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Reconstructing de novo silencing of an active plant retrotransposon: dynamics, mechanisms, biological implications

ABSTRACT: In plants, maintenance-methylation mediated by METHYLTRANSFERASE-1 (MET1), siRNA-directed de-novo methylation, and chromatin remodeling by DECREASE IN DNA METHYLATION -1 (DDM1) promote transcriptional gene-silencing of transposable elements (TEs). This process is mostly investigated at steady states reflecting how long-established silent conditions are maintained, faithfully re-iterated or temporarily modified during growth, stress and over generations. How invasive TEs are detected and silenced de novo, however, remains largely unknown. Using inbred lineages of hybrid Arabidopsis epigenomes combining wild-type and met1 or ddm1 chromosomes, we have deciphered the timing, spatial distribution and mechanisms underpinning the proliferation and eventual demise of the endogenous retrotransposon évadé (EVD). Both developmental and molecular features of EVD biology, including a remarkable ability to evade RNA interference, ultimately contribute to its silencing over multiple generations. The underlying processes are accompanied by widespread diversification of the Arabidopsis genome and de-novo epiallelism creating an extensive reservoir of selectable and potentially adaptive traits. Differential expression of EVADE small RNAs between three generations of one specific Col0 met1 derived EpiRIL.

ORGANISM(S): Arabidopsis thaliana

SUBMITTER: Antonin Marchais

PROVIDER: E-GEOD-43412 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Reconstructing de novo silencing of an active plant retrotransposon: dynamics, mechanisms, biological implications

Project description:In plants, maintenance-methylation mediated by METHYLTRANSFERASE-1 (MET1), siRNA-directed de-novo methylation, and chromatin remodeling by DECREASE IN DNA METHYLATION -1 (DDM1) promote transcriptional gene-silencing of transposable elements (TEs). This process is mostly investigated at steady states reflecting how long-established silent conditions are maintained, faithfully re-iterated or temporarily modified during growth, stress and over generations. How invasive TEs are detected and silenced de novo, however, remains largely unknown. Using inbred lineages of hybrid Arabidopsis epigenomes combining wild-type and met1 or ddm1 chromosomes, we have deciphered the timing, spatial distribution and mechanisms underpinning the proliferation and eventual demise of the endogenous retrotransposon évadé (EVD). Both developmental and molecular features of EVD biology, including a remarkable ability to evade RNA interference, ultimately contribute to its silencing over multiple generations. The underlying processes are accompanied by widespread diversification of the Arabidopsis genome and de-novo epiallelism creating an extensive reservoir of selectable and potentially adaptive traits.

2013-07-02 | GSE43412 | GEO

Arabidopsis small RNAs associated with RDR6-dependent RNA-directed DNA Methylation

Project description:Background: The majority of plant transposable elements (TEs) are found in a silenced state that is epigenetically propagated by the maintenance of symmetrical DNA methylation. TE methylation is established and reinforced by a mechanism of RNA-dependent DNA methylation, which is dependent on transcription of the PolIV RNA polymerase. Recently, a pathway has been described that initiates de novo DNA methylation dependent on components of the RNAi post-transcriptional silencing pathway, independent of PolIV. To define the function of this new pathway, we have focused on the RDR6 protein, which plays a central role in the pathway we refer to as RDR6-dependent RNA-directed DNA Methylation (RDR6-RdDM). Methods: We have sequenced total small RNAs from wild-type and three mutant genotypes: ddm1, ddm1/rdr6, and rdr6. Conclusions: We demonstrate that RDR6-RdDM utilizes 21 and 22 nucleotide siRNAs to de novo methylate actively transcribing TEs. In addition, we find that the RDR6-RdDM pathway functions in the efficient initiation and re-establishment of TE transcriptional silencing, while it is not necessary to maintain trans-generational epigenetic silencing. Examination of flower bud small RNAs from wild-type and 3 mutant genotypes

