Skip to main content
Log in

Tissue-specific regulation of flowering by photoreceptors

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Plants use various kinds of environmental signals to adjust the timing of the transition from the vegetative to reproductive phase (flowering). Since flowering at the appropriate time is crucial for plant reproductive strategy, several kinds of photoreceptors are deployed to sense environmental light conditions. In this review, we will update our current understanding of light signaling pathways in flowering regulation, especially, in which tissue do photoreceptors regulate flowering in response to light quality and photoperiod. Since light signaling is also integrated into other flowering pathways, we also introduce recent progress on how photoreceptors are involved in tissue-specific thermosensation and the gibberellin pathway. Finally, we discuss the importance of cell-type-specific analyses for future plant studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

SAR:

Shade avoidance response

LD:

Long day

SD:

Short day

References

  1. Kutschera U, Briggs WR (2013) Seedling development in buckwheat and the discovery of the photomorphogenic shade-avoidance response. Plant Biol (Stuttg) 15:931–940

    Article  CAS  Google Scholar 

  2. Pierik R, de Wit M (2014) Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues. J Exp Bot 65:2815–2824

    Article  PubMed  Google Scholar 

  3. Garner WW, Allard HA (1923) Further studies on photoperiodism, the response of plants to relative length of day and night. J Agric Res 23:871–920

    Google Scholar 

  4. Endo M, Nakamura S, Araki T, Mochizuki N, Nagatani A (2005) Phytochrome B in the mesophyll delays flowering by suppressing FLOWERING LOCUS T expression in Arabidopsis vascular bundles. Plant Cell 17:1941–1952

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Endo M, Mochizuki N, Suzuki T, Nagatani A (2007) CRYPTOCHROME2 in vascular bundles regulates flowering in Arabidopsis. Plant Cell 19:84–93

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Ranjan A, Fiene G, Fackendahl P, Hoecker U (2001) The Arabidopsis repressor of light signaling SPA1 acts in the phloem to regulate seedling de-etiolation, leaf expansion and flowering time. Development 138:1851–1862

    Article  CAS  Google Scholar 

  7. Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16:19–28

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Jeong J, Choi G (2013) Phytochrome-interacting factors have both shared and distinct biological roles. Mol Cells 35:371–380

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Leivar P, Tepperman JM, Monte E, Calderon RH, Liu TL, Quail PH (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21:3535–3553

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I, Lee HS, Sun TP, Kamiya Y, Choi G (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19:1192–1208

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53:312–323

    Article  CAS  PubMed  Google Scholar 

  12. Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245

    Article  CAS  PubMed  Google Scholar 

  13. Nozue K, Harmer SL, Maloof JN (2011) Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PHYTOCHROME-INTERACTING FACTOR5 as a modulator of auxin signaling in Arabidopsis. Plant Physiol 156:357–372

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Brock MT, Maloof JN, Weinig C (2010) Genes underlying quantitative variation in ecologically important traits: PIF4 (phytochrome interacting factor 4) is associated with variation in internode length, flowering time, and fruit set in Arabidopsis thaliana. Mol Ecol 19:1187–1199

    Article  PubMed  Google Scholar 

  15. Jiménez-Gómez JM, Wallace AD, Maloof JN (2010) Network analysis identifies ELF3 as a QTL for the shade avoidance response in Arabidopsis. PLoS Genet 6:e1001100

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  16. Zagotta MT, Hicks KA, Jacobs CI, Young JC, Hangarter RP, Meeks-Wagner DR (1996) The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J 10:691–702

    Article  CAS  PubMed  Google Scholar 

  17. Hicks KA, Albertson TM, Wagner DR (2001) EARLY FLOWERING3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis. Plant Cell 13:1281–1292

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13:1293–1304

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Yeom M, Kim H, Lim J, Shin AY, Hong S, Kim JI, Nam HG (2014) How do phytochromes transmit the light quality information to the circadian clock in Arabidopsis? Mol Plant 7:1701–1704

