Home LiteratureArticle Details
PMID: 17439825 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch.

Biochimica et biophysica acta ·Vol. 1769 ·No. 5-6 ·2007-00-00 ·Pages 383-92

Preuss S, Pikaard CS

Abstract

Ribosomal RNA (rRNA) gene transcription accounts for most of the RNA in prokaryotic and eukaryotic cells. In eukaryotes, there are hundreds (to thousands) of rRNA genes tandemly repeated head-to-tail within nucleolus organizer regions (NORs) that span millions of basepairs. These nucleolar rRNA genes are transcribed by RNA Polymerase I (Pol I) and their expression is regulated according to the physiological need for ribosomes. Regulation occurs at several levels, one of which is an epigenetic on/off switch that controls the number of active rRNA genes. Additional mechanisms then fine-tune transcription initiation and elongation rates to dictate the total amount of rRNA produced per gene. In this review, we focus on the DNA and histone modifications that comprise the epigenetic on/off switch. In both plants and animals, this system is important for controlling the dosage of active rRNA genes. The dosage control system is also responsible for the chromatin-mediated silencing of one parental set of rRNA genes in genetic hybrids, a large-scale epigenetic phenomenon known as nucleolar dominance.

MeSH Terms
Animals Cell Nucleolus/genetics Chromosomes, Plant/genetics DNA Methylation DNA, Plant/genetics,metabolism Epigenesis, Genetic Gene Dosage Gene Silencing Genes, Plant Genes, rRNA Histones/metabolism Models, Genetic Plants/genetics,metabolism RNA, Plant/genetics RNA, Ribosomal/genetics
Chemicals
DNA, Plant Histones RNA, Plant RNA, Ribosomal
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Preuss Sasha
Biology Department, Washington University, 1 Brookings Drive, St. Louis, MO 63130, USA.
Pikaard Craig S
References (81)
81 references, click to expand
  1. Imprinted X inactivation in eutherians: a model of gametic execution and zygotic relaxation.
    Curr Opin Cell Biol. 2001 Dec;13(6):690-7 PMID: 11698184
  2. LOCALIZATION OF DNA COMPLEMENTARY TO RIBOSOMAL RNA IN THE NUCLEOLUS ORGANIZER REGION OF DROSOPHILA MELANOGASTER.
    Proc Natl Acad Sci U S A. 1965 Apr;53:737-45 PMID: 14324529
  3. Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance.
    Genes Dev. 1997 Aug 15;11(16):2124-36 PMID: 9284051
  4. Cytosine methylation and nucleolar dominance in cereal hybrids.
    Mol Gen Genet. 1997 Jul;255(3):294-301 PMID: 9268020
  5. Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids.
    Plant Mol Biol. 2000 Jun;43(2-3):163-77 PMID: 10999402
  6. Development-dependent inheritance of 5-azacytidine-induced epimutations in triticale: analysis of rDNA expression patterns.
    Chromosome Res. 1997 Nov;5(7):445-50 PMID: 9421260
  7. Purification and characterization of TTFI, a factor that mediates termination of mouse ribosomal DNA transcription.
    Mol Cell Biol. 1988 Sep;8(9):3891-7 PMID: 3221867
  8. An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF.
    Mol Cell. 2001 Nov;8(5):1063-73 PMID: 11741541
  9. Competitive recruitment of CBP and Rb-HDAC regulates UBF acetylation and ribosomal transcription.
    Mol Cell. 2000 Nov;6(5):1059-66 PMID: 11106745
  10. Studies on the Ribosomal RNA Cistrons in Interspecific Drosophila Hybrids. II. Heterochromatic Regions Mediating Nucleolar Dominance.
    Genetics. 1978 May;89(1):37-64 PMID: 17248831
  11. Localization of the RNA polymerase I transcription factor hUBF during the cell cycle.
    J Cell Sci. 1993 Feb;104 ( Pt 2):327-37 PMID: 8505363
  12. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects.
