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

Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH - BMC Genomics (2012)

Bottom Line: We validated MeDIP-seq results by bisulfite sequencing, and compared methylation and gene expression using published microarray data.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Forest Ecosystems and Society, Oregon State University, Corvallis, 97331, USA.

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.

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Differentiation of gene body methylation among selected tissues. A. Venn diagram showing overlaps of gene body methylation among four of the sampled tissue types. Numbers are counts of genes called methylated (RPKM compared to non-immunoprecipitated input, 1% false discovery rate). B. Presence/absence heat map showing blocks of body- methylated genes common (black) among the seven sampled tissues. Left y-axis shows counts of genes.
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Figure 6: Differentiation of gene body methylation among selected tissues. A. Venn diagram showing overlaps of gene body methylation among four of the sampled tissue types. Numbers are counts of genes called methylated (RPKM compared to non-immunoprecipitated input, 1% false discovery rate). B. Presence/absence heat map showing blocks of body- methylated genes common (black) among the seven sampled tissues. Left y-axis shows counts of genes.

Mentions: Genome-wide methylation in different tissues, determined using 1-kb tiled windows across the genome as described above, showed that 33.7% of the genome was differentially methylated. Further, pairwise tissue methylation comparisons based on the 1-kb windows showed substantial differential methylation (Table 3), with an overall mean pairwise similarity of 31.5%. Male catkins had by far the greatest number of gene-body-methylated genes that were not methylated in any other tissue type (2,866) (Figure 6). Seventeen to 31% of gene models methylated in any tissue had both promoter and body methylation (Figure 7). Within a tissue type, promoter-methylated genes were more frequent than body-methylated genes, accounting for 50-60% of all methylated genes. Roots accounted for 41% of promoter-methylated genes that were restricted to one tissue type, and male catkins accounted for 80% of single-tissue body-methylated genes. When gene-associated features were compared among tissues, there was also extensive tissue-associated variation (Table 4). Promoters methylated in common among tissues ranged from a maximum of 16% (leaf vs. root) to less than one percent (male catkin vs. phloem, root, or bud). Gene bodies methylated in common ranged from 11% (root vs. phloem) to less than one percent (male catkin vs. bud or female catkin vs. leaf, root, xylem, of phloem).


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

Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH - BMC Genomics (2012)

Differentiation of gene body methylation among selected tissues. A. Venn diagram showing overlaps of gene body methylation among four of the sampled tissue types. Numbers are counts of genes called methylated (RPKM compared to non-immunoprecipitated input, 1% false discovery rate). B. Presence/absence heat map showing blocks of body- methylated genes common (black) among the seven sampled tissues. Left y-axis shows counts of genes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3298464&req=5

Figure 6: Differentiation of gene body methylation among selected tissues. A. Venn diagram showing overlaps of gene body methylation among four of the sampled tissue types. Numbers are counts of genes called methylated (RPKM compared to non-immunoprecipitated input, 1% false discovery rate). B. Presence/absence heat map showing blocks of body- methylated genes common (black) among the seven sampled tissues. Left y-axis shows counts of genes.
Mentions: Genome-wide methylation in different tissues, determined using 1-kb tiled windows across the genome as described above, showed that 33.7% of the genome was differentially methylated. Further, pairwise tissue methylation comparisons based on the 1-kb windows showed substantial differential methylation (Table 3), with an overall mean pairwise similarity of 31.5%. Male catkins had by far the greatest number of gene-body-methylated genes that were not methylated in any other tissue type (2,866) (Figure 6). Seventeen to 31% of gene models methylated in any tissue had both promoter and body methylation (Figure 7). Within a tissue type, promoter-methylated genes were more frequent than body-methylated genes, accounting for 50-60% of all methylated genes. Roots accounted for 41% of promoter-methylated genes that were restricted to one tissue type, and male catkins accounted for 80% of single-tissue body-methylated genes. When gene-associated features were compared among tissues, there was also extensive tissue-associated variation (Table 4). Promoters methylated in common among tissues ranged from a maximum of 16% (leaf vs. root) to less than one percent (male catkin vs. phloem, root, or bud). Gene bodies methylated in common ranged from 11% (root vs. phloem) to less than one percent (male catkin vs. bud or female catkin vs. leaf, root, xylem, of phloem).

Bottom Line: We validated MeDIP-seq results by bisulfite sequencing, and compared methylation and gene expression using published microarray data.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Forest Ecosystems and Society, Oregon State University, Corvallis, 97331, USA.

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.

Show MeSH
Related in: MedlinePlus