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An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation

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      Abstract

      DNA methylation is an important epigenetic mark in many eukaryotes 1- 5. In plants, 24-nt small interfering RNAs (siRNAs) bound to the effector protein, Argonaute 4 (AGO4) can direct de novo DNA methylation by the methyltransferase DRM2 2, 4- 6. Here we report a new regulator of RNA-directed DNA methylation (RdDM) in Arabidopsis: RDM1. Loss-of-function mutations in the RDM1 gene impair the accumulation of 24-nt siRNAs, reduce DNA methylation, and release transcriptional gene silencing at RdDM target loci. RDM1 encodes a small protein that appears to bind single-stranded methyl DNA, and associates and co-localizes with RNA polymerase II, AGO4 and DRM2 in the nucleus. Our results suggest that RDM1 is a component of the RdDM effector complex and may play a role in linking siRNA production with pre-existing or de novo cytosine methylation. Our results also suggest that although RDM1 and Pol V may function together at some RdDM target sites in the peri-nucleolar siRNA processing center, Pol II rather than Pol V is associated with the RdDM effector complex at target sites in the nucleoplasm.

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      Most cited references 33

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      Highly integrated single-base resolution maps of the epigenome in Arabidopsis.

      Deciphering the multiple layers of epigenetic regulation that control transcription is critical to understanding how plants develop and respond to their environment. Using sequencing-by-synthesis technology we directly sequenced the cytosine methylome (methylC-seq), transcriptome (mRNA-seq), and small RNA transcriptome (smRNA-seq) to generate highly integrated epigenome maps for wild-type Arabidopsis thaliana and mutants defective in DNA methyltransferase or demethylase activity. At single-base resolution we discovered extensive, previously undetected DNA methylation, identified the context and level of methylation at each site, and observed local sequence effects upon methylation state. Deep sequencing of smRNAs revealed a direct relationship between the location of smRNAs and DNA methylation, perturbation of smRNA biogenesis upon loss of CpG DNA methylation, and a tendency for smRNAs to direct strand-specific DNA methylation in regions of RNA-DNA homology. Finally, strand-specific mRNA-seq revealed altered transcript abundance of hundreds of genes, transposons, and unannotated intergenic transcripts upon modification of the DNA methylation state.
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        RNA silencing in plants.

        There are at least three RNA silencing pathways for silencing specific genes in plants. In these pathways, silencing signals can be amplified and transmitted between cells, and may even be self-regulated by feedback mechanisms. Diverse biological roles of these pathways have been established, including defence against viruses, regulation of gene expression and the condensation of chromatin into heterochromatin. We are now in a good position to investigate the full extent of this functional diversity in genetic and epigenetic mechanisms of genome control.
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          Epigenetic reprogramming and small RNA silencing of transposable elements in pollen.

          The mutagenic activity of transposable elements (TEs) is suppressed by epigenetic silencing and small interfering RNAs (siRNAs), especially in gametes that could transmit transposed elements to the next generation. In pollen from the model plant Arabidopsis, we show that TEs are unexpectedly reactivated and transpose, but only in the pollen vegetative nucleus, which accompanies the sperm cells but does not provide DNA to the fertilized zygote. TE expression coincides with downregulation of the heterochromatin remodeler decrease in DNA methylation 1 and of many TE siRNAs. However, 21 nucleotide siRNAs from Athila retrotransposons are generated and accumulate in pollen and sperm, suggesting that siRNA from TEs activated in the vegetative nucleus can target silencing in gametes. We propose a conserved role for reprogramming in germline companion cells, such as nurse cells in insects and vegetative nuclei in plants, to reveal intact TEs in the genome and regulate their activity in gametes.
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            Author and article information

            Affiliations
            [1 ]Institute for Integrative Genome Biology and Department of Botany and Plant Sciences, University of California, Riverside, CA 92521
            [2 ]School of life science and technology, Tongji University, Shanghai 200092, China
            [3 ]Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, 1030 Vienna, Austria
            [4 ]Biology Department, Washington University, Campus Box 1137, One Brookings Drive, St Louis, MO 63130
            [5 ]Center for Plant Stress Genomics and Technology, 4700 King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia
            [6 ]Max F. Perutz Laboratory, Medical University of Vienna, 1030 Vienna, Austria
            [7 ]LGDP, CNRS/IRD/Université de Perpignan, UMR 5096, Perpignan, France
            [8 ]Institute for Integrative Genome Biology and Department of Plant Pathology, University of California, Riverside, California 92521
            [9 ]Department of Biology and Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405
            Author notes
            Correspondence and requests for materials should be addressed to J.K.Z. ( jian-kang.zhu@ 123456ucr.edu )

            *These authors contributed equally.

            Journal
            0410462
            6011
            Nature
            Nature
            0028-0836
            1476-4687
            2 April 2010
            21 April 2010
            6 May 2010
            6 November 2010
            : 465
            : 7294
            : 106-109
            2865564
            20410883
            10.1038/nature09025
            nihpa190934

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            Funding
            Funded by: National Institute of General Medical Sciences : NIGMS
            Award ID: R01 GM070795-06S1 ||GM
            Funded by: National Institute of General Medical Sciences : NIGMS
            Award ID: R01 GM070795-06 ||GM
            Funded by: National Institute of General Medical Sciences : NIGMS
            Award ID: R01 GM059138-12 ||GM
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