Seasonal and developmental timing of flowering

Plant Journal

Volumn 61, Issue 6, 2010, Pages 1001-1013

  Amasino, Richard ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Evolution; Florigen vernalization; Flowering; Juvenile; Photoperiod

Indexed keywords

ARABIDOPSIS; DAY-LENGTH; FLOWERING-TIME; LIFE HISTORY; MOBILE SIGNALS; MOLECULAR LEVELS; PLANT SPECIES; REPRODUCTIVE SUCCESS; SHOOT APICAL MERISTEMS;

PHASE TRANSITIONS; TIME MEASUREMENT;

PLANTS (BOTANY);

PHYTOHORMONE;

ARABIDOPSIS; ARTICLE; COLD; FLOWER; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHOTOPERIODICITY; PHYSIOLOGY; SEASON;

ARABIDOPSIS; COLD TEMPERATURE; EPIGENESIS, GENETIC; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; PHOTOPERIOD; PLANT GROWTH REGULATORS; SEASONS;

ARABIDOPSIS;

EID: 77950420409     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04148.x     Document Type: Article

References (157)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K. Araki, T. (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science, 309, 1052 1056.
2. Adrian, J., Torti, S. Turck, F. (2009) From decision to commitment: the molecular memory of flowering. Mol. Plant, 2, 628 642.
3. Agger, K., Christensen, J., Cloos, P.A. Helin, K. (2008) The emerging functions of histone demethylases. Curr. Opin. Genet. Dev. 18, 159 168.
4. Amasino, R. (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell, 16, 2553 2559.
5. An, H., Roussot, C., Suarez-Lopez, P. et al. (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development, 131, 3615 3626.
6. Aukerman, M.J. Sakai, H. (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell, 15, 2730 2741.
7. Ausin, I., Alonso-Blanco, C., Jarillo, J.A., Ruiz-Garcia, L. Martinez-Zapater, J.M. (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36, 162 166.
8. Ayre, B.G. Turgeon, R. (2004) Graft transmission of a floral stimulant derived from CONSTANS. Plant Physiol. 135, 2271 2278.
9. Bastow, R., Mylne, J.S., Lister, C., Lippman, Z., Martienssen, R.A. Dean, C. (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature, 427, 164 167.
10. Baurle, I. Dean, C. (2008) Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE, 3, e2733.
11. Baurle, I., Smith, L., Baulcombe, D.C. Dean, C. (2007) Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science, 318, 109 112.
12. Bernier, G., Kinet, J.M. Sachs, R.M., eds 1981). The Control of Floral Evocation and Morphogenesis.
13. Bezerra, I.C., Michaels, S.D., Schomburg, F.M. Amasino, R.M. (2004) Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis. Plant J. 40, 112 119.
14. Blazquez, M.A., Green, R., Nilsson, O., Sussman, M.R. Weigel, D. (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell, 10, 791 800.
15. Bohlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H. Nilsson, O. (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science, 312, 1040 1043.
16. Brock, M.T., Stinchcombe, J.R. Weinig, C. (2009) Indirect effects of FRIGIDA: floral trait (co)variances are altered by seasonally variable abiotic factors associated with flowering time. J. Evol. Biol. 22, 1826 1838.
17. Buckler, E.S., Holland, J.B., Bradbury, P.J. et al. (2009) The genetic architecture of maize flowering time. Science, 325, 714 718.
18. Burn, J.E., Smyth, D.R., Peacock, W.J. Dennis, E.S. (1993a) Genes conferring late flowering in Arabidopsis thaliana. Genetica, 90, 147 155.
19. Burn, J.E., Bagnall, D.J., Metzger, J.D., Dennis, E.S. Peacock, W.J. (1993b) DNA methylation, vernalization, and the initiation of flowering. Proc. Natl Acad. Sci. USA, 90, 287 291.
20. Cao, R., Wang, H., He, J., Erdjument-Bromage, H., Tempst, P. Zhang, Y. (2008) Role of hPHF1 in H3K27 methylation and Hox gene silencing. Mol. Cell. Biol. 28, 1862 1872.
21. Cardon, G., Hohmann, S., Klein, J., Nettesheim, K., Saedler, H. Huijser, P. (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene, 237, 91 104.
