Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in

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In this study we have investigated the roles of the Neurospora transcription factors (TFs) WCC and SUB1 in light-activation of transcription. In principle TFs could exert identical functions for transcriptional activation and the extent of transcription will be determined by the sum of activity of the TFs. In this case however, we found that the activity of the main blue-light photoreceptor WCC is essential for the activation of light-inducible genes. SUB1 cooperates synergistically with the WCC to enhance expression of a subset of genes controlled directly by the light-activated WCC but cannot activate its light-inducible target genes in the absence of WCC. WCC evicts nucleosomes at its binding sites. This process is supported by SUB1 at a subset of common target genes. Light-dependent nucleosome loss generally correlates with but is not dependent on induction of transcription. Light-induced nucleosome eviction by the WCC/SUB1 could sensitize promoters for activation via endogenous and exogenous cues other than light, which may modulate the plasticity of the light-responsive transcriptome.

Vyšlo v časopise: Combinatorial Control of Light Induced Chromatin Remodeling and Gene Activation in. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005105
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005105

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Zdroje

1. Hardin PE, Panda S (2013) Circadian timekeeping and output mechanisms in animals. Curr Opin Neurobiol 23: 724–731. doi: 10.1016/j.conb.2013.02.018 23731779

2. Baker CL, Loros JJ, Dunlap JC (2012) The circadian clock of Neurospora crassa. FEMS Microbiol Rev 36: 95–110. doi: 10.1111/j.1574-6976.2011.00288.x 21707668

3. Sancar G, Brunner M (2014) Circadian clocks and energy metabolism. Cell Mol Life Sci 71: 2667–2680. doi: 10.1007/s00018-014-1574-7 24515123

4. Brown SA, Kowalska E, Dallmann R (2012) (Re)inventing the circadian feedback loop. Dev Cell 22: 477–487. doi: 10.1016/j.devcel.2012.02.007 22421040

5. Doyle S, Menaker M (2007) Circadian photoreception in vertebrates. Cold Spring Harb Symp Quant Biol 72: 499–508. doi: 10.1101/sqb.2007.72.003 18419310

6. Helfrich-Forster C (2002) The circadian system of Drosophila melanogaster and its light input pathways. Zoology (Jena) 105: 297–312. 16351879

7. Merrow M, Roenneberg T (2007) Circadian Entrainment of Neurospora crassa. Cold Spring Harb Symp Quant Biol 72: 279–285. doi: 10.1101/sqb.2007.72.032 18419284

8. Purschwitz J, Muller S, Kastner C, Fischer R (2006) Seeing the rainbow: light sensing in fungi. Curr Opin Microbiol 9: 566–571. 17067849

9. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38: 87–117. 15568973

10. Linden H, Macino G (1997) White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J 16: 98–109. 9009271

11. Talora C, Franchi L, Linden H, Ballario P, Macino G (1999) Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J 18: 4961–4968. 10487748

12. Idnurm A, Heitman J (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol 3: e95. 15760278

13. He Q, Cheng P, Yang Y, Wang L, Gardner KH, et al. (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297: 840–843. 12098705

14. Ballario P, Talora C, Galli D, Linden H, 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. 9723912

15. Froehlich AC, Liu Y, Loros JJ, Dunlap JC (2002) White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297: 815–819. 12098706

16. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM, et al. (2007) Conformational switching in the fungal light sensor Vivid. Science 316: 1054–1057. 17510367

17. Zoltowski BD, Crane BR (2008) Light activation of the LOV protein vivid generates a rapidly exchanging dimer. Biochemistry 47: 7012–7019. doi: 10.1021/bi8007017 18553928

18. Conrad KS, Manahan CC, Crane BR (2014) Photochemistry of flavoprotein light sensors. Nat Chem Biol 10: 801–809. doi: 10.1038/nchembio.1633 25229449

19. Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, et al. (2010) Transcription factors in light and circadian clock signaling networks revealed by genome-wide mapping of direct targets for Neurospora WHITE COLLAR COMPLEX. Eukaryot Cell.

20. Crosthwaite SK, Loros JJ, Dunlap JC (1995) Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81: 1003–1012. 7600569

21. Malzahn E, Ciprianidis S, Kaldi K, Schafmeier T, Brunner M (2010) Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142: 762–772. doi: 10.1016/j.cell.2010.08.010 20813262

22. He Q, Liu Y (2005) Molecular mechanism of light responses in Neurospora: from light-induced transcription to photoadaptation. Genes Dev 19: 2888–2899. 16287715

23. Heintzen C, Liu Y (2007) The Neurospora crassa circadian clock. Adv Genet 58: 25–66. 17452245

24. Brunner M, Kaldi K (2008) Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol Microbiol 68: 255–262. doi: 10.1111/j.1365-2958.2008.06148.x 18312266

25. Chen CH, Dunlap JC, Loros JJ (2010) Neurospora illuminates fungal photoreception. Fungal Genet Biol 47: 922–929. doi: 10.1016/j.fgb.2010.07.005 20637887

26. Corrochano LM (2007) Fungal photoreceptors: sensory molecules for fungal development and behaviour. Photochem Photobiol Sci 6: 725–736. 17609765

27. Cha J, Zhou M, Liu Y (2014) CATP is a critical component of the Neurospora circadian clock by regulating the nucleosome occupancy rhythm at the frequency locus. EMBO Rep 15: 1102.

