skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The CCR4‐NOT complex component NOT1 regulates RNA‐directed DNA methylation and transcriptional silencing by facilitating Pol IV‐dependent siRNA production

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.14818· OSTI ID:1635067
 [1];  [1];  [1];  [1];  [1];  [2];  [1]; ORCiD logo [3]
  1. National Institute of Biological Sciences Beijing 102206 China
  2. Shanghai Center for Plant Stress Biology and Center of Excellence for Molecular Plant Sciences Chinese Academy of Sciences Shanghai 201602 China
  3. National Institute of Biological Sciences Beijing 102206 China, Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua University Beijing China

Summary Small interfering RNAs (siRNAs) are responsible for establishing and maintaining DNA methylation through the RNA‐directed DNA methylation (RdDM) pathway in plants. Although siRNA biogenesis is well known, it is relatively unclear about how the process is regulated. By a forward genetic screen in Arabidopsis thaliana , we identified a mutant defective in NOT1 and demonstrated that NOT1 is required for transcriptional silencing at RdDM target genomic loci. We demonstrated that NOT1 is required for Pol IV‐dependent siRNA accumulation and DNA methylation at a subset of RdDM target genomic loci. Furthermore, we revealed that NOT1 is a constituent of a multi‐subunit CCR4‐NOT deadenylase complex by immunoprecipitation combined with mass spectrometry and demonstrated that the CCR4‐NOT components can function as a whole to mediate chromatin silencing. Therefore, our work establishes that the CCR4‐NOT complex regulates the biogenesis of Pol IV‐dependent siRNAs, and hence facilitates DNA methylation and transcriptional silencing in Arabidopsis.

Sponsoring Organization:
USDOE
OSTI ID:
1635067
Journal Information:
The Plant Journal, Journal Name: The Plant Journal Vol. 103 Journal Issue: 4; ISSN 0960-7412
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 7 works
Citation information provided by
Web of Science

References (75)

