Role of transposable elements in heterochromatin and epigenetic control

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.

Repetitive sequence environment distinguishes housekeeping genes

“…Repetitive sequences have been shown to silence nearby genes via the spread of heterochromatin (Lippman et al, 2004;Sun et al, 2004). However, several longer repetitive sequences or tracts of repetitive sequences have been reported to show differences in an important heterochromatin property, DNA methylation (Sano and Sager, 1982;Breznik et al, 1984;Nishioka, 1988;Mietz and Kuff, 1990;Allingham-Hawkins et al, 1996;Hassan et al, 2001;Chalitchagorn et al, 2004;Khodosevich et al, 2004), suggesting that such influences should vary with tissue type.…”

“…One reason why long repeats might be selected against near housekeeping genes is that an abundance of these repeats might reduce gene expression via heterochromatin spread. Long transposons (Lyon, 1998;Marahrens, 1999;Bailey et al, 2000;Allen et al, 2003;Lippman et al, 2004;Sun et al, 2004) and long tracts of tandem repeats (Pieretti et al, 1991;Hansen et al, 1997;Saveliev et al, 2003) have been implicated in gene silencing via the spread of heterochromatin. Another reason why LINE-1 and other long transposons might be scarce around housekeeping genes is that the euchromatin could spread into the transposons and activate their internal promoters (Swergold, 1990;Minakami et al, 1992;Leib-Mösch and Seifarth, 1995;Speek, 2001;Athanikar et al, 2004).…”

“…For example, in fragile X patients expansion mutations of a tandem simple sequence repeat located in an intron of the FMR1 gene result in the transcriptional silencing of the FMR1 gene (Pieretti et al, 1991). Transposable elements in Drosophila and plants have been implicated in the transcriptional silencing of nearby genes by the spread of heterochromatin (Lippman et al, 2004;Sun et al, 2004) raising the possibility that transposons may also be capable of reducing expression if located near genes in humans. DNA methylation is an important feature of heterochromatin that silences gene expression (Stancheva, 2005).…”

Vector integration: Location, location, location

“…Retrotransposons, endogenous relatives of retroviruses, certainly do affect heterochromatin formation. 21,22 Thus noncoding regions might play important regulatory roles in the genome.…”

Current challenges in de novo plant genome sequencing and assembly

“…Plant species are responsible for maintaining the balance of the carbon cycles [2], for developing and maintaining soil from erosion [3], and are promising sources of renewable energy [4]. Plant byproducts are used in many human medicines [5], and plants have been essential model organisms for studying biological systems such as the role of transposons and epigenetics [6]. For all these reasons and many more, there is great interest in sequencing plant genomes, but relatively few plant species have been sequenced compared with the hundreds of thousands of species around the world.…”