GIGANTEA is a co-chaperone which facilitates maturation of ZEITLUPE in the Arabidopsis circadian clock

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Cha, Joon Yung ^a   Kim, Jeongsik ^b,c   Kim, Tae Sung ^b,d   Zeng, Qingning ^b   Wang, Lei ^b,e   Lee, Sang Yeol ^a   Kim, Woe Yeon ^a   Somers, David E ^b  

^a Gyeongsang National University   (South Korea)

^b OHIO STATE UNIVERSITY   (United States)

^c Institute for Basic Science   (South Korea)

^d Korea National Open University   (South Korea)

^e INSTITUTE OF BOTANY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; F BOX PROTEIN; GIGANTEA PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; ZEITLUPE PROTEIN; ARABIDOPSIS PROTEIN; GI PROTEIN, ARABIDOPSIS; PROTEIN BINDING; ZTL PROTEIN, ARABIDOPSIS;

ANGIOSPERM; CIRCADIAN RHYTHM; HOMEOSTASIS; PHYSIOLOGY; PLANT; PROTEIN;

ARABIDOPSIS; ARTICLE; CIRCADIAN RHYTHM; IN VITRO STUDY; NONHUMAN; PROTEIN PROCESSING; CHEMISTRY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; LIGHT; METABOLISM; PHYSIOLOGICAL FEEDBACK; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; RADIATION RESPONSE; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CIRCADIAN CLOCKS; FEEDBACK, PHYSIOLOGICAL; FLOWERS; GENE EXPRESSION REGULATION, PLANT; HSP90 HEAT-SHOCK PROTEINS; KINETICS; LIGHT; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

EID: 85013760599     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-016-0014-9     Document Type: Article

References (68)

