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The role of ROC75 as a daytime component of the circadian oscillator in Chlamydomonas reinhardtii


Autoři: Takuya Matsuo aff001;  Takahiro Iida aff001;  Ayumi Ohmura aff001;  Malavika Gururaj aff001;  Daisaku Kato aff001;  Risa Mutoh aff001;  Kunio Ihara aff001;  Masahiro Ishiura aff001
Působiště autorů: Center for Gene Research, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan aff001;  Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan aff002
Vyšlo v časopise: The role of ROC75 as a daytime component of the circadian oscillator in Chlamydomonas reinhardtii. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008814
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008814

Souhrn

The circadian clocks in chlorophyte algae have been studied in two model organisms, Chlamydomonas reinhardtii and Ostreococcus tauri. These studies revealed that the chlorophyte clocks include some genes that are homologous to those of the angiosperm circadian clock. However, the genetic network architectures of the chlorophyte clocks are largely unknown, especially in C. reinhardtii. In this study, using C. reinhardtii as a model, we characterized RHYTHM OF CHLOROPLAST (ROC) 75, a clock gene encoding a putative GARP DNA-binding transcription factor similar to the clock proteins LUX ARRHYTHMO (LUX, also called PHYTOCLOCK 1 [PCL1]) and BROTHER OF LUX ARRHYTHMO (BOA, also called NOX) of the angiosperm Arabidopsis thaliana. We observed that ROC75 is a day/subjective day-phase-expressed nuclear-localized protein that associates with some night-phased clock genes and represses their expression. This repression may be essential for the gating of reaccumulation of the other clock-related GARP protein, ROC15, after its light-dependent degradation. The restoration of ROC75 function in an arrhythmic roc75 mutant under constant darkness leads to the resumption of circadian oscillation from the subjective dawn, suggesting that the ROC75 restoration acts as a morning cue for the C. reinhardtii clock. Our study reveals a part of the genetic network of C. reinhardtii clock that could be considerably different from that of A. thaliana.

Klíčová slova:

Arabidopsis thaliana – Bioluminescence – Circadian oscillators – Circadian rhythms – Graphs – Chlamydomonas reinhardtii – Sequence motif analysis – Transcription factors


Zdroje

1. Spoelstra K, Wikelski M, Daan S, Loudon ASI, Hau M. Natural selection against a circadian clock gene mutation in mice. Proc Natl Acad Sci U S A. 2016;113: 686–691. doi: 10.1073/pnas.1516442113 26715747

2. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH. Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci. National Academy of Sciences; 1998;95: 8660–4. doi: 10.1073/pnas.95.15.8660 9671734

3. Young MW, Kay SA. Time zones: A comparative genetics of circadian clocks. Nat Rev Genet. 2001;2: 702–715. doi: 10.1038/35088576 11533719

4. Hsu PY, Harmer SL. Wheels within wheels: The plant circadian system. Trends in Plant Science. 2014. pp. 240–249. doi: 10.1016/j.tplants.2013.11.007 24373845

5. Nohales MA, Kay SA. Molecular mechanisms at the core of the plant circadian oscillator. Nature Structural and Molecular Biology. Nature Publishing Group; 2016. pp. 1061–1069. doi: 10.1038/nsmb.3327 27922614

6. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, et al. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science (80-). 2000;289: 768–771. doi: 10.1126/science.289.5480.768 10926537

7. Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science (80-). 2001;293: 880–883. doi: 10.1126/science.1061320 11486091

8. Wang ZY, Tobin EM. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998;93: 1207–1217. doi: 10.1016/s0092-8674(00)81464-6 9657153

9. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, et al. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998;93: 1219–1229. doi: 10.1016/s0092-8674(00)81465-8 9657154

10. Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci U S A. 2005;102: 10387–10392. doi: 10.1073/pnas.0503029102 16006522

11. Onai K, Ishiura M. PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes to Cells. 2005;10: 963–972. doi: 10.1111/j.1365-2443.2005.00892.x 16164597

12. Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA. LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol. 2011;21: 126–133. doi: 10.1016/j.cub.2010.12.021 21236673

13. Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, et al. The ELF4–ELF3–LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature. 2011;475: 398–402. doi: 10.1038/nature10182 21753751

14. Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H. PSEUDO-RESPONSE ReGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell. 2010;22: 594–605. doi: 10.1105/tpc.109.072892 20233950

15. Dai S, Wei X, Pei L, Thompson RL, Liu Y, Heard JE, et al. BROTHER OF LUX ARRHYTHMO is a component of the Arabidopsis circadian clock. Plant Cell. 2011;23: 961–972. doi: 10.1105/tpc.111.084293 21447790

16. Lewis LA, McCourt RM. Green algae and the origin of land plants. American Journal of Botany. 2004. pp. 1535–1556. doi: 10.3732/ajb.91.10.1535 21652308

17. Schulze T, Prager K, Dathe H, Kelm J, Kiessling P, Mittag M. How the green alga Chlamydomonas reinhardtii keeps time. Protoplasma. 2010;244: 3–14. doi: 10.1007/s00709-010-0113-0 20174954

18. Matsuo T, Ishiura M. New insights into the circadian clock in Chlamydomonas. International Review of Cell and Molecular Biology. 2010.

