Extensive demethylation of repetitive elements during seed development underlies gene imprinting - PubMed (original) (raw)

Extensive demethylation of repetitive elements during seed development underlies gene imprinting

Mary Gehring et al. Science. 2009.

Abstract

DNA methylation is an epigenetic mark associated with transposable element silencing and gene imprinting in flowering plants and mammals. In plants, imprinting occurs in the endosperm, which nourishes the embryo during seed development. We have profiled Arabidopsis DNA methylation genome-wide in the embryo and endosperm and found that large-scale methylation changes accompany endosperm development and endosperm-specific gene expression. Transposable element fragments are extensively demethylated in the endosperm. We discovered new imprinted genes by the identification of candidates associated with regions of reduced endosperm methylation and preferential expression in endosperm relative to other parts of the plant. These data suggest that imprinting in plants evolved from targeted methylation of transposable element insertions near genic regulatory elements followed by positive selection when the resulting expression change was advantageous.

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Figures

Figure 1

Figure 1. Endosperm is less methylated than embryo

A) Typical methylation profiles from a gene-rich and gene-poor region of the genome showing highly similar methylation patterns in embryo, endosperm, and dme endosperm from the L_er_ and Col-gl accessions. B) Average methylation in 100-bp windows of protein-coding genes and transposable element genes aligned at either their 5′ or 3′ ends in Col-gl embryo and endosperm. C) Methylation profiles of protein-coding genes when a set of 31,076 transposable element fragments (11) are and are not excluded from the averaging.

Figure 2

Figure 2. Known imprinted genes are associated with top DMRs

A) Histogram of Col-gl embryo - endosperm difference scores for 1.2 million overlapping 300-bp segments. Dashed lines represent the cutoff for the top 0.5% of methylation differences (~6000 300-bp segments). B) Embryo and endosperm methylation profiles of known imprinted genes. Red arrows, regions within the top 0.5% of methylation differences; gray arrow, region below the cutoff.

Figure 3

Figure 3. Methylation is lost 5′ and 3′ of genes in the endosperm

Average methylation profiles in embryo, endosperm, and dme endosperm of the A) 1276 Col-gl and B) 1163 Ler genes associated with more methylation in embryo than endosperm. Genes were aligned at their 5′ or 3′ end and the average methylation determined every 100 bp.

Figure 4

Figure 4. Expression and methylation analysis of new imprinted genes

A) RT-PCR allele-specific expression analysis from endosperm RNA of Col-gl females X L_er_ males and L_er_ females X Col-gl males. FWA is a control imprinted gene; AT3G25260 is biallelic. B) RT-PCR sequencing chromatograms for the paternally expressed genes AT2G32370 and AT5G62110. The biallelically-expressed gene αVPE is shown as a control. C) and D) Methylation profiling and allele-specific bisulfite sequencing analysis of new imprinted genes. Dashed lines represent the cutoff for the top 0.5% of differences. Each line of circles represent a bisulfite sequencing clone from embryo or endosperm. Filled circle, methylated cytosine. Red, CG; blue, CHG; gray, CHH.

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