An atypical epigenetic mechanism affects uniparental expression of Pol IV-dependent sirnas

Rebecca Ann Mosher Harris, Ek Han Tan, Juhyun Shin, Robert L. Fischer, Craig S. Pikaard, David C. Baulcombe

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Background: Small RNAs generated by RNA polymerase IV (Pol IV) are the most abundant class of small RNAs in flowering plants. In Arabidopsis thaliana Pol IV-dependent short interfering (p4-si)RNAs are imprinted and accumulate specifically from maternal chromosomes in the developing seeds. Imprinted expression of protein-coding genes is controlled by differential DNA or histone methylation placed in gametes. To identify epigenetic factors required for maternal-specific expression of p4-siRNAs we analyzed the effect of a series of candidate mutations, including those required for genomic imprinting of protein-coding genes, on uniparental expression of a representative p4-siRNA locus. Results: Paternal alleles of imprinted genes are marked by DNA or histone methylation placed by DNA METHYLTRANSFERASE 1 or the Polycomb Repressive Complex 2. Here we demonstrate that repression of paternal p4-siRNA expression at locus 08002 is not controlled by either of these mechanisms. Similarly, loss of several chromatin modification enzymes, including a histone acetyltransferase, a histone methyltransferase, and two nucleosome remodeling proteins, does not affect maternal expression of locus 08002. Maternal alleles of imprinted genes are hypomethylated by DEMETER DNA glycosylase, yet expression of p4-siRNAs occurs irrespective of demethylation by DEMETER or related glycosylases. Conclusions: Differential DNA methylation and other chromatin modifications associated with epigenetic silencing are not required for maternal-specific expression of p4-siRNAs at locus 08002. These data indicate that there is an as yet unknown epigenetic mechanism causing maternal-specific p4-siRNA expression that is distinct from the well-characterized mechanisms associated with DNA methylation or the Polycomb Repressive Complex 2.

Original languageEnglish (US)
Article numbere25756
JournalPLoS One
Volume6
Issue number10
DOIs
StatePublished - Oct 7 2011

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Epigenomics
epigenetics
Polycomb Repressive Complex 2
small interfering RNA
Genes
Mothers
histones
Small Interfering RNA
glycosylases
loci
Methylation
DNA
RNA
DNA methylation
DNA Methylation
methylation
Histones
Chromatin
chromatin
genes

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

An atypical epigenetic mechanism affects uniparental expression of Pol IV-dependent sirnas. / Harris, Rebecca Ann Mosher; Tan, Ek Han; Shin, Juhyun; Fischer, Robert L.; Pikaard, Craig S.; Baulcombe, David C.

In: PLoS One, Vol. 6, No. 10, e25756, 07.10.2011.

Research output: Contribution to journalArticle

Harris, Rebecca Ann Mosher ; Tan, Ek Han ; Shin, Juhyun ; Fischer, Robert L. ; Pikaard, Craig S. ; Baulcombe, David C. / An atypical epigenetic mechanism affects uniparental expression of Pol IV-dependent sirnas. In: PLoS One. 2011 ; Vol. 6, No. 10.
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abstract = "Background: Small RNAs generated by RNA polymerase IV (Pol IV) are the most abundant class of small RNAs in flowering plants. In Arabidopsis thaliana Pol IV-dependent short interfering (p4-si)RNAs are imprinted and accumulate specifically from maternal chromosomes in the developing seeds. Imprinted expression of protein-coding genes is controlled by differential DNA or histone methylation placed in gametes. To identify epigenetic factors required for maternal-specific expression of p4-siRNAs we analyzed the effect of a series of candidate mutations, including those required for genomic imprinting of protein-coding genes, on uniparental expression of a representative p4-siRNA locus. Results: Paternal alleles of imprinted genes are marked by DNA or histone methylation placed by DNA METHYLTRANSFERASE 1 or the Polycomb Repressive Complex 2. Here we demonstrate that repression of paternal p4-siRNA expression at locus 08002 is not controlled by either of these mechanisms. Similarly, loss of several chromatin modification enzymes, including a histone acetyltransferase, a histone methyltransferase, and two nucleosome remodeling proteins, does not affect maternal expression of locus 08002. Maternal alleles of imprinted genes are hypomethylated by DEMETER DNA glycosylase, yet expression of p4-siRNAs occurs irrespective of demethylation by DEMETER or related glycosylases. Conclusions: Differential DNA methylation and other chromatin modifications associated with epigenetic silencing are not required for maternal-specific expression of p4-siRNAs at locus 08002. These data indicate that there is an as yet unknown epigenetic mechanism causing maternal-specific p4-siRNA expression that is distinct from the well-characterized mechanisms associated with DNA methylation or the Polycomb Repressive Complex 2.",
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