2013-04-11 | E-GEOD-41755 | biostudies-arrayexpress

Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells

Project description:Transposable elements (TEs), whose propagation can result in severe damage to the host genome, are silenced in the animal gonad by Piwi-interacting RNAs (piRNAs). piRNAs produced in the ovaries are deposited in the embryonic germline and initiate TE repression in the germline progeny. Whether the maternally transmitted piRNAs play a role in the silencing of somatic TEs is, however, unknown. Here we show that maternally transmitted piRNAs from the tirant retrotransposon in Drosophila are required for the somatic silencing of the TE and correlate with an increase in histone H3K9 trimethylation an active tirant copy. Comparison of tirant piRNAs in two Drosophila simulans natural populations.

2013-04-09 | E-GEOD-40592 | biostudies-arrayexpress

Small RNA sequencing from Arabidopsis adult leaves and profiling of Arabidopsis transcripts in response to flg22 peptide

Project description:DNA methylation is an epigenetic mark that silences transposable elements (TEs) and repeats. Whereas the establishment and maintenance of DNA methylation are relatively well understood, little is known on their dynamics and biological relevance in plant and animal innate immunity. Here, we show that some TEs are demethylated and transcriptionally reactivated during antibacterial defense in Arabidopsis. This effect is concomitant with the down-regulation of key transcriptional gene silencing factors as well as an active demethylation process. DNA demethylation restricts multiplication and vascular propagation of the bacterial pathogen Pseudomonas syringae in leaves and, accordingly, some immune-response genes, containing repeats in their promoters, are negatively regulated by DNA methylation. This study provides evidence that DNA demethylation is part of a plant-induced immune response, potentially acting to prime transcriptional activation of some defense genes linked to Tes/repeats. We have monitored the transcript changes in Arabidopsis plants treated with a flagellin-derived peptide. DNA methylation is closely related to 24nt sRNAs. This is why we sequenced small RNA population in our study. 5-week-old Col-0 leaf samples (treated with either water or flg22 at 1 ?M concentration for 6 h) and deep sequenced by Fasteris (Geneva) on the Illumina HiSeq 2000 platform.

2013-02-04 | E-GEOD-40044 | biostudies-arrayexpress

Arabidopsis small RNAs associated with RDR6-dependent RNA-directed DNA Methylation

2013-04-11 | GSE41755 | GEO

MicroRNA-dependent transposable element transcriptional silencing in Drosophila somatic ovarian cells [RNA-Seq]

Project description:RNAi-related silencing mechanisms concern as diverse biological processes as gene regulation, mostly via the miRNA pathway, and defense against molecular parasites, mainly controlled by the siRNA and the piRNA pathways. In Drosophila somatic ovarian cells, transposable elements (TEs) are repressed by chromatin changes induced by Piwi-interacting RNAs (piRNAs). We show here that a functional miRNA pathway is required for this piRNA-mediated TE transcriptional silencing to operate in this tissue. A general miRNA depletion, caused by tissue- and stage-specific knock-down of either drosha (involved in miRNA biogenesis) or AG01 and gawky (both responsible for miRNA activity) resulted in chromatin-mediated TE transcriptional desilencing and piRNA loss. For unknown reasons, the amount of piRNA produced by the traffic jam 3' UTR was apparently unaffected in miRNA-defective somatic ovarian cells. Although weaker, similar phenotypes could also be observed upon individual titration (by expression of the complementary miR-sponge) of at least three miRNAs, miR-14, miR-34 and miR-989. This work adds the maintenance of genome stability, via the piRNA-mediated TE repression, to the list of the already reported miRNA-controlled biological functions. Study of small regulatory RNA populations present in ovaries expressing either wild-type Drosha protein or the trans-dominant negative Drosha protein coupled or not with the Tub-GAL80[ts]GAL4 inhibitor.

