SAC3B, a central component of the mRNA export complex TREX-2, is required for prevention of epigenetic gene silencing in Arabidopsis

Epigenetic regulation is important for organismal development and response to the environment. Alteration in epigenetic status has been known mostly from the perspective of enzymatic actions of DNA methylation and/or histone modifications. In a genetic screen for cellular factors involved in preventing epigenetic silencing, we isolated an Arabidopsis mutant defective in SAC3B, a component of the conserved TREX-2 complex that couples mRNA transcription with nuleo-cytoplasmic export. Arabidopsis SAC3B dysfunction causes gene silencing at transgenic and endogenous loci, accompanied by elevation in the repressive histone mark H3K9me2 and by reduction in RNA polymerase Pol II occupancy. SAC3B dysfunction does not alter promoter DNA methylation level of the transgene d35S::LUC, although the DNA demethylase ROS1 is also required for d35S::LUC anti-silencing. THP1 and NUA were identified as SAC3B-associated proteins whose mutations also caused d35S::LUC silencing. RNA-DNA hybrid exists at the repressed loci but is unrelated to gene suppression by the sac3b mutation. Genome-wide analyses demonstrated minor but clear involvement of SAC3B in regulating siRNAs and DNA methylation, particularly at a group of TAS and TAS-like loci. Together our results revealed not only a critical role of mRNA-export factors in transcriptional anti-silencing but also the contribution of SAC3B in shaping plant epigenetic landscapes.

• Publication year

  2016

• Venue

  Nucleic Acids Research

• Publication date

  2016-09-26

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1093/nar/gkw850PMID 27672037PMCID 5224508
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• SUVH1, a Su(var)3–9 family member, promotes the expression of genes targeted by DNA methylation

  2015influential reference
• The methyl-CpG-binding protein MBD7 facilitates active DNA demethylation to limit DNA hyper-methylation and transcriptional gene silencing.

  2015cited by this paper
• Nucleic Acids Research

  2015cited by this paper
• HYPER RECOMBINATION1 of the THO/TREX Complex Plays a Role in Controlling Transcription of the REVERSION-TO-ETHYLENE SENSITIVITY1 Gene in Arabidopsis

  2015cited by this paper
• The Nuclear Pore-Associated TREX-2 Complex Employs Mediator to Regulate Gene Expression

  2015cited by this paper
• Regulatory link between DNA methylation and active demethylation in Arabidopsis

  2015cited by this paper
• RNA-mediated epigenetic regulation of gene expression

  2015cited by this paper
• RNA-directed DNA methylation: an epigenetic pathway of increasing complexity

  2014cited by this paper
• HTSeq—a Python framework to work with high-throughput sequencing data

  2014cited by this paper
• RNA-directed DNA methylation: an epigenetic pathway of increasing complexity

  2014cited by this paper
• Specific but interdependent functions for Arabidopsis AGO4 and AGO6 in RNA‐directed DNA methylation

  2014cited by this paper
• RNA-binding protein regulates plant DNA methylation by controlling mRNA processing at the intronic heterochromatin-containing gene IBM1

  2013cited by this paper
• R-Loop Stabilization Represses Antisense Transcription at the Arabidopsis FLC Locus

  2013cited by this paper
• R loops are linked to histone H3 S10 phosphorylation and chromatin condensation.

  2013cited by this paper
• Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1

  2013cited by this paper
• The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.

  2013cited by this paper
• DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV

  2013cited by this paper
• TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions

  2013cited by this paper
• Roles of DICER-LIKE and ARGONAUTE Proteins in TAS-Derived Small Interfering RNA-Triggered DNA Methylation1[W]

  2012cited by this paper
• DNA–RNA hybrid formation mediates RNAi‐directed heterochromatin formation

  2012cited by this paper
• A Histone Acetyltransferase Regulates Active DNA Demethylation in Arabidopsis

  2012cited by this paper
• BRAT-BW: efficient and accurate mapping of bisulfite-treated reads

  2012cited by this paper
• The nuclear pore complex and nuclear transport.

  2010cited by this paper
• Establishing, maintaining and modifying DNA methylation patterns in plants and animals

  2010cited by this paper
• Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis

  2010influential reference
• Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory.

  2010cited by this paper
• agriGO: a GO analysis toolkit for the agricultural community

  2010cited by this paper
• The Conserved RNA Trafficking Proteins HPR1 and TEX1 Are Involved in the Production of Endogenous and Exogenous Small Interfering RNA in Arabidopsis[C][W]

  2010cited by this paper
• Histone methylation in higher plants.

  2010cited by this paper
• Targeted 3′ Processing of Antisense Transcripts Triggers Arabidopsis FLC Chromatin Silencing

  2010cited by this paper
• Report for Polymerase V Transcripts and RNA-Directed DNA Methylation in Arabidopsis

  2010cited by this paper
• Ultrafast and memory-efficient alignment of short DNA sequences to the human genome

  2009cited by this paper
• edgeR: a Bioconductor package for differential expression analysis of digital gene expression data

  2009cited by this paper
• "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions.

  2009cited by this paper
• Sem1 is a functional component of the nuclear pore complex–associated messenger RNA export machinery

  2009cited by this paper
• Getting to the gate: crystallization of a Sac3(CID):Sus1:Cdc31 complex.

  2009cited by this paper
• Searching for SNPs with cloud computing

  2009cited by this paper
• SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6‐bodies

  2009cited by this paper
• Active DNA demethylation mediated by DNA glycosylases.

  2009cited by this paper
• Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin.

