Cellular and Molecular Life Sciences

, Volume 68, Issue 12, pp 2013–2037 | Cite as

Regulation of flowering time: all roads lead to Rome

Review

Abstract

Plants undergo a major physiological change as they transition from vegetative growth to reproductive development. This transition is a result of responses to various endogenous and exogenous signals that later integrate to result in flowering. Five genetically defined pathways have been identified that control flowering. The vernalization pathway refers to the acceleration of flowering on exposure to a long period of cold. The photoperiod pathway refers to regulation of flowering in response to day length and quality of light perceived. The gibberellin pathway refers to the requirement of gibberellic acid for normal flowering patterns. The autonomous pathway refers to endogenous regulators that are independent of the photoperiod and gibberellin pathways. Most recently, an endogenous pathway that adds plant age to the control of flowering time has been described. The molecular mechanisms of these pathways have been studied extensively in Arabidopsisthaliana and several other flowering plants.

Keywords

Arabidopsis thaliana Flowering time Photoperiod Vernalization Gibberellic acid Pathway integrators 

Abbreviations

GA

Gibberellic acid

SD

Short day

LD

Long day

References

  1. 1.
    Kobayashi Y, Weigel D (2007) Move on up, it’s time for change—mobile signals controlling photoperiod-dependent flowering. Genes Dev 21:2371–2384PubMedGoogle Scholar
  2. 2.
    Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol 25:159–184PubMedGoogle Scholar
  3. 3.
    Pittendrigh C (1972) Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proc Natl Acad Sci USA 69:2734–2737PubMedGoogle Scholar
  4. 4.
    Knott J (1934) Effect of a localized photoperiod on spinach. Proc Soc Hortic Sci 31:152–154Google Scholar
  5. 5.
    Evans LT (1971) Flower induction and the florigen concept. Annu Rev Plant Physiol 22:365–394Google Scholar
  6. 6.
    Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594PubMedGoogle Scholar
  7. 7.
    King RW, Evans LT, Wardlaw IF (1968) Translocation of the floral stimulus in Pharbitis nil in relation to that of assimilates. Z Pflanzenphysiol 59:377–388Google Scholar
  8. 8.
    King RW, Zeevaart JA (1973) Floral stimulus movement in perilla and flower inhibition caused by noninduced leaves. Plant Physiol 51(4):727–738PubMedGoogle Scholar
  9. 9.
    Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20(6):840–844. doi:10.1046/j.1365-3040.1997.d01-104.x Google Scholar
  10. 10.
    Tsuchiya T, Ishiguri Y (1981) Role of the quality of light on the photoperiodic flowering response in four latitudinal ecotypes of Chenopodium rubrum. Plant Cell Physiol 22:525–532Google Scholar
  11. 11.
    Gassner G (1918) Beiträge zur physiologischen Charakteristik sommer- und winterannueller Gewächse, insbesondere der Getreidepflanzen. Z Bot 10:417–480Google Scholar
  12. 12.
    Purvis ON, Gregory FG (1952) The reversibility by high temperature of the vernalised condition in Petkus winter rye. Ann Bot 16:1–21Google Scholar
  13. 13.
    Wang JY (1960) A critique of the heat unit approach to plant-response studies. Ecology 41(4):785–790Google Scholar
  14. 14.
    Samach A, Wigge P (2005) Ambient temperature perception in plants. Curr Opin Plant Biol 8:483–486PubMedGoogle Scholar
  15. 15.
    Lang A (1957) The effect of gibberellin upon flower formation. Proc Natl Acad Sci USA 43:709–717PubMedGoogle Scholar
  16. 16.
    Lang A (1960) Gibberellin-like substances in photoinduced and vegetative Hyoscyamus plants. Planta 54:498–504Google Scholar
  17. 17.
    Langridge J (1957) Effect of day-length and gibberellic acid on the flowering of Arabidopsis. Nature 180:36–37Google Scholar
  18. 18.
    Chandler J, Dean C (1994) Factors influencing the vernalization response and flowering time of late flowering mutants of Arabidopsis thaliana (L.) Heynh. J Exp Bot 45:1279–1288Google Scholar
  19. 19.
    Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993) Physiological signals that induce flowering. Plant Cell 5:1147–1155PubMedGoogle Scholar
  20. 20.
    Bodson M, Outlaw WH (1985) Elevation in the sucrose content of the shoot apical meristem of Sinapis alba at floral evocation. Plant Physiol 79(2):420–424PubMedGoogle Scholar
  21. 21.