22. Chailakhyan, M.K. (1936) New facts in support of the hormonal theory of plant development. C. R. (Dokl.) Acad. Sci. USSR, 13, 79 83.
23. Chan, S.K. Struhl, G. (1997) Sequence-specific RNA binding by Bicoid. Nature, 388, 634.
24. Choi, J., Hyun, Y., Kang, M.J. et al. (2009) Resetting and regulation of flowering locus C expression during Arabidopsis reproductive development. Plant J. 57, 918 931.
25. Chouard, P. (1960) Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 11, 191 238.
26. Chuck, G., Cigan, A.M., Saeteurn, K. Hake, S. (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39, 544 549.
27. Clarke, J.H. Dean, C. (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol. Gen. Genet. 242, 81 89.
28. Corbesier, L., Vincent, C., Jang, S. et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 316, 1030 1033.
29. De Lucia, F., Crevillen, P., Jones, A.M., Greb, T. Dean, C. (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl. Acad. Sci. USA, 105, 16831 16836.
30. Distelfeld, A., Li, C. Dubcovsky, J. (2009) Regulation of flowering in temperate cereals. Curr. Opin. Plant Biol. 12, 178 184.
31. Doyle, M.R. Amasino, R.M. (2009) A single amino acid change in the enhancer of zeste ortholog CURLY LEAF results in vernalization-independent, rapid flowering in Arabidopsis. Plant Physiol. 151, 1688 1697.
32. Finnegan, E.J. Dennis, E.S. (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17, 1978 1983.
33. Fornara, F. Coupland, G. (2009) Plant phase transitions make a SPLash. Cell, 138, 625 627.
34. Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., Coupland, G. Putterill, J. (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18, 4679 4688.
35. Fujiwara, S., Oda, A., Yoshida, R. et al. (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell, 20, 2960 2971.
36. Garner, W.W. Allard, H.A. (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J. Agric. Res. 18, 553 606.
37. Gendall, A.R., Levy, Y.Y., Wilson, A. Dean, C. (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell, 107, 525 535.
38. Geraldo, N., Baurle, I., Kidou, S., Hu, X. Dean, C. (2009) FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol. 150, 1611 1618.
39. Greb, T., Mylne, J.S., Crevillen, P., Geraldo, N., An, H., Gendall, A.R. Dean, C. (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17, 73 78.
40. Greenup, A., Peacock, W.J., Dennis, E.S. Trevaskis, B. (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot. 103, 1165 1172.
41. Gregory, F.G. Hussey, G.G. (1953) Photoperiodic responses of Arabidopsis thaliana. Proc. Linn. Soc. Lond. 164, 137 139.
42. Gregory, B.D., Yazaki, J. Ecker, J.R. (2008) Utilizing tiling microarrays for whole-genome analysis in plants. Plant J. 53, 636 644.
43. Harmer, S.L. (2009) The circadian system in higher plants. Annu. Rev. Plant Biol. 60, 357 377.
44. He, Y. (2009). Control of the transition to flowering by chromatin modifications. Mol. Plant, 2, 554 564.
45. He, Y., Michaels, S.D. Amasino, R.M. (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science, 302, 1751 1754.
46. Helliwell, C.A., Wood, C.C., Robertson, M., James Peacock, W. Dennis, E.S. (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J. 46, 183 192.
47. Henderson, I.R., Liu, F., Drea, S., Simpson, G.G. Dean, C. (2005) An allelic series reveals essential roles for FY in plant development in addition to flowering-time control. Development, 132, 3597 3607.
48. Hennig, L., Bouveret, R. Gruissem, W. (2005) MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol. 15, 295 302.
49. Hepworth, S.R., Valverde, F., Ravenscroft, D., Mouradov, A. Coupland, G. (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21, 4327 4337.
50. Imaizumi, T. (2009) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr. Opin. Plant Biol. 13, 83 89.
51. Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A. Kay, S.A. (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science, 309, 293 297.
52. Jaeger, K.E. Wigge, P.A. (2007) FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17, 1050 1054.
53. Jang, S., Marchal, V., Panigrahi, K.C., Wenkel, S., Soppe, W., Deng, X.W., Valverde, F. Coupland, G. (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J. 27, 1277 1288.
54. Jiang, D., Gu, X. He, Y. (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell, 21, 1733 1746.
55. Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R. Dean, C. (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science, 290, 344 347.
56. Jung, J.H., Seo, Y.H., Seo, P.J., Reyes, J.L., Yun, J., Chua, N.H. Park, C.M. (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell, 19, 2736 2748.
57. Kardailsky, I., Shukla, V.K., Ahn, J.H., Dagenais, N., Christensen, S.K., Nguyen, J.T., Chory, J., Harrison, M.J. Weigel, D. (1999) Activation tagging of the floral inducer FT. Science, 286, 1962 1965.
58. Kim, H.J., Hyun, Y., Park, J.Y., Park, M.J., Park, M.K., Kim, M.D., Lee, M.H., Moon, J., Lee, I. Kim, J. (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet. 36, 167 171.
59. Kim, D.H., Doyle, M.R., Sung, S. Amasino, R.M. (2009) Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell. Dev. Biol. 25, 277 299.
60. Klebs, G. (1918) Über die Blutentbildung bei Sempervivum. Flora (Jena), 128, 111 112.
61. Knott, J.E. (1934) Effect of a localized photoperiod on spinach. Proc. Amer. Soc. Hort. Sci. 31, 152 154.
62. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. Araki, T. (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science, 286, 1960 1962.
63. Koornneef, M., Hanhart, C.J. van der Veen, J.H. (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57 66.
64. Koornneef, M., Blankestijn-de Vries, H., Hanhart, C., Soppe, W. Peeters, T. (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J. 6, 911 919.
65. Koornneef, M., Alonso-Blanco, C., Blankestijn-de Vries, H., Hanhart, C.J. Peeters, A.J. (1998) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics, 148, 885 892.
66. Lang, A. (1965) Physiology of flower initiation. In Encyclopedia of Plant Physiology (Ruhland, W., ed).
67. Laubinger, S., Marchal, V., Le Gourrierec, J., Wenkel, S., Adrian, J., Jang, S., Kulajta, C., Braun, H., Coupland, G. Hoecker, U. (2006) Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development, 133, 3213 3222.
68. Laubinger, S., Sachsenberg, T., Zeller, G., Busch, W., Lohmann, J.U., Ratsch, G. Weigel, D. (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 105, 8795 8800.
69. Lee, I., Bleecker, A. Amasino, R. (1993) Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet. 237, 171 176.
70. Lee, I., Michaels, S.D., Masshardt, A.S. Amasino, R.M. (1994) The late-flowering phenotype of FRIGIDA and LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6, 903 909.
71. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S. Ahn, J.H. (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 21, 397 402.
72. Lee, J., Oh, M., Park, H. Lee, I. (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J. 55, 832 843.
73. Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R. Dean, C. (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science, 297, 243 246.
74. Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E. Yu, H. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell, 15, 110 120.
75. Liljegren, S.J., Gustafson-Brown, C., Pinyopich, A., Ditta, G.S. Yanofsky, M.F. (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell, 11, 1007 1018.
76. Lim, M.H., Kim, J., Kim, Y.S., Chung, K.S., Seo, Y.H., Lee, I., Hong, C.B., Kim, H.J. Park, C.M. (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell, 16, 731 740.
