The F-box protein ZEITLUPE controls stability and nucleocytoplasmic partitioning of GIGANTEA

Development (Cambridge)

Volumn 140, Issue 19, 2013, Pages 4060-4069

  Kim, Jeongsik ^a   Geng, Ruishuang ^a   Gallenstein, Richard A ^a   Somers, David E ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Arabidopsis; Circadian biology; F box protein; GIGANTEA; Nicotiana benthamiana; Nucleocytoplasmic partitioning

Indexed keywords

F BOX PROTEIN; GIGANTEA PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ZEITLUPE PROTEIN;

ARTICLE; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSIENT EXPRESSION;

ARABIDOPSIS; CIRCADIAN BIOLOGY; F-BOX PROTEIN; GIGANTEA; NICOTIANA BENTHAMIANA; NUCLEOCYTOPLASMIC PARTITIONING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; IMMUNOPRECIPITATION; PLANTS, GENETICALLY MODIFIED;

EID: 84884270728     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.096651     Document Type: Article

References (53)

1. Ballario, P., Vittorioso, P., Magrelli, A., Talora, C., Cabibbo, A. and Macino, G. (1996). White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J. 15, 1650-1657.
2. Ballario, P., Talora, C., Galli, D., Linden, H. and Macino, G. (1998). Roles in dimerization and blue light photoresponse of the PAS and LOV domains of Neurospora crassa white collar proteins. Mol. Microbiol. 29, 719-729.
3. Baudry, A., Ito, S., Song, Y. H., Strait, A. A., Kiba, T., Lu, S., Henriques, R., Pruneda-Paz, J. L., Chua, N. H., Tobin, E. M. et al. (2010). F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression. Plant Cell 22, 606-622.
4. Cha, J., Yuan, H. and Liu, Y. (2011). Regulation of the activity and cellular localization of the circadian clock protein FRQ. J. Biol. Chem. 286, 11469-11478.
5. Clough, S. J. and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
6. Crosson, S., Rajagopal, S. and Moffat, K. (2003). The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42, 2-10.
7. David, K. M., Armbruster, U., Tama, N. and Putterill, J. (2006). Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett. 580, 1193-1197.
8. Demarsy, E. and Fankhauser, C. (2009). Higher plants use LOV to perceive blue light. Curr. Opin. Plant Biol. 12, 69-74.
9. Fornara, F., Panigrahi, K. C., Gissot, L., Sauerbrunn, N., Rühl, M., Jarillo, J. A. and 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.
10. Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., Coupland, G. and 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.
11. Fujiwara, S., Wang, L., Han, L., Suh, S. S., Salomé, P. A., McClung, C. R. and Somers, D. E. (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.
12. Godinho, S. I., Maywood, E. S., Shaw, L., Tucci, V., Barnard, A. R., Busino, L., Pagano, M., Kendall, R., Quwailid, M. M., Romero, M. R. et al. (2007). The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316, 897-900.
13. Han, L., Mason, M., Risseeuw, E. P., Crosby, W. L. and Somers, D. E. (2004). Formation of an SCF(ZTL) complex is required for proper regulation of circadian timing. Plant J. 40, 291-301.
14. Harmer, S. L. (2009). The circadian system in higher plants. Annu. Rev. Plant Biol. 60, 357-377.
15. He, Q., Cheng, P., Yang, Y., Wang, L., Gardner, K. H. and Liu, Y. (2002). White collar-1, a DNA binding transcription factor and a light sensor. Science 297, 840-843.
16. He, Q., Cheng, P., Yang, Y., He, Q., Yu, H. and Liu, Y. (2003). FWD1-mediated degradation of FREQUENCY in Neurospora establishes a conserved mechanism for circadian clock regulation. EMBO J. 22, 4421-4430.
17. Herrero, E. and Davis, S. J. (2012). Time for a nuclear meeting: protein trafficking and chromatin dynamics intersect in the plant circadian system. Mol. Plant 5, 554-565.
18. Huq, E., Tepperman, J. M. and Quail, P. H. (2000). GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 97, 9789-9794.
19. Imaizumi, T., Tran, H. G., Swartz, T. E., Briggs, W. R. and Kay, S. A. (2003). FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302-306.
20. Imaizumi, T., Schultz, T. F., Harmon, F. G., Ho, L. A. and Kay, S. A. (2005). FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293-297.
21. Ito, S., Niwa, Y., Nakamichi, N., Kawamura, H., Yamashino, T. and Mizuno, T. (2008). Insight into missing genetic links between two evening-expressed pseudo-response regulator genes TOC1 and PRR5 in the circadian clockcontrolled circuitry in Arabidopsis thaliana. Plant Cell Physiol. 49, 201-213.
22. Ito, S., Song, Y. H. and Imaizumi, T. (2012). LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol. Plant 5, 573-582.