    Laibach F (1943) Arabidopsis thaliana (L.) Heynh. als Objekt für genetische und entwicklungsphysiologische Untersuchungen. Bot Arch 44:439–455Google Scholar
  22. 22.
    Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172. doi:10.1146/annurev.arplant.55.031903.141605 PubMedGoogle Scholar
  23. 23.
    Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1:109–118PubMedGoogle Scholar
  24. 24.
    Sung S, Amasino RM (2004) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7(1):4–10PubMedGoogle Scholar
  25. 25.
    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 290:344–347PubMedGoogle Scholar
  26. 26.
    Michaels S, Amasino R (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956PubMedGoogle Scholar
  27. 27.
    Rédei GP (1962) Supervital mutants of Arabidopsis. Genetics 47:443–460PubMedGoogle Scholar
  28. 28.
    Koornneef M, Hanhart C, van der Veen J (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66PubMedGoogle Scholar
  29. 29.
    Lariguet P, Dunand C (2005) Plant photoreceptors: phylogenetic overview. J Mol Evol 61:559–569PubMedGoogle Scholar
  30. 30.
    Li Q, Yang H (2007) Cryptochrome signaling in plants. Photochem Photobiol 83:94–101PubMedGoogle Scholar
  31. 31.
    Quail P, Boylan M, Parks B, Short T, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268:675–680PubMedGoogle Scholar
  32. 32.
    Tóth R, Kevei E, Hall A, Millar A, Nagy F, Kozma-Bognar L (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol 127:1607–1616PubMedGoogle Scholar
  33. 33.
    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 80:847–857PubMedGoogle Scholar
  34. 34.
    An H, Roussot C, Suárez-López P, Corbesier L, Vincent C, Píniro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626PubMedGoogle Scholar
  35. 35.
    Suárez-López 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 410:1116–1120PubMedGoogle Scholar
  36. 36.
    Fornara F, Panigrahi K, Gissot L, Sauerbrunn N, Rühl M, Jarillo J, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86PubMedGoogle Scholar
  37. 37.
    Imaizumi T, Schultz T, Harmon F, Ho L, Kay S (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297PubMedGoogle Scholar
  38. 38.
    Sawa M, Nusinow D, Kay S, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265PubMedGoogle Scholar
  39. 39.
    Imaizumi T, Tran H, Swartz T, Briggs W, Kay S (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306PubMedGoogle Scholar
  40. 40.
    Liu L, Zhang Y, Li Q, Sang Y, Mao J, Lian H, Wang L, Yang H (2008) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20:292–306PubMedGoogle Scholar
  41. 41.
    Hoecker U, Quail P (2001) The phytochrome A-specific signaling intermediate SPA1 interacts directly with COP1, a constitutive repressor of light signaling in Arabidopsis. J Biol Chem 276:38173–38178PubMedGoogle Scholar
  42. 42.
    Laubinger S, Marchal V, Le Gourrierec J, Gentilhomme 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 133:3213–3222PubMedGoogle Scholar
  43. 43.
    Laubinger S, Hoecker U (2003) The SPA1-like proteins SPA3 and SPA4 repress photomorphogenesis in the light. Plant J 35:373–385PubMedGoogle Scholar
  44. 44.
    Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006PubMedGoogle Scholar
  45. 45.
    Jang S, Marchal V, Panigrahi K, Wenkel S, Soppe W, Deng X, Valverde F, Coupland G (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J 27:1277–1288PubMedGoogle Scholar
  46. 46.
    Morris K, Thornber S, Codrai L, Richardson C, Craig A, Sadanandom A, Thomas B, Jackson S (2010) DAY NEUTRAL FLOWERING represses CONSTANS to prevent Arabidopsis flowering early in short days. Plant Cell 22(4):1118–1128. doi:10.1105/tpc.109.066605 PubMedGoogle Scholar
  47. 47.
    Ayre BG, Turgeon R (2004) Graft transmission of a floral stimulant derived from CONSTANS. Plant Physiol 135(4):2271–2278. doi:10.1104/pp.104.040592 PubMedGoogle Scholar
  48. 48.
    Kardailsky I, Shukla V, Ahn J, Dagenais N, Christensen S, Nguyen J, Chory J, Harrison M, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965PubMedGoogle Scholar
  49. 49.
    Weigel D, Ahn JH, Blazquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrandiz C, Kardailsky I, Malancharuvil EJ, Neff MM, Nguyen JT, Sato S, Wang ZY, Xia Y, Dixon RA, Harrison MJ, Lamb CJ, Yanofsky MF, Chory J (2000) Activation tagging in Arabidopsis. Plant Physiol 122(4):1003–1013PubMedGoogle Scholar
  50. 50.
    Kaya H, Sato S, Tabata S, Kobayashi Y, Iwabuchi M, Araki T (2000) Hosoba toge toge, a syndrome caused by a large chromosomal deletion associated with a T-DNA insertion in Arabidopsis. Plant Cell Physiol 41(9):1055–1066PubMedGoogle Scholar
