Abstract
RNA molecules such as small-interfering RNAs (siRNAs) and antisense RNAs (asRNAs) trigger chromatin silencing of target loci. In the model plant Arabidopsis, RNA–triggered chromatin silencing involves repressive histone modifications such as histone deacetylation, histone H3 lysine-9 methylation, and H3 lysine-27 monomethylation. Here, we report that two Arabidopsis homologs of the human histone-binding proteins Retinoblastoma-Associated Protein 46/48 (RbAp46/48), known as MSI4 (or FVE) and MSI5, function in partial redundancy in chromatin silencing of various loci targeted by siRNAs or asRNAs. We show that MSI5 acts in partial redundancy with FVE to silence FLOWERING LOCUS C (FLC), which is a crucial floral repressor subject to asRNA–mediated silencing, FLC homologs, and other loci including transposable and repetitive elements which are targets of siRNA–directed DNA Methylation (RdDM). Both FVE and MSI5 associate with HISTONE DEACETYLASE 6 (HDA6) to form complexes and directly interact with the target loci, leading to histone deacetylation and transcriptional silencing. In addition, these two genes function in de novo CHH (H = A, T, or C) methylation and maintenance of symmetric cytosine methylation (mainly CHG methylation) at endogenous RdDM target loci, and they are also required for establishment of cytosine methylation in the previously unmethylated sequences directed by the RdDM pathway. This reveals an important functional divergence of the plant RbAp46/48 relatives from animal counterparts.
Highlights
Cytosine DNA methylation is critical for stable silencing of transposable elements (TE) and repetitive sequences and for epigenetic regulation of endogenous gene expression in eukaryotes [1,2,3]
In Arabidopsis, the plant-specific RNA polymerase Pol IV is thought to initiate silencing by generating single-stranded RNA transcripts that are subsequently converted to double-stranded RNAs by RNA-DEPENDENT RNA POLYMERASE 2 (RDR2). dsRNAs are processed by DICER 3 (DCL3) to produce 24-nt small-interfering RNAs (siRNAs), which are subsequently loaded to an ARGONAUTE 4 (AGO4)containing effector complex known as RISC
Using a candidate-gene approach, we explored whether FVE and/or MSI5 could associate with HISTONE DEACETYLASE 6 (HDA6), an histone deacetylase (HDAC) that has been shown to be involved in FLOWERING LOCUS C (FLC) repression, DNA methylation maintenance and gene silencing in Arabidopsis [11,13,49]
Summary
Cytosine DNA methylation is critical for stable silencing of transposable elements (TE) and repetitive sequences and for epigenetic regulation of endogenous gene expression in eukaryotes [1,2,3]. In the model plant Arabidopsis, cytosine methylation occurs in three different sequence contexts: CG, CHG and CHH. DsRNAs are processed by DICER 3 (DCL3) to produce 24-nt siRNAs, which are subsequently loaded to an ARGONAUTE 4 (AGO4)containing effector complex known as RISC (for RNA-Induced Silencing Complex). Through their interaction with long noncoding RNA transcripts from target loci, generated by the RNA polymerase Pol V, the loaded RISC complexes in association with DRM2 are targeted to RdDM target loci to establish cytosine methylation in CG, CHG and CHH contexts, leading to heterochromatin formation and transcriptional silencing [for reviews, see [2,4]]
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