Home LiteratureArticle Details
PMID: 16914525 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1.

Molecular biology of the cell ·Vol. 17 ·No. 10 ·2006-10-00 ·Pages 4576-83

Grimaldi B, Coiro P, Filetici P, Berge E, Dobosy JR, Freitag M, Selker EU, Ballario P

Abstract

Blue light-induced transcription in Neurospora crassa is regulated by the White Collar-1 (WC-1) photoreceptor. We report that residue K14 of histone H3 associated with the light-inducible albino-3 (al-3) promoter becomes transiently acetylated after photoinduction. This acetylation depends on WC-1. The relevance of this chromatin modification was directly evaluated in vivo by construction of a Neurospora strain with a mutated histone H3 gene (hH3(K14Q)). This strain phenocopies a wc-1 blind mutant and shows a strong reduction of light-induced transcriptional activation of both al-3 and vivid (vvd), another light-inducible gene. We mutated Neurospora GCN Five (ngf-1), which encodes a homologue of the yeast HAT Gcn5p, to generate a strain impaired in H3 K14 acetylation and found that it was defective in photoinduction. Together, our findings reveal a direct link between histone modification and light signaling in Neurospora and contribute to the developing understanding of the molecular mechanisms operating in light-inducible gene activation.

MeSH Terms
Acetylation Amino Acid Sequence DNA-Binding Proteins/physiology Fungal Proteins/genetics,metabolism,physiology Genes, Reporter Histone Acetyltransferases/physiology Histones/metabolism Light Lysine Molecular Sequence Data Nerve Growth Factor/pharmacology Neurospora crassa/metabolism,physiology Photoreceptor Cells Promoter Regions, Genetic Sequence Homology, Amino Acid Transcription Factors/physiology
Chemicals
DNA-Binding Proteins Fungal Proteins Histones Transcription Factors wc-1 protein, Neurospora crassa Nerve Growth Factor Histone Acetyltransferases Lysine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Grimaldi Benedetto
Dipartimento di Genetica e Biologia Molecolare, Università di Roma La Sapienza, 00185 Rome, Italy.
Coiro Pierluca
Filetici Patrizia
Berge Emanuela
Dobosy Joseph R
Freitag Michael
Selker Eric U
Ballario Paola
References (54)
54 references, click to expand
  1. Light signal transduction in higher plants.
    Annu Rev Genet. 2004;38:87-117 PMID: 15568973
  2. Cloning and characterization of the gene for beta-tubulin from a benomyl-resistant mutant of Neurospora crassa and its use as a dominant selectable marker.
    Mol Cell Biol. 1986 Jul;6(7):2452-61 PMID: 2946938
  3. Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain.
    Science. 1997 Dec 19;278(5346):2120-3 PMID: 9405347
  4. Premeiotic instability of repeated sequences in Neurospora crassa.
    Annu Rev Genet. 1990;24:579-613 PMID: 2150906
  5. Light-independent phosphorylation of WHITE COLLAR-1 regulates its function in the Neurospora circadian negative feedback loop.
    J Biol Chem. 2005 Apr 29;280(17):17526-32 PMID: 15731099
  6. A chimeric light-regulated amino acid transport system allows the isolation of blue light regulator (blr) mutants of Neurospora crassa.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6612-6 PMID: 7604041
  7. RIP: the evolutionary cost of genome defense.
    Trends Genet. 2004 Sep;20(9):417-23 PMID: 15313550
  8. Histone acetyltransferase-dependent chromatin remodeling and the vascular clock.
    J Biol Chem. 2004 Feb 20;279(8):7091-7 PMID: 14645221
  9. Role of a white collar-1-white collar-2 complex in blue-light signal transduction.
    EMBO J. 1999 Sep 15;18(18):4961-8 PMID: 10487748
  10. The diverse functions of histone acetyltransferase complexes.
    Trends Genet. 2003 Jun;19(6):321-9 PMID: 12801725
  11. Blue light adaptation and desensitization of light signal transduction in Neurospora crassa.
    Mol Microbiol. 2001 Feb;39(4):1080-7 PMID: 11251826
  12. Photoregulation of the Carotenoid Biosynthetic Pathway in Albino and White Collar Mutants of Neurospora crassa.
    Plant Physiol. 1981 Sep;68(3):745-9 PMID: 16661992
  13. White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein.
    EMBO J. 1996 Apr 1;15(7):1650-7 PMID: 8612589
  14. Circadian regulator CLOCK is a histone acetyltransferase.
    Cell. 2006 May 5;125(3):497-508 PMID: 16678094
  15. Chromatin remodeling by nuclear receptors.
    Chromosoma. 2003 May;111(8):495-504 PMID: 12743713
  16. Transcriptional regulation of the Neurospora circadian clock gene wc-1 affects the phase of circadian output.
    EMBO Rep. 2006 Feb;7(2):199-204 PMID: 16374510
  17. Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa.
    Eukaryot Cell. 2005 Dec;4(12):2140-52 PMID: 16339731
  18. The language of covalent histone modifications.
    Nature. 2000 Jan 6;403(6765):41-5 PMID: 10638745
  19. Molecular characterization of upstream regulatory sequences controlling the photoinduced expression of the albino-3 gene of Neurospora crassa.
    Mol Microbiol. 1994 Sep;13(5):787-95 PMID: 7815938
  20. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock.
    Nature. 2003 Jan 9;421(6919):177-82 PMID: 12483227
  21. Protein kinase C modulates light responses in Neurospora by regulating the blue light photoreceptor WC-1.
