Emerging design principles in the Arabidopsis circadian clock

Seminars in Cell and Developmental Biology

Volumn 24, Issue 5, 2013, Pages 393-398

  Carré, Isabelle ^a   Veflingstad, Siren R ^b  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Arabidopsis; Circadian clock; Transcriptional network

Indexed keywords

CYCLIC ADENOSINE DIPHOSPHATE RIBOSE; MESSENGER RNA; TRANSCRIPTION FACTOR;

ARABIDOPSIS; CALCIUM SIGNALING; CIRCADIAN RHYTHM; DNA BINDING; FEEDBACK SYSTEM; FLOWERING; NEGATIVE FEEDBACK; NONHUMAN; OSCILLATION; PLANT GENETICS; PLANT GROWTH; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; TRANSCRIPTION REGULATION; TRANSGENIC PLANT;

ARABIDOPSIS;

EID: 84879156583     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.03.011     Document Type: Review

References (71)

1. Young M.W., Kay S.A. Time zones: a comparative genetics of circadian clocks. Nature Reviews. Genetics 2001, 2:702-715.
2. Heintzen C., Liu Y. The Neurospora crassa circadian clock. Advances in genetics 2007, 25-66. Academic Press, New York. C.H. Jeffery (Ed.).
3. Allada R., Chung B.Y. Circadian organization of behavior and physiology in Drosophila. Annual Review of Physiology 2010, 72:605-624.
4. Mohawk J.A., Green C.B., Takahashi J.S. Central and peripheral circadian clocks in mammals. Annual Review of Neuroscience 2012, 35:445-462.
5. Pokhilko A., Fernandez A.P., Edwards K.D., Southern M.M., Halliday K.J., Millar A.J. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Molecular Systems Biology 2012, 8. 574.
6. McClung C.R. The genetics of plant clocks. Advances in genetics 2011, 105-139. Academic Press, New York, [chapter 4]. B. Stuart (Ed.).
7. Nagel D., Kay S. Complexity in the wiring and regulation of plant circadian networks. Current Biology: CB 2012, 22:R648-R657.
8. Troncoso-Ponce M.A., Mas P. Newly described components and regulatory mechanisms of circadian clock function in Arabidopsis thaliana. Molecular Plant 2012, 5:545-553.
9. Schaffer R., Ramsay N., Samach A., Corden S., Putterill J., Carré I.A., et al. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 1998, 93:1219-1229.
10. Wang Z.-Y., Tobin E.M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 1998, 93:1207-1217.
11. Rawat R., Schwartz J., Jones M.A., Sairanen I., Cheng Y., Andersson C.R., et al. REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:16883-16888.
12. Matsushika A., Makino S., Kojima M., Mizuno T. Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant and Cell Physiology 2000, 41:1002-1012.
13. Strayer C., Oyama T., Schultz T.F., Raman R., Somers D.E., Mas P., et al. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 2000, 289:768-771.
14. Para A., Farre E.M., Imaizumi T., Pruneda-Paz J.L., Harmon F.G., Kay S.A. PRR3 is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock. Plant Cell 2007, 19:3462-3473.
15. Fujiwara S., Wang L., Han L., Suh S.S., Salome P.A., McClung C.R., et al. Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins. Journal of Biological Chemistry 2008, 283:23073-23083.
16. Hazen S.P., Schultz T.F., Pruneda-Paz J.L., Borevitz J.O., Ecker J.R., Kay S.A. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:10387-10392.
17. Onai K., Ishiura M. PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes to Cells 2005, 10:963-972.
18. Hicks K.A., Albertson T.M., Wagner D.R. E ARLY FLOWERING 3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis. Plant Cell 2001, 13:1281-1292.
19. Doyle M.R., Davis S.J., Bastow R.M., McWatters H.G., Kozma-Bognar L., Nagy F., et al. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 2002, 419:74-77.
20. Nusinow D.A., Helfer A., Hamilton E.E., King J.J., Imaizumi T., Schultz T.F., et al. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 2011, 475:398-402.
21. Dai S., Wei X., Pei L., Thompson R.L., Liu Y., Heard J.E., et al. BROTHER OF LUX ARRHYTHMO is a component of the Arabidopsis circadian clock. Plant Cell 2011, 23:961-972.
