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PMID: 27797352 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The DNA demethylase ROS1 targets genomic regions with distinct chromatin modifications.

Nature plants ·Vol. 2 ·No. 11 ·2016-00-31 ·Pages 16169

Tang K, Lang Z, Zhang H, Zhu JK

Abstract

The Arabidopsis ROS1/DEMETER family of 5-methylcytosine (5mC) DNA glycosylases are the first genetically characterized DNA demethylases in eukaryotes. However, the features of ROS1-targeted genomic loci are not well understood. In this study, we characterized ROS1 target loci in Arabidopsis Col-0 and C24 ecotypes. We found that ROS1 preferentially targets transposable elements (TEs) and intergenic regions. Compared with most TEs, ROS1-targeted TEs are closer to protein coding genes, suggesting that ROS1 may prevent DNA methylation spreading from TEs to nearby genes. ROS1-targeted TEs are specifically enriched for H3K18Ac and H3K27me3, and depleted of H3K27me and H3K9me2. Importantly, we identified thousands of previously unknown RNA-directed DNA methylation (RdDM) targets following depletion of ROS1, suggesting that ROS1 strongly antagonizes RdDM at these loci. In addition, we show that ROS1 also antagonizes RdDM-independent DNA methylation at some loci. Our results provide important insights into the genome-wide targets of ROS1 and the crosstalk between DNA methylation and ROS1-mediated active DNA demethylation.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Chromatin/metabolism Demethylation Nuclear Proteins/genetics,metabolism
Chemicals
Arabidopsis Proteins Chromatin Nuclear Proteins ROS1 protein, Arabidopsis
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Tang Kai ORCID
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907, USA.
Lang Zhaobo
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907, USA. | Shanghai Centre for Plant Stress Biology, and Centre for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Zhang Heng
Shanghai Centre for Plant Stress Biology, and Centre for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Zhu Jian-Kang ORCID
Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907, USA. | Shanghai Centre for Plant Stress Biology, and Centre for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 201602, China.
Conflict of Interest

The authors declare no competing financial interests.

