Chromatin regulates expression of small RNAs to help maintain transposon methylome homeostasis in Arabidopsis
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ABSTRACT:
ORGANISM(S): Arabidopsis thaliana
PROVIDER: GSE152971 | GEO | 2020/06/25
REPOSITORIES: GEO
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Project description:BACKGROUND:Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes. However, chromatin is dynamic during growth and development and must be properly re-established after its decondensation. Small interfering RNAs (siRNAs) promote heterochromatin formation, but little is known about how chromatin regulates siRNA expression. RESULTS:We demonstrate that thousands of transposable elements (TEs) produce exceptionally high levels of siRNAs in Arabidopsis thaliana embryos. TEs generate siRNAs throughout embryogenesis according to two distinct patterns depending on whether they are located in euchromatic or heterochromatic regions of the genome. siRNA precursors are transcribed in embryos, and siRNAs are required to direct the re-establishment of DNA methylation on TEs from which they are derived in the new generation. Decondensed chromatin also permits the production of 24-nt siRNAs from heterochromatic TEs during post-embryogenesis, and siRNA production from bipartite-classified TEs is controlled by their chromatin states. CONCLUSIONS:Decondensation of heterochromatin in response to developmental, and perhaps environmental, cues promotes the transcription and function of siRNAs in plants. Our results indicate that chromatin-mediated siRNA transcription provides a cell-autonomous homeostatic control mechanism to help reconstitute pre-existing chromatin states during growth and development including those that ensure silencing of TEs in the future germ line.
| S-EPMC7499886 | biostudies-literature
Project description:Transposable elements (TEs) and repetitive sequences comprise over 40% of rice genome. Different TEs are tightly regulated by distinct epigenetic mechanisms. For example, the activities of LTR retrotransposon Tos17 and non-LTR retrotransposon LINE element Karma are uniquely regulated by histone H3K9 methylation and histone H3K4 demethylation, respectively. Miniature inverted repeat transposable elements (MITEs) are one of the most high-copy-number DNA transposons, which are interspersed around rice genome and might influence nearby gene expression. In plants, 24-nucleotide (24-nt) heterochromatic small interfering RNAs (hc-siRNAs) derived from repeats and TEs. To what extent hc-siRNA associated TEs affect gene expression and therefore contribute to agricultural traits in rice remains elusive. Here, we show that OsDCL3a, one of Dicer-Like 3 (DCL3) homolog, is primarily responsible for 24-nt hc-siRNA processing in rice. Impaired OsDCL3a displayed altered important agricultural traits in rice. We found that genome-wide (281,563) 24-nt hc-siRNA clusters were OsDCL3a-dependent, among which MITEs were significantly enriched. Impaired OsDCL3a caused significant overlapping between reduced hc-siRNAs from MITEs and elevated nearby gene expression. Intriguingly, genes involved in Gibberellin and Brassinosteroid homeostasis were identified as direct targets of OsDCL3a, which may attribute to dwarfism and enlarged flag leaf angle upon OsDCL3a deficiency. Our work uncovers OsDCL3a-dependent hc-siRNAs derived from MITEs as broad spectrum of regulators for fine-tuning gene expression, and this observation may reflect a conserved mechanism in other higher plants with dispersed repeat- or TE-rich genomes. Examination of OsDCL3a-dependent hc-siRNAs derived from MITEs.
2014-02-04 | E-GEOD-50778 | biostudies-arrayexpress
Project description:The control of transposable element (TE) activity in germ cells provides genome integrity over generations. A distinct small RNA-mediated pathway utilizing Piwi-interacting RNAs (piRNAs) suppresses TE expression in gonads of metazoans. In the fly, primary piRNAs derive from so-called piRNA clusters, which are enriched in damaged repeated sequences. These piRNAs launch a cycle of TE and piRNA cluster transcript cleavages resulting in the amplification of piRNA and TE silencing. Using genome-wide comparison of TE insertions and ovarian small RNA libraries from two Drosophila strains, we found that individual TEs inserted into euchromatic loci form novel dual-stranded piRNA clusters. Formation of the piRNA-generating loci by active individual TEs provides a more potent silencing response to the TE expansion. Like all piRNA clusters, individual TEs are also capable of triggering the production of endogenous small interfering (endo-si) RNAs. Small RNA production by individual TEs spreads into the flanking genomic regions including coding cellular genes. We show that formation of TE-associated small RNA clusters can down-regulate expression of nearby genes in ovaries. Integration of TEs into the 3' untranslated region of actively transcribed genes induces piRNA production towards the 3'-end of transcripts, causing the appearance of genic piRNA clusters, a phenomenon that has been reported in different organisms. These data suggest a significant role of TE-associated small RNAs in the evolution of regulatory networks in the germline. The fractions of small RNAs (19-29 nt) from ovaries of y[1]; cn[1] bw[1] sp[1] line of Drosophila melanogaster were sequenced using Illumina HiSeq 2000.
2014-02-07 | E-GEOD-46105 | biostudies-arrayexpress
Project description:Eukaryotic DNA methylation is found in silent transposable elements and active genes. Nucleosome remodelers of the DDM1/Lsh family are thought to be specifically required to maintain transposon methylation, but the reason for this is unknown. Here, we find that a chromatin gradient that extends from the most heterochromatic transposons to euchromatic genes determines the requirement of DDM1 for methylation maintenance in all sequence contexts. We also show that small RNA-directed DNA methylation (RdDM) is inhibited by heterochromatin and absolutely requires the nucleosome remodeler DRD1. DDM1 and RdDM independently mediate nearly all transposon methylation, which is catalyzed by the methyltransferases MET1 (CG), CMT3 (CHG), DRM2 (CHH) and CMT2 (CHH), and collaborate to repress transposition and regulate the methylation and expression of genes. Our results indicate that the Arabidopsis genome is defined by a heterochromatic continuum that governs the access of DNA methyltransferases and potentially all DNA binding proteins. Examination of DNA methylation, transcription and nucleosomes in Arabidopsis wild-type and/or ddm1, RdDM and DNA methylase mutants.