  51. 51.
    Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962PubMedGoogle Scholar
  52. 52.
    Ahn J, Miller D, Winter V, Banfield M, Lee J, Yoo S, Henz S, Brady R, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614PubMedGoogle Scholar
  53. 53.
    Harmer S, Hogenesch J, Straume M, Chang H, Han B, Zhu T, Wang X, Kreps J, Kay S (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113PubMedGoogle Scholar
  54. 54.
    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(12):2856–2865. doi:10.1105/tpc.016345 PubMedGoogle Scholar
  55. 55.
    Farrona S, Coupland G, Turck F (2008) The impact of chromatin regulation on the floral transition. Semin Cell Dev Biol 19(6):560–573. doi:10.1016/j.semcdb.2008.07.015 PubMedGoogle Scholar
  56. 56.
    Exner V, Aichinger E, Shu H, Wildhaber T, Alfarano P, Caflisch A, Gruissem W, Kohler C, Hennig L (2009) The chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS One 4(4):e5335. doi:10.1371/journal.pone.0005335 PubMedGoogle Scholar
  57. 57.
    Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3(6):e86. doi:10.1371/journal.pgen.0030086 PubMedGoogle Scholar
  58. 58.
    Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J, Jacobsen SE (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5(5):e129. doi:10.1371/journal.pbio.0050129 PubMedGoogle Scholar
  59. 59.
    Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22(18):4804–4814. doi:10.1093/emboj/cdg444 PubMedGoogle Scholar
  60. 60.
    Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, Jenuwein T, Goodrich J (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J 25(19):4638–4649. doi:10.1038/sj.emboj.7601311 PubMedGoogle Scholar
  61. 61.
    Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T, Sung ZR, Takahashi S (2001) EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13(11):2471–2481PubMedGoogle Scholar
  62. 62.
    Jiang D, Wang Y, He Y (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS One 3(10):e3404. doi:10.1371/journal.pone.0003404 PubMedGoogle Scholar
  63. 63.
    Hennig L, Derkacheva M (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25(9):414–423. doi:10.1016/j.tig.2009.07.002 PubMedGoogle Scholar
  64. 64.
    Adrian J, Farrona S, Reimer J, Albani M, Coupland G, Turck F (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22(5):1425–1440PubMedGoogle Scholar
  65. 65.
    Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033PubMedGoogle Scholar
  66. 66.
    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(8):1175–1189. doi:10.1093/pcp/pci151 PubMedGoogle Scholar
  67. 67.
    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(2):770–778. doi:10.1104/pp.105.066928 PubMedGoogle Scholar
  68. 68.
    Wigge P, Kim M, Jaeger K, Busch W, Schmid M, Lohmann J, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059PubMedGoogle Scholar
  69. 69.
    Samach A, Onouchi H, Gold S, Ditta G, Schwarz-Sommer Z, Yanofsky M, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616PubMedGoogle Scholar
  70. 70.
    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 309:1052–1056PubMedGoogle Scholar
  71. 71.
    Mathieu J, Warthmann N, Küttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060PubMedGoogle Scholar
  72. 72.
    Jäger K, Wigge P (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054Google Scholar
  73. 73.
    Notaguchi M, Abe M, Kimura T, Daimon Y, Kobayashi T, Yamaguchi A, Tomita Y, Dohi K, Mori M, Araki T (2008) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol 49:1645–1658PubMedGoogle Scholar
  74. 74.
    Li C, Zhang K, Zeng X, Jackson S, Zhou Y, Hong Y (2009) A cis element within flowering locus T mRNA determines its mobility and facilitates trafficking of heterologous viral RNA. J Virol 83:3540–3548PubMedGoogle Scholar
  75. 75.
    Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43(10):1096–1105PubMedGoogle Scholar
  76. 76.
    Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12(12):2473–2484PubMedGoogle Scholar
  77. 77.
    Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774PubMedGoogle Scholar
  78. 78.
    Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) 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(8):926–936. doi:10.1101/gad.1189604 PubMedGoogle Scholar
  79. 79.
    Itoh H, Nonoue Y, Yano M, Izawa T (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat Genet 42(7):635–638. doi:10.1038/ng.606 PubMedGoogle Scholar
