312 2006 1040 1043
13. P.K. Boss, L. Sreekantan, and M.R. Thomas A grapevine TFL1 homologue can delay flowering and alter floral development when overexpressed in heterologous species Funct. Plant Biol. 33 2006 31 41
14. D. Bradley, R. Carpenter, L. Copsey, C. Vincent, S. Rothstein, and E. Coen Control of inflorescence architecture in Antirrhinum Nature 379 1996 791 797
15. D. Bradley, O. Ratcliffe, C. Vincent, R. Carpenter, and E. Coen Inflorescence commitment and architecture in Arabidopsis Science 275 1997 80 83
16. Y. Cai, X. Chen, K. Xie, Q. Xing, Y. Wu, J. Li, C. Du, Z. Sun, and Z. Guo Dlf1, a WRKY transcription factor, is involved in the control of flowering time and plant height in rice PLoS One 9 2014 e102529
17. C. Campoli, B. Drosse, I. Searle, G. Coupland, and M. VonKorff Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS Plant J. 69 2012 868 880
18. M.J. Carmona, M. Calonje, and J.M. Martínez-Zapater The FT/TFL1 gene family in grapevine Plant Mol. Biol. 63 2007 637 650
19. H. Chautard, M. Jacquet, F. Schoentgen, N. Bureaud, and H. Bénédetti Tfs1p, a member of the PEBP family, inhibits the Ira2p but not the Ira1p Ras GTPase-activating protein in Saccharomyces cerevisiae Eukaryot. Cell. 3 2004 459 470
20. Y. Chen, and P. Jiang Characterization of peach TFL1 and comparison with FT/TFL1 gene families of the Rosaceae J. Am. Soc. Hortic. Sci. 138 2013 12 17
21. C.P. Coelho, M.A.A. Minow, A. Chalfun-Júnior, and J. Colasanti Putative sugarcane FT/TFL1 genes delay flowering time and alter reproductive architecture in Arabidopsis Front. Plant Sci. 5 2014 221
22. L. Conti, and D. Bradley TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture Plant Cell 19 2007 767 778
23. L. Corbesier, C. Vincent, S. Jang, F. Fornara, Q. Fan, I. Searle, A. Giakountis, S. Farrona, L. Gissot, C. Turnbull, and et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis Science 316 2007 1030 1033
24. O. Crane, T. Halaly, X. Pang, S. Lavee, A. Perl, R. Vankova, and E. Or Cytokinin-induced VvTFL1A expression may be involved in the control of grapevine fruitfulness Planta 235 2012 181 192
25. O.N. Danilevskaya, X. Meng, Z. Hou, E.V. Ananiev, and C.R. Simmons A genomic and expression compendium of the expanded PEBP gene family from maize Plant Physiol. 146 2008 250 264
26. O.N. Danilevskaya, X. Meng, and E.V. Ananiev Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-like genes in maize Plant Physiol. 153 2010 238 251
27. K. Doi, T. Izawa, T. Fuse, U. Yamanouchi, T. Kubo, Z. Shimatani, M. Yano, and A. Yoshimura Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1 Genes Dev. 18 2004 926 936
28. T. Endo, T. Shimada, H. Fujii, Y. Kobayashi, T. Araki, and M. Omura Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.) Transgenic Res. 14 2005 703 712
29. T. Esumi, R. Tao, and K. Yonemori Isolation of LEAFY and TERMINAL FLOWER 1 homologues from six fruit tree species in the subfamily Maloideae of the Rosaceae Sex. Plant Reprod. 17 2005 277 287
30. T. Esumi, C. Hagihara, Y. Kitamura, H. Yamane, and R. Tao Identification of an FT ortholog in Japanese apricot (Prunus mume Sieb. et Zucc.) J. Hortic. Sci. Biotechnol. 84 2009 149 154
31. T. Esumi, Y. Kitamura, C. Hagihara, H. Yamane, and R. Tao Identification of a TFL1 ortholog in Japanese apricot (Prunus mume Sieb. et Zucc.) Sci. Hortic. 125 2010 608 616
32. S. Faure, J. Higgins, A. Turner, and D.A. Laurie The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare) Genetics 176 2007 599 609
33. L. Fernandez, L. Torregrosa, V. Segura, A. Bouquet, and J.M. Martinez-Zapater Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine Plant J. 61 2010 545 557
34. F. Foucher, J. Morin, J. Courtiade, S. Cadioux, N. Ellis, M.J. Banfield, and C. Rameau DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea Plant Cell 15 2003 2742 2754
