DNA Methylation Signatures of the Plant Chromomethyltransferases

Overview

Journal PLoS Genet

Specialty Genetics

Date 2016 Dec 21

PMID 27997534

Citations 87

Authors

Quentin Gouil

David C Baulcombe

Affiliations

Soon will be listed here.

Abstract

DNA methylation in plants is traditionally partitioned into CG, CHG and CHH contexts (with H any nucleotide but G). By investigating DNA methylation patterns in trinucleotide contexts in four angiosperm species, we show that such a representation hides spatial and functional partitioning of different methylation pathways and is incomplete. CG methylation (mCG) is largely context-independent whereas, at CHG motifs, there is under-representation of mCCG in pericentric regions of A. thaliana and tomato and throughout the chromosomes of maize and rice. In A. thaliana the biased representation of mCCG in heterochromatin is related to specificities of H3K9 methyltransferase SUVH family members. At CHH motifs there is an over-representation of different variant forms of mCHH that, similarly to mCCG hypomethylation, is partitioned into the pericentric regions of the two dicots but dispersed in the monocot chromosomes. The over-represented mCHH motifs in A. thaliana associate with specific types of transposon including both class I and II elements. At mCHH the contextual bias is due to the involvement of various chromomethyltransferases whereas the context-independent CHH methylation in A. thaliana and tomato is mediated by the RNA-directed DNA methylation process that is most active in the gene-rich euchromatin. This analysis therefore reveals that the sequence context of the methylome of plant genomes is informative about the mechanisms associated with maintenance of methylation and the overlying chromatin structure.

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References

Lindroth A, Cao X, Jackson J, Zilberman D, McCALLUM C, Henikoff S . Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science. 2001; 292(5524):2077-80. DOI: 10.1126/science.1059745. View

Jackson J, Lindroth A, Cao X, Jacobsen S . Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature. 2002; 416(6880):556-60. DOI: 10.1038/nature731. View

Herr A, Jensen M, Dalmay T, Baulcombe D . RNA polymerase IV directs silencing of endogenous DNA. Science. 2005; 308(5718):118-20. DOI: 10.1126/science.1106910. View

Kanno T, Huettel B, Mette M, Aufsatz W, Jaligot E, Daxinger L . Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet. 2005; 37(7):761-5. DOI: 10.1038/ng1580. View

Ebbs M, Bender J . Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell. 2006; 18(5):1166-76. PMC: 1456864. DOI: 10.1105/tpc.106.041400. View

Johnson L, Bostick M, Zhang X, Kraft E, Henderson I, Callis J . The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol. 2007; 17(4):379-84. PMC: 1850948. DOI: 10.1016/j.cub.2007.01.009. View

Cokus S, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild C . Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008; 452(7184):215-9. PMC: 2377394. DOI: 10.1038/nature06745. View

Mosher R, Schwach F, Studholme D, Baulcombe D . PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci U S A. 2008; 105(8):3145-50. PMC: 2268599. DOI: 10.1073/pnas.0709632105. View

Buisine N, Quesneville H, Colot V . Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets. Genomics. 2008; 91(5):467-75. DOI: 10.1016/j.ygeno.2008.01.005. View

10.

Lister R, OMalley R, Tonti-Filippini J, Gregory B, Berry C, Millar A . Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008; 133(3):523-36. PMC: 2723732. DOI: 10.1016/j.cell.2008.03.029. View

11.

Sharma R, Mohan Singh R, Malik G, Deveshwar P, Tyagi A, Kapoor S . Rice cytosine DNA methyltransferases - gene expression profiling during reproductive development and abiotic stress. FEBS J. 2009; 276(21):6301-11. DOI: 10.1111/j.1742-4658.2009.07338.x. View

12.

Law J, Jacobsen S . Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010; 11(3):204-20. PMC: 3034103. DOI: 10.1038/nrg2719. View

13.

Feng S, Cokus S, Zhang X, Chen P, Bostick M, Goll M . Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A. 2010; 107(19):8689-94. PMC: 2889301. DOI: 10.1073/pnas.1002720107. View

14.

Rajakumara E, Law J, Simanshu D, Voigt P, Johnson L, Reinberg D . A dual flip-out mechanism for 5mC recognition by the Arabidopsis SUVH5 SRA domain and its impact on DNA methylation and H3K9 dimethylation in vivo. Genes Dev. 2011; 25(2):137-52. PMC: 3022260. DOI: 10.1101/gad.1980311. View

15.

Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S . A modular cloning system for standardized assembly of multigene constructs. PLoS One. 2011; 6(2):e16765. PMC: 3041749. DOI: 10.1371/journal.pone.0016765. View

16.

Krueger F, Andrews S . Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011; 27(11):1571-2. PMC: 3102221. DOI: 10.1093/bioinformatics/btr167. View

17.

Pontvianne F, Blevins T, Chandrasekhara C, Feng W, Stroud H, Jacobsen S . Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes Dev. 2012; 26(9):945-57. PMC: 3347792. DOI: 10.1101/gad.182865.111. View

18.

Chodavarapu R, Feng S, Ding B, Simon S, Lopez D, Jia Y . Transcriptome and methylome interactions in rice hybrids. Proc Natl Acad Sci U S A. 2012; 109(30):12040-5. PMC: 3409791. DOI: 10.1073/pnas.1209297109. View

19.

Wierzbicki A, Cocklin R, Mayampurath A, Lister R, Rowley M, Gregory B . Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 2012; 26(16):1825-36. PMC: 3426761. DOI: 10.1101/gad.197772.112. View

20.

Du J, Zhong X, Bernatavichute Y, Stroud H, Feng S, Caro E . Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell. 2012; 151(1):167-80. PMC: 3471781. DOI: 10.1016/j.cell.2012.07.034. View