  80. 80.
    Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316(5827):1033–1036. doi:10.1126/science.1141753 PubMedGoogle Scholar
  81. 81.
    Hayama R, Agashe B, Luley E, King R, Coupland G (2007) A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 19:2988–3000PubMedGoogle Scholar
  82. 82.
    Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez J, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403PubMedGoogle Scholar
  83. 83.
    Lifschitz E, Eshed Y (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. J Exp Bot 57:3405–3414PubMedGoogle Scholar
  84. 84.
    Alonso-Blanco C, Koornneef M (2000) Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci 5(1):22–29. S1360-1385(99)01510-1 [pii]PubMedGoogle Scholar
  85. 85.
    Napp-Zinn K (1987) Vernalization, environmental and genetic regulation. In: Atherton JG (ed) Manipulation of flowering. Butterworths, London, pp 123–132Google Scholar
  86. 86.
    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 6:911–919Google Scholar
  87. 87.
    Lee I, Aukerman M, Gore S, Lohman K, Michaels S, Weaver L, John M, Feldmann K, Amasino R (1994) Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Plant Cell 6:75–83PubMedGoogle Scholar
  88. 88.
    Geraldo N, Bäurle 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 150:1611–1618PubMedGoogle Scholar
  89. 89.
    Searle I, He Y, Turck F, Vincent C, Fornara F, Krober 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. Genes Dev 20(7):898–912. doi:10.1101/gad.373506 PubMedGoogle Scholar
  90. 90.
    Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11(3):445–458PubMedGoogle Scholar
  91. 91.
    Helliwell C, Wood C, Robertson M, Peacock WJ, Dennis E (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 46:183–192PubMedGoogle Scholar
  92. 92.
    Hepworth SR, 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(16):4327–4337PubMedGoogle Scholar
  93. 93.
    Michaels S, Amasino R (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 13:935–941PubMedGoogle Scholar
  94. 94.
    Gendall A, Levy Y, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535PubMedGoogle Scholar
  95. 95.
    Levy Y, Mesnage S, Mylne J, Gendall A, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243–246PubMedGoogle Scholar
  96. 96.
    Sung S, Amasino R (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164PubMedGoogle Scholar
  97. 97.
    Bond D, Dennis E, Pogson B, Finnegan E (2009) Histone acetylation, VERNALIZATION INSENSITIVE 3, FLOWERING LOCUS C, and the vernalization response. Mol Plant 2:724–737PubMedGoogle Scholar
  98. 98.
    De Lucia F, Crevillen P, Jones AM, 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(44):16831–16836. doi:10.1073/pnas.0808687105 PubMedGoogle Scholar
  99. 99.
    Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103(39):14631–14636. doi:10.1073/pnas.0606385103 PubMedGoogle Scholar
  100. 100.
    Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14(2):155–164. doi:10.1016/j.gde.2004.02.001 PubMedGoogle Scholar
  101. 101.
    Finnegan EJ, Dennis ES (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17(22):1978–1983. doi:10.1016/j.cub.2007.10.026 PubMedGoogle Scholar
  102. 102.
    Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802PubMedGoogle Scholar
  103. 103.
    Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331(6013):76–79. doi:10.1126/science.1197349 PubMedGoogle Scholar
  104. 104.
    De Lucia F, Dean C (2010) Long non-coding RNAs and chromatin regulation. Curr Opin Plant Biol. doi:10.1016/j.pbi.2010.11.006
  105. 105.
    Simpson G (2004) The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr Opin Plant Biol 7:570–574PubMedGoogle Scholar
  106. 106.
    Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97PubMedGoogle Scholar
  107. 107.
    Hecht V, Foucher F, Ferrandiz C, Macknight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltran JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137(4):1420–1434. doi:10.1104/pp.104.057018 PubMedGoogle Scholar
  108. 108.
    Schläppi M, Patel M (2001) Biennialism and vernalization-promoted flowering in Hyoscyamus niger: a comparison with Arabidopsis. Flower Newsl 31:25–32Google Scholar
  109. 109.
    Tadege M, Sheldon CC, Helliwell CA, Upadhyaya NM, Dennis ES, Peacock WJ (2003) Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotechnol J 1(5):361–369. doi:10.1046/j.1467-7652.2003.00034.x PubMedGoogle Scholar