23. Kevei, E., Gyula, P., Hall, A., Kozma-Bognár, L., Kim, W. Y., Eriksson, M. E., Tóth, R., Hanano, S., Fehér, B., Southern, M. M. et al. (2006). Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE. Plant Physiol. 140, 933-945.
24. Kiba, T., Henriques, R., Sakakibara, H. and Chua, N. H. (2007). Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant Cell 19, 2516-2530.
25. Kim, J. and Somers, D. E. (2010). Rapid assessment of gene function in the circadian clock using artificial microRNA in Arabidopsis mesophyll protoplasts. Plant Physiol. 154, 611-621.
26. Kim, W. Y., Fujiwara, S., Suh, S. S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H. G. and Somers, D. E. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356-360.
27. Kim, J., Kim, Y., Yeom, M., Kim, J. H. and Nam, H. G. (2008). FIONA1 is essential for regulating period length in the Arabidopsis circadian clock. Plant Cell 20, 307-319.
28. Kim, Y., Lim, J., Yeom, M., Kim, H., Kim, J., Wang, L., Kim, W. Y., Somers, D. E. and Nam, H. G. (2013). ELF4 regulates GIGANTEA chromatin access through subnuclear sequestration. Cell Rep. 3, 671-677.
29. Ko, H. W., Jiang, J. and Edery, I. (2002). Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420, 673-678.
30. Koh, K., Zheng, X. and Sehgal, A. (2006). JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312, 1809-1812.
31. Martin-Tryon, E. L., Kreps, J. A. and Harmer, S. L. (2007). GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol. 143, 473-486.
32. Más, P. (2008). Circadian clock function in Arabidopsis thaliana: time beyond transcription. Trends Cell Biol. 18, 273-281.
33. Más, P., Kim, W. Y., Somers, D. E. and Kay, S. A. (2003). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567-570.
34. Matsuoka, D. and Tokutomi, S. (2005). Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc. Natl. Acad. Sci. USA 102, 13337-13342.
35. 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.
36. Mouradov, A., Cremer, F. and Coupland, G. (2002). Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14 Suppl., S111-S130.
37. Nakasako, M., Zikihara, K., Matsuoka, D., Katsura, H. and Tokutomi, S. (2008). Structural basis of the LOV1 dimerization of Arabidopsis phototropins 1 and 2. J. Mol. Biol. 381, 718-733.
38. Neff, M. M. and Chory, J. (1998). Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol. 118, 27-35.
39. Nelson, D. C., Lasswell, J., Rogg, L. E., Cohen, M. A. and Bartel, B. (2000). FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101, 331-340.
40. Park, D. H., Somers, D. E., Kim, Y. S., Choy, Y. H., Lim, H. K., Soh, M. S., Kim, H. J., Kay, S. A. and Nam, H. G. (1999). Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579-1582.
41. Sawa, M., Nusinow, D. A., Kay, S. A. and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261-265.
42. Schultz, T. F., Kiyosue, T., Yanovsky, M., Wada, M. and Kay, S. A. (2001). A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13, 2659-2670.
43. Siepka, S. M., Yoo, S. H., Park, J., Song, W., Kumar, V., Hu, Y., Lee, C. and Takahashi, J. S. (2007). Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 129, 1011-1023.
44. Somers, D. E., Schultz, T. F., Milnamow, M. and Kay, S. A. (2000). ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101, 319-329.
45. Somers, D. E., Kim, W. Y. and 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.
46. Song, Y. H., Smith, R. W., To, B. J., Millar, A. J. and Imaizumi, T. (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336, 1045-1049.
47. Takase, T., Nishiyama, Y., Tanihigashi, H., Ogura, Y., Miyazaki, Y., Yamada, Y. and 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.
48. Tataroǧlu, O. and Schafmeier, T. (2010). Of switches and hourglasses: regulation of subcellular traffic in circadian clocks by phosphorylation. EMBO Rep. 11, 927-935.
49. Voinnet, O., Rivas, S., Mestre, P. and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956.
50. Wang, L., Fujiwara, S. and Somers, D. E. (2010). PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock. EMBO J. 29, 1903-1915.
51. Yagita, K., Tamanini, F., Yasuda, M., Hoeijmakers, J. H., van der Horst, G. T. and Okamura, H. (2002). Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of the mPER2 clock protein. EMBO J. 21, 1301-1314.
52. Yakir, E., Hilman, D., Harir, Y. and Green, R. M. (2007). Regulation of output from the plant circadian clock. FEBS J. 274, 335-345.
53. Yu, J. W., Rubio, V., Lee, N. Y., Bai, S., Lee, S. Y., Kim, S. S., Liu, L., Zhang, Y., Irigoyen, M. L., Sullivan, J. A. et al. (2008). COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell 32, 617-630.