    Cell. 2002 Feb 22;108(4):489-500 PMID: 11909520
  13. Regulators of nucleolar functions.
    Prog Cell Cycle Res. 2003;5:301-8 PMID: 14593725
  14. Epigenetic silencing of RNA polymerase I transcription.
    Nat Rev Mol Cell Biol. 2003 Aug;4(8):641-9 PMID: 12923526
  15. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle.
    Cell. 1989 Jun 2;57(5):753-61 PMID: 2720786
  16. Vestiges of a DNA methylation system in Drosophila melanogaster?
    Nat Genet. 1999 Dec;23(4):389-90 PMID: 10581020
  17. NoRC--a novel member of mammalian ISWI-containing chromatin remodeling machines.
    EMBO J. 2001 Sep 3;20(17):4892-900 PMID: 11532953
  18. Structure of recombinant rat UBF by electron image analysis and homology modelling.
    Nucleic Acids Res. 1996 Apr 15;24(8):1472-80 PMID: 8628680
  19. TTF-I determines the chromatin architecture of the active rDNA promoter.
    EMBO J. 1998 Jun 1;17(11):3135-45 PMID: 9606195
  20. The nucleolus.
    Annu Rev Cell Dev Biol. 1995;11:93-121 PMID: 8689574
  21. Nucleolar dominance: a model for rRNA gene silencing.
    Genes Dev. 2006 May 15;20(10):1207-14 PMID: 16702398
  22. Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats.
    Plant Cell. 2004 Apr;16(4):1021-34 PMID: 15037732
  23. RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4.
    Plant J. 1996 Feb;9(2):259-72 PMID: 8820610
  24. Mechanisms of genomic imprinting.
    Curr Opin Genet Dev. 1999 Apr;9(2):164-70 PMID: 10322141
  25. The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription.
    Nat Genet. 2002 Nov;32(3):393-6 PMID: 12368916
  26. The recruitment of RNA polymerase I on rDNA is mediated by the interaction of the A43 subunit with Rrn3.
    EMBO J. 2000 Oct 16;19(20):5473-82 PMID: 11032814
  27. A specialized form of RNA polymerase I, essential for initiation and growth-dependent regulation of rRNA synthesis, is disrupted during transcription.
    EMBO J. 1998 Jul 1;17(13):3692-703 PMID: 9649439
  28. Mechanisms of nucleolar dominance in animals and plants.
    J Cell Biol. 1985 Nov;101(5 Pt 1):2013-6 PMID: 3932369
  29. Spacer sequences regulate transcription of ribosomal gene plasmids injected into Xenopus embryos.
    Cell. 1983 Oct;34(3):989-96 PMID: 6627394
  30. Short-range DNA looping by the Xenopus HMG-box transcription factor, xUBF.
    Science. 1994 May 20;264(5162):1134-7 PMID: 8178172
  31. Ribosomal RNA gene silencing in interpopulation hybrids of Tigriopus californicus: nucleolar dominance in the absence of intergenic spacer subrepeats.
    Genetics. 2006 Jul;173(3):1479-86 PMID: 16648582
  32. Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system.
    EMBO J. 2002 Oct 15;21(20):5498-507 PMID: 12374750
  33. The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription.
    EMBO J. 2002 Sep 2;21(17):4632-40 PMID: 12198165
  34. At the center of eukaryotic life.
    Cell. 2002 May 31;109(5):545-8 PMID: 12062097
  35. rRNA gene activity and control of expression mediated by methylation and imprinting during embryo development in wheat x rye hybrids.
    Theor Appl Genet. 1995 Aug;91(3):529-33 PMID: 24169846
  36. Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads.
    Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):247-52 PMID: 9419361
  37. The dynamics of the nucleolus.
    Crit Rev Eukaryot Gene Expr. 2003;13(1):39-54 PMID: 12839096
  38. Transcription in the yeast rRNA gene locus: distribution of the active gene copies and chromatin structure of their flanking regulatory sequences.