35. A. Freiman, L. Shlizerman, S. Golobovitch, Z. Yablovitz, R. Korchinsky, Y. Cohen, A. Samach, E. Chevreau, P.M. LeRoux, A. Patocchi, and et al. Development of a transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2 Planta 235 2012 1239 1251
36. M. Fukuda, S. Matsuo, K. Kikuchi, Y. Kawazu, R. Fujiyama, and I. Honda Isolation and functional characterization of the FLOWERING LOCUS T homolog, the LsFT gene, in lettuce J. Plant Physiol. 168 2011 1602 1607
37. N.D. González-Schain, M. Díaz-Mendoza, M. Zurczak, and P. Suárez-López Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner Plant J. 70 2012 678 690
38. X. Guo, Z. Zhao, J. Chen, X. Hu, and D. Luo A putative CENTRORADIALIS/TERMINAL FLOWER1-like gene, Ljcen1, plays a role in phase transition in Lotus japonicus J. Plant Physiol. 163 2006 436 444
39. J.L. Guo, C.L. Yu, C.Y. Fan, Q.-N. Lu, J.M. Yin, Y.F. Zhang, and Q. Yang Cloning and characterization of a potato TFL1 gene involved in tuberization regulation Plant Cell Tissue Organ Cult. 103 2010 103 109
40. S. Hanano, and K. Goto Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression Plant Cell 23 2011 3172 3184
41. Y. Hanzawa, T. Money, and D. Bradley A single amino acid converts a repressor to an activator of flowering Proc. Natl. Acad. Sci. USA 102 2005 7748 7753
42. L. Harig, F.A. Beinecke, J. Oltmanns, J. Muth, O. Müller, B. Rüping, R.M. Twyman, R. Fischer, D. Prüfer, and G.A. Noll Proteins from the FLOWERING LOCUS T-like subclade of the PEBP family act antagonistically to regulate floral initiation in tobacco Plant J. 72 2012 908 921
43. U. Hartmann, S. Höhmann, K. Nettesheim, E. Wisman, H. Saedler, and P. Huijser Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis Plant J. 21 2000 351 360
44. R. Hayama, S. Yokoi, S. Tamaki, M. Yano, and K. Shimamoto Adaptation of photoperiodic control pathways produces short-day flowering in rice Nature 422 2003 719 722
45. R. Hayama, B. Agashe, E. Luley, R. King, and G. Coupland A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis Plant Cell 19 2007 2988 3000
46. V. Hecht, F. Foucher, C. Ferrándiz, R. Macknight, C. Navarro, J. Morin, M.E. Vardy, N. Ellis, J.P. Beltrán, C. Rameau, and et al. Conservation of Arabidopsis flowering genes in model legumes Plant Physiol. 137 2005 1420 1434
47. V. Hecht, R.E. Laurie, J.K. Vander Schoor, S. Ridge, C.L. Knowles, L.C. Liew, F.C. Sussmilch, I.C. Murfet, R.C. Macknight, and J.L. Weller The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod Plant Cell 23 2011 147 161
48. H. Hedman, T. Källman, and U. Lagercrantz Early evolution of the MFT-like gene family in plants Plant Mol. Biol. 70 2009 359 369
49. Y. Higuchi, T. Narumi, A. Oda, Y. Nakano, K. Sumitomo, S. Fukai, and T. Hisamatsu The gated induction system of a systemic floral inhibitor, antiflorigen, determines obligate short-day flowering in chrysanthemums Proc. Natl. Acad. Sci. USA 110 2013 17137 17142
50. K. Hiraoka, A. Yamaguchi, M. Abe, and T. Araki The florigen genes FT and TSF modulate lateral shoot outgrowth in Arabidopsis thaliana Plant Cell Physiol. 54 2013 352 368
51. W.W.H. Ho, and D. Weigel Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T Plant Cell 26 2014 552 564
52. C.J. Hou, and C.H. Yang Functional analysis of FT and TFL1 orthologs from orchid (Oncidium Gower Ramsey) that regulate the vegetative to reproductive transition Plant Cell Physiol. 50 2009 1544 1557
53. C.Y. Hsu, J.P. Adams, H. Kim, K. No, C. Ma, S.H. Strauss, J. Drnevich, L. Vandervelde, J.D. Ellis, B.M. Rice, and et al. FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar Proc. Natl. Acad. Sci. USA 108 2011 10756 10761
