Home LiteratureArticle Details
PMID: 15514020 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Centromere-encoded RNAs are integral components of the maize kinetochore.

Topp CN, Zhong CX, Dawe RK

Abstract

RNA is involved in a variety of chromatin modification events, ranging from large-scale structural rearrangements to subtle local affects. Here, we extend the evidence for RNA-chromatin interactions to the centromere core. The data indicate that maize centromeric retrotransposons (CRMs) and satellite repeats (CentC) are not only transcribed, but that nearly half of the CRM and CentC RNA is tightly bound to centromeric histone H3 (CENH3), a key inner kinetochore protein. RNAs from another tandem repeat (180-bp knob sequence) or an abundant euchromatic retroelement (Opie) are undetectable within the same anti-CENH3 immune complexes. Both sense and antisense strands of CRM and CentC, but not small interfering RNAs homologous to either repeat, were found to coimmunoprecipitate with CENH3. The bulk of the immunoprecipitated RNA ranged in size from 40 to 200 nt. These data provide evidence for a pool of protected, single-stranded centromeric RNA within the centromere/kinetochore complex.

MeSH Terms
Base Sequence Centromere/genetics,metabolism DNA, Plant/genetics Histones/metabolism Kinetochores/metabolism Plant Proteins/metabolism RNA, Plant/genetics Retroelements/genetics Zea mays/genetics,metabolism
Chemicals
DNA, Plant Histones Plant Proteins RNA, Plant Retroelements
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Topp Christopher N
Departments of Plant Biology and Genetics, University of Georgia, Athens, GA 30602, USA.
Zhong Cathy X
Dawe R Kelly
References (50)
50 references, click to expand
  1. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat.
    Nat Genet. 2003 Jan;33(1):102-6 PMID: 12483211
  2. Yeast telomerase RNA: a flexible scaffold for protein subunits.
    Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):10024-9 PMID: 15226497
  3. Centromerization.
    Trends Cell Biol. 2000 May;10(5):182-8 PMID: 10754560
  4. A procedure for Northern blot analysis of native RNA.
    Anal Biochem. 1986 Nov 15;159(1):227-32 PMID: 2433961
  5. Retrotransposons as epigenetic mediators of phenotypic variation in mammals.
    Nat Genet. 2001 Apr;27(4):361-5 PMID: 11279513
  6. RNA interference.
    Nature. 2002 Jul 11;418(6894):244-51 PMID: 12110901
  7. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi.
    Science. 2002 Sep 13;297(5588):1833-7 PMID: 12193640
  8. A molecular view of plant centromeres.
    Trends Plant Sci. 2003 Dec;8(12):570-5 PMID: 14659705
  9. Electroblotting of double-stranded DNA for hybridization experiments: DNA transfer is complete within 10 minutes after pulsed-field gel electrophoresis.
    Anal Biochem. 1990 Feb 1;184(2):207-12 PMID: 2327566
  10. Multiple RNA-protein interactions in Drosophila dosage compensation.
    Genome Biol. 2000;1(6):REVIEWS1030 PMID: 11178270
  11. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component.
    Nat Genet. 2002 Mar;30(3):329-34 PMID: 11850619
  12. Architecture of the budding yeast kinetochore reveals a conserved molecular core.
    J Cell Biol. 2003 Oct 27;163(2):215-22 PMID: 14581449
  13. Domain organization at the centromere and neocentromere.
    Dev Cell. 2001 Aug;1(2):165-77 PMID: 11702777
  14. Plant neocentromeres: fast, focused, and driven.
    Chromosome Res. 2004;12(6):655-69 PMID: 15289670
  15. The interaction of core histones with DNA: equilibrium binding studies.
    Nucleic Acids Res. 1978 Oct;5(10):3643-63 PMID: 724497
  16. Structural analysis of the maize rp1 complex reveals numerous sites and unexpected mechanisms of local rearrangement.
    Plant Cell. 2002 Dec;14(12):3213-23 PMID: 12468738
  17. Genomic and genetic definition of a functional human centromere.
    Science. 2001 Oct 5;294(5540):109-15 PMID: 11588252
  18. A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast.
    Mol Cell. 2003 Jan;11(1):175-87 PMID: 12535531
  19. Transcription within a functional human centromere.
    Mol Cell. 2003 Aug;12(2):509-16 PMID: 14536089
  20. XIST RNA associates with specific regions of the inactive X chromatin.
    J Biol Chem. 2000 Nov 24;275(47):36491-4 PMID: 11006266