    Article  CAS  PubMed  Google Scholar 

  20. Nieto C, López-Salmerón V, Davière JM, Prat S (2015) ELF3-PIF4 interaction regulates plant growth independently of the evening complex. Curr Biol 25:187–193

    Article  CAS  PubMed  Google Scholar 

  21. Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426:680–683

    Article  CAS  PubMed  Google Scholar 

  22. Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Cerdán PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423:881–885

    Article  PubMed  CAS  Google Scholar 

  24. Raya-González J, Ortiz-Castro R, Ruíz-Herrera LF, Kazan K, López-Bucio J (2014) PHYTOCHROME AND FLOWERING TIME1/MEDIATOR25 regulates lateral root formation via auxin signaling in Arabidopsis. Plant Physiol 165:880–894

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  25. Koprivova A, Calderwood A, Lee BR, Kopriva S (2014) Do PFT1 and HY5 interact in regulation of sulfate assimilation by light in Arabidopsis? FEBS Lett 588:1116–1121

    Article  CAS  PubMed  Google Scholar 

  26. Yang Y, Ou B, Zhang J, Si W, Gu H, Qin G, Qu LJ (2014) The Arabidopsis Mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25. Plant J 77:838–851

    Article  CAS  PubMed  Google Scholar 

  27. Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66

    Article  CAS  PubMed  Google Scholar 

  29. Li J, Li G, Wang H, Deng XW (2011) Phytochrome signaling mechanisms. Arabidopsis Book 9:e0148

    Article  PubMed Central  PubMed  Google Scholar 

  30. Liu H, Liu B, Zhao C, Pepper M, Lin C (2011) The action mechanisms of plant cryptochromes. Trends Plant Sci 16:684–691

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Ahmad M, Jarillo JA, Cashmore AR (1998) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell 10:197–207

    PubMed Central  CAS  PubMed  Google Scholar 

  32. Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA 95:2686–2690

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Huang Y, Baxter R, Smith BS, Partch CL, Colbert CL, Deisenhofer J (2006) Crystal structure of cryptochrome 3 from Arabidopsis thaliana and its implications for photolyase activity. Proc Natl Acad Sci USA 103:17701–17706

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Pokorny R, Klar T, Hennecke U, Carell T, Batschauer A, Essen LO (2008) Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proc Natl Acad Sci USA 105:21023–21027

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Brudler R, Hitomi K, Daiyasu H, Toh H, Kucho K, Ishiura M, Kanehisa M, Roberts VA, Todo T, Tainer JA, Getzoff ED (2003) Identification of a new cryptochrome class. Structure, function, and evolution. Mol Cell 11:59–67

    Article  CAS  PubMed  Google Scholar 

  36. Brunelle SA, Starr Hazard E, Sotka EE, Van Dolah FM (2007) Characterization of a dinoflagellate Cryptochrome blue-light receptor with a possible role in a circadian control of the cell cycle. J Phycol 43:509–518

    Article  Google Scholar 

  37. Froehlich AC, Chen CH, Belden WJ, Madeti C, Roenneberg T, Merrow M, Loros JJ, Dunlap JC (2010) Genetic and molecular characterization of a cryptochrome from the filamentous fungus Neurospora crassa. Eukaryot Cell 9:738–750

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol Plant 5:573–582

    Article  PubMed  CAS  Google Scholar 

  39. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302–306

    Article  CAS  PubMed  Google Scholar 

  40. Jenkins GI (2014) The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell 26:21–37

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Liu L, Zhu Y, Shen L, Yu H (2013) Emerging insights into florigen transport. Curr Opin Plant Biol 16:607–613

    Article  CAS  PubMed  Google Scholar 

  42. Taoka K, Ohki I, Tsuji H, Kojima C, Shimamoto K (2013) Structure and function of florigen and the receptor complex. Trends Plant Sci 18:287–294