54. N. Huang, W. Jane, J. Chen, and T. Yu Arabidopsis thaliana CENTRORADIALIS homologue (ATC) acts systemically to inhibit floral initiation in Arabidopsis Plant J. 72 2012 175 184
55. W. Huang, Z. Fang, S. Zeng, J. Zhang, K. Wu, Z. Chen, J. Teixeira da Silva, and J. Duan Molecular cloning and functional analysis of three FLOWERING LOCUS T (FT) homologous genes from Chinese cymbidium Int. J. Mol. Sci. 13 2012 11385 11398
56. T. Igasaki, Y. Watanabe, M. Nishiguchi, and N. Kotoda The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar Plant Cell Physiol. 49 2008 291 300
57. H. Ikegami, H. Nogata, Y. Inoue, S. Himeno, H. Yakushiji, and C. Hirata Expression of FcFT1, a FLOWERING LOCUS T-like gene, is regulated by light and associated with inflorescence differentiation in fig (Ficus carica L.) BMC Plant Biol. 13 2013 216
58. T. Imamura, T. Nakatsuka, A. Higuchi, M. Nishihara, and H. Takahashi The gentian orthologs of the FT/TFL1 gene family control floral initiation in Gentiana Plant Cell Physiol. 52 2011 1031 1041
59. H. Iwata, A. Gaston, A. Remay, T. Thouroude, J. Jeauffre, K. Kawamura, L.H.S. Oyant, T. Araki, B. Denoyes, and F. Foucher The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry Plant J. 69 2012 116 125
60. T. Izawa, T. Oikawa, N. Sugiyama, T. Tanisaka, M. Yano, and K. Shimamoto Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice Genes Dev. 16 2002 2006 2020
61. S. Jang, S. Torti, and G. Coupland Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis Plant J. 60 2009 614 625
62. C.S. Jensen, K. Salchert, and K.K. Nielsen A TERMINAL FLOWER1-like gene from perennial ryegrass involved in floral transition and axillary meristem identity Plant Physiol. 125 2001 1517 1528
63. K. Jiang, K.L. Liberatore, S.J. Park, J.P. Alvarez, and Z.B. Lippman Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture PLoS Genet. 9 2013 e1004043
64. I. Kardailsky, V.K. Shukla, J.H. Ahn, N. Dagenais, S.K. Christensen, J.T. Nguyen, J. Chory, M.J. Harrison, and D. Weigel Activation tagging of the floral inducer FT Science 286 1999 1962 1965
65. A. Karlgren, N. Gyllenstrand, T. Källman, J.F. Sundström, D. Moore, M. Lascoux, and U. Lagercrantz Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution Plant Physiol. 156 2011 1967 1977
66. A. Karlgren, N. Gyllenstrand, D. Clapham, and U. Lagercrantz FLOWERING LOCUS T/TERMINAL FLOWER1-like genes affect growth rhythm and bud set in Norway spruce Plant Physiol. 163 2013 792 803
67. R. Kikuchi, H. Kawahigashi, T. Ando, T. Tonooka, and H. Handa Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering Plant Physiol. 149 2009 1341 1353
68. T. Kinoshita, N. Ono, Y. Hayashi, S. Morimoto, S. Nakamura, M. Soda, Y. Kato, M. Ohnishi, T. Nakano, S. Inoue, and et al. FLOWERING LOCUS T regulates stomatal opening Curr. Biol. 21 2011 1232 1238
69. M. Klintenäs, P.A. Pin, R. Benlloch, P.K. Ingvarsson, and O. Nilsson Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage New Phytol. 196 2012 1260 1273
70. Y. Kobayashi, H. Kaya, K. Goto, M. Iwabuchi, and T. Araki A pair of related genes with antagonistic roles in mediating flowering signals Science 286 1999 1960 1962
71. S. Kojima, Y. Takahashi, Y. Kobayashi, L. Monna, T. Sasaki, T. Araki, and M. Yano Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions Plant Cell Physiol. 43 2002 1096 1105
72. R. Komiya, A. Ikegami, S. Tamaki, S. Yokoi, and K. Shimamoto Hd3a and RFT1 are essential for flowering in rice Development 135 2008 767 774
73. R. Komiya, S. Yokoi, and K. Shimamoto A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice Development 136 2009 3443 3450
74. F. Kong, B. Liu, Z. Xia, S. Sato, B.M. Kim, S. Watanabe, T. Yamada, S. Tabata, A. Kanazawa, K. Harada, and et al. Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean Plant Physiol. 154 2010 1220 1231