77. Lin, M.K., Belanger, H., Lee, Y.J. et al. (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell, 19, 1488 1506.
78. Liu, C., Chen, H., Er, H.L., Soo, H.M., Kumar, P.P., Han, J.H., Liou, Y.C. Yu, H. (2008a) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development, 135, 1481 1491.
79. Liu, L.J., Zhang, Y.C., Li, Q.H., Sang, Y., Mao, J., Lian, H.L., Wang, L. Yang, H.Q. (2008b) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell, 20, 292 306.
80. Macknight, R., Bancroft, I., Page, T. et al. (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell, 89, 737 745.
81. Maison, C. Almouzni, G. (2004) HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5, 296 304.
82. Manzano, D., Marquardt, S., Jones, A.M., Baurle, I., Liu, F. Dean, C. (2009) Altered interactions within FY/AtCPSF complexes required for Arabidopsis FCA-mediated chromatin silencing. Proc. Natl. Acad. Sci. USA, 106, 8772 8777.
83. Martinez-Zapater, J.M. Somerville, C.R. (1990) Effect of light quality and vernalization of late-flowering mutants of Arabidopsis thaliana. Plant Physiol. 92, 770 776.
84. Mas, P. Yanovsky, M.J. (2009) Time for circadian rhythms: plants get synchronized. Curr. Opin. Plant Biol. 12, 574 579.
85. Mathieu, J., Yant, L.J., Murdter, F., Kuttner, F. Schmid, M. (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol. 7, e1000148.
86. McClung, C.R. (2009) Circadian rhythms. Linking the loops. Science, 323, 1440 1441.
87. McKay, J.K., Richards, J.H. Mitchell-Olds, T. (2003) Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol. Ecol. 12, 1137 1151.
88. McMillan, C. (1974) Photoperiodic adaptation of Xanthium-strumarium in Europe Asia-minor and Northern Africa. Can. J. Bot. 52, 1779 1792.
89. Mellor, J. (2006) It takes a PHD to read the histone code. Cell, 126, 22 24.
90. Michaels, S.D. (2009) Flowering time regulation produces much fruit. Curr. Opin. Plant Biol. 12, 75 80.
91. Michaels, S.D. Amasino, R.M. (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell, 11, 949 956.
92. Michaels, S.D. Amasino, R.M. (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell, 13, 935 942.
93. Michaels, S.D., Bezerra, I.C. Amasino, R.M. (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proc. Natl. Acad. Sci. USA, 101, 3281 3285.
94. Michaels, S.D., Himelblau, E., Kim, S.Y., Schomburg, F.M. Amasino, R.M. (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137, 149 156.
95. Muller, J., Hart, C.M., Francis, N.J., Vargas, M.L., Sengupta, A., Wild, B., Miller, E.L., O'Connor, M.B., Kingston, R.E. Simon, J.A. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell, 111, 197 208.
96. Mylne, J.S., Barrett, L., Tessadori, F., Mesnage, S., Johnson, L., Bernatavichute, Y.V., Jacobsen, S.E., Fransz, P. Dean, C. (2006) LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl. Acad. Sci. USA, 103, 5012 5017.
97. Napp-Zinn, K. (1987) Vernalization: environmental and genetic regulation. In Manipulation of Flowering (Atherton, J.G., ed).
98. Niu, L., Zhang, Y., Pei, Y., Liu, C. Cao, X. (2008) Redundant requirement for a pair of PROTEIN ARGININE METHYLTRANSFERASE4 homologs for the proper regulation of Arabidopsis flowering time. Plant Physiol. 148, 490 503.
99. Noh, B., Lee, S.H., Kim, H.J., Yi, G., Shin, E.A., Lee, M., Jung, K.J., Doyle, M.R., Amasino, R.M. Noh, Y.S. (2004) Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell, 16, 2601 2613.
100. Park, D.H., Somers, D.E., Kim, Y.S., Choy, Y.H., Lim, H.K., Soh, M.S., Kim, H.J., Kay, S.A. Nam, H.G. (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science, 285, 1579 1582.
101. Poethig, R.S. (2003) Phase change and the regulation of developmental timing in plants. Science, 301, 334 336.
102. Poethig, R.S. (2009) Small RNAs and developmental timing in plants. Curr. Opin. Genet. Dev. 19, 374 378.
