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RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA.

ABSTRACT: Ribonucleic acid-mediated transcriptional gene silencing (known as RNA-directed DNA methylation, or RdDM, in Arabidopsis thaliana) is important for influencing gene expression and the inhibition of transposons by the deposition of repressive chromatin marks such as histone modifications and DNA methylation. A key event in de novo methylation of DNA by RdDM is the production of long non-coding RNA (lncRNA) by RNA polymerase V (Pol V). Little is known about the events that connect Pol V transcription to the establishment of repressive chromatin modifications. Using RNA immunoprecipitation, we elucidated the order of events downstream of lncRNA production and discovered interdependency between lncRNA-associated proteins. We found that the effector protein ARGONAUTE4 (AGO4) binds lncRNA independent of the RNA-binding protein INVOLVED IN DE NOVO2 (IDN2). In contrast, IDN2 binds lncRNA in an AGO4-dependent manner. We further found that the de novo DNA methyltransferase DOMAINS REARRANGED METHYLTRANSFERASE2 (DRM2) also associates with lncRNA produced by Pol V and that this event depends on AGO4 and IDN2. We propose a model where the silencing proteins AGO4, IDN2 and DRM2 bind to lncRNA in a stepwise manner, resulting in DNA methylation of RdDM target loci.

SUBMITTER: Bohmdorfer G

PROVIDER: S-EPMC4321213 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA.

Böhmdorfer Gudrun G Rowley M Jordan MJ Kuciński Jan J Zhu Yongyou Y Amies Ivan I Wierzbicki Andrzej T AT

The Plant journal : for cell and molecular biology 20140623 2

Ribonucleic acid-mediated transcriptional gene silencing (known as RNA-directed DNA methylation, or RdDM, in Arabidopsis thaliana) is important for influencing gene expression and the inhibition of transposons by the deposition of repressive chromatin marks such as histone modifications and DNA methylation. A key event in de novo methylation of DNA by RdDM is the production of long non-coding RNA (lncRNA) by RNA polymerase V (Pol V). Little is known about the events that connect Pol V transcript ...[more]

PMID: 24862207

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Project description:RNA-directed DNA methylation (RdDM) is a biological process in which non-coding RNA molecules direct the addition of DNA methylation to specific DNA sequences. The RdDM pathway is unique to plants, although other mechanisms of RNA-directed chromatin modification have also been described in fungi and animals. To date, the RdDM pathway is best characterized within angiosperms (flowering plants), and particularly within the model plant Arabidopsis thaliana. However, conserved RdDM pathway components and associated small RNAs (sRNAs) have also been found in other groups of plants, such as gymnosperms and ferns. The RdDM pathway closely resembles other sRNA pathways, particularly the highly conserved RNAi pathway found in fungi, plants, and animals. Both the RdDM and RNAi pathways produce sRNAs and involve conserved Argonaute, Dicer and RNA-dependent RNA polymerase proteins. RdDM has been implicated in a number of regulatory processes in plants. The DNA methylation added by RdDM is generally associated with transcriptional repression of the genetic sequences targeted by the pathway. Since DNA methylation patterns in plants are heritable, these changes can often be stably transmitted to progeny. As a result, one prominent role of RdDM is the stable, transgenerational suppression of transposable element (TE) activity. RdDM has also been linked to pathogen defense, abiotic stress responses, and the regulation of several key developmental transitions. Although the RdDM pathway has a number of important functions, RdDM-defective mutants in Arabidopsis thaliana are viable and can reproduce, which has enabled detailed genetic studies of the pathway. However, RdDM mutants can have a range of defects in different plant species, including lethality, altered reproductive phenotypes, TE upregulation and genome instability, and increased pathogen sensitivity. Overall, RdDM is an important pathway in plants that regulates a number of processes by establishing and reinforcing specific DNA methylation patterns, which can lead to transgenerational epigenetic effects on gene expression and phenotype.

Dataset Information

RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA.

Publications

RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA.

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