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Methylation of cytosines in DNA sequences is a major part of epigenetic regulation, resulting in proximal transcriptional silencing and enabling the stable inheritance of a pattern of transcriptional activity. DNA methylation in higher eukaryotes is involved in transposon silencing and regulation of gene expression; however, the full extent to which this mechanism regulates the genome has remained unknown. Tiling arrays representing the entire genome of the flowering plant Arabidopsis thaliana, tiled at 35-bp resolution, provide a platform upon which to analyze the methylated component of the Arabidopsis genome. Hybridization of methylated genomic DNA isolated by 5-methyl-cytosine immunoprecipitation to the whole-genome tiling arrays produced the first comprehensive DNA methylation map of an entire genome, identifying heavy DNA methylation at pericentromeric heterochromatin, repetitive sequences, and regions producing small interfering RNAs. Over one-third of expressed genes contain methylation within transcribed regions, whereas only ~5% of genes show methylation within promoter regions. Genes methylated in transcribed regions are highly expressed and constitutively active, whereas promoter-methylated genes show a greater degree of tissue-specific expression. Whole-genome tiling-array transcriptional profiling of DNA methyltransferase null mutants identified hundreds of genes and intergenic noncoding RNAs with altered expression levels, many of which may be epigenetically controlled by DNA methylation. The approaches developed should assist in the study of DNA methylation in larger and more complex genomes, for which whole-genome tiling arrays are now available.