103. Prigge, M.J. Wagner, D.R. (2001) The Arabidopsis serrate gene encodes a zinc-finger protein required for normal shoot development. Plant Cell, 13, 1263 1279.
104. Putterill, J., Robson, F., Lee, K., Simon, R. Coupland, G. (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell, 80, 847 857.
105. Ratcliffe, O.J., Kumimoto, R.W., Wong, B.J. Riechmann, J.L. (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell, 15, 1159 1169.
106. Ray, P.M. Alexander, W.E. (1966) Photoperiodic adaptation to latitude in Xanthium strumarium. Am. J. Bot. 43, 806 816.
107. Redei, G.P. (1962) Supervital mutants in Arabidopsis. Genetics, 47, 443 460.
108. Ruiz-Garcia, L., Madueno, F., Wilkinson, M., Haugn, G., Salinas, J. Martinez-Zapater, J.M. (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell, 9, 1921 1934.
109. Sablowski, R. (2007) Flowering and determinacy in Arabidopsis. J. Exp. Bot. 58, 899 907.
110. Sarma, K., Margueron, R., Ivanov, A., Pirrotta, V. Reinberg, D. (2008) Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol. Cell. Biol. 28, 2718 2731.
111. Sawa, M., Nusinow, D.A., Kay, S.A. Imaizumi, T. (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science, 318, 261 265.
112. Scarcelli, N. Kover, P.X. (2009) Standing genetic variation in FRIGIDA mediates experimental evolution of flowering time in Arabidopsis. Mol. Ecol. 18, 2039 2049.
113. Schlappi, M.R. (2006) FRIGIDA LIKE 2 is a functional allele in Landsberg erecta and compensates for a nonsense allele of FRIGIDA LIKE 1. Plant Physiol. 142, 1728 1738.
114. Schmitz, R.J., Hong, L., Michaels, S. Amasino, R.M. (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development, 132, 5471 5478.
115. Schmitz, R.J., Hong, L., Fitzpatrick, K.E. Amasino, R.M. (2007) DICER-LIKE 1 and DICER-LIKE 3 redundantly act to promote flowering via repression of FLOWERING LOCUS C in Arabidopsis thaliana. Genetics, 176, 1359 1362.
116. Schmitz, R.J., Sung, S. Amasino, R.M. (2008) Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 105, 411 416.
117. Schomburg, F.M., Patton, D.A., Meinke, D.W. Amasino, R.M. (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell, 13, 1427 1436.
118. Schubert, D., Clarenz, O. Goodrich, J. (2005) Epigenetic control of plant development by Polycomb-group proteins. Curr. Opin. Plant Biol. 8, 553 561.
119. Scortecci, K.C., Michaels, S.D. Amasino, R.M. (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J. 26, 229 236.
120. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Krober, S., Amasino, R.A. Coupland, G. (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898 912.
121. Serrano, G., Herrera-Palau, R., Romero, J.M., Serrano, A., Coupland, G. Valverde, F. (2009) Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr. Biol. 19, 359 368.
122. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J. Dennis, E.S. (1999) The FLF MADS box gene. A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell, 11, 445 458.
123. Sheldon, C.C., Hills, M.J., Lister, C., Dean, C., Dennis, E.S. Peacock, W.J. (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl. Acad. Sci. USA, 105, 2214 2219.
124. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A. Shi, Y. (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119, 941 953.
125. Simpson, G.G. Dean, C. (2002) Arabidopsis, the Rosetta stone of flowering time? Science, 296, 285 289.
126. Simpson, G.G., Dijkwel, P.P., Quesada, V., Henderson, I. Dean, C. (2003) FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell, 113, 777 787.
127. Soltis, D.E., Bell, C.D., Kim, S. Soltis, P.S. (2008) Origin and early evolution of angiosperms. Ann. N Y Acad. Sci. 1133, 3 25.
128. Suarez-Lopez, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F. Coupland, G. (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature, 410, 1116 1120.