22. Chow B.Y., Helfer A., Nusinow D.A., Kay S.A. ELF3 recruitment to the PRR9 promoter requires other Evening Complex members in the Arabidopsis circadian clock. Plant Signaling and Behaviour 2012, 7:170-173.
23. Alabadi D., Oyama T., Yanovsky M.J., Harmon F.G., Mas P., Kay S.A. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 2001, 293:880-883.
24. Mas P., Alabadi D., Yanovsky M.J., Oyama T., Kay S.A. Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 2003, 15:223-236.
25. Makino S., Matsushika A., Kojima M., Yamashino T., Mizuno T. The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: I. characterization with APRR1-overexpressing plants. Plant and Cell Physiology 2002, 43:58-69.
26. Locke J., Southern M., Kozma-Bognár L., Hibberd V., Brown P., Turner M., et al. Extension of a genetic network model by iterative experimentation and mathematical analysis. Molecular Systems Biology 2005, 1(1). 205.0013.
27. Gendron J.M., Pruneda-Paz J.L., Doherty C.J., Gross A.M., Kang S.E., Kay S.A. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(8):3167-3172.
28. Huang W., Pérez-García P., Pokhilko A., Millar A.J., Antoshechkin I., Riechmann J.L., et al. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 2012, 336:75-79.
29. Fowler S., Lee K., Onouchi H., Samach A., Richardson K., Morris B., 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 Journal 1999, 18:4679-4688.
30. Kikis E.A., Khanna R., Quail P.H. ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant Journal 2005, 44:300-313.
31. Kolmos E., Nowak M., Werner M., Fischer K., Schwarz G., Mathews S., et al. Integrating ELF4 into the circadian system through combined structural and functional studies. HFSP Journal 2009, 3:350-366.
32. Dixon L.E., Knox K., Kozma-Bognar L., Southern M.M., Pokhilko A., Millar A.J. Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis. Current Biology: CB 2011, 21:120-125.
33. Helfer A., Nusinow D.A., Chow B.Y., Gehrke A.R., Bulyk M.L., Kay S.A. LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Current Biology 2011, 21:126-133.
34. Nakamichi N., Kita M., Ito S., Yamashino T., Mizuno T. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant and Cell Physiology 2005, 46:686-698.
35. Nakamichi N., Kiba T., Henriques R., Mizuno T., Chua N.H., Sakakibara H. PSEUDO-RESPONSE REGULATORS 9,7 and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 2010, 22:594-605.
36. Makino S., Matsushika A., Kojima M., Oda Y., Mizuno T. Light response of the circadian waves of the APRR1/TOC1 quintet: when does the quintet start singing rhythmically in Arabidopsis?. Plant and Cell Physiology 2001, 42:334-339.
37. Yamamoto Y., Sato E., Shimizu T., Nakamich N., Sato S., Kato T., et al. Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant and Cell Physiology 2003, 44:1119-1130.
38. Farré E.M., Harmer S.L., Harmon F.G., Yanovsky M.J., Kay S.A. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis clock. Current Biology 2005, 15:47-54.
39. Yamashino T., Ito S., Niwa Y., Kunihiro A., Nakamichi N., Mizuno T. Involvement of Arabidopsis clock-associated pseudo-response regulators in diurnal oscillations of gene expression in the presence of environmental time cues. Plant and Cell Physiology 2008, 49:1839-1850.
40. Herrero E., Kolmos E., Bujdoso N., Yuan Y., Wang M., Berns M.C., et al. EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 2012, 24:428-443.
41. Nakamichi N., Kiba T., Kamioka M., Suzuki T., Yamashino T., Higashiyama T., et al. Transcriptional repressor PRR5 directly regulates clock-output pathways. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:17123-17128.
42. Mizoguchi T., Wheatley K., Hanzawa Y., Wright L., Mizoguchi M., Song H.R., et al. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Developmental Cell 2002, 2:629-641.
43. Alabadi D., Yanovsky M.J., Mas P., Harmer S.L., Kay S.A. Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Current Biology: CB 2002, 12:757-761.
44. Elowitz M.B., Leibler S. A synthetic network of transcriptional oscillators. Nature 2000, 403:335-338.
45. Niwa Y., Yamashino T., Mizuno T. The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant and Cell Physiology 2009, 50:838-854.
