Abstract
Plants have evolved a mechanism to synchronize flowering time in response to environments. How plants recognize specific seasons for flowering has been a long sought question, thus, more than 100 years of research has been focused on this question. Especially in the past two decades, remarkable achievements have been made in identifying the molecular mechanism for flowering. Here we summarize the breakthroughs made in this field over the past century including discoveries of photoperiodic and vernalization-induced flowering, the identification of complex genetic pathways, and the recently proposed identity of florigen. In addition, we present the currently accepted model for a molecular mechanism toward flowering.
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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. Science309: 1052–1056
An H, Roussot C, Suarez-Lopez R Corbesier L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland C (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering ofArabidopsis. Development131: 3615–3626
Aukerman MJ, Lee I, Weigel D, Amasino RM (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 J18: 195–203
Ausfn I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet36: 162–166
Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature427: 164–167
Blazquez MA, Weigel D (2000) Integration of floral inductive signals inArabidopsis, Nature404: 889–892
Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006)CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science312: 1040–1043
Burn JE, Bagnall DJ, Metzger JM, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci USA90: 287–291
Chailakhyan MK (1937) Concerning the hormonal nature of plant development processes. Doklady Akad Nauk SSSR16: 227–230
Chanvivattana Y, Bishop A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J (2004) Interaction of Polycomb-group proteins controlling flowering inArabidopsis. Development131: 5263–5276
Choi K, Kim S, Kim SY, Kim M, Hyun Y, Lee H, Choe S, Kim SG, Michaels S, Lee I (2005)SUPPRESSOR OF FRICIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repressionin Arabidopsis. Plant Cell17: 2647–2660
Clarke JH, Dean C (1994) MappingFRI, a locus controlling flowering time and vernalization response inArabidopsis thaliana. Mol Gen Genet242: 81–89
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 ofArabidopsis. Sciencexpress Doi 10.1126/science 1141752
Curtis OF, Chang HT (1930) The relative effectiveness of the temperature of the crown as contrasted with that of the rest of the plant upon the flowering of celery plants. Amer J Bot17: 1047–1048
Deal RB, Kandasamy MK, McKinney EC, Meagher RB (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance ofFLOWERING LOCUS C expression and repression of flowering inArabidopsis. Plant Cell17: 2633–2646
Deal RB, Topp CN, McKinney EC, Meagher RB (2007) Repression of flowering inArabidopsis requires activation ofFLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell doi tpc.106.048447
Finnegan EJ, Genger CN, Kovac K, Peacock WJ, Dennis ES (1998) DNA methylation and the promotion of flowering by vernalization. Proc Natl Acad Sci USA95: 5824–5829
Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland C, Putterill J (1999)GICANTEA: A circadian clock-controlled gene that regulates photoperiodic flowering inArabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J18: 4679–4688
Garner WW, Allard HA (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res18: 553–606
Gassner G (1918) Beiträge zur physiologiischen Charakteristik sommerund winterannueller Gewächse, insbesondere der Getreidepflanzen. Z Bot10: 417–480
Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation inArabidopsis accessions. Plant Physiol132: 1107–1114
Gendall, AR, Levy YY, Wilson A, Dean C (2001) TheVERNALIZATION 2 gene mediates the epigenetic regulation of vernalization inArabidopsis. Cell107: 525–535
Hamner KC, Bonner J (1938) Photoperiodism in relation to hormones as factors in floral initiation and development. Bot Gaz100: 518–530
Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responsesof Arabidopsis and rice. Plant Physiol135: 677–684
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature422: 719–722
He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation ofFLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit inArabidopsis. Genes Dev18: 2774–2784
He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation inArabidopsis. Science302: 1751–1754
Henderson IR, Dean C (2004) Control ofArabidopsis flowering: The chill before the bloom. Development131: 3829–3838
Huang T, Böhlenius H, Eriksson S, Parcy F, Nilsson O (2005) The mRNA of theArabidopsis geneFT moves from leaf to shoot apex and induces flowering. Science309: 1694–1696
Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev16: 2006–2020
Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducerFT. Science286: 1962–1965
Karlsson BH, Sills GR, Nienhuis J (1993) Effects of photoperiod and vernalization on the number of leaves at flowering in 32Arabidopsis thaliana (Brassicaceae) ecotypes. Amer J Bot80: 646–648
Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Kim HJ, Lee MH, Moon J, Lee I, Kim J (2004) A genetic link between cold responses and flowering time through FVE inArabidopsis thaliana. Nat Genet36: 167–171
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 ofArabidopsis FLOWERING LOCUS C. Plant Cell18: 2985–2998
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science286: 1960–1962
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002)Hd3a, a rice ortholog of theArabidopsis FT gene, promotes transition to flowering downstream ofHd1 under short-day conditions. Plant Cell Physiol43: 1096–1105
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 phenotype. Plant J6: 911–919
Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants inArabidopsis thaliana. Mol Gen Genet229: 57–66
Laibach F (1951) Über Sommer und Winterannuelle Rasse vonArabidopsis thalianum (L.) Heynh. Ein Beitrag zur Ätiologie der Blütenbildung. Beitr Biol Pflanz28: 173–210
Lang A, Melchers G (1943) Die photoperiodische reackion vonHyoscyamus niger. Planta33: 653–702