    Article  CAS  PubMed  Google Scholar 

  43. Goosey L, palecanda L, Sharrock RA (1997) Differential patterns of expression of the Arabidopsis PHYB, PHYD, and PHE phytochrome genes. Plant Physiol 115:959–969

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Somers DE, Quail PH (1995) Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis. Plant J 7:413–427

    Article  CAS  PubMed  Google Scholar 

  45. Tóth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognár L (2001) Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiol 127:1607–1616

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  46. Song YH, Ito S, Imaizumi T (2013) Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci 18:575–583

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515:419–422

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Brunkard JO, Runkel AM, Zambryski PC (2015) The cytosol must flow: intercellular transport through plasmodesmata. Curr Opin Cell Biol 35:13–20

    Article  CAS  PubMed  Google Scholar 

  49. Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464

    Article  CAS  PubMed  Google Scholar 

  50. Johansson M, Staiger D (2015) Time to flower: interplay between photoperiod and the circadian clock. J Exp Bot 66:719–730

    Article  PubMed  CAS  Google Scholar 

  51. Koornneef M, Hanhart CJ, van der Veen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66

    Article  CAS  PubMed  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  CAS  PubMed  Google Scholar 

  54. Onouchi H, Igeño MI, Périlleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12:885–900

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG, Imaizumi T (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc Natl Acad Sci USA 109:3582–3587

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297

    Article  CAS  PubMed  Google Scholar 

  58. Schultz TF, Kiyosue T, Yanovsky M, Wada M, Kay SA (2001) A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13:2659–2670

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Somers DE, Kim WY, Geng R (2004) The F-box protein ZEITLUPE confers dosage-dependent control on the circadian clock, photomorphogenesis, and flowering time. Plant Cell 16:769–782

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Takase T, Nishiyama Y, Tanihigashi H, Ogura Y, Miyazaki Y, Yamada Y, Kiyosue T (2011) LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. Plant J 67:608–621

    Article  CAS  PubMed  Google Scholar 

  61. Ito S, Niwa Y, Nakamichi N, Kawamura H, Yamashino T, Mizuno T (2008) Insight into missing genetic links between two evening-expressed pseudo-response regulator genes TOC1 and PRR5 in the circadian clock-controlled circuitry in Arabidopsis thaliana. Plant Cell Physiol 49:201–213

    Article  CAS  PubMed  Google Scholar 

  62. Más P, Kim WY, Somers DE, Kay SA (2003) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426:567–570

    Article  PubMed  CAS  Google Scholar 

  63. Kiba T, Henriques R, Sakakibara H, Chua NH (2007) Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant Cell 19:2516–2530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Fujiwara S, Wang L, Han L, Suh SS, Salomé PA, McClung CR, Somers DE (2008) Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J Biol Chem 283:23073–23083

    Article  CAS  PubMed  Google Scholar 

  65. Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86

    Article  CAS  PubMed  Google Scholar 

  66. Nakamichi N, Kita M, Niinuma K, Ito S, Yamashino T, Mizoguchi T, Mizuno T (2007) Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol 48:822–832

    Article  CAS  PubMed  Google Scholar 

  67. Nakamichi N, Kiba T, Kamioka M, Suzuki T, Yamashino T, Higashiyama T, Sakakibara H, Mizuno T (2012) Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc Natl Acad Sci USA 109:17123–17128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Kidd BN, Edgar CI, Kumar KK, Aitken EA, Schenk PM, Manners JM, Kazan K (2009) The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21:2237–2252

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Iñigo S, Alvarez MJ, Strasser B, Califano A, Cerdán PD (2012) PFT1, the MED25 subunit of the plant mediator complex, promotes flowering through CONSTANS dependent and independent mechanisms in Arabidopsis. Plant J 69:601–612

    Article  PubMed  CAS  Google Scholar 

  70. 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

    Article  CAS  PubMed  Google Scholar 

  71. Lazaro A, Valverde F, Piñeiro M, Jarillo JA (2012) The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24:982–999

