title: RNA-binding protein regulates plant DNA methylation by controlling mRNA processing at the intronic heterochromatin-containing gene IBM1.
abstract: DNA methylation-dependent heterochromatin formation is a conserved mechanism of epigenetic silencing of transposons and other repeat elements in many higher eukaryotes. Genes adjacent to repetitive elements are often also subjected to this epigenetic silencing. Consequently, plants have evolved antisilencing mechanisms such as active DNA demethylation mediated by the REPRESSOR OF SILENCING 1 (ROS1) family of 5-methylcytosine DNA glycosylases to protect these genes from silencing. Some transposons and other repeat elements have found residence in the introns of genes. It is unclear how these intronic repeat elements-containing genes are regulated. We report here the identification of ANTI-SILENCING 1 (ASI1), a bromo-adjacent homology domain and RNA recognition motif-containing protein, from a forward genetic screen for cellular antisilencing factors in Arabidopsis thaliana. ASI1 is required to prevent promoter DNA hypermethylation and transcriptional silencing of some transgenes. Genome-wide DNA methylation analysis reveals that ASI1 has a similar role to that of the histone H3K9 demethylase INCREASE IN BONSAI METHYLATION 1 (IBM1) in preventing CHG methylation in the bodies of thousands of genes. We found that ASI1 is an RNA-binding protein and ensures the proper expression of IBM1 full-length transcript by associating with an intronic heterochromatic repeat element of IBM1. Through mRNA sequencing, we identified many genes containing intronic transposon elements that require ASI1 for proper expression. Our results suggest that ASI1 associates with intronic heterochromatin and binds the gene transcripts to promote their 3' distal polyadenylation. The study thus reveals a unique mechanism by which higher eukaryotes deal with the collateral effect of silencing intronic repeat elements.
authors.affiliation: Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.
authors.forename: Xingang
authors.initials: X
authors.lastname: Wang
authors.forename: Cheng-Guo
authors.initials: CG
authors.lastname: Duan
authors.forename: Kai
authors.initials: K
authors.lastname: Tang
authors.forename: Bangshing
authors.initials: B
authors.lastname: Wang
authors.forename: Huiming
authors.initials: H
authors.lastname: Zhang
authors.forename: Mingguang
authors.initials: M
authors.lastname: Lei
authors.forename: Kun
authors.initials: K
authors.lastname: Lu
authors.forename: Satendra K
authors.initials: SK
authors.lastname: Mangrauthia
authors.forename: Pengcheng
authors.initials: P
authors.lastname: Wang
authors.forename: Guohui
authors.initials: G
authors.lastname: Zhu
authors.forename: Yang
authors.initials: Y
authors.lastname: Zhao
authors.forename: Jian-Kang
authors.initials: JK
authors.lastname: Zhu
mesh_terms: D017360:Arabidopsis / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001483:Base Sequence; D015152:Blotting, Northern; D047369:Chromatin Immunoprecipitation; D003001:Cloning, Molecular; D019175:DNA Methylation / Q000502:physiology*; D024202:Electrophoretic Mobility Shift Assay; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D006570:Heterochromatin / Q000502:physiology*; D007438:Introns / Q000235:genetics; D056484:Jumonji Domain-Containing Histone Demethylases / Q000378:metabolism; D008969:Molecular Sequence Data; D026723:Polyadenylation; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D016601:RNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D060888:Real-Time Polymerase Chain Reaction; D017422:Sequence Analysis, DNA
chemical_list: C584540:ASI1 protein, Arabidopsis; D029681:Arabidopsis Proteins; D006570:Heterochromatin; D012333:RNA, Messenger; D016601:RNA-Binding Proteins; C526313:IBM1 protein, Arabidopsis; D056484:Jumonji Domain-Containing Histone Demethylases
keywords: ChIP; DNA methylome; gene expression