46. Yanovsky M.J., Kay S.A. Living by the calendar: how plants know when to flower. Nature Reviews Molecular Cell Biology 2003, 4:265-275.
47. Ding Z., Millar A.J., Davis A.M., Davis S.J. TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell 2007, 19:1522-1536.
48. Pruneda-Paz J.L., Breton G., Para A., Kay S.A. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 2009, 323:1481-1485.
49. Wang Y., Wu J.-F., Nakamichi N., Sakakibara H., Nam H.-G., Wu S.-H. LIGHT-REGULATED WD1 and PSEUDO-RESPONSE REGULATOR9 form a positive feedback regulatory loop in the Arabidopsis circadian clock. Plant Cell 2011, 23:486-498.
50. Rawat R., Takahashi N., Hsu P.Y., Jones M.A., Schwartz J., Salemi M.R., et al. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock. PLoS Genetics 2011, 7:e1001350.
51. Farinas B., Mas P. Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation. Plant Journal 2011, 66:318-329.
52. Perales M., Mas P. A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 2007, 19:2111-2123.
53. Sanchez S.E., Petrillo E., Beckwith E.J., Zhang X., Rugnone M.L., Hernando C.E., et al. A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 2010, 468:112-116.
54. Wang X., Wu F., Xie Q., Wang H., Wang Y., Yue Y., et al. SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 2012, 24:3278-3295.
55. Filichkin S., Mockler T. Unproductive alternative splicing and nonsense mRNAs: a widespread phenomenon among plant circadian clock genes. Biology Direct 2012, 7:20.
56. James A.B., Syed N.H., Bordage S., Marshall J., Nimmo G.A., Jenkins G.I., et al. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 2012, 24(3):961-981.
57. Kusakina J., Dodd A.N. Phosphorylation in the plant circadian system. Trends in Plant Science 2012, 17:575-583.
58. Lu S.X., Liu H., Knowles S.M., Li J., Ma L., Tobin E.M., et al. A role for protein kinase CK2 alpha subunits in the Arabidopsis circadian clock. Plant Physiology 2011, 157(3):1537-1545.
59. Mas P., Kim W.Y., Somers D.E., Kay S.A. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 2003, 426:567-570.
60. 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 Online 2007, 19:2516-2530.
61. Harmon F., Imaizumi T., Gray W.M. CUL1 regulates TOC1 protein stability in the Arabidopsis circadian clock. Plant Journal 2008, 55:568-579.
62. Kim T.-S., Kim W.Y., Fujiwara S., Kim J., Cha J.-Y., Park J.H., et al. HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:16843-16848.
63. Ito S., Song Y.H., Imaizumi T. LOV domain-containing F-Box proteins: light-dependent protein degradation modules in Arabidopsis. Molecular Plant 2012, 5:573-582.
64. Haydon M.J., Hearn T.J., Bell L.J., Hannah M.A., Webb A.A.R. Metabolic regulation of circadian clocks. Seminars in Cell and Developmental Biology 2013, 24:414-421.
65. Dodd A.N., Gardner M.J., Hotta C.T., Hubbard K.E., Dalchau N., Love J., et al. The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 2007, 318:1789-1792.
66. Galon Y., Finkler A., Fromm H. Calcium-regulated transcription in plants. Molecular Plant 2010, 3:653-669.
67. O'Neill J.S., van Ooijen G., Le Bihan T., Millar A.J. Circadian clock parameter measurement: characterization of clock transcription factors using surface plasmon resonance. Journal of Biological Rhythms 2011, 26:91-98.
68. Edgar R.S., Green E.W., Zhao Y., van Ooijen G., Olmedo M., Qin X., et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature 2012, 485:459-464.
69. Lai A.G., Doherty C.J., Mueller-Roeber B., Kay S.A., Schippers J.H.M., Dijkwel P.P. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:17129-17134.
70. McClung C.R. Beyond Arabidopsis: the circadian clock in non-model plant species. Seminars in Cell and Developmental Biology 2013, 24:430-436.
71. Mockler T.C., Michael T.P., Priest H.D., Shen R., Sullivan C.M., Givan S.A., et al. The DIURNAL project: diurnal and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harbor Symposia on Quantitative Biology: Clocks and Rhythms 2007, 72:353-363.