CUL1 regulates TOC1 protein stability in the Arabidopsis circadian clock

Plant Journal

Volumn 55, Issue 4, 2008, Pages 568-579

  Harmon, Frank ^a,b   Imaizumi, Takato ^c   Gray, William M ^d  

^a PLANT GENE EXPRESSION CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Arabidopsis; Circadian rhythms; CUL1; Post translational regulation; Proteasome; Ubiquitin ligase

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 49249122160     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03527.x     Document Type: Article

References (57)

1. Abramoff, M.D., Magelhaes, P.J. Ram, S.J. (2004) Image processing with ImageJ. Biophotonics Int. 11, 36 42.
2. Alabadi, D., Oyama, T., Yanovsky, M.J., Harmon, F.G., Mas, P. Kay, S.A. (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science, 293, 880 883.
3. Alabadi, D., Yanovsky, M.J., Mas, P., Harmer, S.L. Kay, S.A. (2002) Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr. Biol. 12, 757 761.
4. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
5. Bachmair, A., Novatchkova, M., Potuschak, T. Eisenhaber, F. (2001) Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci. 6, 463 470.
6. Blasing, O.E., Gibon, Y., Gunther, M., Hohne, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheible, W.R. Stitt, M. (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell, 17, 3257 3281.
7. Covington, M.F. Harmer, S.L. (2007) The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol. 5, e222.
8. Dodd, A.N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J.M., Millar, A.J. Webb, A.A. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309, 630 633.
9. Durfee, T., Roe, J.L., Sessions, R.A., Inouye, C., Serikawa, K., Feldmann, K.A., Weigel, D. Zambryski, P.C. (2003) The F-box-containing protein UFO and AGAMOUS participate in antagonistic pathways governing early petal development in Arabidopsis. Proc. Natl Acad. Sci. USA, 100, 8571 8576.
10. Engelmann, W. Johnsson, A. (1998) Rhythms in organ movement. In Biological Rhythms and Photoperiodism in Plants (Lumsden, P.J. Millar, A.J., eds). Oxford : Bios Scientific Publishers pp. 35 50.
11. 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.
12. Gagne, J.M., Downes, B.P., Shiu, S.H., Durski, A.M. Vierstra, R.D. (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl Acad. Sci. USA, 99, 11519 11524.
13. Gray, W.M., Hellmann, H., Dharmasiri, S. Estelle, M. (2002) Role of the Arabidopsis RING-H2 protein RBX1 in RUB modification and SCF function. Plant Cell, 14, 2137 2144.
14. Green, R.M. Tobin, E.M. (1999) Loss of the circadian clock-associated protein I in Arabidopsis results in altered clock-regulated gene expression. Proc. Natl Acad. Sci. USA, 96, 4176 4179.
15. Green, R.M., Tingay, S., Wang, Z.Y. Tobin, E.M. (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol. 129, 576 584.
16. Guo, H. Ecker, J.R. (2003) Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell, 115, 667 677.
17. Han, L., Mason, M., Risseeuw, E.P., Crosby, W.L. Somers, D.E. (2004) Formation of an SCF(ZTL) complex is required for proper regulation of circadian timing. Plant J. 40, 291 301.
18. Hanano, S., Domagalska, M.A., Nagy, F. Davis, S.J. (2006) Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells, 11, 1381 1392.
19. Harmer, S.L., Covington, M.F., Blasing, O.E. Stitt, M. (2005) Circadian regulation of global gene expression and metabolism. In Endogenous Plant Rhythms (Hall, A. McWatters, H.G., eds). Oxford : Blackwell Publishing Ltd, pp. 133 166.
20. Harmon, F.G., Imaizumi, T. Kay, S.A. (2005) The plant circadian clock: review of a clockwork Arabidopsis. In Endogenous Plant Rhythms (Hall, A.J.W. McWatters, H.G., eds). Oxford : Blackwell Publishing Ltd, pp. 1 23.
21. Hazen, S.P., Schultz, T.F., Pruneda-Paz, J.L., Borevitz, J.O., Ecker, J.R. Kay, S.A. (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc. Natl Acad. Sci. USA, 102, 10387 10392.
22. Hellmann, H., Hobbie, L., Chapman, A., Dharmasiri, S., Dharmasiri, N., del Pozo, C., Reinhardt, D. Estelle, M. (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J. 22, 3314 3325.
23. Hershko, A. Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425 479.
24. Hotta, C.T., Gardner, M.J., Hubbard, K.E., Baek, S.J., Dalchau, N., Suhita, D., Dodd, A.N. Webb, A.A. (2007) Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ. 30, 333 349.
25. Imaizumi, T. Kay, S.A. (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci. 11, 550 558.
26. Jarillo, J.A., Capel, J., Tang, R.H., Yang, H.Q., Alonso, J.M., Ecker, J.R. Cashmore, A.R. (2001) An Arabidopsis circadian clock component interacts with both CRY1 and phyB. Nature, 410, 487 490.
27. Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G. Somers, D.E. (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature, 449, 356 360.
28. Kreps, J.A. Kay, S.A. (1997) Coordination of plant metabolism and development by the circadian clock. Plant Cell, 9, 1235 1244.
29. Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X. Harper, J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129 2141.
30. Makino, S., Matsushika, A., Kojima, M., Yamashino, T. Mizuno, T. (2002) The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: I. Characterization with APRR1-overexpressing plants. Plant Cell Physiol. 43, 58 69.
31. Mas, P., Alabadi, D., Yanovsky, M.J., Oyama, T. Kay, S.A. (2003a) Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell, 15, 223 236.
32. Mas, P., Kim, W.Y., Somers, D.E. Kay, S.A. (2003b) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature, 426, 567 570.
33. Matsushika, A., Makino, S., Kojima, M., Yamashino, T. Mizuno, T. (2002) The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: II. Characterization with CCA1-overexpressing plants. Plant Cell Physiol. 43, 118 122.
34. Millar, A.J., Short, S.R., Chua, N.H. Kay, S.A. (1992) A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell, 4, 1075 1087.
35. Millar, A.J., Carre, I.A., Strayer, C.A., Chua, N.H. Kay, S.A. (1995a) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science, 267, 1161 1163.
36. Millar, A.J., Straume, M., Chory, J., Chua, N.H. Kay, S.A. (1995b) The regulation of circadian period by phototransduction pathways in Arabidopsis. Science, 267, 1163 1166.
37. Murashige, T. Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant, 15, 473 497.
38. Perales, M. Mas, P. (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell, 19, 2111 2123.
39. Pickart, C.M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503 533.
40. Plautz, J.D., Straume, M., Stanewsky, R., Jamison, C.F., Brandes, C., Dowse, H.B., Hall, J.C. Kay, S.A. (1997) Quantitative analysis of Drosophila period gene transcription in living animals. J. Biol. Rhythms, 12, 204 217.
41. Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C. Genschik, P. (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell, 115, 679 689.
42. Quint, M., Ito, H., Zhang, W. Gray, W.M. (2005) Characterization of a novel temperature-sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases. Plant J. 43, 371 383.
43. Risseeuw, E.P., Daskalchuk, T.E., Banks, T.W., Liu, E., Cotelesage, J., Hellmann, H., Estelle, M., Somers, D.E. Crosby, W.L. (2003) Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J. 34, 753 767.
44. Salter, M.G., Franklin, K.A. Whitelam, G.C. (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature, 426, 680 683.
45. Sambrook, J. Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
46. Schaffer, R., Ramsay, N., Samach, A., Corden, S., Putterill, J., Carre, I.A. Coupland, G. (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell, 93, 1219 1229.
47. Shen, W.H., Parmentier, Y., Hellmann, H., Lechner, E., Dong, A., Masson, J., Granier, F., Lepiniec, L., Estelle, M. Genschik, P. (2002) Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis. Mol. Biol. Cell, 13, 1916 1928.
48. Smalle, J. Vierstra, R.D. (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555 590.
49. Somers, D.E., Webb, A.A., Pearson, M. Kay, S.A. (1998) The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development, 125, 485 494.
50. Somers, D.E., Schultz, T.F., Milnamow, M. Kay, S.A. (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell, 101, 319 329.
51. Somers, D.E., Kim, W.Y. 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.
52. Strayer, C., Oyama, T., Schultz, T.F., Raman, R., Somers, D.E., Mas, P., Panda, S., Kreps, J.A. Kay, S.A. (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science, 289, 768 771.
53. Vierstra, R.D. (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135 142.
54. 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.
55. Woo, H.R., Chung, K.M., Park, J.H., Oh, S.A., Ahn, T., Hong, S.H., Jang, S.K. Nam, H.G. (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell, 13, 1779 1790.
56. Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W.L., Ma, H., Peng, W., Huang, D. Xie, D. (2002) The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell, 14, 1919 1935.
57. Zheng, N., Schulman, B.A., Song, L. et al. (2002) Structure of the Cul1-Rbx1-Skp1-F box(Skp2)SCF ubiquitin ligase complex. Nature, 416, 703 709.