75. E.A. Koskela, K. Mouhu, M.C. Albani, T. Kurokura, M. Rantanen, D.J. Sargent, N.H. Battey, G. Coupland, P. Elomaa, and T. Hytönen Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca Plant Physiol. 159 2012 1043 1054
76. T. Kotake, S. Takada, K. Nakahigashi, M. Ohto, and K. Goto Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes Plant Cell Physiol. 44 2003 555 564
77. N. Kotoda, and M. Wada MdTFL1, a TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic Arabidopsis Plant Sci. 168 2005 95 104
78. N. Kotoda, H. Hayashi, M. Suzuki, M. Igarashi, Y. Hatsuyama, S.I. Kidou, T. Igasaki, M. Nishiguchi, K. Yano, T. Shimizu, and et al. Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus x domestica Borkh.) Plant Cell Physiol. 51 2010 561 575
79. S.V. Kumar, D. Lucyshyn, K.E. Jaeger, E. Alós, E. Alvey, N.P. Harberd, and P.A. Wigge Transcription factor PIF4 controls the thermosensory activation of flowering Nature 484 2012 242 245
80. M. Kwak, D. Velasco, and P. Gepts Mapping homologous sequences for determinacy and photoperiod sensitivity in common bean (Phaseolus vulgaris) J. Hered. 99 2008 283 291
81. M. Kwak, O. Toro, D.G. Debouck, and P. Gepts Multiple origins of the determinate growth habit in domesticated common bean (Phaseolus vulgaris) Ann. Bot. 110 2012 1573 1580
82. R.E. Laurie, P. Diwadkar, M. Jaudal, L. Zhang, V. Hecht, J. Wen, M. Tadege, K.S. Mysore, J. Putterill, J.L. Weller, and et al. The Medicago FLOWERING LOCUS T homolog, MtFTa1, is a key regulator of flowering time Plant Physiol. 156 2011 2207 2224
83. C.M. Lazakis, V. Coneva, and J. Colasanti ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize J. Exp. Bot. 62 2011 4833 4842
84. J.H. Lee, S.J. Yoo, S.H. Park, I. Hwang, J.S. Lee, and J.H. Ahn Role of SVP in the control of flowering time by ambient temperature in Arabidopsis Genes Dev. 21 2007 397 402
85. R. Lee, S. Baldwin, F. Kenel, J. McCallum, and R. Macknight FLOWERING LOCUS T genes control onion bulb formation and flowering Nat. Commun. 4 2013 2884
86. C. Li, and J. Dubcovsky Wheat FT protein regulates VRN1 transcription through interactions with FDL2 Plant J. 55 2008 543 554
87. X.F. Li, L.Y. Jia, J. Xu, X.J. Deng, Y. Wang, W. Zhang, X.P. Zhang, Q. Fang, D.M. Zhang, Y. Sun, and L. Xu FT-like NFT1 gene may play a role in flower transition induced by heat accumulation in Narcissus tazetta var. chinensis Plant Cell Physiol. 54 2013 270 281
88. C. Li, L. Luo, Q. Fu, L. Niu, and Z. Xu Isolation and functional characterization of JcFT, a FLOWERING LOCUS T (FT) homologous gene from the biofuel plant Jatropha curcas BMC Plant Biol. 14 2014 125
89. D.M. Li, F.B. Lu, G.F. Zhu, Y.B. Sun, H.L. Liu, J.W. Liu, and Z. Wang Molecular characterization and functional analysis of a Flowering locus T homolog gene from a Phalaenopsis orchid Genet. Mol. Res. 13 2014 5982 5994
90. Q. Li, C. Fan, X. Zhang, X. Wang, F. Wu, R. Hu, and Y. Fu Identification of a soybean MOTHER OF FT AND TFL1 homolog involved in regulation of seed germination PLoS One 9 2014 e99642
91. H. Liang, T. Zhebentyayeva, B. Olukolu, D. Wilde, G.L. Reighard, and A. Abbott Comparison of gene order in the chromosome region containing a TERMINALFLOWER 1 homolog in apricot and peach reveals microsynteny across angiosperms Plant Sci. 179 2010 390 398
92. E. Lifschitz, T. Eviatar, A. Rozman, A. Shalit, A. Goldshmidt, Z. Amsellem, J.P. Alvarez, and Y. Eshed The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli Proc. Natl. Acad. Sci. USA 103 2006 6398 6403
93. M.K. Lin, H. Belanger, Y.J. Lee, E. Varkonyi-Gasic, K.I. Taoka, E. Miura, B. Xoconostle-Cázares, K. Gendler, R.A. Jorgensen, B. Phinney, and et al. FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits Plant Cell 19 2007 1488 1506
