Role of transposable elements in heterochromatin and epigenetic control

Nature. 2004 Jul 22;430(6998):471-6. doi: 10.1038/nature02651.

Abstract

Heterochromatin has been defined as deeply staining chromosomal material that remains condensed in interphase, whereas euchromatin undergoes de-condensation. Heterochromatin is found near centromeres and telomeres, but interstitial sites of heterochromatin (knobs) are common in plant genomes and were first described in maize. These regions are repetitive and late-replicating. In Drosophila, heterochromatin influences gene expression, a heterochromatin phenomenon called position effect variegation. Similarities between position effect variegation in Drosophila and gene silencing in maize mediated by "controlling elements" (that is, transposable elements) led in part to the proposal that heterochromatin is composed of transposable elements, and that such elements scattered throughout the genome might regulate development. Using microarray analysis, we show that heterochromatin in Arabidopsis is determined by transposable elements and related tandem repeats, under the control of the chromatin remodelling ATPase DDM1 (Decrease in DNA Methylation 1). Small interfering RNAs (siRNAs) correspond to these sequences, suggesting a role in guiding DDM1. We also show that transposable elements can regulate genes epigenetically, but only when inserted within or very close to them. This probably accounts for the regulation by DDM1 and the DNA methyltransferase MET1 of the euchromatic, imprinted gene FWA, as its promoter is provided by transposable-element-derived tandem repeats that are associated with siRNAs.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis Proteins / genetics
  • Chromosomes, Plant / genetics
  • Cluster Analysis
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Methylation
  • DNA Transposable Elements / genetics*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Epigenesis, Genetic / genetics*
  • Gene Expression Regulation, Plant*
  • Genomic Imprinting
  • Heterochromatin / genetics*
  • Homeodomain Proteins / genetics
  • Oligonucleotide Array Sequence Analysis
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Tandem Repeat Sequences / genetics
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • DDM1 protein, Arabidopsis
  • DNA Transposable Elements
  • DNA-Binding Proteins
  • FWA protein, Arabidopsis
  • Heterochromatin
  • Homeodomain Proteins
  • RNA, Small Interfering
  • Transcription Factors
  • MET1 protein, Arabidopsis
  • DNA (Cytosine-5-)-Methyltransferases