  110. 110.
    Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459(7245):423–427. doi:10.1038/nature07988 PubMedGoogle Scholar
  111. 111.
    Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303(5664):1640–1644. doi:10.1126/science.1094305 PubMedGoogle Scholar
  112. 112.
    Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2:e106PubMedGoogle Scholar
  113. 113.
    Halliday KJ, Salter MG, Thingnaes E, Whitelam GC (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J 33(5):875–885PubMedGoogle Scholar
  114. 114.
    Blázquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33(2):168–171. doi:10.1038/ng1085 PubMedGoogle Scholar
  115. 115.
    Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170(3):1197–1207. doi:10.1534/genetics.104.036533 PubMedGoogle Scholar
  116. 116.
    Hartmann U, Höhmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360PubMedGoogle Scholar
  117. 117.
    Lee J, Yoo S, Park S, Hwang I, Lee J, Ahn J (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21:397–402PubMedGoogle Scholar
  118. 118.
    Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell C, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15:110–120PubMedGoogle Scholar
  119. 119.
    Kumar S, Wigge P (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147PubMedGoogle Scholar
  120. 120.
    Choi K, Kim S, Kim SY, Kim M, Hyun Y, Lee H, Choe S, Kim SG, Michaels S, Lee I (2005) SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell 17(10):2647–2660. doi:10.1105/tpc.105.035485 PubMedGoogle Scholar
  121. 121.
    Deal RB, Kandasamy MK, McKinney EC, Meagher RB (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell 17(10):2633–2646. doi:10.1105/tpc.105.035196 PubMedGoogle Scholar
  122. 122.
    Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5(12):523–530PubMedGoogle Scholar
  123. 123.
    Koornneef M, van der Veen J (1980) Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 58(6):257–263Google Scholar
  124. 124.
    Sun T, Goodman H, Ausubel F (1992) Cloning the Arabidopsis GA1 locus by genomic subtraction. Plant Cell 4:119–128PubMedGoogle Scholar
  125. 125.
    Koornneef M, Vaneden J, Hanhart CJ, Dejongh AMM (1983) Genetic fine-structure of the Ga-1 locus in the higher-plant Arabidopsis thaliana (L.) Heynh. Genet Res 41(1):57Google Scholar
  126. 126.
    Wilson R, Heckman J, Somerville C (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408PubMedGoogle Scholar
  127. 127.
    Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5(8):887–896. doi:10.1105/tpc.5.8.887 PubMedGoogle Scholar
  128. 128.
    Shimada A, Ueguchi-Tanaka M, Sakamoto T, Fujioka S, Takatsuto S, Yoshida S, Sazuka T, Ashikari M, Matsuoka M (2006) The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. Plant J 48(3):390–402. doi:10.1111/j.1365-313X.2006.02875.x PubMedGoogle Scholar
  129. 129.
    Swain S, Tseng T, Olszewski N (2001) Altered expression of SPINDLY affects gibberellin response and plant development. Plant Physiol 126:1174–1185PubMedGoogle Scholar
  130. 130.
    Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T, Hsing Y, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698PubMedGoogle Scholar
  131. 131.
    Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z, Powers S, Gong F, Phillips A, Hedden P, Sun T, Thomas S (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414PubMedGoogle Scholar
  132. 132.
    Willige B, Ghosh S, Nill C, Zourelidou M, Dohmann E, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:1209–1220PubMedGoogle Scholar
  133. 133.
    King RW, Moritz T, Evans LT, Junttila O, Herlt AJ (2001) Long-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiol 127(2):624–632PubMedGoogle Scholar
  134. 134.
    Silverstone A, Ciampaglio C, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169PubMedGoogle Scholar
  135. 135.
    Hisamatsu T, King R (2008) The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin. J Exp Bot 59:3821–3829PubMedGoogle Scholar
  136. 136.
    Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21(5):1328–1339. doi:10.1105/tpc.109.066969 PubMedGoogle Scholar
  137. 137.
    Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154(2):567–570. doi:10.1104/pp.110.161554 PubMedGoogle Scholar
  138. 138.
    Koornneef M, Elgersma A, Hanhart CJ, Vanloenenmartinet EP, Vanrijn L, Zeevaart JAD (1985) A gibberellin insensitive mutant of Arabidopsis thaliana. Physiol Plant 65(1):33–39Google Scholar