94. B. Liu, S. Watanabe, T. Uchiyama, F. Kong, A. Kanazawa, Z. Xia, A. Nagamatsu, M. Arai, T. Yamada, K. Kitamura, and et al. The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1 Plant Physiol. 153 2010 198 210
95. L. Liu, C. Liu, X. Hou, W. Xi, L. Shen, Z. Tao, Y. Wang, and H. Yu FTIP1 is an essential regulator required for florigen transport PLoS Biol. 10 2012 e1001313
96. L. Lv, J. Duan, J. Xie, C. Wei, Y. Liu, S. Liu, and G. Sun Isolation and characterization of a FLOWERING LOCUS T homolog from pineapple (Ananas comosus (L.) Merr) Gene 505 2012 368 373
97. B. Lv, R. Nitcher, X. Han, S. Wang, F. Ni, K. Li, S. Pearce, J. Wu, J. Dubcovsky, and D. Fu Characterization of FLOWERING LOCUS T1 (FT1) gene in Brachypodium and wheat PLoS One 9 2014 e94171
98. C. Martínez, E. Pons, G. Prats, and J. León Salicylic acid regulates flowering time and links defence responses and reproductive development Plant J. 37 2004 209 217
99. K. Matsubara, U. Yamanouchi, Z.X. Wang, Y. Minobe, T. Izawa, and M. Yano Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1 Plant Physiol. 148 2008 1425 1435
100. N. Matsuda, K. Ikeda, M. Kurosaka, T. Takashina, K. Isuzugawa, T. Endo, and M. Omura Early flowering phenotype in transgenic pears (Pyrus communis L.) expressing the CiFT gene J. Japanese Soc. Hortic. Sci. 78 2009 410 416
101. X. Meng, M.G. Muszynski, and O.N. Danilevskaya The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize Plant Cell 23 2011 942 960
102. S.D. Michaels, and R.M. Amasino FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering Plant Cell 11 1999 949 956
103. S.D. Michaels, E. Himelblau, S.Y. Kim, F.M. Schomburg, R.M. Amasino, and E.H. Wisconsin Integration of flowering signals in winter-annual Arabidopsis Plant Physiol. 137 2005 149 156
104. N. Mimida, N. Kotoda, T. Ueda, M. Igarashi, Y. Hatsuyama, H. Iwanami, S. Moriya, and K. Abe Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus x domestica Borkh.) Plant Cell Physiol. 50 2009 394 412
105. R. Mohamed, C.T. Wang, C. Ma, O. Shevchenko, S.J. Dye, J.R. Puzey, E. Etherington, X. Sheng, R. Meilan, S.H. Strauss, and et al. Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus Plant J. 62 2010 674 688
106. M.G. Muszynski, T. Dam, B. Li, D.M. Shirbroun, Z. Hou, E. Bruggemann, R. Archibald, E.V. Ananiev, and O.N. Danilevskaya delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize Plant Physiol. 142 2006 1523 1536
107. E. Mutasa-Göttgens, and P. Hedden Gibberellin as a factor in floral regulatory networks J. Exp. Bot. 60 2009 1979 1989
108. M. Nakagawa, K. Shimamoto, and J. Kyozuka Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice Plant J. 29 2002 743 750
109. S. Nakamura, F. Abe, H. Kawahigashi, K. Nakazono, A. Tagiri, T. Matsumoto, S. Utsugi, T. Ogawa, H. Handa, H. Ishida, and et al. A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination Plant Cell 23 2011 3215 3229
110. Y. Nakamura, F. Andrés, K. Kanehara, Y. Liu, P. Dörmann, and G. Coupland Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering Nat. Commun. 5 2014 3553
111. Y. Nakano, Y. Higuchi, K. Sumitomo, and T. Hisamatsu Flowering retardation by high temperature in chrysanthemums: involvement of FLOWERING LOCUS T-like 3 gene repression J. Exp. Bot. 64 2013 909 920
112. H. Nan, D. Cao, D. Zhang, Y. Li, S. Lu, L. Tang, X. Yuan, B. Liu, and F. Kong GmFT2a and GmFT5a redundantly and differentially regulate flowering through interaction with and upregulation of the bZIP transcription factor GmFDL19 in soybean PLoS One 9 2014 e97669
113. C. Navarro, J.A. Abelenda, E. Cruz-Oró, C.A. Cuéllar, S. Tamaki, J. Silva, K. Shimamoto, and S. Prat Control of flowering and storage organ formation in potato by FLOWERING LOCUS T Nature 478 2011 119 122
114. F. Nishikawa, T. Endo, T. Shimada, H. Fujii, T. Shimizu, M. Omura, and Y. Ikoma Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.) J. Exp. Bot. 58 2007 3915 3927
