scholarly journals RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays

PLoS Genetics ◽  
2021 ◽  
Vol 17 (6) ◽  
pp. e1009326
Author(s):  
Wei Guo ◽  
Dafang Wang ◽  
Damon Lisch
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Histone H3 ◽  
Transcriptional Silencing ◽  
Epigenetic Silencing ◽  
Terminal Inverted Repeat ◽  
Wild Type ◽  
Rna Dependent Rna Polymerase ◽  
Plant Genomes ◽  
Transposon Silencing

In large complex plant genomes, RNA-directed DNA methylation (RdDM) ensures that epigenetic silencing is maintained at the boundary between genes and flanking transposable elements. In maize, RdDM is dependent on Mediator of Paramutation 1 (Mop1), a putative RNA dependent RNA polymerase. Here we show that although RdDM is essential for the maintenance of DNA methylation of a silenced MuDR transposon in maize, a loss of that methylation does not result in a restoration of activity. Instead, heritable maintenance of silencing is maintained by histone modifications. At one terminal inverted repeat (TIR) of this element, heritable silencing is mediated via histone H3 lysine 9 dimethylation (H3K9me2), and histone H3 lysine27 dimethylation (H3K27me2), even in the absence of DNA methylation. At the second TIR, heritable silencing is mediated by histone H3 lysine 27 trimethylation (H3K27me3), a mark normally associated with somatically inherited gene silencing. We find that a brief exposure of high temperature in a mop1 mutant rapidly reverses both of these modifications in conjunction with a loss of transcriptional silencing. These reversals are heritable, even in mop1 wild-type progeny in which methylation is restored at both TIRs. These observations suggest that DNA methylation is neither necessary to maintain silencing, nor is it sufficient to initiate silencing once has been reversed. However, given that heritable reactivation only occurs in a mop1 mutant background, these observations suggest that DNA methylation is required to buffer the effects of environmental stress on transposable elements.

scholarly journals RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays.

2021 ◽  
Author(s):  
Damon Lisch ◽  
Wei Guo ◽  
Dafang Wang
Keyword(s):  
Dna Methylation ◽  
Heat Stress ◽  
Transposable Elements ◽  
Transcriptional Silencing ◽  
Epigenetic Silencing ◽  
Terminal Inverted Repeat ◽  
Wild Type ◽  
Rna Dependent Rna Polymerase ◽  
Plant Genomes ◽  
Transposon Silencing

In large complex plant genomes, RNA-directed DNA methylation (RdDM) ensures that epigenetic silencing is maintained at the boundary between genes and flanking transposable elements. In maize, RdDM is dependent on  Modifer of Paramutation 1 (Mop1 ), a putative RNA dependent RNA polymerase. Here we show that although RdDM is essential for the maintenance of DNA methylation of a silenced  MuDR  transposon in maize, a loss of that methylation does not result in a restoration of activity. Instead, heritable maintenance of silencing is maintained by histone modifications. At one terminal inverted repeat (TIR) of this element, heritable silencing is mediated via H3K9 and H3K27 dimethylation, even in the absence of DNA methylation. At the second TIR, heritable silencing is mediated by H3K29 trimethylation, a mark normally associated with somatically inherited gene silencing. We find that a brief exposure of high temperature in a  mop1  mutant rapidly reverses both of these modifications in conjunction with a loss of transcriptional silencing. These reversals are heritable, even in  mop1  wild type progeny in which methylation is restored at both TIRs. These observations suggest that DNA methylation is neither necessary to maintain silencing, nor is it sufficient to initiate silencing once has been reversed. However, given that heritable reactivation only occurs in a  mop1  mutant background, these observations suggest that DNA methylation is required to buffer the effects of environmental stress on transposable elements.

scholarly journals Mu killer Causes the Heritable Inactivation of the Mutator Family of Transposable Elements in Zea mays

Genetics ◽  
2003 ◽  
Vol 165 (2) ◽  
pp. 781-797
Author(s):  
R Keith Slotkin ◽  
Michael Freeling ◽  
Damon Lisch
Keyword(s):  
Dna Methylation ◽  
Zea Mays ◽  
Transposable Elements ◽  
Plant Development ◽  
Epigenetic Silencing ◽  
The Other ◽  
Transcript Levels ◽  
Transposon Silencing ◽  
Number Of Genes

Abstract Mutations in a number of genes responsible for the maintenance of transposon silencing have been reported. However, the initiation of epigenetic silencing of transposable elements is poorly characterized. Here, we report the identification of a single dominant locus, Mu killer (Muk), that acts to silence MuDR, the autonomous regulatory transposon of the Mutator family of transposable elements in maize. Muk results in the methylation of MuDR TIRs and is competent to silence one or several active MuDR elements. Silencing by Muk is not dependent on the position of the MuDR element and occurs gradually during plant development. Transcript levels of the MuDR transposase, mudrA, decrease substantially when Muk is present. The other transcript encoded by MuDR, mudrB, also fails to accumulate in the poly(A) RNA fraction when MuDR and Muk are combined. Additionally, plants undergoing MuDR silencing produce small, mudrA-homologous ∼26-nt RNAs, suggesting a role for RNA-directed DNA methylation in MuDR silencing. MuDR elements silenced by Muk remain silenced even in plants that do not inherit Muk, suggesting that Muk is required for the initiation of MuDR silencing but not for its maintenance.

