Open Access Highly Accessed Research article

Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression

Kelly J Vining1, Kyle R Pomraning23, Larry J Wilhelm4, Henry D Priest56, Matteo Pellegrini7, Todd C Mockler568, Michael Freitag36 and Steven H Strauss1*

Author Affiliations

1 Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR 97331, USA

2 Molecular and Cellular Biology Program, Oregon State University, Corvallis, OR 97331, USA

3 Dept. of Biochemistry and Biophysics, Oregon State University, Corvallis, OR 97331, USA

4 Oregon Health Sciences University, Portland, OR 97002 USA

5 Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA

6 Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331, USA

7 Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, CA, 90024, USA

8 The Donald Danforth Plant Science Center, St. Louis, MO 63132, USA

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BMC Genomics 2012, 13:27  doi:10.1186/1471-2164-13-27

Published: 17 January 2012

Abstract

Background

DNA cytosine methylation is an epigenetic modification that has been implicated in many biological processes. However, large-scale epigenomic studies have been applied to very few plant species, and variability in methylation among specialized tissues and its relationship to gene expression is poorly understood.

Results

We surveyed DNA methylation from seven distinct tissue types (vegetative bud, male inflorescence [catkin], female catkin, leaf, root, xylem, phloem) in the reference tree species black cottonwood (Populus trichocarpa). Using 5-methyl-cytosine DNA immunoprecipitation followed by Illumina sequencing (MeDIP-seq), we mapped a total of 129,360,151 36- or 32-mer reads to the P. trichocarpa reference genome. We validated MeDIP-seq results by bisulfite sequencing, and compared methylation and gene expression using published microarray data. Qualitative DNA methylation differences among tissues were obvious on a chromosome scale. Methylated genes had lower expression than unmethylated genes, but genes with methylation in transcribed regions ("gene body methylation") had even lower expression than genes with promoter methylation. Promoter methylation was more frequent than gene body methylation in all tissues except male catkins. Male catkins differed in demethylation of particular transposable element categories, in level of gene body methylation, and in expression range of genes with methylated transcribed regions. Tissue-specific gene expression patterns were correlated with both gene body and promoter methylation.

Conclusions

We found striking differences among tissues in methylation, which were apparent at the chromosomal scale and when genes and transposable elements were examined. In contrast to other studies in plants, gene body methylation had a more repressive effect on transcription than promoter methylation.

Keywords:
Epigenetics; epigenomics; DNA methylation; 5-methylcytosine; Populus