115. M. Niwa, Y. Daimon, K. Kurotani, A. Higo, J.L. Pruneda-Paz, G. Breton, N. Mitsuda, S.A. Kay, M. Ohme-Takagi, M. Endo, and et al. BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis Plant Cell 25 2013 1228 1242
116. M. Notaguchi, M. Abe, T. Kimura, Y. Daimon, T. Kobayashi, A. Yamaguchi, Y. Tomita, K. Dohi, M. Mori, and T. Araki Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering Plant Cell Physiol. 49 2008 1645 1658
117. T. Noy-Porat, D. Cohen, D. Mathew, A. Eshel, R. Kamenetsky, and M.A. Flaishman Turned on by heat: differential expression of FT and LFY-like genes in Narcissus tazetta during floral transition J. Exp. Bot. 64 2013 3273 3284
118. A. Oda, T. Narumi, T. Li, T. Kando, Y. Higuchi, K. Sumitomo, S. Fukai, and T. Hisamatsu CsFTL3, a chrysanthemum FLOWERING LOCUS T-like gene, is a key regulator of photoperiodic flowering in chrysanthemums J. Exp. Bot. 63 2012 1461 1477
119. N. Ono, K. Ishida, T. Yamashino, H. Nakanishi, S. Sato, S. Tabata, and T. Mizuno Genomewide characterization of the light-responsive and clock-controlled output pathways in Lotus japonicus with special emphasis of its uniqueness Plant Cell Physiol. 51 2010 1800 1814
120. S.J. Park, S.L. Kim, S. Lee, B.I. Je, H.L. Piao, S.H. Park, C.M. Kim, C.H. Ryu, S.H. Park, Y. Xuan, and et al. Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod Plant J. 56 2008 1018 1029
121. L.J. Pillitteri, C.J. Lovatt, and L.L. Walling Isolation and characterization of a TERMINAL FLOWER homolog and its correlation with juvenility in citrus Plant Physiol. 135 2004 1540 1551
122. P.A. Pin, R. Benlloch, D. Bonnet, E. Wremerth-Weich, T. Kraft, J.J.L. Gielen, and O. Nilsson An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet Science 330 2010 1397 1400
123. P.A. Pin, W. Zhang, S.H. Vogt, N. Dally, B. Büttner, G. Schulze-Buxloh, N.S. Jelly, T.Y.P. Chia, E.S. Mutasa-Göttgens, J.C. Dohm, and et al. The role of a pseudo-response regulator gene in life cycle adaptation and domestication of beet Curr. Biol. 22 2012 1095 1101
124. L. Pnueli, L. Carmel-Goren, D. Hareven, T. Gutfinger, J. Alvarez, M. Ganal, D. Zamir, and E. Lifschitz The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1 Development 125 1998 1979 1989
125. L. Pnueli, T. Gutfinger, D. Hareven, O. Ben-Naim, N. Ron, N. Adir, and E. Lifschitz Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering Plant Cell 13 2001 2687 2702
126. J. Putterill, F. Robson, K. Lee, R. Simon, and 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
127. J. Putterill, L. Zhang, C.C. Yeoh, M. Balcerowicz, M. Jaudal, and E.V. Gasic FT genes and regulation of flowering in the legume Medicago truncatula Funct. Plant Biol. 40 2013 1199 1207
128. M. Randoux, J.M. Davière, J. Jeauffre, T. Thouroude, S. Pierre, Y. Toualbia, J. Perrotte, J.P. Reynoird, M.J. Jammes, L. Hibrand-Saint Oyant, and et al. RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose New Phytol. 202 2014 161 173
129. M. Rantanen, T. Kurokura, K. Mouhu, P. Pinho, E. Tetri, L. Halonen, P. Palonen, P. Elomaa, and T. Hytönen Light quality regulates flowering in FvFT1/FvTFL1 dependent manner in the woodland strawberry Fragaria vesca Front. Plant Sci. 5 2014 271
130. O.J. Ratcliffe, I. Amaya, C.A. Vincent, S. Rothstein, R. Carpenter, E.S. Coen, and D.J. Bradley A common mechanism controls the life cycle and architecture of plants Development 125 1998 1609 1615
131. O.J. Ratcliffe, D.J. Bradley, and E.S. Coen Separation of shoot and floral identity in Arabidopsis Development 126 1999 1109 1120
132. A. Remay, D. Lalanne, T. Thouroude, F. Le Couviour, L. Hibrand-Saint Oyant, and F. Foucher A survey of flowering genes reveals the role of gibberellins in floral control in rose Theor. Appl. Genet. 119 2009 767 781
