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Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression

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Abstract

Lysine residue 9 of histone H3 can either be acetylated or mono-, di-, or tri-methylated. These epigenetic states have a diverse impact on regulating gene transcriptional activity and chromatin organization. H3K9ac is invariably correlated with transcriptional activation, whereas H3K9me2 has been reported to be mainly located in constitutive heterochromatin in Arabidopsis. Here, we present epigenetic landscapes for histone H3 lysine 9 acetylation (H3K9ac) and dimethylation (H3K9me2) in Arabidopsis seedlings. The results show that H3K9ac targeted 5,206 non-transposable element (non-TE) genes and 321 transposable elements (TEs), whereas H3K9me2 targeted 2,281 TEs and 1,112 non-TE genes. H3K9ac was biased towards the 5′ end of genes and peaked at the ATG position, while H3K9me2 tended to span the entire gene body. H3K9ac correlated with high gene expression, while H3K9me2 correlated with low expression. Analyses of H3K9ac and H3K9me2 with the available datasets of H3K27me3 and DNA methylation revealed a correlation between the occurrence of multiple epigenetic modifications and gene expression. Genes with H3K9ac alone were actively transcribed, while genes that were also modified by either H3K27me3 or DNA methylation showed a lower expression level, suggesting that a combination of repressive marks weakened the positive regulatory effect of H3K9ac. Furthermore, we observed a significant increase of the H3K9ac modification level of selected target genes in hda19 (histone deacetylase 19) mutant seedlings, which indicated that HDA19 plays an important role in regulating the level of H3K9ac and thereby influencing the transcriptional activity in young seedlings.

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References

  • Agalioti T, Chen G, Thanos D (2002) Deciphering the transcriptional histone acetylation code for a human gene. Cell 111:381–392

    Article  CAS  PubMed  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Ausín I, Alonso-Blanco C, Jarillo JA, Ruiz-García L, Martínez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36:162–166

    Article  PubMed  Google Scholar 

  • Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z et al (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  CAS  PubMed  Google Scholar 

  • Benhamed M, Bertrand C, Servet C, Zhou DX (2006) Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18:2893–2903

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 57:289–300

    Google Scholar 

  • Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE (2008) Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3:e3156

    Article  PubMed  Google Scholar 

  • Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS et al (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci USA 99:8695–8700

    Article  CAS  PubMed  Google Scholar 

  • Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ et al (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169–181

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M et al (2004) Chromatin techniques for plant cells. Plant J 39:776–789

    Article  CAS  PubMed  Google Scholar 

  • Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M et al (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38:1378–1385

    Article  CAS  PubMed  Google Scholar 

  • Feng S, Shen Y, Sullivan JA, Rubio V, Xiong Y, Sun TP et al (2004) Arabidopsis CAND1, an unmodified CUL1-interacting protein, is involved in multiple developmental pathways controlled by ubiquitin/proteasome-mediated protein degradation. Plant Cell 16:1870–1882

    Article  CAS  PubMed  Google Scholar 

  • Frank SR, Schroeder M, Fernandez P, Taubert S, Amati B (2001) Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev 15:2069–2082

    Article  CAS  PubMed  Google Scholar 

  • Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns–from conservation to diversity. Trends Plant Sci 11:199–208

    Article  CAS  PubMed  Google Scholar 

  • Gartler SM, Varadarajan KR, Luo P, Canfield TK, Traynor J, Francke U et al (2004) Normal histone modifications on the inactive X chromosome in ICF and Rett syndrome cells: implications for methyl-CpG binding proteins. BMC Biol 2:21

    Article  PubMed  Google Scholar 

  • Hollander M, Wolfe DA (1999) Nonparametric statistical methods. Wiley, New York, pp 228–235

    Google Scholar 

  • Houben A, Demidov D, Gernand D, Meister A, Leach CR, Schubert I (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J 33:967–973

    Article  CAS  PubMed  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Ma L, Strickland E, Deng XW (2005) Conservation and divergence of ight-Regulated genome Expression Patterns during Seedling Development in Rice and Arabidopsis. Plant Cell 17:3239–3256

    Article  CAS  PubMed  Google Scholar 

  • Johnson L, Cao X, Jacobsen S (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12:1360–1367

    Article  CAS  PubMed  Google Scholar 

  • Kondo Y, Shen L, Yan PS, Huang TH, Issa JP (2004) Chromatin immunoprecipitation microarrays for identification of genes silenced by histone H3 lysine 9 methylation. Proc Natl Acad Sci USA 101:7398–7403

    Article  CAS  PubMed  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  CAS  PubMed  Google Scholar 

  • Kuo MH, Zhou J, Jambeck P, Churchill ME, Allis CD (1998) Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo. Genes Dev 12:627–639

    Article  CAS  PubMed  Google Scholar 

  • Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global histone acetylation patterns to gene expression. Cell 117:721–733

    Article  CAS  PubMed  Google Scholar 

  • Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y et al (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749

    Article  CAS  PubMed  Google Scholar 

  • Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    Article  CAS  PubMed  Google Scholar 

  • Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, Friedman N et al (2005) Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3:e328

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Millar CB, Grunstein M (2006) Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol 7:657–666

    Article  CAS  PubMed  Google Scholar 

  • Ng DW, Chandrasekharan MB, Hall TC (2006) Ordered histone modifications are associated with transcriptional poising and activation of the phaseolin promoter. Plant Cell 18:119–132

