A complementary role for ELF3 and TFL1 in the regulation of flowering time by ambient temperature

Plant Journal

Volumn 58, Issue 4, 2009, Pages 629-640

  Strasser, Bárbara ^a   Alvarez, Mariano J ^b   Califano, Andrea ^b   Cerdán, Pablo D ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Ambient temperature; Arabidopsis; ELF3; Flowering; Microarrays; TFL1

Indexed keywords

ARABIDOPSIS PROTEIN; ELF3 PROTEIN, ARABIDOPSIS; PLANT RNA; TFL1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; DNA MICROARRAY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOPERIODICITY; TEMPERATURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTOPERIOD; RNA, PLANT; TEMPERATURE; TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 66149178807     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03811.x     Document Type: Article

References (64)

1. Ahn, J.H., Miller, D., Winter, V.J., Banfield, M.J., Lee, J.H., Yoo, S.Y., Henz, S.R., Brady, R.L. Weigel, D. (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 25, 605 614. (Pubitemid 43237667)
2. Balasubramanian, S., Sureshkumar, S., Lempe, J. Weigel, D. (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2, e106.
3. Blazquez, M.A., Ahn, J.H. Weigel, D. (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nature Genet. 33, 168 171. (Pubitemid 36177068)
4. Boss, P.K., Bastow, R.M., Mylne, J.S. Dean, C. (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell, 16 Suppl, S18 S31. (Pubitemid 38774214)
5. Bradley, D., Ratcliffe, O., Vincent, C., Carpenter, R. Coen, E. (1997) Inflorescence commitment and architecture in Arabidopsis. Science, 275, 80 83. (Pubitemid 27020312)
6. Buchovsky, A.S., Strasser, B., Cerdan, P.D. Casal, J.J. (2008) Suppression of pleiotropic effects of functional CRYPTOCHROME genes by TERMINAL FLOWER 1. Genetics, 180, 1467 1474. Jiang, S. (2005) Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep. 24, 683 690.
7. Conti, L. Bradley, D. (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell, 19, 767 778. (Pubitemid 46953226)
8. Corbesier, L., Vincent, C., Jang, S. et al. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 316, 1030 1033. (Pubitemid 46799490)
9. Covington, M.F., Panda, S., Liu, X.L., Strayer, C.A., Wagner, D.R. Kay, S.A. (2001) ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell, 13, 1305 1315. (Pubitemid 32592905)
10. Doyle, M.R., Davis, S.J., Bastow, R.M., McWatters, H.G., Kozma-Bognar, L., Nagy, F., Millar, A.J. Amasino, R.M. (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature, 419, 74 77.
11. El-Assal, S.E., Alonso-Blanco, C., Peeters, A.J., Wagemaker, C., Weller, J.L. Koornneef, M. (2003) The role of cryptochrome 2 in flowering in Arabidopsis. Plant Physiol. 133, 1504 1516. (Pubitemid 38047282)
12. Fowler, S.G., Cook, D. Thomashow, M.F. (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137, 961 968. (Pubitemid 43138168)
13. Gautier, L., Cope, L., Bolstad, B.M. Irizarry, R.A. (2004) affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics, 20, 307 315. (Pubitemid 38262761)
14. Halliday, K.J. Whitelam, G.C. (2003) Changes in photoperiod or temperature alter the functional relationships between phytochromes and reveal roles for phyD and phyE. Plant Physiol. 131, 1913 1920. (Pubitemid 36463615)
15. Halliday, K.J., Salter, M.G., Thingnaes, E. Whitelam, G.C. (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J. 33, 875 885. (Pubitemid 36339379)
16. Hanzawa, Y., Money, T. Bradley, D. (2005) A single amino acid converts a repressor to an activator of flowering. Proc. Natl Acad. Sci. USA, 102, 7748 7753. (Pubitemid 40741042)
17. He, Y. Amasino, R.M. (2005) Role of chromatin modification in flowering-time control. Trends Plant Sci. 10, 30 35. (Pubitemid 40084626)