  139. 139.
    Murase K, Hirano Y, Sun T, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463PubMedGoogle Scholar
  140. 140.
    Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X, Harberd N (2007) DELLAs contribute to plant photomorphogenesis. Plant Physiol 143:1163–1172PubMedGoogle Scholar
  141. 141.
    Alvey L, Harberd N (2005) DELLA proteins: integrators of multiple plant growth regulatory inputs? Physiol Plant 123(2):153–160. doi:10.1111/j.1399-3054.2004.00412.x Google Scholar
  142. 142.
    Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421(6924):740–743. doi:10.1038/nature01387 PubMedGoogle Scholar
  143. 143.
    de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480–484. doi:10.1038/nature06520 PubMedGoogle Scholar
  144. 144.
    Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12(1):57–62. doi:10.1016/j.pbi.2008.09.004 PubMedGoogle Scholar
  145. 145.
    Oda A, Fujiwara S, Kamada H, Coupland G, Mizoguchi T (2004) Antisense suppression of the Arabidopsis PIF3 gene does not affect circadian rhythms but causes early flowering and increases FT expression. FEBS Lett 557(1–3):259–264. S0014579303014704 [pii]PubMedGoogle Scholar
  146. 146.
    Blázquez MA, Soowal LN, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124(19):3835–3844PubMedGoogle Scholar
  147. 147.
    Blázquez M, Green R, Nilsson O, Sussman M, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800PubMedGoogle Scholar
  148. 148.
    Eriksson S, Böhlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18:2172–2181PubMedGoogle Scholar
  149. 149.
    Blázquez M, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404:889–892PubMedGoogle Scholar
  150. 150.
    Gocal G, Sheldon C, Gubler F, Moritz T, Bagnall D, MacMillan C, Li S, Parish R, Dennis E, Weigel D, King R (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127:1682–1693PubMedGoogle Scholar
  151. 151.
    Gocal G, Poole A, Gubler F, Watts R, Blundell C, King R (1999) Long-day up-regulation of a GAMYB gene during Lolium temulentum inflorescence formation. Plant Physiol 119:1271–1278PubMedGoogle Scholar
  152. 152.
    Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263. doi:10.1038/nature01958 PubMedGoogle Scholar
  153. 153.
    Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12(17):1484–1495. S0960982202010175 [pii]PubMedGoogle Scholar
  154. 154.
    Achard P, Herr A, Baulcombe D, Harberd N (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365PubMedGoogle Scholar
  155. 155.
    Moon J, Suh S, Lee H, Choi K, Hong C, Paek N, Kim S, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623PubMedGoogle Scholar
  156. 156.
    Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd N (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489PubMedGoogle Scholar
  157. 157.
    Yu H, Xu Y, Tan E, Kumar P (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci USA 99:16336–16341PubMedGoogle Scholar
  158. 158.
    Liu C, Chen H, Er H, Soo H, Kumar P, Han J, Liou Y, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135:1481–1491PubMedGoogle Scholar
  159. 159.
    Richter R, Behringer C, Müller I, Schwechheimer C (2010) The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev 24:2093–2104PubMedGoogle Scholar
  160. 160.
    Madhusudanan KN, Nandakumar S (1983) Carbohydrate changes in shoot tip and subtending leaves during ontogenetic development of pineapple. Z Pflanzenphysiol 110(5):429–438Google Scholar
  161. 161.
    Komarova EN, Milyaeva EL (1991) Changes in content and distribution of starch in stem apices of bicolored coneflower during the period of flowering evocation. Sov Plant Physiol 38(1):46–51Google Scholar
  162. 162.
    Lejeune P, Bernier G, Requier MC, Kinet JM (1993) Sucrose increase during floral induction in the phloem sap collected at the apical part of the shoot of the long-day plant Sinapis alba L. Planta 190(1):71–74Google Scholar
  163. 163.
    King RW, Evans LT (1991) Shoot apex sugars in relation to long-day induction of flowering in Lolium temulentum L. Aust J Plant Physiol 18(2):121–135Google Scholar
  164. 164.
    Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127:252–261PubMedGoogle Scholar
  165. 165.
    Roldán M, Gómez-Mena C, Ruiz-García L, Salinas J, Martínez-Zapater J (1999) Sucrose availability on the aerial part of the plant promotes morphogenesis and flowering of Arabidopsis in the dark. Plant J 20:581–590PubMedGoogle Scholar
