Silencing of transposable elements in plants

doi:10.1016/S1360-1385(01)02105-7

Trends in Plant Science

Volume 6, Issue 11, 1 November 2001, Pages 527-534

https://doi.org/10.1016/S1360-1385(01)02105-7 Get rights and content

Abstract

Plant genomes contain many transposable elements, most of which are inactivated or ‘silenced’. Recent studies have brought significant new insights into the regulation of transposable elements. In Caenorhabditis elegans, they are silenced post-transcriptionally, whereas transposable elements in Arabidopsis are silenced by a chromatin-remodelling factor, one of the components of transcriptional gene silencing. These observations provide the functional correlation between gene silencing and the suppression of transposable elements, and have major implications for our understanding of the maintenance of genomic integrity.

Section snippets

Epigenetic regulation of transposable elements

TEs make up 14% of the Arabidopsis genome, in contrast with an estimated 50–80% for the maize genome 1, 2. The genome sequence of Arabidopsis has revealed that TEs are enriched in the centromeric region, which is highly methylated and packed into heterochromatin ¹. TEs in Arabidopsis are also concentrated in other heterochromatin regions such as the knob ³, which also have a concentration of repetitive sequences and are highly methylated. It has been shown for the maize genome that most TEs

Molecular genetics of transposable element silencing

Several loci affecting the activity of TEs have been investigated. Additionally, recent studies add insights into the molecular genetics of TE silencing (Table 1). Genes involved in TGS are candidates for TE silencing. The DDM1 gene, whose mutation leads to DNA hypomethylation, is involved in TGS of PAI genes, which encode phosphoribosylanthranilate isomerase in Arabidopsis ¹⁷. All of the Mu-like elements (MULEs) in Arabidopsis are methylated in the wild-type background but are rarely active

Transposable element silencing in other organisms

TEs are subjected to repression in any organism, even those lacking DNA methylation, such as Drosophila and C. elegans (although a recent report has shown the existence of trace amounts of DNA methylation in Drosophila ²⁹). Recent investigations have indicated that there might be a common mechanism of silencing between plants and other organisms. Here, we mention some of the analyses in organisms other than plants.

Mechanisms of silencing

The accumulated results imply that there are two pathways through which organisms silence TEs. First, transcripts of TEs are degraded by PTGS. Second, methylation and/or chromatin configuration has a role in suppressing the transcription of TEs. These pathways have been elucidated by investigations on transgene silencing and we speculate that these two pathways act independently or synergistically to silence plant TEs. Here, we describe the details of each pathway, together with parallels

Conclusions

Recent advances in research on gene silencing and epigenetic phenomena add significant insights into the mechanisms of TE silencing. In particular, molecular genetic studies on Arabidopsis provide direct evidence for the role of repressive chromatin in TE silencing. Based on these results, we envision silencing as acting as follows. Mechanistically, TEs for which aberrant RNA or dsRNA is generated would be silenced by PTGS. However, actively transposing multicopy TEs would be silenced by TGS

Acknowledgements

We thank David Baulcombe, Vicki Chandler and Eric Richards for communicating unpublished results. We also thank anonymous referees for constructive advice. We apologize to those researchers whose work we were unable to cite owing to space limitations. Work in H.H.'s laboratory is supported by grants from the Ministry of Agriculture, Forestry and Fisheries of Japan, the Bio-oriented Technology Research Advancement Institution, and the Science and Technology Agency of Japan. H.O. is supported by

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Dedifferentiation, that is, the acquisition of stem cell-like state, commonly induced by stress (e.g., protoplasting), is characterized by open chromatin conformation, a chromatin state that could lead to activation of transposable elements (TEs). Here, we studied the activation of the Arabidopsis class II TE Tag1, in which two copies, situated close to each other (near genes) on chromosome 1 are found in Landsberg erecta (Ler) but not in Columbia (Col). We first transformed protoplasts with a construct in which a truncated Tag1 (ΔTag1 non-autonomous) blocks the expression of a reporter gene AtMBD5-GFP and found a relatively high ectopic excision of ΔTag1 accompanied by expression of AtMBD5-GFP in protoplasts derived from Ler compared to Col; further increase was observed in ddm1 (decrease in DNA methylation1) protoplasts (Ler background). Ectopic excision was associated with transcription of the endogenous Tag1 and changes in histone H3 methylation at the promoter region. Focusing on the endogenous Tag1 elements we found low level of excision in Ler protoplasts, which was slightly and strongly enhanced in ddm1 and cmt3 (chromomethylase3) protoplasts, respectively, concomitantly with reduction in Tag1 gene body (GB) CHG methylation and increased Tag1 transcription; strong activation of Tag1 was also observed in cmt3 leaves. Notably, in cmt3, but not in ddm1, Tag1 elements were excised out from their original sites and transposed elsewhere in the genome. Our results suggest that dedifferentiation is associated with Tag1 activation and that CMT3 rather than DDM1 plays a central role in restraining Tag1 activation via inducing GB CHG methylation.
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Trends in Plant Science

ReviewSilencing of transposable elements in plants

Abstract

Section snippets

Epigenetic regulation of transposable elements

Molecular genetics of transposable element silencing

Transposable element silencing in other organisms

Mechanisms of silencing

Conclusions

Acknowledgements

Nature

Nat. Genet.

Trends Plant Sci.

Nat. Genet.

Nature

Curr. Opin. Genet. Dev.

Trends. Biol. Sci.

Nat. Genet.

Curr. Biol.

Mol. Gen. Genet.

Annu. Rev. Genet.

Genes Cells

Mol. Cell. Biol.

Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons

Ann. Bot.

The complete sequence of a heterochromatic island from a higher eukaryote

Cell

Nested retrotransposons in the intergenic regions of the maize genome

Science

The significance of responses of the genome to challenge

Science

Epigenetic silencing of Mu transposable elements in maize

Epigenetic regulation of the maize Spm transposable element

DNA modification of a maize transposable element correlates with loss of activity

Proc. Natl. Acad. Sci. U. S. A.

Activity of the transposon Tam3 in Antirrhinum and tobacco: possible role of DNA methylation

EMBO J.

DNA methylation in health and disease

Nat. Rev. Genet.

The maize transposable element Activator (Ac)

Curr. Top. Microbiol. Immunol.

Hybrid speciation accompanied by genomic reorganization in wild sunflowers

Nature

Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids

Plant Cell

Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid

Nature

The DNA methylation locus DDM1 is required for maintenance of gene silencing in Arabidopsis

Genes Dev.

Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1)

Genes Dev.

Developmental abnormalities and epimutations associated with DNA hypomethylation mutations

Proc. Natl. Acad. Sci. U. S. A.

Review
Silencing of transposable elements in plants