18. Hicks, K.A., Albertson, T.M. Wagner, D.R. (2001) EARLY FLOWERING3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis. Plant Cell, 13, 1281 1292. (Pubitemid 32592903)
19. Holm, M., Ma, L.G., Qu, L.J. Deng, X.W. (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16, 1247 1259. (Pubitemid 34553105)
20. Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A. Kay, S.A. (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science, 309, 293 297. (Pubitemid 40967864)
21. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249 264.
22. Jaeger, K.E. Wigge, P.A. (2007) FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17, 1050 1054. (Pubitemid 46899530)
23. Jang, S., Marchal, V., Panigrahi, K.C., Wenkel, S., Soppe, W., Deng, X.W., Valverde, F. Coupland, G. (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J. 27, 1277 1288.
24. Kandasamy, M.K., Deal, R.B., McKinney, E.C. Meagher, R.B. (2005) Silencing the nuclear actin-related protein AtARP4 in Arabidopsis has multiple effects on plant development, including early flowering and delayed floral senescence. Plant J. 41, 845 858. (Pubitemid 40398714)
25. Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S. Amasino, R. (2005a) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell, 17, 3301 3310.
26. Kim, W.Y., Hicks, K.A. Somers, D.E. (2005b) Independent roles for EARLY FLOWERING 3 and ZEITLUPE in the control of circadian timing, hypocotyl length, and flowering time. Plant Physiol. 139, 1557 1569. (Pubitemid 43786854)
27. Lamb, J., Crawford, E.D., Peck, D. et al. (2006) The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science, 313, 1929 1935. (Pubitemid 44497995)
28. Laubinger, S., Marchal, V., 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 3222. (Pubitemid 44404344)
29. Ledger, S., Strayer, C., Ashton, F., Kay, S.A. Putterill, J. (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J. 26, 15 22. (Pubitemid 32489180)
30. Lee, H., Suh, S.S., Park, E., Cho, E., Ahn, J.H., Kim, S.G., Lee, J.S., Kwon, Y.M. Lee, I. (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366 2376.
31. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S. Ahn, J.H. (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 21, 397 402. (Pubitemid 46310175)
32. Lee, J.H., Lee, J.S. Ahn, J.H. (2008) Ambient temperature signaling in plants: an emerging field in the regulation of flowering time. J. Plant Biol. 51, 321 326.
33. Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E. Yu, H. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell, 15, 110 120.
34. Liu, X.L., Covington, M.F., Fankhauser, C., Chory, J. Wagner, D.R. (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell, 13, 1293 1304. (Pubitemid 32592904)
35. Mansilla, M.C., Cybulski, L.E., Albanesi, D. de Mendoza, D. (2004) Control of membrane lipid fluidity by molecular thermosensors. J. Bacteriol. 186, 6681 6688. (Pubitemid 39332104)
36. 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. (Pubitemid 46899531)
37. Mazzella, M.A., Bertero, D. Casal, J.J. (2000) Temperature-dependent internode elongation in vegetative plants of Arabidopsis thaliana lacking phytochrome B and cryptochrome 1. Planta, 210, 497 501. (Pubitemid 30146901)
38. McWatters, H.G., Bastow, R.M., Hall, A. Millar, A.J. (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature, 408, 716 720. (Pubitemid 32015986)
39. Mizoguchi, T., Wright, L., Fujiwara, S. et al. (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell, 17, 2255 2270. (Pubitemid 41672945)
40. Mockler, T.C., Guo, H., Yang, H., Duong, H. Lin, C. (1999) Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development, 126, 2073 2082. (Pubitemid 29271693)
