Home LiteratureArticle Details
PMID: 21177966 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

High nucleosome occupancy is encoded at X-linked gene promoters in C. elegans.

Genome research ·Vol. 21 ·No. 2 ·2011-02-00 ·Pages 237-44

Ercan S, Lubling Y, Segal E, Lieb JD

Abstract

We mapped nucleosome occupancy by paired-end Illumina sequencing in C. elegans embryonic cells, adult somatic cells, and a mix of adult somatic and germ cells. In all three samples, the nucleosome occupancy of gene promoters on the X chromosome differed from autosomal promoters. While both X and autosomal promoters exhibit a typical nucleosome-depleted region upstream of transcript start sites and a well-positioned +1 nucleosome, X-linked gene promoters on average exhibit higher nucleosome occupancy relative to autosomal promoters. We show that the difference between X and autosomes does not depend on the somatic dosage compensation machinery. Instead, the chromatin difference at promoters is partly encoded by DNA sequence, because a model trained on nucleosome sequence preferences from S. cerevisiae in vitro data recapitulate nearly completely the experimentally observed difference between X and autosomal promoters. The model predictions also correlate very well with experimentally determined occupancy values genome-wide. The nucleosome occupancy differences observed on X promoters may bear on mechanisms of X chromosome dosage compensation in the soma, and chromosome-wide repression of X in the germline.