    Mol Cell Biol. 1995 Oct;15(10):5294-303 PMID: 7565678
  39. Right-handed DNA supercoiling by an octameric form of histone-like protein HU: modulation of cellular transcription.
    J Biol Chem. 2006 Dec 29;281(52):40144-53 PMID: 17062578
  40. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF.
    Mol Cell Biol. 2003 Dec;23(23):8862-77 PMID: 14612424
  41. RNA-polymerase-I-directed rDNA transcription, life and works.
    Trends Biochem Sci. 2005 Feb;30(2):87-96 PMID: 15691654
  42. X-chromosome inactivation in mammals.
    Annu Rev Genet. 1997;31:571-610 PMID: 9442908
  43. Correlation between the size of the intergenic regulatory region, the status of cytosine methylation of rRNA genes and nucleolar expression in wheat.
    Mol Gen Genet. 1993 Jan;236(2-3):155-62 PMID: 8437559
  44. Ribosomal cistrons and the nucleolar organizer.
    Biochim Biophys Acta. 1966 Feb 21;114(2):296-310 PMID: 5943882
  45. DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat.
    J Mol Biol. 1988 Dec 5;204(3):535-48 PMID: 3225845
  46. Rrn3 phosphorylation is a regulatory checkpoint for ribosome biogenesis.
    J Biol Chem. 2002 Jul 26;277(30):27423-32 PMID: 12015311
  47. Intergenic transcripts regulate the epigenetic state of rRNA genes.
    Mol Cell. 2006 May 5;22(3):351-61 PMID: 16678107
  48. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat.
    Mol Cell Biol. 2002 Jan;22(2):657-68 PMID: 11756560
  49. RNA polymerase I transcription on nucleosomal templates: the transcription termination factor TTF-I induces chromatin remodeling and relieves transcriptional repression.
    EMBO J. 1997 Feb 17;16(4):760-8 PMID: 9049305
  50. Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids.
    Plant Mol Biol. 2004 Oct;56(3):439-63 PMID: 15604755
  51. Visualization of nucleolar genes.
    Science. 1969 May 23;164(3882):955-7 PMID: 5813982
  52. The mechanism of nucleolar dominance in Xenopus hybrids.
    Cell. 1984 Aug;38(1):38-44 PMID: 6467369
  53. The uniqueness of the imprinting mechanism.
    Curr Opin Genet Dev. 2000 Apr;10(2):229-33 PMID: 10753780
  54. Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster.
    Cell. 1976 Jun;8(2):305-19 PMID: 822943
  55. The Xenopus ribosomal gene enhancers bind an essential polymerase I transcription factor, xUBF.
    Genes Dev. 1989 Nov;3(11):1779-88 PMID: 2606347
  56. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 May 25;21(10):2331-8 PMID: 8506130
  57. Nucleolar biogenesis: the first small steps.
    Biochem Soc Trans. 2005 Dec;33(Pt 6):1441-3 PMID: 16246141
  58. Nucleoside triphosphate-dependent restriction enzymes.
    Nucleic Acids Res. 2001 Sep 15;29(18):3728-41 PMID: 11557806
  59. Evidence for nucleolus organizer regions as the units of regulation in nucleolar dominance in Arabidopsis thaliana interecotype hybrids.
    Genetics. 2004 Jun;167(2):931-9 PMID: 15238541
  60. Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3442-7 PMID: 9096413
  61. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus.
    Genes Dev. 2003 Jul 15;17(14):1691-702 PMID: 12865296
  62. Nucleosome binding by the polymerase I transactivator upstream binding factor displaces linker histone H1.
    Mol Cell Biol. 1997 Oct;17(10):5833-42 PMID: 9315641
  63. Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14891-6 PMID: 9843986
  64. Preferential transcription of Xenopus laevis ribosomal RNA in interspecies hybrids between Xenopus laevis and Xenopus mulleri.