1. Hsu, P. Y. & Harmer, S. L. Wheels within wheels: the plant circadian system. Trends Plant. Sci. 19, 240 (2014).
2. Tataroglu, O. & Emery, P. The molecular ticks of the Drosophila circadian clock. Curr. Opin. Insect. Sci. 7, 51 (2015).
3. Seo, P. J. & Mas, P. Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis. Plant. Cell 26, 79 (2014).
4. Crane, B. R. & Young, M. W. Interactive features of proteins composing eukaryotic circadian clocks. Annu. Rev. Biochem. 83, 191 (2014).
5. Mas, P., Kim, W. Y., Somers, D. E. & Kay, S. A. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426, 567 (2003).
6. Kiba, T., Henriques, R., Sakakibara, H. & Chua, N. H. Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant. Cell 19, 2516 (2007).
7. Fujiwara, S. et al. Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. J. Biol. Chem. 283, 23073 (2008).
8. Ito, S., Song, Y. H. & Imaizumi, T. LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol. Plant. 5, 573 (2012).
9. Kim, W. Y. et al. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356 (2007).
10. Fowler, S. et al. 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 (1999).
11. Park, D. et al. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579 (1999).
12. Kim, W. Y., Geng, R. & Somers, D. E. Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome. Proc. Natl Acad. Sci. USA 100, 4933 (2003).
13. Gagic, M., Faville, M., Kardailsky, I. & Putterill, J. Comparative genomics and functional characterisation of the GIGANTEA gene from the temperate forage perennial ryegrass Lolium perenne. Plant. Mol. Biol. Rep. 33, 1098 (2015).
14. Huq, E., Tepperman, J. M. & Quail, P. H. GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 97, 9789 (2000).
15. Mishra, P. & Panigrahi, K. C. GIGANTEA - an emerging story. Front. Plant. Sci. 6, 8 (2015).
16. Dalchau, N. et al. The circadian oscillator gene GIGANTEA mediates a longterm response of the Arabidopsis thaliana circadian clock to sucrose. Proc. Natl. Acad. Sci. USA 108, 5104 (2011).
17. Kim, W. Y. et al. Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat. Commun. 4, 1352 (2013).
18. Sawa, M., Nusinow, D. A., Kay, S. A. & Imaizumi, T. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261 (2007).
19. Martin-Tryon, E. L., Kreps, J. A. & Harmer, S. L. GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant. Physiol. 143, 473 (2007).
20. Mizoguchi, T. et al. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant. Cell 17, 2255 (2005).
21. Gould, P. D. et al. The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant. Cell 18, 1177 (2006).
22. Kim, J., Geng, R., Gallenstein, R. A. & Somers, D. E. The F-box protein ZEITLUPE controls stability and nucleocytoplasmic partitioning of GIGANTEA. Development 140, 4060 (2013).
23. David, K. M., Armbruster, U., Tama, N. & Putterill, J. Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett. 580, 1193 (2006).
24. Kim, Y. et al. ELF4 regulates GIGANTEA chromatin access through subnuclear sequestration. Cell Rep. 3, 671 (2013).
25. Yu, J. W. et al. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell 32, 617 (2008).
26. Lee, G. J. Assaying proteins for molecular chaperone activity. Methods Cell Biol. 50, 325 (1995).
27. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M. & Hartl, F. U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323 (2013).
28. Chang, H. C., Tang, Y. C., Hayer-Hartl, M. & Hartl, F. U. SnapShot: molecular chaperones, Part I. Cell 128, 212 (2007).
29. Tang, Y. C., Chang, H. C., Hayer-Hartl, M. & Hartl, F. U. SnapShot: molecular chaperones, Part II. Cell 128, 412 (2007).
30. Blatch, G. L. & Edkins, A. L. (eds). Networking of Chaperones by Co- Chaperones, Subcellular Biochemistry Vol. 78, 1-276 (Springer International Publishing Switzerland, 2015).
31. Echtenkamp, F. J. & Freeman, B. C. Expanding the cellular molecular chaperone network through the ubiquitous cochaperones. Biochim. Biophys. Acta. 1823, 668 (2012).
32. Kim, T. S. et al. HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE. Proc. Natl. Acad. Sci. USA 108, 16843 (2011).
33. Veinger, L., Diamant, S., Buchner, J. & Goloubinoff, P. The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273, 11032 (1998).
34. Sharma, S. K., Christen, P. & Goloubinoff, P. Disaggregating chaperones: an unfolding story. Curr. Protein. Pept. Sci. 10, 432 (2009).
35. Haslbeck, M. & Buchner, J. Assays to characterize molecular chaperone function in vitro. Methods Mol. Biol. 1292, 39 (2015).
36. Lee, G. J., Roseman, A. M., Saibil, H. R. & Vierling, E. A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO. J. 16, 659 (1997).
37. Hansen, J. E. & Gafni, A. Thermal switching between enhanced and arrested reactivation of bacterial glucose-6-phosphate dehydrogenase assisted by GroEL in the absence of ATP. J. Biol. Chem. 268, 21632 (1993).