Locus-specific control of the de novo DNA methylation pathway in Arabidopsis by the CLASSY family journal May 2018
The PRP6-like splicing factor STA1 is involved in RNA-directed DNA methylation by facilitating the production of Pol V-dependent scaffold RNAs journal July 2013
An atypical component of RNA-directed DNA methylation machinery has both DNA methylation-dependent and -independent roles in locus-specific transcriptional gene silencing journal November 2011
Complexity of the Alternative Splicing Landscape in Plants journal October 2013
Identification of Arabidopsis CCR4-NOT Complexes with Pumilio RNA-Binding Proteins, APUM5 and APUM2 journal May 2019
Mechanisms of deadenylation-dependent decay: Mechanisms of deadenylation-dependent decay journal September 2010
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome journal January 2009
SUVR2 is involved in transcriptional gene silencing by associating with SNF2-related chromatin-remodeling proteins in Arabidopsis journal November 2014
The Ccr4–Not complex journal January 2012
The Not3/5 subunit of the Ccr4-Not complex: A central regulator of gene expression that integrates signals between the cytoplasm and the nucleus in eukaryotic cells journal April 2013
Establishing epigenetic variation during genome reprogramming journal April 2013
RNAi triggered by specialized machinery silences developmental genes and retrotransposons journal November 2012
Multifunctional roles of the mammalian CCR4–NOT complex in physiological phenomena journal August 2014
Comprehensive Analysis of Silencing Mutants Reveals Complex Regulation of the Arabidopsis Methylome journal January 2013
An Effector of RNA-Directed DNA Methylation in Arabidopsis Is an ARGONAUTE 4- and RNA-Binding Protein journal May 2009
The splicing machinery promotes RNA-directed DNA methylation and transcriptional silencing in Arabidopsis journal March 2013
The SUMO E3 Ligase-Like Proteins PIAL1 and PIAL2 Interact with MOM1 and Form a Novel Complex Required for Transcriptional Silencing journal April 2016
Dynamics and function of DNA methylation in plants journal May 2018
Folate Polyglutamylation Is Involved in Chromatin Silencing by Maintaining Global DNA Methylation and Histone H3K9 Dimethylation in Arabidopsis journal July 2013
The Arabidopsis Chromatin-Modifying Nuclear siRNA Pathway Involves a Nucleolar RNA Processing Center journal July 2006
RNA-directed DNA methylation: an epigenetic pathway of increasing complexity journal May 2014
Arabidopsis Deadenylases AtCAF1a and AtCAF1b Play Overlapping and Distinct Roles in Mediating Environmental Stress Responses journal December 2009
On the importance of being co-transcriptional journal October 2002
Structural and Biochemical Insights to the Role of the CCR4-NOT Complex and DDX6 ATPase in MicroRNA Repression journal June 2014
DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV journal May 2013
The splicing factor SR45 affects the RNA-directed DNA methylation pathway in Arabidopsis journal January 2012
AtNOT1 Is a Novel Regulator of Gene Expression during Pollen Development journal October 2019
Novel roles of the multi-functional CCR4-NOT complex in post-transcriptional regulation journal May 2014
Splicing Factors Facilitate RNAi-Directed Silencing in Fission Yeast journal October 2008
DNA methylation pathways and their crosstalk with histone methylation journal August 2015
Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing journal July 2011
Non-Coding RNA Transcription and RNA-Directed DNA Methylation in Arabidopsis journal September 2014
SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation journal January 2014
A Two-Step Process for Epigenetic Inheritance in Arabidopsis journal April 2014
Establishing, maintaining and modifying DNA methylation patterns in plants and animals journal February 2010
ROS1, a Repressor of Transcriptional Gene Silencing in Arabidopsis, Encodes a DNA Glycosylase/Lyase journal December 2002
A Dicer-Independent Route for Biogenesis of siRNAs that Direct DNA Methylation in Arabidopsis journal January 2016
Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis journal October 2015
Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1 journal May 2013
Insights into the structure of the CCR4-NOT complex by electron microscopy journal June 2011
Role of RNA polymerase IV in plant small RNA metabolism journal March 2007
Ccr4-Not complex: the control freak of eukaryotic cells journal March 2012
Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading journal June 2008
RNA decay machines: Deadenylation by the Ccr4–Not and Pan2–Pan3 complexes journal June 2013
Molecular Mechanism of Action of Plant DRM De Novo DNA Methyltransferases journal May 2014
Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis journal November 2014
PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis journal February 2008
Messenger RNA Degradation: Beginning at the End journal April 2002
Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome journal August 2012
Two Components of the RNA-Directed DNA Methylation Pathway Associate with MORC6 and Silence Loci Targeted by MORC6 in Arabidopsis journal May 2016
Regulation and function of DNA methylation in plants and animals journal February 2011
IDN2 and Its Paralogs Form a Complex Required for RNA–Directed DNA Methylation journal May 2012
Deadenylation of mRNA by the CCR4–NOT complex in Drosophila: molecular and developmental aspects journal May 2014
Identification of small RNA pathway genes using patterns of phylogenetic conservation and divergence journal December 2012
The Arabidopsis Nucleosome Remodeler DDM1 Allows DNA Methyltransferases to Access H1-Containing Heterochromatin journal March 2013
Regulation of Alternative Splicing Through Coupling with Transcription and Chromatin Structure journal June 2015
Dicer-independent RNA-directed DNA methylation in Arabidopsis journal December 2015
Intergenic transcription by RNA Polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis journal November 2009
An Importin β Protein Negatively Regulates MicroRNA Activity in Arabidopsis journal October 2011
Four putative SWI2/SNF2 chromatin remodelers have dual roles in regulating DNA methylation in Arabidopsis journal October 2018
RNA Polymerase IV Directs Silencing of Endogenous DNA journal April 2005
RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats journal July 2012
RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA journal June 2014
The SET Domain Proteins SUVH2 and SUVH9 Are Required for Pol V Occupancy at RNA-Directed DNA Methylation Loci journal January 2014
NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation journal February 2009
GW182 Proteins Directly Recruit Cytoplasmic Deadenylase Complexes to miRNA Targets journal October 2011
In Vitro Transcription Activities of Pol IV, Pol V, and RDR2 Reveal Coupling of Pol IV and RDR2 for dsRNA Synthesis in Plant RNA Silencing journal December 2012
Cytoplasmic Assembly and Selective Nuclear Import of Arabidopsis ARGONAUTE4/siRNA Complexes journal June 2012
Genetic and Functional Diversification of Small RNA Pathways in Plants journal February 2004
The highways and byways of mRNA decay journal February 2007
NOT2 Proteins Promote Polymerase II–Dependent Transcription and Interact with Multiple MicroRNA Biogenesis Factors in Arabidopsis journal February 2013
Noncoding Transcription by RNA Polymerase Pol IVb/Pol V Mediates Transcriptional Silencing of Overlapping and Adjacent Genes journal November 2008
AtCCR4a and AtCCR4b are Involved in Determining the Poly(A) Length of Granule-bound starch synthase 1 Transcript and Modulating Sucrose and Starch Metabolism in Arabidopsis thaliana journal January 2015
A One Precursor One siRNA Model for Pol IV-Dependent siRNA Biogenesis journal October 2015
An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis journal May 2014