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  73. 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

    Article  CAS  PubMed  Google Scholar 

  74. Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W, Deng XW, Valverde F, Coupland G (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J 27:1277–1288

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Zuo Z, Liu H, Liu B, Liu X, Lin C (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21:841–847

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Saijo Y, Zhu D, Li J, Rubio V, Zhou Z, Shen Y, Hoecker U, Wang H, Deng XW (2008) Arabidopsis COP1/SPA1 complex and FHY1/FHY3 associate with distinct phosphorylated forms of phytochrome A in balancing light signaling. Mol Cell 31:607–613

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  77. Lian HL, He SB, Zhang YC, Zhu DM, Zhang JY, Jia KP, Sun SX, Li L, Yang HQ (2011) Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev 25:1023–1028

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Liu B, Zuo Z, Liu H, Liu X, Lin C (2011) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev 25:1029–1034

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Sheerin DJ, Menon C, zur Oven-Krockhaus S, Enderle B, Zhu L, Johnen P, Schleifenbaum F, Stierhof YD, Huq E, Hiltbrunner A (2015) Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex. Plant Cell 27:189–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Mockler T, Yang H, Yu X, Parikh D, Cheng YC, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100:2140–2145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  81. Guo H, Yang H, Mockler TC, Lin C (1998) Regulation of flowering time by Arabidopsis photoreceptors. Science 279:1360–1363

    Article  CAS  PubMed  Google Scholar 

  82. Song YH, Estrada DA, Johnson RS, Kim SK, Lee SY, MacCoss MJ, Imaizumi T (2014) Distinct roles of FKF1, GIGANTEA, and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering. Proc Natl Acad Sci USA 111:17672–17677

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. Endo M, Tanigawa Y, Murakami T, Araki T, Nagatani A (2013) PHYTOCHROME-DEPENDENT LATE-FLOWERING accelerates flowering through physical interactions with phytochrome B and CONSTANS. Proc Natl Acad Sci USA 110:18017–18022

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Liu H, Yu X, Li K, Klejnot J, Yang H, Lisiero D, Lin C (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322:1535–1539

    Article  CAS  PubMed  Google Scholar 

  85. Liu Hongtao, Wang Qin, Liu Yawen, Zhao Xiaoying, Imaizumi Takato, Somers David E, Tobin Elaine M, Lin Chentao (2013) Arabidopsis CRY2 and ZTL mediate blue-light regulation of the transcription factor CIB1 by distinct mechanisms. Proc Natl Acad Sci USA 110:17582–17587

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  86. Sawa M, Kay SA (2011) GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:11698–11703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  87. Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci USA 97:9789–9794

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  88. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  89. Shimizu H, Katayama K, Koto T, Torii K, Araki T, Endo M (2015) Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues. Nature Plants 1, Article number: 15163

  90. Sheldon CC, Hills MJ, Lister C, Dean C, Dennis ES, Peacock WJ (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc Natl Acad Sci USA 105:2214–2229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  91. Marrocco K, Thomann A, Parmentier Y, Genschik P, Criqui MC (2009) The APC/C E3 ligase remains active in most post-mitotic Arabidopsis cells and is required for proper vasculature development and organization. Development 136:1475–1485

    Article  CAS  PubMed  Google Scholar 

  92. Zhu D, Rosa S, Dean C (2015) Nuclear organization changes and the epigenetic silencing of FLC during vernalization. J Mol Biol  427:659–669

    Article  CAS  PubMed  Google Scholar 

  93. Capovilla G, Schmid M, Posé D (2015) Control of flowering by ambient temperature. J Exp Bot 66:59–69

    Article  CAS  PubMed  Google Scholar 

  94. Davis SJ (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant, Cell Environ 32:1201–1210

    Article  CAS  Google Scholar 

  95. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  96. 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 11:445–458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  97. Helliwell CA, Wood CC, Robertson M, James Peacock W, Dennis ES (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