133. S.L. Repinski, M. Kwak, and P. Gepts The common bean growth habit gene PvTFL1y is a functional homolog of Arabidopsis TFL1 Theor. Appl. Genet. 124 2012 1539 1547
134. J.Y. Ryu, C.-M. Park, and P.J. Seo The floral repressor BROTHER OF FT AND TFL1 (BFT) modulates flowering initiation under high salinity in Arabidopsis Mol. Cells 32 2011 295 303
135. J.Y. Ryu, H.J. Lee, P.J. Seo, J.H. Jung, J.H. Ahn, and C.M. Park The Arabidopsis floral repressor BFT delays flowering by competing with FT for FD binding under high salinity Mol. Plant 7 2014 377 387
136. I. Searle, Y. He, F. Turck, C. Vincent, F. Fornara, S. Kröber, R.A. Amasino, and G. Coupland The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis Genes Dev. 20 2006 898 912
137. A. Shalit, A. Rozman, A. Goldshmidt, J.P. Alvarez, J.L. Bowman, Y. Eshed, and E. Lifschitz The flowering hormone florigen functions as a general systemic regulator of growth and termination Proc. Natl. Acad. Sci. USA 106 2009 8392 8397
138. S. Shannon, and D.R. Meeks-Wagner A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development Plant Cell 3 1991 877 892
139. R. Simon, M.I. Igeño, and G. Coupland Activation of floral meristem identity genes in Arabidopsis Nature 384 1996 59 62
140. S.R. Singer, L.P. Hsiung, and S.C. Huber Determinate (det) mutant of Pisum sativum (Leguminosae: Papilionoideae) exhibits an indeterminate growth pattern Am. J. Bot. 77 1990 1330 1335
141. E.J. Sohn, M. Rojas-Pierce, S. Pan, C. Carter, A. Serrano-Mislata, F. Madueño, E. Rojo, M. Surpin, and N.V. Raikhel The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole Proc. Natl. Acad. Sci. USA 104 2007 18801 18806
142. G. Song, A. Walworth, D. Zhao, N. Jiang, and J.F. Hancock The Vaccinium corymbosum FLOWERING LOCUS T-like gene (VcFT): a flowering activator reverses photoperiodic and chilling requirements in blueberry Plant Cell Rep. 32 2013 1759 1769
143. P. Suárez-López, K. Wheatley, F. Robson, H. Onouchi, F. Valverde, and G. Coupland CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis Nature 410 2001 1116 1120
144. H. Sun, Z. Jia, D. Cao, B. Jiang, C. Wu, W. Hou, Y. Liu, Z. Fei, D. Zhao, and T. Han GmFT2a, a soybean homolog of FLOWERING LOCUS T, is involved in flowering transition and maintenance PLoS One 6 2011 e29238
145. S. Tamaki, S. Matsuo, H.L. Wong, S. Yokoi, and K. Shimamoto Hd3a protein is a mobile flowering signal in rice Science 316 2007 1033 1036
146. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: Molecular Evolutionary Genetics Analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729
147. K. Taoka, I. Ohki, H. Tsuji, K. Furuita, K. Hayashi, T. Yanase, M. Yamaguchi, C. Nakashima, Y.A. Purwestri, S. Tamaki, and et al. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen Nature 476 2011 332 335
148. P. Teper-Bamnolker, and A. Samach The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves Plant Cell 17 2005 2661 2675
149. Z. Tian, X. Wang, R. Lee, Y. Li, J.E. Specht, R.L. Nelson, P.E. McClean, L. Qiu, and J. Ma Artificial selection for determinate growth habit in soybean Proc. Natl. Acad. Sci. USA 107 2010 8563 8568
150. F. Turck, F. Fornara, and G. Coupland Regulation and identity of florigen: FLOWERING LOCUS T moves center stage Annu. Rev. Plant Biol. 59 2008 573 594
151. F. Valverde CONSTANS and the evolutionary origin of photoperiodic timing of flowering J. Exp. Bot. 62 2011 2453 2463
152. E. Varkonyi-Gasic, S.M.A. Moss, C. Voogd, T. Wang, J. Putterill, and R.P. Hellens Homologs of FT, CEN and FD respond to developmental and environmental signals affecting growth and flowering in the perennial vine kiwifruit New Phytol. 198 2013 732 746
