Differentiation of epigenetic modifications between transposons and genes
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.
References (65)
- et al.
Diversity of polycombe group complexes in plants: same rules, different players?
Trends Genet
(2009) - et al.
Parental memories shape seeds
Trends Plant Sci
(2009) - et al.
Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis
Cell
(2006) - et al.
Highly integrated single-base resolution maps of the epigenome in Arabidopsis
Cell
(2008) - et al.
A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis
Curr Biol
(2010) - et al.
An RNA-dependent RNA polymerase in required for paramutation in maize
Nature
(2006) - et al.
A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing
Proc Natl Acad Sci USA
(2002) - et al.
Endogenous targets of RNA-directed DNA methylation and PolIV in Arabidopsis
EMBO J
(2006) - et al.
Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells
Science
(2010) - et al.
Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase
Nature
(2002)
Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin
Proc Natl Acad Sci USA
Seasonal and developmental timing of flowering
Plant J
Role of transposable elements in heterochromatin and epigenetic control
Nature
Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription
Nat Genet
Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning
Nature
Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis
Nature
Robertsons Mutator transposons in A. thaliana are regulated by the chromatin-remodelling gene Decrease in DNA methylation (DDM1)
Genes Dev
Bursts of retrotransposition reproduced in Arabidopsis
Nature
Selective epigenetic control of retrotransposition in Arabidopsis
Nature
Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification
PLoS Biol
Epigenetic control of CACTA transposon mobility in Arabidopsis thaliana
Genetics
Suppressor-mutator system of control of gene action in maize
A role for RNAi in the selective correction of DNA methylation defects
Science
RNA-directed de novo methylation of genomic sequences in plants
Cell
Transcriptional silencing and promoter methylation triggered by double-stranded RNA
EMBO J
RNA-mediated chromatin-based silencing in plants
Curr Opin Cell Biol
Establishing, maintaining and modifying DNA methylation patterns in plants and animals
Nat Rev Genet
An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation
Nature
An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein
Cell
Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II
Mol Cell
Extensive demethylation of repetitive elements during seed development underlies gene imprinting
Science
Genome-wide demethylation of Arabidopsis endosperm
Science
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