19. Matsuo T, Ishiura M. Chlamydomonas reinhardtii as a new model system for studying the molecular basis of the circadian clock. FEBS Letters. 2011. pp. 1495–1502. doi: 10.1016/j.febslet.2011.02.025 21354416

20. Noordally ZB, Millar AJ. Clocks in algae. Biochemistry. American Chemical Society; 2015;54: 171–183. doi: 10.1021/bi501089x 25379817

21. Bouget FY, Lefranc M, Thommen Q, Pfeuty B, Lozano JC, Schatt P, et al. Transcriptional versus non-transcriptional clocks: A case study in Ostreococcus. Marine Genomics. Elsevier; 2014. pp. 17–22. doi: 10.1016/j.margen.2014.01.004 24512973

22. Corellou F, Schwartz C, Motta JP, Djouani-Tahri EB, Sanchez F, Bougeta FY. Clocks in the green lineage: Comparative functional analysis of the circadian architecture of the picoeukaryote ostreococcus. Plant Cell. 2009;21: 3436–3449. doi: 10.1105/tpc.109.068825 19948792

23. Thommen Q, Pfeuty B, Morant PE, Corellou F, Bouget FY, Lefranc M. Robustness of circadian clocks to daylight fluctuations: Hints from the picoeucaryote ostreococcus tauri. PLoS Comput Biol. 2010;6: e1000990. doi: 10.1371/journal.pcbi.1000990 21085637

24. Morant PE, Thommen Q, Pfeuty B, Vandermoere C, Corellou F, Bouget FY, et al. A robust two-gene oscillator at the core of Ostreococcus tauri circadian clock. Chaos. American Institute of Physics Inc.; 2010;20: 045108. doi: 10.1063/1.3530118 21198120

25. Matsuo T, Okamoto K, Onai K, Niwa Y, Shimogawara K, Ishiura M. A systematic forward genetic analysis identified components of the Chlamydomonas circadian system. Genes Dev. 2008;22: 918–930. doi: 10.1101/gad.1650408 18334618

26. Ledger S, Strayer C, Ashton F, Kay SA, Putterill J. Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J. 2001;26: 15–22. doi: 10.1046/j.1365-313x.2001.01003.x 11359606

27. Heijde M, Zabulon G, Corellou F, Ishikawa T, Brazard J, Usman A, et al. Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes. Plant, Cell Environ. Blackwell Publishing Ltd; 2010;33: 1614–1626. doi: 10.1111/j.1365-3040.2010.02168.x 20444223

28. Djouani-Tahri EB, Christie JM, Sanchez-Ferandin S, Sanchez F, Bouget FY, Corellou F. A eukaryotic LOV-histidine kinase with circadian clock function in the picoalga Ostreococcus. Plant J. 2011;65: 578–588. doi: 10.1111/j.1365-313X.2010.04444.x 21235644

29. Iliev D, Voytsekh O, Schmidt E-M, Fiedler M, Nykytenko A, Mittag M. A heteromeric RNA-binding protein is involved in maintaining acrophase and period of the circadian clock. Plant Physiol. 2006;142: 797–806. doi: 10.1104/pp.106.085944 16920878

30. Dathe H, Prager K, Mittag M. Novel interaction of two clock-relevant RNA-binding proteins C3 and XRN1 in Chlamydomonas reinhardtii. FEBS Lett. 2012;586: 3969–73. doi: 10.1016/j.febslet.2012.09.046 23068615

31. Matsuo T, Iida T, Ishiura M. N-terminal acetyltransferase 3 gene is essential for robust circadian rhythm of bioluminescence reporter in Chlamydomonas reinhardtii. Biochem Biophys Res Commun. 2012;418: 342–346. doi: 10.1016/j.bbrc.2012.01.023 22266323

32. Müller N, Wenzel S, Zou Y, Künzel S, Sasso S, Weiß D, et al. A plant cryptochrome controls key features of the chlamydomonas circadian clock and its life cycle. Plant Physiol. American Society of Plant Biologists; 2017;174: 185–201. doi: 10.1104/pp.17.00349 28360233

33. Kottke T, Oldemeyer S, Wenzel S, Zou Y, Mittag M. Cryptochrome photoreceptors in green algae: Unexpected versatility of mechanisms and functions. Journal of Plant Physiology. Elsevier GmbH; 2017. pp. 4–14. doi: 10.1016/j.jplph.2017.05.021 28619534

34. Devlin PF, Kay SA. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell. 2000;12: 2499–2509. doi: 10.1105/tpc.12.12.2499 11148293

35. Niwa Y, Matsuo T, Onai K, Kato D, Tachikawa M, Ishiura M. Phase-resetting mechanism of the circadian clock in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 2013;110: 13666–71. doi: 10.1073/pnas.1220004110 23898163

36. Matsuo T, Onai K, Okamoto K, Minagawa J, Ishiura M. Real-time monitoring of chloroplast gene expression by a luciferase reporter: evidence for nuclear regulation of chloroplast circadian period. Mol Cell Biol. 2006;26: 863–870. doi: 10.1128/MCB.26.3.863-870.2006 16428442