28. Wang B, Kettenbach AN, Gerber SA, Loros JJ, Dunlap JC (2014) Neurospora WC-1 Recruits SWI/SNF to Remodel frequency and Initiate a Circadian Cycle. PLoS Genet 10: e1004599. doi: 10.1371/journal.pgen.1004599 25254987

29. Belden WJ, Loros JJ, Dunlap JC (2007) Execution of the circadian negative feedback loop in Neurospora requires the ATP-dependent chromatin-remodeling enzyme CLOCKSWITCH. Mol Cell 25: 587–600. 17317630

30. Chen CH, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ (2009) Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J 28: 1029–1042. doi: 10.1038/emboj.2009.54 19262566

31. Wu C, Yang F, Smith KM, Peterson M, Dekhang R, et al. (2014) Genome-wide characterization of light-regulated genes in Neurospora crassa. G3 (Bethesda) 4: 1731–1745. doi: 10.1534/g3.114.012617 25053707

32. Cesbron F, Oehler M, Ha N, Sancar G, Brunner M (2015) Transcriptional refractoriness is dependent on core promoter architecture. Nat Commun Accepted.

33. Sancar G, Sancar C, Brugger B, Ha N, Sachsenheimer T, et al. (2011) A global circadian repressor controls antiphasic expression of metabolic genes in Neurospora. Mol Cell 44: 687–697. doi: 10.1016/j.molcel.2011.10.019 22152473

34. Sancar G, Sancar C, Brunner M, Schafmeier T (2009) Activity of the circadian transcription factor White Collar Complex is modulated by phosphorylation of SP-motifs. FEBS Lett 583: 1833–1840. doi: 10.1016/j.febslet.2009.04.042 19427309

35. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208. doi: 10.1093/nar/gkp335 19458158

36. Schones DE, Cui K, Cuddapah S, Roh TY, Barski A, et al. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132: 887–898. doi: 10.1016/j.cell.2008.02.022 18329373

37. Lee W, Tillo D, Bray N, Morse RH, Davis RW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235–1244. 17873876

38. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453: 358–362. doi: 10.1038/nature06929 18408708

39. Lee K, Dunlap JC, Loros JJ (2003) Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 163: 103–114. 12586700

40. Barth TK, Imhof A (2010) Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem Sci 35: 618–626. doi: 10.1016/j.tibs.2010.05.006 20685123

41. Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128: 707–719. 17320508

42. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154: 490–503. doi: 10.1016/j.cell.2013.07.011 23911317

43. Magnani L, Eeckhoute J, Lupien M (2011) Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends Genet 27: 465–474. doi: 10.1016/j.tig.2011.07.002 21885149

44. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447: 407–412. 17522673

45. Becker PB, Workman JL (2013) Nucleosome remodeling and epigenetics. Cold Spring Harb Perspect Biol 5.

46. Menet JS, Pescatore S, Rosbash M (2014) CLOCK:BMAL1 is a pioneer-like transcription factor. Genes Dev 28: 8–13. doi: 10.1101/gad.228536.113 24395244

47. Grimaldi B, Coiro P, Filetici P, Berge E, Dobosy JR, et al. (2006) The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol Biol Cell 17: 4576–4583. 16914525

48. Froehlich AC, Loros JJ, Dunlap JC (2003) Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc Natl Acad Sci U S A 100: 5914–5919. 12714686

49. Cesbron F, Brunner M, Diernfellner AC (2013) Light-dependent and circadian transcription dynamics in vivo recorded with a destabilized luciferase reporter in Neurospora. PLoS One 8: e83660. doi: 10.1371/journal.pone.0083660 24391804

50. Schafmeier T, Diernfellner A, Schafer A, Dintsis O, Neiss A, et al. (2008) Circadian activity and abundance rhythms of the Neurospora clock transcription factor WCC associated with rapid nucleo-cytoplasmic shuttling. Genes Dev 22: 3397–3402. doi: 10.1101/gad.507408 19141472

51. Cheng P, Yang Y, Wang L, He Q, Liu Y (2003) WHITE COLLAR-1, a multifunctional neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2. J Biol Chem 278: 3801–3808. 12454012

52. Neiss A, Schafmeier T, Brunner M (2008) Transcriptional regulation and function of the Neurospora clock gene white collar 2 and its isoforms. EMBO Rep 9: 788–794. doi: 10.1038/embor.2008.113 18583987

53. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103: 10352–10357. 16801547

54. Schafmeier T, Kaldi K, Diernfellner A, Mohr C, Brunner M (2006) Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator. Genes Dev 20: 297–306. 16421276

55. Gorl M, Merrow M, Huttner B, Johnson J, Roenneberg T, et al. (2001) A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa. EMBO J 20: 7074–7084. 11742984

56. Gonzalez R, Scazzocchio C (1997) A rapid method for chromatin structure analysis in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 25: 3955–3956. 9380523

57. Lantermann A, Stralfors A, Fagerstrom-Billai F, Korber P, Ekwall K (2009) Genome-wide mapping of nucleosome positions in Schizosaccharomyces pombe. Methods 48: 218–225. doi: 10.1016/j.ymeth.2009.02.004 19233281

58. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174

59. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106. doi: 10.1186/gb-2010-11-10-r106 20979621

60. Robinson MD, Smyth GK (2008) Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics 9: 321–332. 17728317

61. Thorvaldsdottir H, Robinson JT, Mesirov JP (2012) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14: 178–192. doi: 10.1093/bib/bbs017 22517427