  2009cited by this paper
• An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants

  2008cited by this paper
• Kismeth: Analyzer of plant methylation states through bisulfite sequencing

  2008cited by this paper
• The THP1-SAC3-SUS1-CDC31 complex works in transcription elongation-mRNA export preventing RNA-mediated genome instability.

  2008cited by this paper
• Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading.

  2008cited by this paper
• Transposable elements and the epigenetic regulation of the genome

  2007cited by this paper
• Exporting RNA from the nucleus to the cytoplasm

  2007cited by this paper
• Genome-Wide Analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 Pathway in Arabidopsis Reveals Dependency on miRNA- and tasiRNA-Directed Targeting[W][OA]

  2007cited by this paper
• Role of RNA polymerase IV in plant small RNA metabolism

  2007cited by this paper
• H2A.Z-Mediated Localization of Genes at the Nuclear Periphery Confers Epigenetic Memory of Previous Transcriptional State

  2007cited by this paper
• CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing.

  2007cited by this paper
• The Nuclear Pore Protein AtTPR Is Required for RNA Homeostasis, Flowering Time, and Auxin Signaling1[C][W][OA]

  2007cited by this paper
• Impairment of transcription elongation by R-loops in vitro.

  2007cited by this paper
• Nuclear pore association confers optimal expression levels for an inducible yeast gene

  2006cited by this paper
• MicroRNA-Dependent Trans-Acting siRNA Production

  2005cited by this paper
• Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization.

  2004cited by this paper
• Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery.

  2004cited by this paper
• SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis.

  2004cited by this paper
• Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery

  2004cited by this paper
• Gene Recruitment of the Activated INO1 Locus to the Nuclear Membrane

  2004cited by this paper
• Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination.

  2003cited by this paper
• Two regulatory levels of transcriptional gene silencing in Arabidopsis

  2002cited by this paper
• ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase.

  2002cited by this paper
• Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing.

  2002cited by this paper
• Chromatin boundaries in budding yeast: the nuclear pore connection.

  2002cited by this paper
• The mRNA export machinery requires the novel Sac3p–Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores

  2002cited by this paper
• TREX is a conserved complex coupling transcription with messenger RNA export

  2002cited by this paper
• Stable mRNP Formation and Export Require Cotranscriptional Recruitment of the mRNA Export Factors Yra1p and Sub2p by Hpr1p

  2002cited by this paper
• The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene.

  2000cited by this paper
• Regulation of chromatin structure by site-specific histone H3 methyltransferases

  2000cited by this paper
• Yeast microarrays for genome wide parallel genetic and gene expression analysis.

  1997cited by this paper
• Sugar-Inducible Expression of a Gene for [beta]-Amylase in Arabidopsis thaliana

  1995cited by this paper
• Characterization of monoclonal antibody to DNA.RNA and its application to immunodetection of hybrids.

  1986cited by this paper
• Gene gating: a hypothesis.

  1985cited by this paper

• Mutation in THO2, a component of THO/TREX complex, causes transcriptional gene silencing and genome-wide DNA methylation changes.

  2026cites this paper
• Mutations in Components of the TREX‐2 Complex Result in Misexpression of the Kelch‐Domain F‐Box Protein KFB39 Promoter in Arabidopsis thaliana

  2025cites this paper
• SHH1 cooperates with the DNA methylation reader MBD7 to suppress transcriptional silencing of promoter-methylated genes in Arabidopsis

  2025cites this paper
• ZC3HC1 is a structural element of the nuclear basket effecting interlinkage of TPR polypeptides

  2022cites this paper
• Fine mapping and characterization of RLL6 locus required for anti-silencing of a transgene and DNA demethylation in Arabidopsis thaliana

  2022cites this paper
• Identification of quantitative trait loci for tillering, root, and shoot biomass at the maximum tillering stage in rice

  2022cites this paper
• Evolution and diversification of the nuclear pore complex

  2021cites this paper
• OsTPR boosts the superior grains through increase in upper secondary rachis branches without incurring a grain quality penalty

  2021cites this paper
• Nucleocytoplasmic Communication in Healthy and Diseased Plant Tissues

  2021influential citation
• HN1 interacts with γ-tubulin to regulate centrosomes in advanced prostate cancer cells

  2021cites this paper
• Structural Basis for the Functional Diversity of Centrins: A Focus on Calcium Sensing Properties and Target Recognition

  2021cites this paper
• Nuclear pore complex-mediated gene expression in Arabidopsis thaliana

  2020cites this paper
• Linking Key Steps of MicroRNA Biogenesis by TREX-2 and the Nuclear Pore Complex in Arabidopsis

  2020cites this paper
• SAC3B is a target of CML19, the centrin 2 of Arabidopsis thaliana.

  2019cites this paper
• Characterization and fine mapping of Arabidopsis RLL3, a locus required for DNA demethylation pathway

  2019cites this paper
• Genome-wide mapping reveals conserved and diverged R-loop activities in the unusual genetic landscape of the African trypanosome genome

  2018cites this paper
• RNA-DNA hybrid (R-loop) immunoprecipitation mapping: an analytical workflow to evaluate inherent biases

  2017influential citation
• The R-loop is a common chromatin feature of the Arabidopsis genome

  2017cites this paper
• Roles of Nuclear Pores and Nucleo-cytoplasmic Trafficking in Plant Stress Responses

  2017influential citation
• Dynamic regulation of DNA demethylation and RNA-directed DNA methylation in Arabidopsis

  2016cites this paper
• Edinburgh Research Explorer Genome-wide mapping reveals conserved and diverged R-loop activities in the unusual genetic landscape of the African trypanosome genome

  year unknowncites this paper