41. Mockler, T., Yang, H., Yu, X., Parikh, D., Cheng, Y.C., Dolan, S. Lin, C. (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc. Natl Acad. Sci. USA, 100, 2140 2145. (Pubitemid 36254587)
42. Neff, M.M., Neff, J.D., Chory, J. Pepper, A.E. (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J. 14, 387 392. (Pubitemid 28236003)
43. Nesi, N., Debeaujon, I., Jond, C., Pelletier, G., Caboche, M. Lepiniec, L. (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell, 12, 1863 1878.
44. Niwa, Y., Ito, S., Nakamichi, N., Mizoguchi, T., Niinuma, K., Yamashino, T. Mizuno, T. (2007) Genetic linkages of the circadian clock-associated genes, TOC1, CCA1 and LHY, in the photoperiodic control of flowering time in Arabidopsis thaliana. Plant Cell Physiol. 48, 925 937. (Pubitemid 47216628)
45. Page, T., Macknight, R., Yang, C.H. Dean, C. (1999) Genetic interactions of the Arabidopsis flowering time gene FCA, with genes regulating floral initiation. Plant J. 17, 231 239. (Pubitemid 129527741)
46. Penfield, S. (2008) Temperature perception and signal transduction in plants. New Phytol. 179, 615 628.
47. R-Development Core Team (2008) R: A Language and Environment for Statistical Computing. Vienna : R Foundation for Statistical Computing.
48. Reed, J.W., Nagpal, P., Bastow, R.M., Solomon, K.S., Dowson-Day, M.J., Elumalai, R.P. Millar, A.J. (2000) Independent action of ELF3 and phyB to control hypocotyl elongation and flowering time. Plant Physiol. 122, 1149 1160. (Pubitemid 30221394)
49. Ruiz-Garcia, L., Madueno, F., Wilkinson, M., Haughn, G., Salinas, J. Martinez-Zapater, J.M. (1997) Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell, 9, 1921 1934. (Pubitemid 28174066)
50. Samach, A. Wigge, P.A. (2005) Ambient temperature perception in plants. Curr. Opin. Plant Biol. 8, 483 486. (Pubitemid 41188181)
51. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Krober, S., Amasino, R.A. Coupland, G. (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898 912.
52. Shannon, S. Meeks-Wagner, D.R. (1993) Genetic interactions that regulate inflorescence development in Arabidopsis. Plant Cell, 5, 639 655. (Pubitemid 223001467)
53. Smyth, G.K. (2005) Limma: Linear Models for Microarray Data. New York : Springer.
54. Sohn, E.J., Rojas-Pierce, M., Pan, S., Carter, C., Serrano-Mislata, A., Madueno, F., Rojo, E., Surpin, M. Raikhel, N.V. (2007) The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole. Proc. Natl Acad. Sci. USA, 104, 18801 18806. (Pubitemid 350210777)
55. Soppe, W.J., Bentsink, L. Koornneef, M. (1999) The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. Development, 126, 4763 4770.
56. 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. (Pubitemid 32391045)
57. Subramanian, A., Tamayo, P., Mootha, V.K. et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA, 102, 15545 15550. (Pubitemid 41528093)
58. Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S. Shimamoto, K. (2007) Hd3a protein is a mobile flowering signal in rice. Science, 316, 1033 1036. (Pubitemid 46799491)
59. 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. (Pubitemid 38209702)
60. Wang, Z.Y. Tobin, E.M. (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell, 93, 1207 1217. (Pubitemid 28307425)
61. Yanovsky, M.J. Kay, S.A. (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature, 419, 308 312.
62. Yoo, S.K., Chung, K.S., Kim, J., Lee, J.H., Hong, S.M., Yoo, S.J., Yoo, S.Y., Lee, J.S. Ahn, J.H. (2005) CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol. 139, 770 778. (Pubitemid 43907105)
63. Yoo, S.Y., Kim, Y., Kim, S.Y., Lee, J.S. Ahn, J.H. (2007) Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS ONE, 2, e642.
64. Zhao, Z., Yu, Y., Meyer, D., Wu, C. Shen, W.H. (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat. Cell Biol. 7, 1156 1160. (Pubitemid 41741739)