MeSH Terms
Animals Base Composition/genetics Caenorhabditis elegans/genetics Dosage Compensation, Genetic/genetics Genes, X-Linked Male Models, Genetic Molecular Sequence Data Nucleosomes/metabolism Operon/genetics Promoter Regions, Genetic
Chemicals
Nucleosomes
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ercan Sevinç
Department of Biology, Carolina Center for the Genome Sciences, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA. ercan@email.unc.edu
Lubling Yaniv
Segal Eran
Lieb Jason D
References (61)
61 references, click to expand
  1. Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization.
    Nat Genet. 2009 Apr;41(4):438-45 PMID: 19252487
  2. Trans-splicing and polycistronic transcription in Caenorhabditis elegans.
    Trends Genet. 1995 Apr;11(4):132-6 PMID: 7732590
  3. SDC-3 coordinates the assembly of a dosage compensation complex on the nematode X chromosome.
    Development. 1997 Mar;124(5):1019-31 PMID: 9056777
  4. Micrococcal nuclease as a probe of DNA sequence organization and chromatin structure.
    Cell. 1981 Nov;27(1 Pt 2):57-64 PMID: 6799212
  5. Single-molecule imaging of DNA curtains reveals intrinsic energy landscapes for nucleosome deposition.
    Nat Struct Mol Biol. 2009 Oct;16(10):1056-62 PMID: 19734899
  6. Genome-scale identification of nucleosome positions in S. cerevisiae.
    Science. 2005 Jul 22;309(5734):626-30 PMID: 15961632
  7. Unique features of the apoptotic endonuclease DFF40/CAD relative to micrococcal nuclease as a structural probe for chromatin.
    Biochem Cell Biol. 2006 Aug;84(4):405-10 PMID: 16936813
  8. Nucleosome landscape and control of transcription in the human malaria parasite.
    Genome Res. 2010 Feb;20(2):228-38 PMID: 20054063
  9. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo.
    Nat Struct Mol Biol. 2009 Aug;16(8):847-52 PMID: 19620965
  10. Two strategies for gene regulation by promoter nucleosomes.
    Genome Res. 2008 Jul;18(7):1084-91 PMID: 18448704
  11. A yeast hybrid provides insight into the evolution of gene expression regulation.
    Science. 2009 May 1;324(5927):659-62 PMID: 19407207
  12. Nucleosome positioning signals in genomic DNA.
    Genome Res. 2007 Aug;17(8):1170-7 PMID: 17620451
  13. The histone H3K36 methyltransferase MES-4 acts epigenetically to transmit the memory of germline gene expression to progeny.
    PLoS Genet. 2010 Sep 02;6(9):e1001091 PMID: 20824077
  14. G+C content dominates intrinsic nucleosome occupancy.
    BMC Bioinformatics. 2009 Dec 22;10:442 PMID: 20028554
  15. Whole-genome sequencing and variant discovery in C. elegans.
    Nat Methods. 2008 Feb;5(2):183-8 PMID: 18204455
  16. Genome-wide maps of mononucleosomes and dinucleosomes containing hyperacetylated histones of Aspergillus fumigatus.
    PLoS One. 2010 Mar 26;5(3):e9916 PMID: 20361043
  17. Germline expression influences operon organization in the Caenorhabditis elegans genome.
    Genetics. 2009 Apr;181(4):1219-28 PMID: 19204375
  18. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome.
    Nature. 2007 Mar 29;446(7135):572-6 PMID: 17392789
  19. Sequence-dependent nucleosome positioning.
    J Mol Biol. 2009 Mar 13;386(5):1411-22 PMID: 19070622
  20. The structure of DNA in a nucleosome.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405-9 PMID: 2170977
  21. A global analysis of Caenorhabditis elegans operons.
    Nature. 2002 Jun 20;417(6891):851-4 PMID: 12075352
  22. Analysis of chromatin structure and DNA sequence organization: use of the 1,10-phenanthroline-cuprous complex.
    Nucleic Acids Res. 1982 Oct 11;10(19):5835-52 PMID: 6292854
  23. Three distinct condensin complexes control C. elegans chromosome dynamics.
    Curr Biol. 2009 Jan 13;19(1):9-19 PMID: 19119011
  24. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning.
    Genome Res. 2008 Jul;18(7):1051-63 PMID: 18477713
  25. The role of nucleosome positioning in the evolution of gene regulation.
    PLoS Biol. 2010 Jul 06;8(7):e1000414 PMID: 20625544
  26. A native chromatin purification system for epigenomic profiling in Caenorhabditis elegans.
    Nucleic Acids Res. 2010 Mar;38(4):e26 PMID: 19966274
  27. A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome.
    Genes Dev. 2009 Mar 1;23(5):602-18 PMID: 19270160
  28. C. elegans dosage compensation: a window into mechanisms of domain-scale gene regulation.
    Chromosome Res. 2009;17(2):215-27 PMID: 19308702
  29. MES-4: an autosome-associated histone methyltransferase that participates in silencing the X chromosomes in the C. elegans germ line.
    Development. 2006 Oct;133(19):3907-17 PMID: 16968818
  30. A trans-spliced leader sequence on actin mRNA in C. elegans.
    Cell. 1987 Jun 19;49(6):753-61 PMID: 3581169
  31. Broad chromosomal domains of histone modification patterns in C. elegans.
    Genome Res. 2011 Feb;21(2):227-36 PMID: 21177964
  32. Divergence of nucleosome positioning between two closely related yeast species: genetic basis and functional consequences.
    Mol Syst Biol. 2010 May 11;6:365 PMID: 20461072
  33. A high-resolution atlas of nucleosome occupancy in yeast.
    Nat Genet. 2007 Oct;39(10):1235-44 PMID: 17873876
  34. The C. elegans dosage compensation complex propagates dynamically and independently of X chromosome sequence.
    Curr Biol. 2009 Nov 17;19(21):1777-87 PMID: 19853451
  35. PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls.
    Nat Biotechnol. 2009 Jan;27(1):66-75 PMID: 19122651
  36. Nucleosome positioning, nucleosome spacing and the nucleosome code.
    J Biomol Struct Dyn. 2010 Jun;27(6):781-93 PMID: 20232933
  37. Mapping nucleosome position at single base-pair resolution by using site-directed hydroxyl radicals.
    Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1370-5 PMID: 8643638
  38. Role of DNA sequence in nucleosome stability and dynamics.
    Q Rev Biophys. 2001 Aug;34(3):269-324 PMID: 11838235
  39. Chromatin organization marks exon-intron structure.
    Nat Struct Mol Biol. 2009 Sep;16(9):990-5 PMID: 19684600
  40. SL trans-splicing: easy come or easy go?
    Trends Genet. 2005 Apr;21(4):240-7 PMID: 15797620
  41. Dynamic regulation of nucleosome positioning in the human genome.
    Cell. 2008 Mar 7;132(5):887-98 PMID: 18329373
  42. Analogous cleavage of DNA by micrococcal nuclease and a 1-10-phenanthroline-cuprous complex.
    Nucleic Acids Res. 1982 Oct 11;10(19):5823-34 PMID: 6216458
  43. Dosage compensation: the beginning and end of generalization.
    Nat Rev Genet. 2007 Jan;8(1):47-57 PMID: 17173057
  44. Structure of the nucleosome core particle at 7 A resolution.
    Nature. 1984 Oct 11-17;311(5986):532-7 PMID: 6482966
  45. Meiotic silencing and the epigenetics of sex.
    Chromosome Res. 2007;15(5):633-51 PMID: 17674151
  46. Variable center to center distance of nucleosomes in chromatin.
    J Mol Biol. 1982 Jan 25;154(3):515-23 PMID: 7077669
  47. The structure of DNA in the nucleosome core.
    Nature. 2003 May 8;423(6936):145-50 PMID: 12736678
  48. Nucleosome positions predicted through comparative genomics.
    Nat Genet. 2006 Oct;38(10):1210-5 PMID: 16964265
  49. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals.
    PLoS Comput Biol. 2008 Nov;4(11):e1000216 PMID: 18989395
  50. X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation.
    Nat Genet. 2007 Mar;39(3):403-8 PMID: 17293863
  51. Caenorhabditis elegans compensates for the difference in X chromosome dosage between the sexes by regulating transcript levels.
    Cell. 1986 Dec 26;47(6):871-81 PMID: 3779843
  52. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project.
    Science. 2010 Dec 24;330(6012):1775-87 PMID: 21177976
  53. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  54. The DNA-encoded nucleosome organization of a eukaryotic genome.
    Nature. 2009 Mar 19;458(7236):362-6 PMID: 19092803
  55. Cleavage of chromatin with methidiumpropyl-EDTA . iron(II).
    Proc Natl Acad Sci U S A. 1983 Jun;80(11):3213-7 PMID: 6407008
  56. X-chromosome silencing in the germline of C. elegans.
    Development. 2002 Jan;129(2):479-92 PMID: 11807039
  57. DNase II digestion of the nucleosome core: precise locations and relative exposures of sites.
    Nucleic Acids Res. 1981 Sep 11;9(17):4251-65 PMID: 6272201
  58. Nucleosome displacement in transcription.
    Genes Dev. 2006 Aug 1;20(15):2009-17 PMID: 16882978
  59. Precise location of DNase I cutting sites in the nucleosome core determined by high resolution gel electrophoresis.
    Nucleic Acids Res. 1979 Jan;6(1):41-56 PMID: 424299
  60. Nucleosome organization in the Drosophila genome.
    Nature. 2008 May 15;453(7193):358-62 PMID: 18408708
  61. High nucleosome occupancy is encoded at human regulatory sequences.
    PLoS One. 2010 Feb 09;5(2):e9129 PMID: 20161746
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1549-5469
Published
2011-02-00
Epub
2010-00-22
Pages
237-44
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC3032927
Subset
IM
Grants
NHGRI NIH HHS · U01 HG0044270 · United States
Databases
GEO
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