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PMID: 18263775 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression.

The Plant cell ·Vol. 20 ·No. 2 ·2008-02-00 ·Pages 259-76

Li X, Wang X, He K, Ma Y, Su N, He H, Stolc V, Tongprasit W, Jin W, Jiang J, Terzaghi W, Li S, Deng XW

Abstract

We present high-resolution maps of DNA methylation and H3K4 di- and trimethylation of two entire chromosomes and two fully sequenced centromeres in rice (Oryza sativa) shoots and cultured cells. This analysis reveals combinatorial interactions between these epigenetic modifications and chromatin structure and gene expression. Cytologically densely stained heterochromatin had less H3K4me2 and H3K4me3 and more methylated DNA than the less densely stained euchromatin, whereas centromeres had a unique epigenetic composition. Most transposable elements had highly methylated DNA but no H3K4 methylation, whereas more than half of protein-coding genes had both methylated DNA and di- and/or trimethylated H3K4. Methylation of DNA but not H3K4 was correlated with suppressed transcription. By contrast, when both DNA and H3K4 were methylated, transcription was only slightly reduced. Transcriptional activity was positively correlated with the ratio of H3K4me3/H3K4me2: genes with predominantly H3K4me3 were actively transcribed, whereas genes with predominantly H3K4me2 were transcribed at moderate levels. More protein-coding genes contained all three modifications, and more transposons contained DNA methylation in shoots than cultured cells. Differential epigenetic modifications correlated to tissue-specific expression between shoots and cultured cells. Collectively, this study provides insights into the rice epigenomes and their effect on gene expression and plant development.