    J Mol Biol. 1973 Oct 25;80(2):217-28 PMID: 4763983
  65. Xenopus ribosomal RNA gene intergenic spacer elements conferring transcriptional enhancement and nucleolar dominance-like competition in oocytes.
    J Biol Chem. 2002 Aug 30;277(35):31577-84 PMID: 12080048
  66. Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat.
    J Mol Biol. 1988 Dec 5;204(3):523-34 PMID: 3225844
  67. Enhancer-like properties of the 60/81 bp elements in the ribosomal gene spacer of Xenopus laevis.
    Cell. 1984 May;37(1):285-9 PMID: 6722873
  68. RNA polymerase I transcription in a Brassica interspecific hybrid and its progenitors: Tests of transcription factor involvement in nucleolar dominance.
    Genetics. 1999 May;152(1):451-60 PMID: 10224274
  69. The (epi)genetic control of mammalian X-chromosome inactivation.
    Curr Opin Genet Dev. 1997 Apr;7(2):274-80 PMID: 9115428
  70. Cooperative binding of the Xenopus RNA polymerase I transcription factor xUBF to repetitive ribosomal gene enhancers.
    Mol Cell Biol. 1992 Nov;12(11):4970-80 PMID: 1406673
  71. When rDNA transcription is arrested during mitosis, UBF is still associated with non-condensed rDNA.
    J Cell Sci. 1997 Oct;110 ( Pt 19):2429-40 PMID: 9410881
  72. An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae.
    Mol Cell Biol. 2006 May;26(9):3672-9 PMID: 16612005
  73. A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance.
    Mol Cell. 2004 Feb 27;13(4):599-609 PMID: 14992728
  74. Ribosomal gene promoter domains can function as artificial enhancers of RNA polymerase I transcription, supporting a promoter origin for natural enhancers in Xenopus.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):464-8 PMID: 8290549
  75. Molecular coevolution: DNA divergence and the maintenance of function.
    Cell. 1984 Oct;38(3):622-3 PMID: 6488313
  76. DNAase I sensitivity and methylation of active versus inactive rRNA genes in xenopus species hybrids.
    Cell. 1982 May;29(1):211-8 PMID: 6286140
  77. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance.
    Genes Dev. 2006 May 15;20(10):1283-93 PMID: 16648464
  78. Repeated genes in eukaryotes.
    Annu Rev Biochem. 1980;49:727-64 PMID: 6996571
  79. The RNA polymerase I transactivator upstream binding factor requires its dimerization domain and high-mobility-group (HMG) box 1 to bend, wrap, and positively supercoil enhancer DNA.
    Mol Cell Biol. 1994 Oct;14(10):6476-88 PMID: 7935371
  80. A role for upstream binding factor in organizing ribosomal gene chromatin.
    Biochem Soc Symp. 2006;(73):77-84 PMID: 16626289
  81. UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery.
    Genes Dev. 2005 Jan 1;19(1):50-64 PMID: 15598984
Article Info
Journal
Biochimica et biophysica acta
Abbr.
Biochim Biophys Acta
ISSN
0006-3002
DOI
10.1016/j.bbaexp.2007.02.005
Published
2007-00-00
Epub
2007-00-12
Pages
383-92
Language
English
Region
Netherlands
NLM ID
0217513
PMCID
PMC2000449
Subset
IM
Grants
NIGMS NIH HHS · F32 GM069206 · United States
NIGMS NIH HHS · R01 GM060380 · United States
NIGMS NIH HHS · R01-GM60380 · United States
NCRR NIH HHS · P41 RR000954 · United States
NIGMS NIH HHS · R01 GM060380-07 · United States
NCRR NIH HHS · P41 RR000954-296583 · United States
NIGMS NIH HHS · F32 GM69206 · United States
External Links
PubMed source DOI: 10.1016/j.bbaexp.2007.02.005 PMC Full Text
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