129. Sung, S. Amasino, R.M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature, 427, 159 164.
130. Sung, S., Schmitz, R.J. Amasino, R.M. (2006) A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev. 20, 3244 3248.
131. Swiezewski, S., Liu, F., Magusin, A. Dean, C. (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature, 462, 799 802.
132. Takada, S. Goto, K. (2003) Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell, 15, 2856 2865.
133. Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S. Shimamoto, K. (2007) Hd3a protein is a mobile flowering signal in rice. Science, 316, 1033 1036.
134. Tooke, F., Ordidge, M., Chiurugwi, T. Battey, N. (2005) Mechanisms and function of flower and inflorescence reversion. J. Exp. Bot. 56, 2587 2599.
135. Tournois, J. (1914) Etudes sur la sexualite du houblon. Annals des Sciences Naturelles, 19, 49 191.
136. Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M.L., Guillaume, E., Buisine, N., Gagnot, S., Martienssen, R.A., Coupland, G. Colot, V. (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3, e86.
137. Turck, F., Fornara, F. Coupland, G. (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573 594.
138. 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.
139. Veley, K.M. Michaels, S.D. (2008) Functional redundancy and new roles for genes of the autonomous floral-promotion pathway. Plant Physiol. 147, 682 695.
140. Wang, X., Zhang, Y., Ma, Q., Zhang, Z., Xue, Y., Bao, S. Chong, K. (2007) SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis. EMBO J. 26, 1934 1941.
141. 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.
142. Wang, R., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F., Alonso-Blanco, C., Coupland, G. Albani, M.C. (2009b) PEP1 regulates perennial flowering in Arabis alpina. Nature, 459, 423 427.
143. Wellensiek, S.J. (1962) Dividing cells as the locus for vernalization. Nature, 195, 307 308.
144. Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U. Weigel, D. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309, 1056 1059.
145. Wilczek, A.M., Roe, J.L., Knapp, M.C. et al. (2009) Effects of genetic perturbation on seasonal life history plasticity. Science, 323, 930 934.
146. Wood, C.C., Robertson, M., Tanner, G., Peacock, W.J., Dennis, E.S. Helliwell, C.A. (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc. Natl. Acad. Sci. USA, 103, 14631 14636.
147. Wu, G. Poethig, R.S. (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development, 133, 3539 3547.
148. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D. Poethig, R.S. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 138, 750 759.
149. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. Araki, T. (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175 1189.
150. Yamaguchi, A., Wu, M.F., Yang, L., Wu, G., Poethig, R.S. Wagner, D. (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev. Cell, 17, 268 278.
151. Yan, L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., SanMiguel, P., Bennetzen, J.L., Echenique, V. Dubcovsky, J. (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science, 303, 1640 1644.
152. Yanovsky, M.J. Kay, S.A. (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature, 419, 308 312.
153. Yant, L., Mathieu, J. Schmid, M. (2009) Just say no: floral repressors help Arabidopsis bide the time. Curr. Opin. Plant Biol. 12, 580 586.
154. Yoo, S.K., Chung, K.S., Kim, J., Lee, J.H., Hong, S.M., Yoo, S.J., Yoo, S.Y., Lee, J.S. Ahn, J.H. (2005) CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol. 139, 770 778.
155. Zeevaart, J.A. (1976) Physiology of flower formation. Annu. Rev. Plant. Physiology, 27, 321 348.
156. Zeevaart, J.A.D. (1985) Perilla. In Handbook, CRC of Flowering (Halevy, A.H., ed).
157. Zeevaart, J.A. (2008) Leaf-produced floral signals. Curr. Opin. Plant. Biol. 11, 541 547.