  166. 166.
    El-Lithy M, Reymond M, Stich B, Koornneef M, Vreugdenhil D (2010) Relation among plant growth, carbohydrates and flowering time in the Arabidopsis Landsberg erecta × Kondara recombinant inbred line population. Plant Cell Environ 33(8):1369–1382PubMedGoogle Scholar
  167. 167.
    Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79(1):11–17PubMedGoogle Scholar
  168. 168.
    Caspar T, Lin TP, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol 95(4):1181–1188PubMedGoogle Scholar
  169. 169.
    Corbesier L, Lejeune P, Bernier G (1998) The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206:131–137PubMedGoogle Scholar
  170. 170.
    Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441. doi:10.1146/annurev.arplant.59.032607.092945 PubMedGoogle Scholar
  171. 171.
    Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29(2):225–235. 1220 [pii]PubMedGoogle Scholar
  172. 172.
    van Dijken AJ, Schluepmann H, Smeekens SC (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135(2):969–977. doi:10.1104/pp.104.039743 PubMedGoogle Scholar
  173. 173.
    Wang J, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749PubMedGoogle Scholar
  174. 174.
    Noh B, Lee SH, Kim HJ, Yi G, Shin EA, Lee M, Jung KJ, Doyle MR, Amasino RM, Noh YS (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(10):2601–2613. doi:10.1105/tpc.104.025353 PubMedGoogle Scholar
  175. 175.
    Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Peeters AJ (1998) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148(2):885–892PubMedGoogle Scholar
  176. 176.
    He Y, Michaels S, Amasino R (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302:1751–1754PubMedGoogle Scholar
  177. 177.
    Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28:398–407PubMedGoogle Scholar
  178. 178.
    Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89:737–745PubMedGoogle Scholar
  179. 179.
    Quesada V, Macknight R, Dean C, Simpson G (2003) Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J 22:3142–3152PubMedGoogle Scholar
  180. 180.
    Ausín I, Alonso-Blanco C, Jarillo J, Ruiz-García L, Martínez-Zapater J (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36:162–166PubMedGoogle Scholar
  181. 181.
    Schomburg F, Patton D, Meinke D, Amasino R (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13:1427–1436PubMedGoogle Scholar
  182. 182.
    Bäurle I, Smith L, Baulcombe D, Dean C (2007) Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318:109–112PubMedGoogle Scholar
  183. 183.
    Hornyik C, Terzi LC, Simpson GG (2010) The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18(2):203–213. doi:10.1016/j.devcel.2009.12.009 PubMedGoogle Scholar
  184. 184.
    Simpson GG, Dijkwel PP, 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(6):777–787. S0092867403004252 [pii]PubMedGoogle Scholar
  185. 185.
    Adams S, Allen T, Whitelam GC (2009) Interaction between the light quality and flowering time pathways in Arabidopsis. Plant J 60(2):257–267. doi:10.1111/j.1365-313X.2009.03962.x PubMedGoogle Scholar
  186. 186.
    Lim MH, Kim J, Kim YS, Chung KS, Seo YH, Lee I, Hong CB, Kim HJ, Park CM (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(3):731–740. doi:10.1105/tpc.019331 PubMedGoogle Scholar
  187. 187.
    Aukerman M, Lee I, Weigel D, Amasino R (1999) The Arabidopsis flowering-time gene LUMINIDEPENDENS is expressed primarily in regions of cell proliferation and encodes a nuclear protein that regulates LEAFY expression. Plant J 18:195–203PubMedGoogle Scholar
  188. 188.
    Kim S, Choi K, Park C, Hwang HJ, Lee I (2006) SUPPRESSOR OF FRIGIDA4, encoding a C2H2-type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C. Plant Cell 18(11):2985–2998. doi:10.1105/tpc.106.045179 PubMedGoogle Scholar
  189. 189.
    Simpson G, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289PubMedGoogle Scholar
  190. 190.
    Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23(1):107–120. doi:10.1093/molbev/msj014 PubMedGoogle Scholar
  191. 191.
    Mathieu J, Yant LJ, Murdter F, Küttner F, Schmid M (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7(7):e1000148. doi:10.1371/journal.pbio.1000148 PubMedGoogle Scholar
  192. 192.
    Yant L, Mathieu J, Dinh T, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22:2156–2170PubMedGoogle Scholar
  193. 193.
    Castillejo C, Pelaz S (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr Biol 18(17):1338–1343. doi:10.1016/j.cub.2008.07.075 PubMedGoogle Scholar