    Article  CAS  PubMed  Google Scholar 

  98. Yasui Y, Mukougawa K, Uemoto M, Yokofuji A, Suzuri R, Nishitani A, Kohchi T (2012) The phytochrome-interacting vascular plant one-zinc finger1 and VOZ2 redundantly regulate flowering in Arabidopsis. Plant Cell 24:3248–3263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  99. Yasui Y, Kohchi T (2014) VASCULAR PLANT ONE-ZINC FINGER1 and VOZ2 repress the FLOWERING LOCUS C clade members to control flowering time in Arabidopsis. Biosci Biotechnol Biochem 78:1850–1855

    Article  CAS  PubMed  Google Scholar 

  100. 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 33:875–885

    Article  CAS  PubMed  Google Scholar 

  101. Blázquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171

    Article  PubMed  CAS  Google Scholar 

  102. Strasser B, Alvarez MJ, Califano A, Cerdán PD (2009) A complementary role for ELF3 and TFL1 in the regulation of flowering time by ambient temperature. Plant J 58:629–640

    Article  CAS  PubMed  Google Scholar 

  103. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2:e106

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  104. Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245

    Article  CAS  PubMed  Google Scholar 

  105. de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484

    Article  PubMed  CAS  Google Scholar 

  106. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53:312–323

    Article  CAS  PubMed  Google Scholar 

  107. Michael TP, Salome PA, McClung CR (2003) Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc Natl Acad Sci USA 100:6878–6883

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  108. Xiaofeng Gu, Jiang Danhua, Yang Wannian, Jacob Yannick, Michaels Scott D, He Yuehui (2011) Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. PLoS Genet 7:e1002366

    Article  CAS  Google Scholar 

  109. Quesada V, Macknight R, Dean C, Simpson GG (2003) Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time. EMBO J 22:3142–3152

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  110. Staiger D, Allenbach L, Salathia N, Fiechter V, Davis SJ, Millar AJ, Chory J, Fankhauser C (2003) The Arabidopsis SRR1 gene mediates phyB signaling and is required for normal circadian clock function. Genes Dev 17:256–268

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  111. Castillejo C, Pelaz S (2008) The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr Biol 18:1338–1343

    Article  CAS  PubMed  Google Scholar 

  112. Osnato M, Castillejo C, Matías-Hernández L, Pelaz S (2012) TEMPRANILLO genes link photoperiod and gibberellin pathways to control flowering in Arabidopsis. Nat Commun 3:808

    Article  PubMed  CAS  Google Scholar 

  113. de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484

    Article  PubMed  CAS  Google Scholar 

  114. Galvão VC, Horrer D, Küttner F, Schmid M (2012) Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139:4072–4082

    Article  PubMed  CAS  Google Scholar 

  115. Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  116. Morgan DC, Warrington IJ, Rook DA (1985) Some observations on the spectral distribution characteristics of short-wave radiation within Pinus radiata D. Don canopies. Plant cell Environ 8:201–206

    Google Scholar 

  117. Eskins K (1992) Light-quality effects on Arabidopsis development. Red, blue and far-red regulation of flowering and morphology. Physiol Plant 86:439–444

    Article  Google Scholar 

Download references

Acknowledgments

We thank J. A. Hejna for English proofreading. This work was partially supported by Grant-in-Aid for Scientific Research (B) 17370018 (to A.N.); Grants-in-Aid for Scientific Research on Priority Areas 17084002 (to A.N.), and 19060012 and 19060016 (to T.A.); Grant-in-Aid for Young Scientists (B) 22770036 (to M.E.); and a Grant-in-Aid for 21st Century Circle of Excellence Research, Kyoto University (A14).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Nagatani.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Endo, M., Araki, T. & Nagatani, A. Tissue-specific regulation of flowering by photoreceptors. Cell. Mol. Life Sci. 73, 829–839 (2016). https://doi.org/10.1007/s00018-015-2095-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-015-2095-8

Keywords

Navigation