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Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription

Nature Genetics volume 39, pages 61–69 (2007)Cite this article

Abstract

Cytosine methylation, a common form of DNA modification that antagonizes transcription, is found at transposons and repeats in vertebrates, plants and fungi. Here we have mapped DNA methylation in the entire Arabidopsis thaliana genome at high resolution. DNA methylation covers transposons and is present within a large fraction of A. thaliana genes. Methylation within genes is conspicuously biased away from gene ends, suggesting a dependence on RNA polymerase transit. Genic methylation is strongly influenced by transcription: moderately transcribed genes are most likely to be methylated, whereas genes at either extreme are least likely. In turn, transcription is influenced by methylation: short methylated genes are poorly expressed, and loss of methylation in the body of a gene leads to enhanced transcription. Our results indicate that genic transcription and DNA methylation are closely interwoven processes.

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Figure 1: Genome-wide mapping of DNA methylation in A. thaliana.
Figure 2: Distribution of methylated genes and transposable elements along chromosome arms.
Figure 3: Functional annotation of methylated (M) and unmethylated (U) genes.
Figure 4: Analysis of the distribution of DNA methylation within the A. thaliana genome.
Figure 5: Relationship between DNA methylation and transcription.
Figure 6: Correspondence between RNA polymerase II (Pol II) and DNA methylation.
Figure 7: Analysis of expression in met1-6 mutant plants.
Figure 8: Model for transcription-coupled DNA methylation.

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Acknowledgements

We thank J. Penterman (University of California Berkeley) for providing genomic DNA, R.L. Fischer (University of California Berkeley) for met1-6 seeds, M.E. Figueroa and J. Greally for help with the linear amplification protocol, T.D. Bryson for technical assistance and P. Talbert for comments on the manuscript. D.Z. is a Leukemia and Lymphoma Society Fellow. M.G. is a Howard Hughes Medical Institute Fellow of the Life Sciences Research Foundation.

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Author notes

  1. Robert K Tran

    Present address: University of California Davis Genome Center, 451 E. Health Sciences Drive, Davis, California, 95616, USA

Authors and Affiliations

  1. Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, 98109, Washington, USA

    Daniel Zilberman, Mary Gehring, Robert K Tran, Tracy Ballinger & Steven Henikoff

  2. Howard Hughes Medical Institute,

    Mary Gehring, Robert K Tran, Tracy Ballinger & Steven Henikoff

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Contributions

This study was designed by D.Z. and S.H.; D.Z., M.G. and R.K.T. performed the experiments; D.Z., T.B. and S.H. analyzed the data and D.Z. and S.H. wrote the paper.

Corresponding author

Correspondence to Steven Henikoff.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Bisulfite sequencing analysis of Arabidopsis genes. (PDF 274 kb)

Supplementary Fig. 2

Functional annotation of methylated and unmethylated genes. (PDF 437 kb)

Supplementary Fig. 3

Box plots of genic methylation. (PDF 406 kb)

Supplementary Fig. 4

Relationship between DNA methylation and expression in Arabidopsis. (PDF 1189 kb)

Supplementary Table 1

Bisulfite sequencing data, methylated vs. unmethylated gene calls and correlation between methylation in wild-type and expression in met1-6. (XLS 1352 kb)

Supplementary Table 2

Average transcription levels and lengths of genes in functional categories. (PDF 12 kb)

Supplementary Table 3

Methylated genes are preferentially targeted by siRNAs. (PDF 8 kb)

Supplementary Note (PDF 1154 kb)

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Zilberman, D., Gehring, M., Tran, R. et al. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39, 61–69 (2007). https://doi.org/10.1038/ng1929

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