Differentiation of epigenetic modifications between transposons and genes

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Transposable elements (TEs) and repeats are methylated and silenced epigenetically in a variety of organisms including plants. Recent results in Arabidopsis suggest that the TE silencing can be reprogrammed by small RNA during gametogenesis. On the other hand, TE-specific DNA methylation independent of small RNA can be induced by H3K9 methylation through mechanisms conserved between plants and fungi. Methylation of CG sites is found not only in TEs but also in the body of constitutively transcribed genes. Although the function of gene-body methylation is still elusive, the distribution and control of this type of DNA methylation are very similar between plants and animals. Possible interactions of these multiple layers of epigenetic marks and their evolution are discussed.

Research highlights

Transposons are marked by specific epigenetic modifications in the plant genome. ▶ Small RNAs reprogram the epigenetic marking of transposons during gametogenesis. ▶ Transcribed sequences lose H3K9 methylation by active demethylation. ▶ CG sites are methylated in the body of transcribed genes.

Introduction

Active and inactive states of a transcription unit are often inherited over cell division. This property, heritable variation without a difference in the nucleotide sequence, is referred to as ‘epigenetic’. Epigenetic information is marked on the chromosome by covalent modifications of cytosine residues and histones, and associated small RNA. Epigenetic silencing can be constitutive (long-lasting) or facultative (programmable). Facultative silencing is important for maintaining tissue-specific gene expression patterns, as well as embryogenesis and memory of environmental stimuli [1, 2, 3]. On the other hand, the constitutive silencing is involved in control of transposable elements (TEs) and other repetitive elements (Table 1); it tends to be more stable and often heritable over multiple plant generations. Interestingly, recent findings suggest that TE silencing can also be regulated developmentally through ‘germ-soma’ interaction by small RNA. In addition, the combination of epigenetics and genomics is revealing several unexpected features of epigenetic controls mediated by DNA methylation, some of which turned out to be conserved in organisms of other kingdoms. In this review, we try to convey the recent excitement in this field and discuss remaining mysteries.

Section snippets

DNA methylation and TE silencing

Genome-wide analyses of DNA methylation have revealed that it is enriched in TEs and repeats [4, 5, 6, 7, 8] (Table 1). This biased distribution of DNA methylation is found in cytosines in all three sequence contexts: CG, CHG, and CHH (H can be A, T, or C). The role of DNA methylation in TE silencing has been directly demonstrated using mutants of Arabidopsis; when DNA methylation is lost in the mutants of DNA methyltransferases or a chromatin remodeler DDM1 (decrease in DNA methylation 1),

Developmental control of TEs in gametophytes and seeds

If you are a developmental biologist, the inheritance of an epigenetic state over multiple generations may sound strange. However, the inheritance of the silent state of TEs over generations seems a good strategy to prevent them from proliferating in the germline and to protect the host genome from deleterious mutations; if the host identified and silenced TEs, there is no reason to reactivate them in each generation [14]; the exception would be when the activation is beneficial to the host.

Control of H3K9me

Obviously, RdDM, which directs DNA cytosine methylation in all three sequence contexts, is important for establishing DNA methylation of TEs. However, RdDM is not generally associated with another TE-specific epigenetic mark, H3K9me2 (dimethylation of histone H3 lysine9, Table 1) [27]. H3K9me is an epigenetic mark of silent chromatin conserved among most eukaryotic species including those without (or with undetectably low levels of) genomic cytosine methylation, such as fission yeast or

Methylation of gene bodies

Another unexpected feature of DNA methylation revealed by the genome-wide analyses is methylation in the body of transcribed genes [5, 6, 7, 8]. Unlike DNA methylation in TEs and repeats, genic DNA methylation is limited to CG sites (Table 1) [7, 8]. This gene-body CG methylation is high in the central part of genes, with 5′ and 3′ terminal regions unmethylated.

What is the function of the gene-body DNA methylation? Loss of the CG methylation by met1 mutation does not substantially affect the

Conclusions and perspectives

The very intriguing observations on DNA methylation dynamics in pollen, megaspore, and endosperm have provided a new framework for the establishment of TE silencing. The germline companion cells provide TE-derived small RNAs that inactivate TEs in gametes. Although this strategy makes sense, it is still not known how transcripts from TEs and genes are distinguished when small RNA is generated specifically from TEs. That could be an important remaining piece of the puzzle.

We have discussed three

References and recommended reading

Papers of particular interest published within the period of review have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Marjori Matzke, Eric Richards, and Daniel Zilberman for critical comments. Supported by Japan Science and Technology Agency (JST) PRESTO program (to H.S.), and Japanese Ministry of Education, Culture, Sports, Science and Technology (19207002 and 19060014) (to T.K.). We apologize to authors whose work was not cited owing to space limitations.

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