Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between Flowering Locus C-mediated repression and photoperiodic induction of flowering

Plant Physiology

Volumn 148, Issue 3, 2008, Pages 1681-1694

  Wollenberg, Amanda C ^a   Strasser, Bárbara ^b   Cerdán, Pablo D ^b,c   Amasino, Richard M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 57749093217     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.125468     Document Type: Article

References (123)

1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056
2. An H, Roussot C, Suarez-Lopez P, Corbesier L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, et al (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131: 3615-3626
3. Aukerman MJ, Hirschfeld M, Wester L, Weaver M, Clack T, Amasino RM, Sharrock RA (1997) A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell 9: 1317-1326
4. Backstrom S, Elfving N, Nilsson R, Wingsle G, Bjorklund S (2007) Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol Cell 26: 717-729
5. Bagnall DJ (1992) Control of flowering in Arabidopsis thaliana by light, vernalisation and gibberellins. Aust J Plant Physiol 19: 401-409
6. Bagnall DJ (1993) Light quality and vernalization interact in controlling late flowering in Arabidopsis ecotypes and mutants. Ann Bot (Lond) 71: 75-83
7. Bagnall DJ, King RW, Whitelam GC, Boylan MT, Wagner D, Quail PH (1995) Flowering responses to altered expression of phytochrome in mutants and transgenic lines of Arabidopsis thaliana (L.) Heynh. Plant Physiol 108: 1495-1503
8. Balasubramanian S, Sureshkumar S, Agrawal M, Michael TP, Wessinger C, Maloof JN, Clark R, Warthmann N, Chory J, Weigel D (2006a) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nat Genet 38: 711-715
9. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006b) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2: 0980-0989
10. Ballare CL (1999) Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends Plant Sci 4: 97-102
11. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167
12. Blazquez MA, Weigel D (1999) Independent regulation of flowering by phytochrome B and gibberellins in Arabidopsis. Plant Physiol 120: 1025-1032
13. Borner R, Kampmann G, Chandler J, Gleissner R, Wisman E, Apel K, Melzer S (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J 24: 591-599
14. Callahan HS, Pigliucci M (2005) Indirect consequences of artificial selection on plasticity to light quality in Arabidopsis thaliana. J Evol Biol 18: 1403-1415
15. Carabelli M, Sessa G, Balma S, Morelli G, Ruberti I (1993) The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J 4: 469-479
16. Cerdan PD, Chory J (2003) Regulation of flowering time by light quality. Nature 423: 881-885
17. Clack T, Matthews S, Sharrock RA (1994) The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol 25: 413-427
18. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316: 1030-1033
19. David KM, Armbruster U, Tama N, Putterill J (2006) Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett 580: 1193-1197
20. Deitzer GF, Hayes RG, Jabben M (1979) Kinetics and time dependence of the effect of far red light on the photoperiodic induction of flowering in winter barley. Plant Physiol 64: 1015-1021
21. Deitzer GF, Hayes RG, Jabben M (1982) Phase shift in the circadian rhythm of floral promotion by far red energy in Hordeum vulgare L. Plant Physiol 69: 597-601
22. Dennis ES, Peacock WJ (2007) Epigenetic regulation of flowering. Curr Opin Plant Biol 10: 520-527
23. Devlin PF, Halliday KJ, Harberd NP, Whitelam GC (1996) The rosette habit of Arabidopsis thaliana is dependent upon phytochrome action: novel phytochromes control internode elongation and flowering time. Plant J 10: 1127-1134
24. Devlin PF, Patel SR, Whitelam GC (1998) Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 10: 1479-1487
25. Devlin PF, Robson PRH, Patel SR, Goosey L, Sharrock RA, Whitelam GC (1999) Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiol 119: 909-915
26. Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133: 1617-1629
27. Edwards KD, Lynn JR, Gyula P, Nagy F, Millar AJ (2005) Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170: 387-400
28. 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
29. Foster KR, Morgan PW (1995) Genetic regulation of development in Sorghum bicolor. IX. The ma3R allele disrupts diurnal control of gibberellin biosynthesis. Plant Physiol 108: 337-343
30. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18: 4679-4688
31. Franklin KA, Praekelt U, Stoddart WM, Billingham OE, Halliday KJ, Whitelam GC (2003) Phytochromes B, D, and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiol 131: 1340-1346
32. Franklin KA, Whitelam GC (2005) Phytochromes and shade-avoidance responses in plants. Ann Bot (Lond) 96: 169-175
33. Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39: 1410-1413
34. Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132: 1107-1114