    Mol Microbiol. 2005 Apr;56(2):334-45 PMID: 15813728
  22. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter.
    Science. 2002 Aug 2;297(5582):815-9 PMID: 12098706
  23. PAS domain-mediated WC-1/WC-2 interaction is essential for maintaining the steady-state level of WC-1 and the function of both proteins in circadian clock and light responses of Neurospora.
    Mol Cell Biol. 2002 Jan;22(2):517-24 PMID: 11756547
  24. Light induces chromatin modification in cells of the mammalian circadian clock.
    Nat Neurosci. 2000 Dec;3(12):1241-7 PMID: 11100144
  25. Swi/SNF-GCN5-dependent chromatin remodelling determines induced expression of GDH3, one of the paralogous genes responsible for ammonium assimilation and glutamate biosynthesis in Saccharomyces cerevisiae.
    Mol Microbiol. 2005 Jul;57(1):291-305 PMID: 15948967
  26. Molecular mechanism of light responses in Neurospora: from light-induced transcription to photoadaptation.
    Genes Dev. 2005 Dec 1;19(23):2888-99 PMID: 16287715
  27. Clock genes, oscillators, and cellular networks in the suprachiasmatic nuclei.
    J Biol Rhythms. 2004 Oct;19(5):400-13 PMID: 15534320
  28. The neurospora circadian system.
    J Biol Rhythms. 2004 Oct;19(5):414-24 PMID: 15534321
  29. The coactivator LXXLL nuclear receptor recognition motif.
    J Pept Res. 2004 Mar;63(3):207-12 PMID: 15049832
  30. White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa.
    EMBO J. 1997 Jan 2;16(1):98-109 PMID: 9009271
  31. Action Spectrum between 260 and 800 Nanometers for the Photoinduction of Carotenoid Biosynthesis in Neurospora crassa.
    Plant Physiol. 1976 Mar;57(3):440-5 PMID: 16659499
  32. Histone acetylation and an epigenetic code.
    Bioessays. 2000 Sep;22(9):836-45 PMID: 10944586
  33. GCN5-related N-acetyltransferases: a structural overview.
    Annu Rev Biophys Biomol Struct. 2000;29:81-103 PMID: 10940244
  34. Interaction between major nitrogen regulatory protein NIT2 and pathway-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa.
    Mol Cell Biol. 1998 Jul;18(7):3983-90 PMID: 9632783
  35. Histone acetyltransferases.
    Annu Rev Biochem. 2001;70:81-120 PMID: 11395403
  36. The effects of light on a circadian rhythm of conidiation in neurospora.
    Plant Physiol. 1967 Nov;42(11):1504-10 PMID: 16656687
  37. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa.
    Nature. 2001 Nov 15;414(6861):277-83 PMID: 11713521
  38. Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation.
    Mol Cell Biol. 2004 Jul;24(14):6278-87 PMID: 15226430
  39. Photoregulation of the albino-3 gene in Neurospora crassa.
    J Photochem Photobiol B. 1991 Nov;11(2):107-15 PMID: 1837560
  40. A feel for the template: zinc finger protein transcription factors and chromatin.
    Biochem Cell Biol. 2002;80(3):321-33 PMID: 12123285
  41. White collar-1, a DNA binding transcription factor and a light sensor.
    Science. 2002 Aug 2;297(5582):840-3 PMID: 12098705
  42. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  43. The Neurospora crassa carotenoid biosynthetic gene (albino 3) reveals highly conserved regions among prenyltransferases.
    J Biol Chem. 1991 Mar 25;266(9):5854-9 PMID: 1826006
  44. The fungal GATA factors.
    Curr Opin Microbiol. 2000 Apr;3(2):126-31 PMID: 10745000
  45. Photoinduction of albino-3 gene expression in Neurospora crassa conidia.
    J Photochem Photobiol B. 1992 Aug 31;15(3):233-8 PMID: 1453275
  46. Photoreception in Neurospora: a tale of two White Collar proteins.
    Cell Mol Life Sci. 2003 Oct;60(10):2131-8 PMID: 14618260
  47. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism.
    Microbiol Mol Biol Rev. 2004 Mar;68(1):1-108 PMID: 15007097
  48. Nuclear receptor recruitment of histone-modifying enzymes to target gene promoters.
    Vitam Horm. 2004;68:93-122 PMID: 15193452
  49. The genome sequence of the filamentous fungus Neurospora crassa.
    Nature. 2003 Apr 24;422(6934):859-68 PMID: 12712197
  50. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines.
    Nature. 1996 Sep 19;383(6597):269-72 PMID: 8805705
  51. Cytosine methylation associated with repeat-induced point mutation causes epigenetic gene silencing in Neurospora crassa.
    Genetics. 1997 Jun;146(2):509-23 PMID: 9178002
  52. GCN5 and ADA adaptor proteins regulate triiodothyronine/GRIP1 and SRC-1 coactivator-dependent gene activation by the human thyroid hormone receptor.
    Mol Endocrinol. 2000 May;14(5):718-32 PMID: 10809234
  53. Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription.
    EMBO J. 1992 Nov;11(11):4145-52 PMID: 1396595
  54. Signaling to chromatin through histone modifications.
    Cell. 2000 Oct 13;103(2):263-71 PMID: 11057899
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.e06-03-0232
Published
2006-10-00
Epub
2006-00-16
Pages
4576-83
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1635368
Subset
IM
Grants
NIGMS NIH HHS · R01 GM035690 · United States
NIGMS NIH HHS · R37 GM035690 · United States
NIGMS NIH HHS · GM-35690 · United States
External Links
PubMed source DOI: 10.1091/mbc.e06-03-0232 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2