The characterization of DINE-1, a short, interspersed repetitive element present on chromosome and in the centric heterochromatin of Drosophila melanogaster

Abstract

The banded portion of chromosome 4 (the "dot" chromosome) in Drosophila melanogaster displays some properties of beta-heterochromatin, which is normally found within the centric domain of the chromosomes. The nature and distribution of repetitive elements on chromosome 4 could play a role in the establishment of this unusual chromatin configuration. We describe here one such element: a short, interspersed repetitive sequence named DINE-1. Determination of a consensus sequence for the element reveals that there are two conserved regions (A and B) separated by a highly variable spacer. The conserved sequences are approximately 400 bp long but degenerate at both ends, opening the possibility that a yet-to-be-discovered mother element may be present in the genome. DINE-1 bears few of the properties of the mammalian short interspersed elements (SINEs) to which it bears a superficial resemblance in size. It does not appear to be the product of reverse transcription and lacks any polymerase III promoter consensus. The elements are not flanked by target site duplications and their termini lack direct or inverted repeats, suggesting that they themselves are not transposable. Our analysis of cosmid clones from chromosome 4, and elsewhere in the genome, revealed that the euchromatic locations of DINE-1 are almost exclusively confined to chromosome 4. In situ hybridization of a DINE-1 probe to polytene chromosomes confirmed the preferential distribution along 4, in addition to its presence in the centric heterochromatin. This unusual genomic distribution of bias toward chromosome 4 is also seen in the sibling species, D. simulans, whose dot chromosomes exhibit poorly resolved polytene bands and lack crossing over during meiosis like those of D. melanogaster. However, the dot chromosome of D. virilis, which exhibits a well-defined banded structure on polytene chromosomes and can cross over, has only a single, discrete site of DINE-1 element hybridization. The presence of DINE-1 within these regions suggests a role in the heterochromatic nature of chromosome 4 in D. melanogaster and supports the contention that repeats accumulate in regions of diminished crossing over.

A Helitron-Like Transposon Superfamily from Lepidoptera Disrupts (GAAA)n Microsatellites and is Responsible for Flanking Sequence Similarity within a Microsatellite Family

“…For example, Drosophila DINE-1 superfamily members show a high level of intraspecific sequence variation and presence of truncated copies which cause difficulty in copy number estimations from the WGS of 12 species (Yang and Barbash 2008). Despite the high level of divergence, DINE-1s retain structural features that may be necessary for MITE-or Helitron-like mobility (Yang et al 2006;Yang and Barbash 2008): conserved 5 0 and 3 0 SIRs, an inverted repeat (IR) complementary to the 5 0 SIR, and a stem-loop structure in the 3 0 terminal region (Locke et al 1999;Vivas et al 1999;Miller et al 2000;Wilder and Hollocher 2001;Yang and Barbash 2008). Analogously, Helitron-like transposons have conserved 5 0 TC and 3 0 CTRR termini (R = A or G nucleotides; Kapitonov and Jurka 2001), but show optional requirements for 3 0 terminal stem-loop structures (Galagan et al 2005;Kapitonov and Jurka 2007b).…”

“…Since sequence downstream of DINE-1s are more highly polymorphic and can show little intraspecific homology that show limited use in homology-based searches (Locke et al 1999;Vivas et al 1999;Miller et al 2000), we correspondingly used the (GAAA) n and 5 0 SIR sequence of OnMINE-1 (positions 156-215 in Fig. 1) to query GenBank nr, dbEST, and dbGSS in our search #2.…”

“…MITEs lack an internal protein coding region, and mobility is mediated by trans-acting factors encoded by related autonomous TEs (Dufresne et al 2006). MITEs are found ubiquitously within eukaryotic genomes, including mosquito (Tu 2000;Quesneville et al 2006), Drosophila (Locke et al 1999;Vivas et al 1999;Miller et al 2000;Wilder and Hollocher 2001;Yang and Barbash 2008), and Lepidoptera (Chen and Li 2007;Coates et al 2009) and have a role in altering genome structure including insertion at microsatellite loci (Akagi et al 2001).…”

Genomic regions harboring insecticide resistance-associated Cyp genes are enriched by transposable element fragments carrying putative transcription factor binding sites in two sibling Drosophila species

“…DNAREP1 elements were highly abundant in 12 out of 23 sequenced Drosophila genomes analyzed by Yang and Barbash (2008). These elements are classified in Repbase as DNA transposons of the Helitron family (Kapitonov and Jurka, 2007) but have also been designated DINE-1 or INE-1 and have been proposed to be SINE-like retroelements (Locke et al, 1999), TIR transposons (Bergman et al, 2006) or even MITEs (Yang and Barbash, 2008). Here, we maintain the classification of Repbase, where two consensus sequences of DNAREP1 are deposited: DNAREP1_DM and DNAREP1_DYak.…”

Molecular mapping of deletion breakpoints on chromosome 4 of Drosophila melanogaster

“…The difference between the densities is made up almost exclusively in LINE-like and TIR elements, and these elements are distributed all along the chromosome, both between and within genes (Kaminker et al 2002). Chromosome 4 is also highly enriched for the repetitive element DINE-1, which has been localized almost exclusively to chromosome 4 and centric heterochromatic regions (Locke et al 1999). Heterochromatic protein 1 (HP1), an important constituent of heterochromatin, has been shown to bind extensively to chromosome 4 (James et al 1989).…”