35. Goto N, Kumagai T, Koornneef M (1991) Flowering responses to light-breaks in photomorphogenic mutants of Arabidopsis thaliana, a long-day plant. Physiol Plant 83: 209-215
36. Gould PD, Locke JC, Larue C, Southern MM, Davis SJ, Hanano S, Moyle R, Milich R, Putterill J, Millar AJ, et al (2006) The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18: 1177-1187
37. Halliday KJ, Koornneef M, Whitelam GC (1994) Phytochrome B and at least one other phytochrome mediate the accelerated flowering response of Arabidopsis thaliana L. to low red/far-red ratio. Plant Physiol 104: 1311-1315
38. 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
39. Halliday KJ, Whitelam GC (2003) Changes in photoperiod or temperature alter the functional relationships between phytochromes and reveal roles for phyD and phyE. Plant Physiol 131: 1913-1920
40. 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
41. 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: 4327-4337
42. 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
43. Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11: 550-558
44. 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
45. 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
46. Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17: 1050-1054
47. 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
48. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347
49. Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis: phytochrome A is required for the perception of daylength extensions. Plant Physiol 105: 141-149
50. Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19: 2736-2748
51. 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
52. Kebrom TH, Brutnell TP (2007) The molecular analysis of the shade avoidance syndrome in the grasses has begun. J Exp Bot 58: 3079-3089
53. Kim SY, Yu X, Michaels SD (2008) Regulation of CONSTANS and FLOWERING LOCUS T expression in response to changing light quality. Plant Physiol 148: 269-279
54. Kircher S, Gil P, Kozma-Bognar L, Fejes E, Speth V, Husselstein-Muller T, Bauer D, Adam E, Schafer E, Nagy F (2002) Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14: 1541-1555
55. 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
56. Le Corre V, Roux F, Reboud X (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Mol Biol Evol 19: 1261-1271
57. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14: 2366-2376
58. Lee I, Amasino RM (1995) Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol 108: 157-162
59. Lee JH, Hong SM, Yoo SJ, Park OK, Lee JS, Ahn JH (2006) Integration of floral inductive signals by flowering locus T and suppressor of overexpression of constans 1. Physiol Plant 126: 475-483
60. Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, Lian HL, Wang L, Yang HQ (2008) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20: 292-306
61. Locke JC, Southern MM, Kozma-Bognar L, Hibberd V, Brown PE, Turner MS, Millar AJ (2005) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1: 1-9
62. Lorrain S, Allen T, Duek P, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53: 312-323
63. Martin-Tryon EL, Kreps JA, Harmer SL (2007) GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol 143: 473-486
64. Martinez-Zapater JM, Somerville CR (1990) Effect of light quality and vernalization on late-flowering mutants of Arabidopsis thaliana. Plant Physiol 92: 770-776
65. Mathews S (2006) Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments. Mol Ecol 15: 3483-3503
66. Mathieu J, Warthmann N, Kuttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17: 1055-1060
67. 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
68. Michaels SD, Amasino RM (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: 935-941
69. Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci USA 100: 10102-10107
70. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137: 149-156
71. Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, et al (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17: 2255-2270
72. 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
73. Mockler TC, Yu X, Shalitin D, Parikh D, Michael TP, Liou J, Huang J, Smith Z, Alonso JM, Ecker JR, et al (2004) Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc Natl Acad Sci USA 101: 12759-12764
74. Monte E, Alonso JM, Ecker JR, Zhang Y, Li X, Young J, Austin-Phillips S, Quail PH (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15: 1962-1980
75. Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46: 292-299
76. Napp-Zinn K (1961) Vernalisation und verwandte Erscheinungen. In W Ruhland, ed, Handbuch der Pflanzenphysiologie, Vol 16. Springer, Berlin, pp 24-75
77. Napp-Zinn K (1964) Uber genetische und entwicklungsphysiologische Grundlagen jahreszeitlicher Aspekte von Pflanzengesellschaften. In K Kreeb, ed, Beitrage zur Phytologie. E Ulmer, Stuttgart, Germany, pp 33-49
78. Oliverio KA, Crepy M, Martin-Tryon EL, Milich R, Harmer SL, Putterill J, Yanovsky MJ, Casal JJ (2007) GIGANTEA regulates phytochrome A-mediated photomorphogenesis independently of its role in the circadian clock. Plant Physiol 144: 495-502