MeSH Terms
Chromatin Immunoprecipitation DNA Methylation Epigenesis, Genetic/genetics Euchromatin/genetics,metabolism Gene Expression Regulation, Plant/genetics Genome, Plant Histones/metabolism Methylation Oryza/genetics,metabolism Polymerase Chain Reaction Reverse Transcriptase Polymerase Chain Reaction Transcription, Genetic
Chemicals
Euchromatin Histones
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Li Xueyong
National Institute of Biological Sciences, Beijing 102206, China.
Wang Xiangfeng
He Kun
Ma Yeqin
Su Ning
He Hang
Stolc Viktor
Tongprasit Waraporn
Jin Weiwei
Jiang Jiming
Terzaghi William
Li Songgang
Deng Xing Wang
References (53)
53 references, click to expand
  1. Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice.
    Plant J. 2006 Jan;45(1):123-32 PMID: 16367959
  2. Histone H3 Lys 4 methylation: caught in a bind?
    Genes Dev. 2006 Oct 15;20(20):2779-86 PMID: 17043307
  3. Structural features of the rice chromosome 4 centromere.
    Nucleic Acids Res. 2004 Apr 02;32(6):2023-30 PMID: 15064362
  4. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA.
    EMBO J. 2002 Dec 16;21(24):6832-41 PMID: 12486004
  5. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase.
    Nature. 2002 Apr 4;416(6880):556-60 PMID: 11898023
  6. It takes a PHD to read the histone code.
    Cell. 2006 Jul 14;126(1):22-4 PMID: 16839870
  7. Rice as a model for centromere and heterochromatin research.
    Chromosome Res. 2007;15(1):77-84 PMID: 17295128
  8. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription.
    Nat Genet. 2007 Jan;39(1):61-9 PMID: 17128275
  9. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis.
    Cell. 2006 Sep 22;126(6):1189-201 PMID: 16949657
  10. Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome.
    Plant Cell. 2003 Aug;15(8):1771-80 PMID: 12897251
  11. Methylation of histone H3 Lys 4 in coding regions of active genes.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8695-700 PMID: 12060701
  12. The role of chromatin during transcription.
    Cell. 2007 Feb 23;128(4):707-19 PMID: 17320508
  13. A tiling microarray expression analysis of rice chromosome 4 suggests a chromosome-level regulation of transcription.
    Plant Cell. 2005 Jun;17(6):1641-57 PMID: 15863518
  14. Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells.
    Nat Struct Mol Biol. 2004 Nov;11(11):1068-75 PMID: 15467727
  15. DNA methylation and epigenetic inheritance in plants and filamentous fungi.
    Science. 2001 Aug 10;293(5532):1070-4 PMID: 11498574
  16. A pilot study of transcription unit analysis in rice using oligonucleotide tiling-path microarray.
    Plant Mol Biol. 2005 Sep;59(1):137-49 PMID: 16217608
  17. Genes and transposons are differentially methylated in plants, but not in mammals.
    Genome Res. 2003 Dec;13(12):2658-64 PMID: 14656970
  18. The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference.
    Genetics. 2007 Jun;176(2):749-61 PMID: 17409063
  19. DNA methylation and epigenetics.
    Annu Rev Plant Biol. 2004;55:41-68 PMID: 15725056
  20. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa.
    Nature. 2001 Nov 15;414(6861):277-83 PMID: 11713521
  21. Biology of chromatin dynamics.
    Annu Rev Plant Biol. 2005;56:327-51 PMID: 15862099
  22. Toward a cytological characterization of the rice genome.
    Genome Res. 2001 Dec;11(12):2133-41 PMID: 11731505
  23. Role of transposable elements in heterochromatin and epigenetic control.
    Nature. 2004 Jul 22;430(6998):471-6 PMID: 15269773
  24. A genome-wide transcriptional activity survey of rice transposable element-related genes.
    Genome Biol. 2007;8(2):R28 PMID: 17326825
  25. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  26. Genome-wide transcription analyses in rice using tiling microarrays.
    Nat Genet. 2006 Jan;38(1):124-9 PMID: 16369532
  27. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99 Suppl 4:16491-8 PMID: 12151602
  28. Distinct reorganization of the genome transcription associates with organogenesis of somatic embryo, shoots, and roots in rice.
    Plant Mol Biol. 2007 Feb;63(3):337-49 PMID: 17072560
  29. Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere.
    Plant Cell. 2006 Sep;18(9):2123-33 PMID: 16877494
  30. DNA methylation dictates histone H3K4 methylation.
    Mol Cell Biol. 2007 Apr;27(7):2746-57 PMID: 17242185
  31. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome.
    Nat Genet. 2007 Mar;39(3):311-8 PMID: 17277777
  32. Gene silencing and DNA methylation processes.
    Curr Opin Plant Biol. 2001 Apr;4(2):123-9 PMID: 11228434
  33. Core histone N-termini play an essential role in mitotic chromosome condensation.
    EMBO J. 2000 Feb 1;19(3):379-91 PMID: 10654937
  34. DNA methylation inhibits elongation but not initiation of transcription in Neurospora crassa.
    Genes Dev. 1997 Sep 15;11(18):2383-95 PMID: 9308966
  35. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II.
    Cell. 2006 May 19;125(4):703-17 PMID: 16713563
  36. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin.
    Nat Struct Mol Biol. 2004 Nov;11(11):1076-83 PMID: 15475964
  37. Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting.
    Plant Cell. 2006 Jun;18(6):1360-72 PMID: 16648367
  38. Rice genome organization: the centromere and genome interactions.
    Ann Bot. 2002 Oct;90(4):427-35 PMID: 12324265
  39. Sequencing of a rice centromere uncovers active genes.
    Nat Genet. 2004 Feb;36(2):138-45 PMID: 14716315
  40. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes.
    Nat Cell Biol. 2004 Jan;6(1):73-7 PMID: 14661024
  41. Methylation of coding region alone inhibits gene expression in plant protoplasts.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8334-9 PMID: 8710871
  42. DNA methylation and plant development.
    Trends Genet. 1997 Aug;13(8):319-23 PMID: 9260518
  43. Genomic maps and comparative analysis of histone modifications in human and mouse.
    Cell. 2005 Jan 28;120(2):169-81 PMID: 15680324
  44. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene.
    Mol Cell. 2000 Oct;6(4):791-802 PMID: 11090618
  45. A microarray analysis of the rice transcriptome and its comparison to Arabidopsis.
    Genome Res. 2005 Sep;15(9):1274-83 PMID: 16140994
  46. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa.
    Nat Genet. 2003 May;34(1):75-9 PMID: 12679815
  47. Active genes are tri-methylated at K4 of histone H3.
    Nature. 2002 Sep 26;419(6905):407-11 PMID: 12353038
  48. Global identification and characterization of transcriptionally active regions in the rice genome.
    PLoS One. 2007 Mar 14;2(3):e294 PMID: 17372628
  49. Position-effect variegation and the genetic dissection of chromatin regulation in Drosophila.
    Semin Cell Dev Biol. 2003 Feb;14(1):67-75 PMID: 12524009
  50. RNA silencing genes control de novo DNA methylation.
    Science. 2004 Feb 27;303(5662):1336 PMID: 14988555
  51. The diverse functions of histone lysine methylation.
    Nat Rev Mol Cell Biol. 2005 Nov;6(11):838-49 PMID: 16261189
  52. DNA methylation as a mechanism of transcriptional regulation in nonphotosynthetic plastids in plant cells.
    Proc Natl Acad Sci U S A. 1988 Jul;85(13):4750-4 PMID: 3387435
  53. The map-based sequence of the rice genome.
    Nature. 2005 Aug 11;436(7052):793-800 PMID: 16100779
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2008-02-00
Epub
2008-00-08
Pages
259-76
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2276441
Subset
IM
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