References (44)
44 references, click to expand
  1. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity.
    Nat Rev Genet. 2014 Jun;15(6):394-408 PMID: 24805120
  2. BRAT-BW: efficient and accurate mapping of bisulfite-treated reads.
    Bioinformatics. 2012 Jul 1;28(13):1795-6 PMID: 22563065
  3. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase.
    Cell. 2002 Dec 13;111(6):803-14 PMID: 12526807
  4. Methylation-sensitive expression of a DNA demethylase gene serves as an epigenetic rheostat.
    PLoS Genet. 2015 Mar 31;11(3):e1005142 PMID: 25826366
  5. An AP endonuclease functions in active DNA demethylation and gene imprinting in Arabidopsis [corrected].
    PLoS Genet. 2015 Jan 08;11(1):e1004905 PMID: 25569774
  6. A Pre-mRNA-splicing factor is required for RNA-directed DNA methylation in Arabidopsis.
    PLoS Genet. 2013;9(9):e1003779 PMID: 24068953
  7. Regulation and function of DNA methylation in plants and animals.
    Cell Res. 2011 Mar;21(3):442-65 PMID: 21321601
  8. Epigenetic reprogramming: preparing the epigenome for the next generation.
    Biochem Soc Trans. 2013 Jun;41(3):809-14 PMID: 23697942
  9. An Rrp6-like protein positively regulates noncoding RNA levels and DNA methylation in Arabidopsis.
    Mol Cell. 2014 May 8;54(3):418-30 PMID: 24726328
  10. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.
    Cell. 2013 Mar 28;153(1):193-205 PMID: 23540698
  11. Dicer-independent RNA-directed DNA methylation in Arabidopsis.
    Cell Res. 2016 Jan;26(1):66-82 PMID: 26642813
  12. Regulatory link between DNA methylation and active demethylation in Arabidopsis.
    Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3553-7 PMID: 25733903
  13. A Dicer-Independent Route for Biogenesis of siRNAs that Direct DNA Methylation in Arabidopsis.
    Mol Cell. 2016 Jan 21;61(2):222-35 PMID: 26711010
  14. Highly integrated single-base resolution maps of the epigenome in Arabidopsis.
    Cell. 2008 May 2;133(3):523-36 PMID: 18423832
  15. Methylation-independent DNA binding modulates specificity of Repressor of Silencing 1 (ROS1) and facilitates demethylation in long substrates.
    J Biol Chem. 2010 Jul 23;285(30):23032-9 PMID: 20489198
  16. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis.
    Science. 2012 Jun 15;336(6087):1445-8 PMID: 22700931
  17. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis.
    Curr Biol. 2007 Jan 9;17(1):54-9 PMID: 17208187
  18. INVOLVED IN DE NOVO 2-containing complex involved in RNA-directed DNA methylation in Arabidopsis.
    Proc Natl Acad Sci U S A. 2012 May 29;109(22):8374-81 PMID: 22592791
  19. DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis.
    Genome Biol. 2014 Sep 17;15(9):458 PMID: 25228471
  20. Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation.
    Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11796-801 PMID: 16864782
  21. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1.
    Nature. 2013 Jun 20;498(7454):385-9 PMID: 23636332
  22. A DNA 3' phosphatase functions in active DNA demethylation in Arabidopsis.
    Mol Cell. 2012 Feb 10;45(3):357-70 PMID: 22325353
  23. Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production.
    Plant J. 2013 Jan;73(1):77-90 PMID: 22962860
  24. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation.
    Nature. 2010 May 6;465(7294):106-9 PMID: 20410883
  25. DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):6853-8 PMID: 16624880
  26. DNA demethylation in the Arabidopsis genome.
    Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6752-7 PMID: 17409185
  27. Epigenetic regulation of the bacterial cell cycle.
    Curr Opin Microbiol. 2009 Dec;12 (6):722-9 PMID: 19783470
  28. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
    Genome Biol. 2009;10(3):R25 PMID: 19261174
  29. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis.
    EMBO J. 2006 Jun 21;25(12):2828-36 PMID: 16724114
  30. Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation.
    Nat Commun. 2014 Jun 05;5:4062 PMID: 24898766
  31. Active DNA demethylation in plants and animals.
    Cold Spring Harb Symp Quant Biol. 2012;77:161-73 PMID: 23197304
  32. A One Precursor One siRNA Model for Pol IV-Dependent siRNA Biogenesis.
    Cell. 2015 Oct 8;163(2):445-55 PMID: 26451488
  33. A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection.
    Science. 2013 Aug 2;341(6145):1238858 PMID: 23908241
  34. The methyl-CpG-binding protein MBD7 facilitates active DNA demethylation to limit DNA hyper-methylation and transcriptional gene silencing.
    Mol Cell. 2015 Mar 19;57(6):971-83 PMID: 25684209
  35. Methyl-CpG-binding domain protein MBD7 is required for active DNA demethylation in Arabidopsis.
    Plant Physiol. 2015 Mar;167(3):905-14 PMID: 25593350
  36. Genetic interactions between DNA demethylation and methylation in Arabidopsis.
    Plant Physiol. 2007 Dec;145(4):1549-57 PMID: 17951456
  37. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis.
    Nat Struct Mol Biol. 2014 Jan;21(1):64-72 PMID: 24336224
  38. Active DNA demethylation mediated by DNA glycosylases.
    Annu Rev Genet. 2009;43:143-66 PMID: 19659441
  39. Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis.
    Elife. 2015 Oct 02;4:e09591 PMID: 26430765
  40. A DNA ligase required for active DNA demethylation and genomic imprinting in Arabidopsis.
    Cell Res. 2015 Jun;25(6):757-60 PMID: 25906993
  41. A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development.
    Genes Dev. 2009 Dec 1;23(23):2717-22 PMID: 19903758
  42. Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing.
    EMBO J. 2007 Mar 21;26(6):1691-701 PMID: 17332757
  43. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation.
    Cell. 2007 Sep 7;130(5):851-62 PMID: 17803908
  44. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes.
    Science. 2012 Sep 14;337(6100):1360-4 PMID: 22984074
Article Info
Journal
Nature plants
Abbr.
Nat Plants
ISSN
2055-0278
Published
2016-00-31
Epub
2016-00-31
Pages
16169
Language
English
Region
England
NLM ID
101651677
PMCID
PMC5123759
Subset
IM
Grants
NIGMS NIH HHS · R01 GM070795 · United States
Corrections
CommentIn
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