79. Onouchi H, Igeno MI, Perilleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12: 885-900
80. Paltiel J, Amin R, Gover A, Ori N, Samach A (2006) Novel roles for GIGANTEA revealed under environmental conditions that modify its expression in Arabidopsis and Medicago truncatula. Planta 224: 1255-1268
81. 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 the Arabidopsis GIGANTEA gene. Science 285: 1579-1582
82. Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3: 85-93
83. Ratcliffe OJ, Kumimoto RW, Wong BJ, Riechmann JL (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15: 1159-1169
84. Ratcliffe OJ, Nadzan GC, Reuber TL, Riechmann JL (2001) Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol 126: 122-132
85. Redei GP (1962) Supervital mutants of Arabidopsis. Genetics 47: 443-460
86. Reed JW, Nagatani A, Elich TD, Fagan M, Chory J (1994) Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol 104: 1139-1149
87. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5: 147-157
88. Robson P, Whitelam GC, Smith H (1993) Selected components of the shade-avoidance syndrome are displayed in a normal manner in mutants of Arabidopsis thaliana and Brassica rapa deficient in phytochrome B. Plant Physiol 102: 1179-1184
89. Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57: 837-858
90. Roden LC, Song HR, Jackson S, Morris K, Carre IA (2002) Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis. Proc Natl Acad Sci USA 99: 13313-13318
91. Roig-Villanova I, Bou J, Sorin C, Devlin PF, Martinez-Garcia JF (2006) Identification of primary target genes of phytochrome signaling: early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol 141: 85-96
92. Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portoles S, Rodriguez-Concepcion M, Martinez-Garcia JF (2007) Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. EMBO J 26: 4756-4767
93. Roux F, Touzet P, Cuguen J, Le Corre V (2006) How to be early flowering: an evolutionary perspective. Trends Plant Sci 11: 375-381
94. Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426: 680-683
95. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288: 1613-1616
96. 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
97. Schmitz RJ, Amasino RM (2007) Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. Biochim Biophys Acta 1769: 269-275
98. Schmitz RJ, Hong L, Michaels S, Amasino RM (2005) FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana. Development 132: 5471-5478
99. Scortecci K, Michaels SD, Amasino RM (2003) Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Mol Biol 52: 915-922
100. Scortecci KC, Michaels SD, Amasino RM(2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26: 229-236
101. Searle I, Coupland G (2004) Induction of flowering by seasonal changes in photoperiod. EMBO J 23: 1217-1222
102. 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: 898-912
103. Sessa G, Carabelli M, Sassi M, Ciolfi A, Possenti M, Mittempergher F, Becker J, Morelli G, Ruberti I (2005) A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev 19: 2811-2815
104. Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130: 442-456
105. Sharrock RA, Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev 3: 1745-1757
106. 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
107. Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296: 285-289
108. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33: 481-518
109. Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I (1999) Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 126: 4235-4245
110. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116-1120
111. Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164
112. 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
113. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316: 1033-1036
114. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133: 177-191
115. 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
116. Weller JL, Murfet IC, Reid JB (1997) Pea mutants with reduced sensitivity to far-red light define an important role for phytochrome A in day-length detection. Plant Physiol 114: 1225-1236
117. Wester L, Somers DE, Clack T, Sharrock RA (1994) Transgenic complementation of the hy3 phytochrome B mutation and response to PHYB gene copy number in Arabidopsis. Plant J 5: 261-272
118. Whitelam GC, Johnson E, Peng J, Carol P, Anderson ML, Cowl JS, Harberd NP (1993) Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5: 757-768
119. Whitelam GC, Smith H (1991) Retention of phytochrome-mediated shade avoidance responses in phytochrome-deficient mutants of Arabidopsis, cucumber, and tomato. J Plant Physiol 39: 119-125
120. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059
121. Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46: 1175-1189
122. Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308-312
123. 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: 770-778