  21. Epigenetic assembly of centromeric chromatin at ectopic alpha-satellite sites on human chromosomes.
    J Cell Sci. 2003 Oct 1;116(Pt 19):4021-34 PMID: 12953060
  22. Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres.
    Genetics. 2003 Feb;163(2):759-70 PMID: 12618412
  23. Ribonucleoprotein staining of centrioles and kinetochores in newt lung cell spindles.
    J Cell Biol. 1979 Jan;80(1):1-9 PMID: 84814
  24. CENP-A, -B, and -C chromatin complex that contains the I-type alpha-satellite array constitutes the prekinetochore in HeLa cells.
    Mol Cell Biol. 2002 Apr;22(7):2229-41 PMID: 11884609
  25. Heterochromatin and epigenetic control of gene expression.
    Science. 2003 Aug 8;301(5634):798-802 PMID: 12907790
  26. Highly repeated DNA sequence limited to knob heterochromatin in maize.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4490-4 PMID: 16593063
  27. Histone H3.3 is enriched in covalent modifications associated with active chromatin.
    Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1525-30 PMID: 14732680
  28. Nucleosomes unfold completely at a transcriptionally active promoter.
    Mol Cell. 2003 Jun;11(6):1587-98 PMID: 12820971
  29. Molecular structure of a functional Drosophila centromere.
    Cell. 1997 Dec 26;91(7):1007-19 PMID: 9428523
  30. Sim4: a novel fission yeast kinetochore protein required for centromeric silencing and chromosome segregation.
    J Cell Biol. 2003 Apr 28;161(2):295-307 PMID: 12719471
  31. A solid foundation: functional specialization of centromeric chromatin.
    Curr Opin Genet Dev. 2001 Apr;11(2):182-8 PMID: 11250142
  32. RNAs templating chromatin structure for dosage compensation in animals.
    Bioessays. 2003 May;25(5):434-42 PMID: 12717814
  33. The centromere paradox: stable inheritance with rapidly evolving DNA.
    Science. 2001 Aug 10;293(5532):1098-102 PMID: 11498581
  34. Conserved organization of centromeric chromatin in flies and humans.
    Dev Cell. 2002 Mar;2(3):319-30 PMID: 11879637
  35. Maize centromeres: organization and functional adaptation in the genetic background of oat.
    Plant Cell. 2004 Mar;16(3):571-81 PMID: 14973167
  36. Distinct protein interaction domains and protein spreading in a complex centromere.
    Genes Dev. 2000 Apr 1;14(7):783-91 PMID: 10766735
  37. Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A.
    J Cell Sci. 2001 Oct;114(Pt 19):3529-42 PMID: 11682612
  38. Building the centromere: from foundation proteins to 3D organization.
    Trends Cell Biol. 2004 Jul;14(7):359-68 PMID: 15246429
  39. RNA interference, transposons, and the centromere.
    Plant Cell. 2003 Feb;15(2):297-301 PMID: 12566573
  40. Nested retrotransposons in the intergenic regions of the maize genome.
    Science. 1996 Nov 1;274(5288):765-8 PMID: 8864112
  41. Chromatin assembly at kinetochores is uncoupled from DNA replication.
    J Cell Biol. 2000 Nov 27;151(5):1113-8 PMID: 11086012
  42. RNA interference is required for normal centromere function in fission yeast.
    Chromosome Res. 2003;11(2):137-46 PMID: 12733640
  43. Sequencing of a rice centromere uncovers active genes.
    Nat Genet. 2004 Feb;36(2):138-45 PMID: 14716315
  44. Micrococcal nuclease: its specificity and use for chromatin analysis.
    Int J Biochem. 1989;21(2):127-37 PMID: 2663558
  45. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis.
    Cell. 2004 Jan 9;116(1):51-61 PMID: 14718166
  46. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3.
    Plant Cell. 2002 Nov;14(11):2825-36 PMID: 12417704
  47. Distribution of retroelements in centromeres and neocentromeres of maize.
    Genetics. 2003 Oct;165(2):809-19 PMID: 14573490
  48. Dicer is essential for formation of the heterochromatin structure in vertebrate cells.
    Nat Cell Biol. 2004 Aug;6(8):784-91 PMID: 15247924
  49. RNAi-mediated targeting of heterochromatin by the RITS complex.
    Science. 2004 Jan 30;303(5658):672-6 PMID: 14704433
  50. RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast.
    Proc Natl Acad Sci U S A. 2003 Jan 7;100(1):193-8 PMID: 12509501
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2004-11-09
Epub
2004-00-28
Pages
15986-91
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC528775
Subset
IM
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