2015-04-08 | E-GEOD-60972 | biostudies-arrayexpress

A balance of de novo and maintenance activities governs epigenetic inheritance of CG methylation in Arabidopsis transposons

Project description:Dnmt1/MET1 methyltransferases mediate the epigenetic inheritance of cytosine methylation within CG dinucleotides (mCG). These enzymes use a semiconservative mechanism previously expected to produce binary present/absent methylation patterns. However, we show here that in Arabidopsis thaliana h1ddm1 mutants, intermediate heterochromatic mCG is quantitatively associated with transposon expression and is stably inherited across many generations. We develop a mathematical model that estimates the rates of semiconservative maintenance failure and de novo methylation at each transposon, demonstrating that mCG can be stably inherited at any level via a dynamical balance of these activities. We find that DRM2 – the core methyltransferase of the RNA-directed DNA methylation pathway – catalyzes most of the heterochromatic de novo mCG, with de novo rates orders of magnitude higher than previously thought, whereas chromomethylases make smaller contributions. Our results demonstrate that mCG epigenetic inheritance in plant heterochromatin is highly dynamic, with CG sites frequently switching methylation states.

2023-02-17 | GSE197718 | GEO

Methyl DIP-chip from self-pollinated ddm1 mutant and ddm1 kyp double mutant

Project description:Methylation of histone H3 lysine 9 (H3K9me) and small RNA are associated with constitutively silent chromatin in diverse eukaryotes including plants. In plants, silent transposons are also marked by cytosine methylation, especially at non-CpG sites. The transposon-specific non-CpG methylation in plants is controlled by small RNA and H3K9me. Although it is often assumed that small RNA directs H3K9me,　interaction between small RNA and H3K9me has not been directly shown in plants. We have previously shown that a mutation in a chromatin remodeling gene DDM1 (decrease in DNA methylation) induces a global decrease as well as local increase of cytosine methylation and accumulation of small RNA in a locus called BONSAI. Here we show that the de novo BONSAI methylation does not depend on RNAi but depends on H3K9me. Notably, in mutant of H3K9 methylase gene KRYPTONITE or H3K9me-dependent DNA methylase gene CHROMOMETHYALSE3, the ddm1-induced de novo cytosine methylation was abolished for all three contexts, CpG, CpHpG, and CpHpH. Furthermore, RNAi mutants showed strong developmental defects when combined with ddm1 mutation. Our results revealed unexpected interactions of epigenetic modifications, which could be conserved among diverse eukaryotes. comparison of DNA methylation between WT, 2G ddm1 (2 replications), 8G ddm1 (2 replications), and 8G ddm1 kyp

2011-12-25 | E-GEOD-34222 | biostudies-arrayexpress

RTEL1 modulates H3 occupancy in heterochromatic regions and acts synergistically with MET1/DDM1 to maintain genome integrity

Project description:RTEL1 mainly mediates histone H3 occupancy in heterochromatic regions and functions in parallel with DDM1 and MET1 to maintain genome integrity.

2019-09-06 | GSE86447 | GEO

DDM1/Lsh remodelers allow methylation of DNA wrapped in nucleosomes

Project description:Eukaryotic DNA is wrapped around histone octamers to form nucleosomes, which are separated by linker DNA bound by histone H1. In many species, the DNA exhibits methylation of CG dinucleotides, which is epigenetically inherited via a semiconservative mechanism. How methyltransferases access DNA within nucleosomes remains mysterious. Here we show that methylation of nucleosomes requires DDM1/Lsh nucleosome remodelers in Arabidopsis thaliana and mouse. We also show that removal of histone H1, which partially restores methylation in ddm1 mutants, does so primarily in the linker DNA between nucleosomes. In h1ddm1 compound mutants, substantial portions of the genome exhibit dramatically periodic methylation that approaches wild-type levels in linker DNA but is virtually absent in nucleosomes. We also present evidence that de novo methylation supplements semiconservative maintenance of CG methylation across generations. Overall, our results demonstrate that nucleosomes and H1 are barriers to DNA methylation, which are overcome by DDM1/Lsh nucleosome remodelers.

2017-11-15 | GSE96994 | GEO

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