  194. 194.
    Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J 55(5):832–843. doi:10.1111/j.1365-313X.2008.03552.x PubMedGoogle Scholar
  195. 195.
    Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69(5):843–859PubMedGoogle Scholar
  196. 196.
    Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377(6549):495–500. doi:10.1038/377495a0 PubMedGoogle Scholar
  197. 197.
    Yu H, Ito T, Wellmer F, Meyerowitz E (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36:157–161PubMedGoogle Scholar
  198. 198.
    Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16(5):711–722. doi:10.1016/j.devcel.2009.03.011 PubMedGoogle Scholar
  199. 199.
    Wagner D (2009) Flower morphogenesis: timing is key. Dev Cell 16(5):621–622. doi:10.1016/j.devcel.2009.05.005 PubMedGoogle Scholar
  200. 200.
    Liu Z, Mara C (2010) Regulatory mechanisms for floral homeotic gene expression. Semin Cell Dev Biol 21:80–86PubMedGoogle Scholar
  201. 201.
    Moyroud E, Kusters E, Monniaux M, Koes R, Parcy F (2010) LEAFY blossoms. Trends Plant Sci 15(6):346–352. doi:10.1016/j.tplants.2010.03.007 PubMedGoogle Scholar
  202. 202.
    Gregis V, Sessa A, Colombo L, Kater MM (2008) AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J 56(6):891–902. doi:10.1111/j.1365-313X.2008.03648.x PubMedGoogle Scholar
  203. 203.
    Kaufmann K, Wellmer F, Muiño J, Ferrier T, Wuest S, Kumar V, Serrano-Mislata A, Madueño F, Krajewski P, Meyerowitz E, Angenent G, Riechmann J (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89PubMedGoogle Scholar
  204. 204.
    Michaels SD, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino RM (2003) AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J 33(5):867–874PubMedGoogle Scholar
  205. 205.
    Yant L, Mathieu J, Schmid M (2009) Just say no: floral repressors help Arabidopsis bide the time. Curr Opin Plant Biol 12(5):580–586. doi:10.1016/j.pbi.2009.07.006 PubMedGoogle Scholar
  206. 206.
    Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101(3):331–340PubMedGoogle Scholar
  207. 207.
    Lee I, Michaels SD, Masshardt AS RMA (1994) The late-flowering phenotype of FRIGIDA and LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J 6:903–909Google Scholar
  208. 208.
    Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26(2):229–236PubMedGoogle Scholar
  209. 209.
    Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Lee MH, Moon J, Lee I, Kim J (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36(2):167–171. doi:10.1038/ng1298 PubMedGoogle Scholar
  210. 210.
    Henderson IR, Liu F, Drea S, Simpson GG, Dean C (2005) An allelic series reveals essential roles for FY in plant development in addition to flowering-time control. Development 132(16):3597–3607. doi:10.1242/dev.01924 PubMedGoogle Scholar
  211. 211.
    Koornneef M, Rolff E, Spruit CJP (1980) Genetic-control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z Pflanzenphysiol 100(2):147–160Google Scholar
  212. 212.
    Rubio V, Deng XW (2007) Plant science. Standing on the shoulders of GIGANTEA. Science 318(5848):206–207. doi:10.1126/science.1150213 PubMedGoogle Scholar
  213. 213.
    Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, Lefebvre D, Grandjean O (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128(23):4847–4858PubMedGoogle Scholar
  214. 214.
    Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254PubMedGoogle Scholar
  215. 215.
    Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759. doi:10.1016/j.cell.2009.06.031 PubMedGoogle Scholar
  216. 216.
    Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17(2):268–278. doi:10.1016/j.devcel.2009.06.007 PubMedGoogle Scholar
  217. 217.
    Tseng T, Swain S, Olszewski N (2001) Ectopic expression of the tetratricopeptide repeat domain of SPINDLY causes defects in gibberellin response. Plant Physiol 126:1250–1258PubMedGoogle Scholar
  218. 218.
    Blázquez M, Santos E, Flores C, Martínez-Zapater J, Salinas J, Gancedo C (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13:685–689PubMedGoogle Scholar
  219. 219.
    Vogel G, Aeschbacher R, Müller J, Boller T, Wiemken A (1998) Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J 13:673–683PubMedGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  1. 1.Department of Molecular BiologyMax Planck Institute for Developmental BiologyTübingenGermany

Personalised recommendations