38. Sanz-Barrio, R. et al. Chaperone-like properties of tobacco plastid thioredoxins f and m. J. Exp. Bot. 63, 365 (2012).
39. Hayer-Hartl, M., Bracher, A. & Hartl, F. U. The GroEL-GroES chaperonin machine: a nano-cage for protein folding. Trends Biochem. Sci. 41, 62 (2016).
40. Park, J. H. et al. Heat-induced chaperone activity of serine/threonine protein phosphatase 5 enhances thermotolerance in Arabidopsis thaliana. New. Phytol. 191, 692 (2011).
41. Hutchinson, M. H. & Chase, H. A. Adsorptive refolding of histidine-tagged glutathione S-transferase using metal affinity chromatography. J. Chromatogr. A. 1128, 125 (2006).
42. Cha, J. Y., Kim, M., Kim, W. Y. & Kim, M. Development of in vitro HSP90 foldase chaperone assay using a GST-fused real-substrate. ZTL (ZEITLUPE) 58, 236 (2015).
43. Karagoz, G. E. & Rudiger, S. G. Hsp90 interaction with clients. Trends Biochem. Sci. 40, 117 (2015).
44. Freeman, B. C., Michels, A., Song, J., Kampinga, H. H. & Morimoto, R. I. Analysis of molecular chaperone activities using in vitro and in vivo approaches. Methods Mol. Biol. 99, 393 (2000).
45. Walther, T. V. & Maddalo, D. Intracellular refolding assay. J. Vis. Exp. 59, 3540 (2012).
46. Bepperling, A. et al. Alternative bacterial two-component small heat shock protein systems. Proc. Natl. Acad. Sci. USA 109, 20407 (2012).
47. Black, M. M., Stockum, C., Dickson, J. M., Putterill, J. & Arcus, V. L. Expression, purification and characterisation of GIGANTEA: a circadian clock-controlled regulator of photoperiodic flowering in plants. Protein. Expr. Purif. 76, 197 (2011).
48. Li, J. & Buchner, J. Structure, function and regulation of the Hsp90 machinery. Biomed. J. 36, 106 (2013).
49. Taipale, M., Jarosz, D. F. & Lindquist, S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 11, 515 (2010).
50. Rohl, A., Rohrberg, J. & Buchner, J. The chaperone Hsp90: changing partners for demanding clients. Trends Biochem. Sci. 38, 253 (2013).
51. Li, J., Soroka, J. & Buchner, J. The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim. Biophys. Acta. 1823, 624 (2012).
52. Prodromou, C. The "active life" of Hsp90 complexes. Biochim. Biophys. Acta. 1823, 614 (2012).
53. Taipale, M. et al. A quantitative chaperone interaction network reveals the architecture of cellular protein homeostasis pathways. Cell 158, 434 (2014).
54. Taipale, M. et al. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150, 987 (2012).
55. Genest, O., Hoskins, J. R., Camberg, J. L., Doyle, S. M. & Wickner, S. Heat shock protein 90 from Escherichia coli collaborates with the DnaK chaperone system in client protein remodeling. Proc. Natl. Acad. Sci. USA 108, 8206 (2011).
56. Takahashi, S. & Mendelsohn, M. E. Synergistic activation of endothelial nitric-oxide synthase (eNOS) by HSP90 and Akt: calcium-independent eNOS activation involves formation of an HSP90-Akt-CaM-bound eNOS complex. J. Biol. Chem. 278, 30821 (2003).
57. Panaretou, B., et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 10, 1307 (2002)
58. Kadota, Y. & Shirasu, K. The HSP90 complex of plants. Biochim. Biophys. Acta. 1823, 689 (2012).
59. Breiman, A. Plant Hsp90 and its co-chaperones. Curr. Protein. Pept. Sci. 15, 232 (2014).
60. Freeman, B. C., Toft, D. O. & Morimoto, R. I. Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptorassociated protein p23. Science 274, 1718 (1996).
61. Echtenkamp, F. J. et al. Global functional map of the p23 molecular chaperone reveals an extensive cellular network. Mol. Cell 43, 229 (2011).
62. Kim, J. & Somers, D. E. Rapid assessment of gene function in the circadian clock using artificial microRNA in Arabidopsis mesophyll protoplasts. Plant. Physiol. 154, 611 (2010).
63. Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant. Physiol. 133, 462 (2003).
64. Kim, Y. et al. GIGANTEA and EARLY FLOWERING 4 in Arabidopsis exhibit differential phase-specific genetic influences over a diurnal cycle. Mol. Plant. 5, 678 (2012).
65. Han, L., Mason, M., Risseeuw, E. P., Crosby, W. L. & Somers, D. E. Formation of an SCF complex is required for proper regulation of circadian timing. Plant. J. 40, 291 (2004).
66. Cha, J. Y. et al. Functional characterization of orchardgrass cytosolic Hsp70 (DgHsp70) and the negative regulation by Ca2+/AtCaM2 binding. Plant. Physiol. Biochem. 58, 29 (2012).
67. Kwon, Y. S. et al. Proteomic analyses of the interaction between the plant-growth promoting rhizobacterium Paenibacillus polymyxa E681 and Arabidopsis thaliana. Proteomics 16, 122 (2016).
68. Wang, L., Kim, J. & Somers, D. E. Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proc. Natl. Acad. Sci. USA 110, 761 (2013).