    Article  CAS  PubMed  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652

    Article  CAS  PubMed  Google Scholar 

  • Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI et al (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517–527

    Article  CAS  PubMed  Google Scholar 

  • Rao B, Shibata Y, Strahl BD, Lieb JD (2005) Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide. Mol Cell Biol 25:9447–9459

    Article  CAS  PubMed  Google Scholar 

  • Ren XY, Vorst O, Fiers MW, Stiekema WJ, Nap JP (2006) In plants, highly expressed genes are the least compact. Trends Genet 22:528–532

    Article  CAS  PubMed  Google Scholar 

  • Roh TY, Ngau WC, Cui K, Landsman D, Zhao K (2004) High-resolution genome-wide mapping of histone modifications. Nat Biotechnol 22:1013–1016

    Article  CAS  PubMed  Google Scholar 

  • Roh TY, Cuddapah S, Zhao K (2005) Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19:542–552

    Article  CAS  PubMed  Google Scholar 

  • Roh TY, Cuddapah S, Cui K, Zhao K (2006) The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci USA 103:15782–15787

    Article  CAS  PubMed  Google Scholar 

  • Schübeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F et al (2004) The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18:1263–1271

    Article  PubMed  Google Scholar 

  • Sims RJ III, Nishioka K, Reinberg D (2003) Histone lysine methylation: a signature for chromatin function. Trends Genet 19:629–639

    Article  CAS  PubMed  Google Scholar 

  • Sinha I, Wirén M, Ekwall K (2006) Genome-wide patterns of histone modifications in fission yeast. Chromosome Res 14:95–105

    Article  CAS  PubMed  Google Scholar 

  • Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21:2067–2075

    Article  CAS  PubMed  Google Scholar 

  • Stolc V, Samanta MP, Tongprasit W, Sethi H, Liang S, Nelson DC et al (2005) Identification of transcribed sequences in Arabidopsis thaliana by using high-resolution genome tiling arrays. Proc Natl Acad Sci USA 102:4453–4458

    Article  CAS  PubMed  Google Scholar 

  • Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100:8823–8827

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Chen ZJ (2001) Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc Natl Acad Sci USA 98:200–205

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Wang J, Fong MP, Chen M, Cao H, Gelvin SB et al (2003) Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (HD1) expression. Genetics 165:399–409

    CAS  PubMed  Google Scholar 

  • Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N et al (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:e86

    Article  PubMed  Google Scholar 

  • Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y et al (2004) Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat Genet 36:1296–1300

    Article  CAS  PubMed  Google Scholar 

  • Verbsky ML, Richards EJ (2001) Chromatin remodeling in plants. Curr Opin Plant Biol 4:494–500

    Article  CAS  PubMed  Google Scholar 

  • Wirén M, Silverstein RA, Sinha I, Walfridsson J, Lee HM, Laurenson P et al (2005) Genomewide analysis of nucleosome density histone acetylation and HDAC function in fission yeast. EMBO J 24:2906–2918

    Article  PubMed  Google Scholar 

  • Wu K, Malik K, Tian L, Brown D, Miki B (2000) Functional analysis of a RPD3 histone deacetylase homolog in Arabidopsis thaliana. Plant Mol Biol 44:167–176

    Article  CAS  PubMed  Google Scholar 

  • Yan PS, Chen CM, Shi H, Rahmatpanah F, Wei SH, Caldwell CW et al (2001) Dissecting complex epigenetic alterations in breast cancer using CpG island microarrays. Cancer Res 61:8375–8380

    CAS  PubMed  Google Scholar 

  • Zhang Y, Fatima N, Dufau ML (2005) Coordinated changes in DNA methylation and histone modifications regulate silencing/derepression of luteinizing hormone receptor gene transcription. Mol Cell Biol 25:7929–7939

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Clarenz O, Cokus S, Bernatavichute YV, Pellegrini M, Goodrich J et al (2007) Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5:e129

    Article  PubMed  Google Scholar 

  • Zhao W, Soejima H, Higashimoto K, Nakagawachi T, Urano T, Kudo S et al (2005) The essential role of histone H3 Lys9 di-methylation and MeCP2 binding in MGMT silencing with poor DNA methylation of the promoter CpG island. J Biochem 137:431–440

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a grant from the National “863” High-Tech Project of the National Ministry of Science and Technology, People’s Republic of China (2003AA 210070) and the National Institute of Biological Sciences, as well as by a grant from the NSF Plant Genome Program (DBI-0421675).

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Authors and Affiliations

  1. National Institute of Biological Sciences, 7 Science Park Road, Zhongguancun Life Science Park, 102206, Beijing, People’s Republic of China

    Junli Zhou, Xiangfeng Wang & Xing Wang Deng

  2. Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, 06520, USA

    Junli Zhou, Xiangfeng Wang, Kun He, Jean-Benoit F. Charron, Axel A. Elling & Xing Wang Deng

  3. Peking-Yale Joint Center of Plant Molecular Genetics and Agrobiotechnology, College of Life Sciences, Peking University, 100871, Beijing, People’s Republic of China

    Kun He & Xing Wang Deng

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  1. Junli Zhou
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Correspondence to Xing Wang Deng.

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Junli Zhou and Xiangfeng Wang contributed equally to this work.

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Zhou, J., Wang, X., He, K. et al. Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression. Plant Mol Biol 72, 585–595 (2010). https://doi.org/10.1007/s11103-009-9594-7

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