HeT-A elements in Drosophila virilis : Retrotransposon telomeres are conserved across the Drosophila genus

Abstract

Drosophila melanogaster telomeres are composed of two retrotransposons, HeT-A and TART. Drosophila virilis has recently been shown to have telomere-specific TART elements with many of the characteristics of their D. melanogaster homologues. We now report identification of the second telomere-specific retrotransposon, HeT-A, from D. virilis. These results show that HeT-A and TART have been maintaining telomeres in Drosophila for more than the 60 million years that separate D. melanogaster and D. virilis. All Drosophila species and stocks studied have both of these telomeric elements, suggesting that the elements collaborate, an assumption supported by evidence from D. melanogaster that their Gag proteins interact. Although the HeT-A sequence evolves at a high rate, the element retains the unusual structural features that characterize all HeT-A homologues. These features may be involved in the role of HeT-A at the telomere. The Gag protein from HeT-A vir is as much like TART Gag from other species as it is like HeT-A Gag, suggesting that these Gags are evolving under similar constraints, probably to maintain appropriate interactions with host telomeres and possibly to allow collaborative interactions like those seen in D. melanogaster. In addition, we have identified a chimeric element, U vir , carrying a pol coding sequence only distantly related to sequences thus far found in any telomere arrays.T elomeres of eukaryotic chromosomes are composed of long arrays of DNA repeats. In most animals, plants, and unicellular eukaryotes, these repeats are short species-specific sequences (5-10 bp) reverse transcribed onto chromosome ends by the enzyme telomerase. Telomeres in Drosophila melanogaster are a surprising exception to the general type. D. melanogaster telomeres are arrays of repeated sequences but these arrays are produced by successive transpositions of two non-LTR retrotransposons. Rather than successive additions of a telomerase repeat (1), each repeat in these telomeres is a copy of one of the telomeric elements, HeT-A and TART.HeT-A and TART group into the Jockey clade based on the sequences of their coding regions. The Jockey clade contains several of the more abundant retrotransposable elements in the D. melanogaster genome, including Doc, jockey, and X, but HeT-A and TART have several characteristics that set them apart from the other elements. The most obvious difference is the targeting of transposition: HeT-A and TART transpose only onto chromosome ends, whereas the other members of the clade (generally considered parasitic elements) transpose into many parts of the genome but are never found in these telomere regions. This targeting appears to involve Gag proteins because Gags from both HeT-A and TART move efficiently to specific intranuclear sites and associate with chromosome ends, whereas Gags from other members of the clade remain almost entirely in the cytoplasm (2). Another difference is the large amount of noncoding sequence (5Ј and 3Ј UTR) in HeT-A and TART in D. melanogaster and Drosophila y...

Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

“…2), where a TART-like element (a TR) and a HeT-A-like element (a HTR) had been previously identified. 58,59 The comparison between all Drosophila telomeric retrotransposons clearly shows an extensive evolution of these elements over a 60 million years time frame. Thus, it is normal to find deletions of varied sizes in different upstream regions with respect to the zinc knuckles domain of the ORF1.…”

Genomic organization of the Drosophila telomere retrotransposable elements

“…Nonetheless, HeT-A and TART arrays maintain the strand composition bias seen on other telomeres-the sense strand is always A+C-rich (Danilevskaya et al 1998), like telomerase template sequences (Henderson 1995). In addition, HeT-A 3Ј UTRs have a pattern of irregularly spaced A-rich regions in every Drosophila species studied (Danilevskaya et al 1998;Casacuberta and Pardue 2003).…”

Telomere Maintenance in Organisms without Telomerase

“…A HeT-A element was found in the terminal array next to a TART from D. virilis. As with its homolog in D. melanogaster, the HeT-A element carried only a single ORF for a Gag protein and had a long 3' UTR (Casacuberta & Pardue, 2003b). Experiments to localize GFP-tagged Gag proteins indicated that the Gag encoded by the D. virilis TART element requires HeT-A Gag to target the telomeres, similar to the situation found in D. melanogaster (Casacuberta et al, 2007).…”