scholarly journals Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

2021 ◽  
Author(s):  
Jaemyung Choi ◽  
David Bruce Lyons ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Small Rna ◽  
Histone H3 ◽  
Histone H1 ◽  
Dna Methyltransferases ◽  
Flowering Plants ◽  
Genomic Sequences ◽  
Rna Molecules ◽  
Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically required for small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

scholarly journals Impact of transposable elements on methylation and gene expression across natural accessions of Brachypodium distachyon

2020 ◽  
Author(s):  
Michele Wyler ◽  
Christoph Stritt ◽  
Jean-Claude Walser ◽  
Célia Baroux ◽  
Anne C. Roulin
Keyword(s):  
Gene Expression ◽  
Dna Methylation ◽  
Transposable Elements ◽  
Plant Species ◽  
Brachypodium Distachyon ◽  
Expression Patterns ◽  
Small Subset ◽  
Molecular Evidence ◽  
Specific Gene ◽  
Plant Genomes

AbstractTransposable elements (TEs) constitute a large fraction of plant genomes and are mostly present in a transcriptionally silent state through repressive epigenetic modifications such as DNA methylation. TE silencing is believed to influence the regulation of adjacent genes, possibly as DNA methylation spreads away from the TE. Whether this is a general principle or a context-dependent phenomenon is still under debate, pressing for studying the relationship between TEs, DNA methylation and nearby gene expression in additional plant species. Here we used the grass Brachypodium distachyon as a model and produced DNA methylation and transcriptome profiles for eleven natural accessions. In contrast to what is observed in Arabidopsis thaliana, we found that TEs have a limited impact on methylation spreading and that only few TE families are associated to a low expression of their adjacent genes. Interestingly, we found that a subset of TE insertion polymorphisms is associated with differential gene expression across accessions. Thus, although not having a global impact on gene expression, distinct TE insertions may contribute to specific gene expression patterns in B. distachyon.Significance statementTransposable elements (TEs) are a major component of plant genomes and a source of genetic and epigenetic innovations underlying adaptation to changing environmental conditions. Yet molecular evidence linking TE silencing and nearby gene expression are lacking for many plant species. We show that in the model grass Brachypodium DNA methylation spreads over very short distances around TEs, with an influence on gene expression for a small subset of TE families.

scholarly journals Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jaemyung Choi ◽  
David B Lyons ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Small Rna ◽  
Histone H3 ◽  
Histone H1 ◽  
Dna Methyltransferases ◽  
Flowering Plants ◽  
Genomic Sequences ◽  
Rna Molecules ◽  
Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically associated with small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

Plant transposable elements: Their role in evolution

1988 ◽  
Vol 8 (6) ◽  
pp. 585-588 ◽  
Author(s):  
Heinz Saedler
Keyword(s):  
Transposable Elements ◽  
Biological Significance ◽  
Normal Plant ◽  
Wild Type ◽  
Induced Mutations ◽  
Plant Genomes ◽  
Plant Genes ◽  
Structure And Functions

Transposable elements (TE) are natural constituents of plant genomes. However, their presence only becomes apparent if they become dislodged from their resident positions in the genome and transpore into another gene, thereby inducing a mutation. Such TE-induced mutations are somatically unstable because they revert to wild type and hence reconstitute the expression of the mutated gene. The frequent somatic excision of the TE results in a variegated phenotype. Since this instability is inherited in a Mendelian manner the variegated phenotype is nuclear determined. By this criterion TE have been shown to occur in more than 30 species belonging to different families and genera. Many questions arise when dealing with TE: their structure and functions, and the biological significance of the activity of elements in the differentiation of a normal plant or in the evolution of plant genes.

scholarly journals Epigenetic Regulation of A Heat-Activated Retrotransposon in Cruciferous Vegetables

2017 ◽  
Author(s):  
Kosuke Nozawa ◽  
Yuki Kawagishi ◽  
Akira Kawabe ◽  
Mio Sato ◽  
Yukari Masuta ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Environmental Stress ◽  
Epigenetic Regulation ◽  
Copy Number ◽  
Brassica Species ◽  
Cruciferous Vegetables ◽  
Brussels Sprout ◽  
Plant Genomes ◽  
Multiple Copies

Transposable elements (TEs) are highly abundant in plant genomes. Environmental stress is one of the critical stimuli that activate TEs. We analyzed a heat-activated retrotransposon named ONSEN in cruciferous vegetables. The multiple copies of ONSEN-like elements (OLEs) were found in all the cruciferous vegetables that were analyzed. The copy number of OLE was abundant in Brassica oleracea, which includes cabbage, cauliflower, broccoli, Brussels sprout, and kale. Phylogenic analysis demonstrated that some OLEs transposed after the allopolyploidization of parental Brassica species. Furthermore, we found that the increasing number of OLEs in B. oleracea appeared to be induced transpositional silencing by epigenetic regulation, including DNA methylation. The results of this study would be relevant to the understanding of evolutionary adaptations to thermal environmental stress in different species.

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