153. K.C. Wada, M. Yamada, T. Shiraya, and K. Takeno Salicylic acid and the flowering gene FLOWERING LOCUS T homolog are involved in poor-nutrition stress-induced flowering of Pharbitis nil J. Plant Physiol. 167 2010 447 452
154. Y. Wang, and P.M. Pijut Isolation and characterization of a TERMINAL FLOWER 1 homolog from Prunus serotina Ehrh Tree Physiol. 33 2013 855 865
155. R. Wang, M.C. Albani, C. Vincent, S. Bergonzi, M. Luan, Y. Bai, C. Kiefer, R. Castillo, and G. Coupland Aa TFL1 confers an age-dependent response to vernalization in perennial Arabis alpina Plant Cell 23 2011 1307 1321
156. P.A. Wigge, M.C. Kim, K.E. Jaeger, W. Busch, M. Schmid, J.U. Lohmann, and D. Weigel Integration of spatial and temporal information during floral induction in Arabidopsis Science 309 2005 1056 1059
157. P. Winterhagen, P. Tiyayon, A. Samach, M. Hegele, and J.N. Wünsche Isolation and characterization of FLOWERING LOCUS T subforms and APETALA1 of the subtropical fruit tree Dimocarpus longan Plant Physiol. Biochem. 71 2013 184 190
158. C. Wu, C. You, C. Li, T. Long, G. Chen, M.E. Byrne, and Q. Zhang RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice Proc. Natl. Acad. Sci. USA 105 2008 12915 12920
159. L. Wu, D. Liu, J. Wu, R. Zhang, Z. Qin, D. Liu, A. Li, D. Fu, W. Zhai, and L. Mao Regulation of FLOWERING LOCUS T by a microRNA in Brachypodium distachyon Plant Cell 25 2013 4363 4377
160. W. Wu, X.M. Zheng, G. Lu, Z. Zhong, H.H. Gao, L. Chen, C. Wu, H.-J.H. Wang, Q. Wang, K. Zhou, and et al. Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia Proc. Natl. Acad. Sci. USA 11025 2013 2775 2780
161. W. Xi, C. Liu, X. Hou, and H. Yu MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis Plant Cell 22 2010 1733 1748
162. L. Xiang, X. Li, D. Qin, F. Guo, C. Wu, L. Miao, and C. Sun 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 2012 98 105
163. M. Yamada, and K. Takeno Stress and salicylic acid induce the expression of PnFT2 in the regulation of the stress-induced flowering of Pharbitis nil J. Plant Physiol. 171 2014 205 212
164. A. Yamaguchi, Y. Kobayashi, K. Goto, M. Abe, and T. Araki TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT Plant Cell Physiol. 46 2005 1175 1189
165. L. Yan, D. Fu, C. Li, A. Blechl, G. Tranquilli, M. Bonafede, A. Sanchez, M. Valarik, S. Yasuda, and J. Dubcovsky The wheat and barley vernalization gene VRN3 is an orthologue of FT Proc. Natl. Acad. Sci. USA 103 2006 19581 19586
166. J. Ye, Y. Geng, B. Zhang, H. Mao, J. Qu, and N.-H. Chua The Jatropha FT ortholog is a systemic signal regulating growth and flowering time Biotechnol. Biofuels 7 2014 10.1186/1754-6834-7-91
167. K. Yeung, T. Seitz, S. Li, P. Janosch, B. McFerran, C. Kaiser, F. Fee, K.D. Katsanakis, D.W. Rose, H. Mischak, and et al. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP Nature 401 1999 173 177
168. S. Yoo, I. Kardailsky, J.S. Lee, D. Weigel, and J.H. Ahn Acceleration of flowering by overexpression of MFT (MOTHER OF FT AND TFL1) Mol. Cells 17 2004 95 101
169. S.J. Yoo, K.S. Chung, S.H. Jung, S.Y. Yoo, J.S. Lee, and J.H. Ahn BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis Plant J. 63 2010 241 253
170. S.C. Yoo, C. Chen, M. Rojas, Y. Daimon, B.K. Ham, T. Araki, and W.J. Lucas Phloem long-distance delivery of FLOWERING LOCUS T (FT) to the apex Plant J. 75 2013 456 468
171. H. Zhai, S. Lü, S. Liang, H. Wu, X. Zhang, B. Liu, F. Kong, X. Yuan, J. Li, and Z. Xia GmFT4, a homolog of FLOWERING LOCUS T, is positively regulated by E1 and functions as a flowering repressor in soybean PLoS One 9 2014 e89030
172. J. Zhang, G. Liu, C. Guo, Y. He, Z. Li, G. Ning, X. Shi, and M. Bao The FLOWERING LOCUS T orthologous gene of Platanus acerifolia is expressed as alternatively spliced forms with distinct spatial and temporal patterns Plant Biol. (Stuttg) 13 2011 809 820