2013-04-17 | E-GEOD-41302 | biostudies-arrayexpress
Project description:RNA polymerase IV (Pol IV) transcribes transposable elements (TEs) into precursors for small interfering RNAs (siRNAs) that guide DNA methylation to silence these potentially dangerious mobile elements in plants. Pol IV is recruited to TEs via SNF2-like CLASSY (CLSY) proteins. How Pol IV evolved to partner with the CLSYs is unknown. Using phylogenetics, we identified a conserved CYC-YPMF motif that is specific to Pol IV’s largest subunit. Modeling predicts that this motif coordinates a zinc ion and is exposed near Pol IV’s surface in a domain contacting downstream DNA. Via immunoprecipitation and mass spectrometry we found that this motif is essential for the association of all four CLSYs with Pol IV and hereby designate it as a CLSY-docking motif. Consistent with these biochemical results, mutations in the CLSY-docking motif or in neighboring sites of the Pol IV clamp domain, phenocopy pol iv null mutants and display a near-total loss of siRNA biogenesis, resulting in defects in DNA methylation and TE silencing. Together, our findings provide structural and functional insights into a critical protein feature that distinguishes Pol IV from other RNA polymerases, allowing Pol IV to target, transcribe and limit the expression of TE regions, thereby protecting genome integrity.
2024-11-28 | PXD047743 | Pride
Project description:Heterochromatin is believed to be associated with increased levels of cytosine methylation. With the recent availability of genome-wide, high-resolution molecular data reflecting cytosine methylation or heterochromatic organization, such relationships can be explored systematically. As a well-defined surrogate for heterochromatin, we tested the relationship between DNA replication timing and cytosine methylation in two human cell types, unexpectedly finding that the later-replicating, more heterochromatic regions to be less methylated than early-replicating regions. When we integrated gene expression data into the study, we found that regions of increased gene expression were earlier replicating, as previously identified, and that transcription-targeted cytosine methylation (TTCM) in gene bodies accounts for the positive correlation with early replication. A Self-Organising Map (SOM) approach was able to identify genomic regions with early replication and increased methylation but lacking annotated transcripts, which would have been missed in simple two variable analyses and may encode unrecognized intergenic transcripts. We conclude that the relationship of cytosine methylation with heterochromatin is not simple, and depends on whether the genomic context is tandemly-repetitive sequences often found near centromeres, which are known to be heterochromatic and methylated, or the remaining majority of the genome, where cytosine methylation is targeted preferentially to the transcriptionally-active, euchromatic compartment of the genome.
2011-08-06 | GSE27537 | GEO
Project description:Eukaryotic DNA methylation is found in silent transposable elements and active genes. Nucleosome remodelers of the DDM1/Lsh family are thought to be specifically required to maintain transposon methylation, but the reason for this is unknown. Here, we find that a chromatin gradient that extends from the most heterochromatic transposons to euchromatic genes determines the requirement of DDM1 for methylation maintenance in all sequence contexts. We also show that small RNA-directed DNA methylation (RdDM) is inhibited by heterochromatin and absolutely requires the nucleosome remodeler DRD1. DDM1 and RdDM independently mediate nearly all transposon methylation, which is catalyzed by the methyltransferases MET1 (CG), CMT3 (CHG), DRM2 (CHH) and CMT2 (CHH), and collaborate to repress transposition and regulate the methylation and expression of genes. Our results indicate that the Arabidopsis genome is defined by a heterochromatic continuum that governs the access of DNA methyltransferases and potentially all DNA binding proteins.
2013-04-17 | GSE41302 | GEO
Project description:We study the relatively unexplored evolutionary consequences of the epigenetic effects of transpoable elements (TEs) by providing the first genome-wide quantification of such effects in wild-derived D. melanogaster and D. simulans strains. Surprisingly, over half of euchromatic TEs show spread of repressive epigenetic marks to nearby DNA, resulting in differential epigenetic states of homologous genic alleles and, in return, selection against TEs. Interestingly, compared to D. melanogaster, the lower TE content in D. simulans is correlated with stronger epigenetic effects of TEs and higher levels of host genetic factors known to promote epigenetic silencing. We conclude that the epigenetic effects of euchromatic TEs, and host genetic factors modulating such effects, play a critical role in the population dynamics of TEs within and between species.
2017-07-01 | GSE94741 | GEO
Project description:We study the relatively unexplored evolutionary consequences of the epigenetic effects of transpoable elements (TEs) by providing the first genome-wide quantification of such effects in wild-derived D. melanogaster and D. simulans strains. Surprisingly, over half of euchromatic TEs show spread of repressive epigenetic marks to nearby DNA, resulting in differential epigenetic states of homologous genic alleles and, in return, selection against TEs. Interestingly, compared to D. melanogaster, the lower TE content in D. simulans is correlated with stronger epigenetic effects of TEs and higher levels of host genetic factors known to promote epigenetic silencing. We conclude that the epigenetic effects of euchromatic TEs, and host genetic factors modulating such effects, play a critical role in the population dynamics of TEs within and between species.
2017-07-01 | GSE94735 | GEO
Project description:Chromatin regulates expression of small RNAs to help maintain transposon methylome homeostasis in Arabidopsis
| PRJNA641096 | ENA