Lee H, Suh S, Park E, Cho E, Ahn JH, Kim S, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways inArabidopsis. Genes Dev14: 2366–2376
Lee I (2005) Multiple regulatory mechanisms of the floral repressorFLC, a gene conferring a vernalization requirement in Arabidopsis. Flowering Newsletter40: 52–59
Lee I, Aukerman MJ, Gore SL, Lohman KN, Michaels SD, Weaver LM, John MC, Feldmann KA, Amasino RM (1994a) Isolation ofLUMINIDEPENDENS: A gene involved in the control of flowering time inArabidopsis. Plant Cell6: 75–83
Lee I, Bleecker A, Amasino RM (1993) Analysis of naturally occurring late flowering inArabidopsis thaliana. Mol Gen Genet237: 171–176
Lee I, Michaels SD, Masshardt AS, Amasino RM (1994b) The late-flowering phenotype ofFRICIDA andLUMINIDEPENDENS is suppressed in the Landsberg erecta strain ofArabidopsis. Plant J6: 903–909
Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles ofArabidopsis VRN1 in vernalization and flowering time control. Science297: 243–246
Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomatoFT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA103: 6398–6403
Liu J, He Y, Amasino R, Chen X (2004) siRNAs targeting an intronic transposon in the regulation of natural flowering behavior inArabidopsis. Genes Dev18: 2873–2878
Macknight R, Bancroft I, Lister C, Page T, Love K, Schmidt R, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997)FCA, a gene controlling flowering time inArabidopsis, encodes a protein containing RNA-binding domains. Cell89: 737–745
Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C (2002) Functional significance of the alternative transcript processing of theArabidopsis floral promoterFCA. Plant Cell14: 877–888
March-Díaz R, García-Domínguez M, Florencio FJ, Reyes JC (2007) SEF, a New Protein Required for Flowering Repression inArabidopsis, Interacts with PIE1 and ARP6. Plant Physiol143: 893–901
Martin-Trillo M, Lazaro A, Poethig RS, Gomez-Mena C, Pineiro MA, Martinez-Zapater JM, Jarillo JA (2006)EARLY IN SHORT DAYS 1 (ESDI) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation inArabidopsis. Development133: 1241–1252
Michaels SD, Amasino RM (1999)FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell11:949–956
Michaels SD, Amasino RM (2001) Loss ofFLOWERING LOCUS C activity eliminates the late-flowering phenotype ofFRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell13: 935–941
Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit inArabidopsis. Proc Natl Acad Sci USA101: 3281–3285
Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation ofFLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior inArabidopsis. Proc Natl Acad Sci USA100: 10102–10107
Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SC, Lee I (2003) TheSOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering inArabidopsis. Plant J35: 613–623
Napp-Zinn K (1969)Arabidopsis thaliana (L.) Heynh,In LT Evans, ed, The Induction of Flowering: Some Case Histories. Melbourne, Macmillan, pp 291–304
Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of circadian rhythms and photoperiodic flowering by theArabidopsis GIGANTEA gene. Science285: 1579–1582
Putterill J, Laurie R, Macknight R (2004) It’s time to flower: The genetic control of flowering time. Bioessays26: 363–373
Putterill J, Robson F, Lee K, Simon R, Coupland C (1995) TheCONSTANS gene ofArabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell80: 847–857
Redei GP (1962) Supervital mutants ofArabidopsis. Genetics47: 443–460
Samach A, Onouchi H, Cold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development ofArabidopsis. Science288: 1613–1618
Schmitz RJ, Hong L, Michaels S, Amasino RM (2005)FRICIDAESSENTIAL1 interacts genetically withFRIGIDA andFRIGIDALIKE1 to promote the winter-annual habit ofArabidopsis thaliana. Development132: 5471–5478
Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: A repressor of flowering inArabidopsis regulated by vernalization and methylation. Plant Cell11: 445–458
Simpson GG, Dean C (2002)Arabidopsis, the Rosetta stone of flowering time? Science296: 285–289
Súarez-López, P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001)CONSTANS mediates between the circadian clock and the control of flowering inArabidopsis. Nature410: 1116–1120
Sung S, Amasino RM (2004a) Vernalization inArabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature427: 159–164
Sung S, Amasino RM (2004b) Vernalization and epigenetics: How plants remember winter. Curr Opin Plant Biol7: 4–10
Takada S, Goto K (2003) TERMINAL FLOWER2, anArabidopsis homolog of HETEROCHROMATIN PROTEIN1, counteracts the activation ofFLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell15: 2856–2865
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Sciencexpress Doi 10.1126/science 1141753
Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science303: 1003–1006
Wellensiek SJ (1962) Dividing cells as the locus for vernalization. Nature195: 307–308
Wellensiek SJ (1964) Dividing cells as the prerequisite for vernalization. Plant Physiol39: 832–835
Weiler JL, Reid JB, Taylor SA, Murfet IC (1997) The genetic control of flowering in pea. Trends Plant Sci2: 412–418
Werner JD, Borevitz JO, Uhlenhaut H, Ecker JR, Chory J, Weigel D (2005) FRIGIDA-independent variation in flowering time of naturalArabidopsis thaliana accessions. Genetics170: 1197–1207
Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral inductionIn Arabidopsis. Science309: 1056–1059
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, San-Miguel R, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheatVRN2 gene is a flowering repressor down-regulated by vernalization. Science303: 1640–1644
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 theArabidopsis flowering time geneCONSTANS. Plant Cell12: 2473–2484
Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement inArabidopsis. Nature419: 308–312
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Oh, M., Lee, U. Historical perspective on breakthroughs in flowering field. J. Plant Biol. 50, 249–256 (2007). https://doi.org/10.1007/BF03030652
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DOI: https://doi.org/10.1007/BF03030652