37. Satbhai SB, Yamashino T, Okada R, Nomoto Y, Mizuno T, Tezuka Y, et al. Pseudo-response regulator (PRR) homologues of the moss physcomitrella patens: Insights into the evolution of the prr family in land plants. DNA Res. 2011;18: 39–52. doi: 10.1093/dnares/dsq033 21186242

38. Beel B, Prager K, Spexard M, Sasso S, Weiss D, Müller N, et al. A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell. 2012;24: 2992–3008. doi: 10.1105/tpc.112.098947 22773746

39. Kinoshita A, Niwa Y, Onai K, Yamano T, Fukuzawa H, Ishiura M, et al. CSL encodes a leucine-rich-repeat protein implicated in red/violet light signaling to the circadian clock in Chlamydomonas. Dutcher SK, editor. PLoS Genet. 2017;13: e1006645. doi: 10.1371/journal.pgen.1006645 28333924

40. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 2003;34: 733–739. doi: 10.1046/j.1365-313x.2003.01759.x 12787253

41. Beerli RR, Segal DJ, Dreier B, Barbas CF. Toward controlling gene expression at will: Specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc Natl Acad Sci U S A. 1998;95: 14628–14633. doi: 10.1073/pnas.95.25.14628 9843940

42. Simon R, Igeno MI, Coupland G. Activation of floral meristem identity genes in Arabidopsis. Nature. 1996;384: 59–62. doi: 10.1038/384059a0 8900276

43. Ducos E, Vergès V, de Bernonville TD, Blanc N, Giglioli-Guivarc’h N, Dutilleul C. Remarkable evolutionary conservation of antiobesity ADIPOSE/WDTC1 homologs in animals and plants. Genetics. 2017;207: 153–162. doi: 10.1534/genetics.116.198382 28663238

44. Groh BS, Yan F, Smith MD, Yu Y, Chen X, Xiong Y. The antiobesity factor WDTC 1 suppresses adipogenesis via the CRL 4 WDTC 1 E3 ligase. EMBO Rep. 2016;17: 638–647. doi: 10.15252/embr.201540500 27113764

45. Suh JM, Zeve D, McKay R, Seo J, Salo Z, Li R, et al. Adipose Is a Conserved Dosage-Sensitive Antiobesity Gene. Cell Metab. 2007;6: 195–207. doi: 10.1016/j.cmet.2007.08.001 17767906

46. Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ, Robbens S, et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A. National Academy of Sciences; 2006;103: 11647–11652. doi: 10.1073/pnas.0604795103 16868079

47. Monnier A, Liverani S, Bouvet R, Jesson B, Smith JQ, Mosser J, et al. Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles. BMC Genomics. BioMed Central Ltd.; 2010;11: 192. doi: 10.1186/1471-2164-11-192 20307298

48. Schmidt M, Gessner G, Luff M, Heiland I, Wagner V, Kaminski M, et al. Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements. Plant Cell. 2006;18: 1908–30. doi: 10.1105/tpc.106.041749 16798888

49. Uehara TN, Mizutani Y, Kuwata K, Hirota T, Sato A, Mizoi J, et al. Casein kinase 1 family regulates PRR5 and TOC1 in the Arabidopsis circadian clock. Proc Natl Acad Sci. 2019;116: 11528–11536. doi: 10.1073/pnas.1903357116 31097584

50. van Ooijen G, Hindle M, Martin SF, Barrios-Llerena M, Sanchez F, Bouget FY, et al. Functional Analysis of Casein Kinase 1 in a Minimal Circadian System. PLoS One. 2013;8: e70021. doi: 10.1371/journal.pone.0070021 23936135

51. Gorman DS, Levine RP. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci U S A. 1965;54: 1665–9. doi: 10.1073/pnas.54.6.1665 4379719

52. Shimogawara K, Fujiwara S, Grossman A, Usuda H. High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics. 1998;148: 1821–8. 9560396

53. Yamano T, Iguchi H, Fukuzawa H. Rapid transformation of Chlamydomonas reinhardtii without cell-wall removal. J Biosci Bioeng. 2013;115: 691–694. doi: 10.1016/j.jbiosc.2012.12.020 23333644

54. Okamoto K, Onai K, Ishiura M. RAP, an integrated program for monitoring bioluminescence and analyzing circadian rhythms in real time. Anal Biochem. 2005;340: 193–200. doi: 10.1016/j.ab.2004.11.007 15840491

55. Kuchimaru T, Iwano S, Kiyama M, Mitsumata S, Kadonosono T, Niwa H, et al. A luciferin analogue generating near-infrared bioluminescence achieves highly sensitive deep-tissue imaging. Nat Commun. 2016;7: 11856. doi: 10.1038/ncomms11856 27297211

56. Sueoka N. Mitotic replication of deoxiribonucleic acid in Chlamydomonas reinhardti. Proc Natl Acad Sci U S A. 1960;46: 83–91. doi: 10.1073/pnas.46.1.83 16590601

57. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, et al. The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions. Science. 2007;318: 245–250. doi: 10.1126/science.1143609 17932292


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