Adapting to life at the end of the line: How Drosophila telomeric retrotransposons cope with their job.

Drosophila telomeres are remarkable because they are maintained by telomere-specific retrotransposons, rather than the enzyme telomerase that maintains telomeres in almost every other eukaryotic organism. Successive transpositions of the Drosophila retrotransposons onto chromosome ends produce long head-to-tail arrays that are analogous in form and function to the long arrays of short repeats produced by telomerase in other organisms. Nevertheless, Drosophila telomere repeats are retrotransposons, complex entities three orders of magnitude longer than simple telomerase repeats.

Retrotransposons that maintain chromosome ends.

Reverse transcriptases have shaped genomes in many ways. A remarkable example of this shaping is found on telomeres of the genus Drosophila, where retrotransposons have a vital role in chromosome structure. Drosophila lacks telomerase; instead, three telomere-specific retrotransposons maintain chromosome ends.

Evolution of diverse mechanisms for protecting chromosome ends by Drosophila TART telomere retrotransposons.

The retrotransposons HeT-A, TART, and TAHRE, which maintain Drosophila telomeres, transpose specifically onto chromosome ends to form long arrays that extend the chromosome and compensate for terminal loss. Because they transpose by target-primed reverse transcription, each element is oriented so that its 5' end serves as the extreme end of the chromosome until another element transposes to occupy the terminal position. Thus 5' sequences are at risk for terminal erosion while the element is at the chromosome end.

Differential maintenance of DNA sequences in telomeric and centromeric heterochromatin.

Repeated DNA in heterochromatin presents enormous difficulties for whole-genome sequencing; hence, sequence organization in a significant portion of the genomes of multicellular organisms is relatively unknown. Two sequenced BACs now allow us to compare telomeric retrotransposon arrays from Drosophila melanogaster telomeres with an array of telomeric retrotransposons that transposed into the centromeric region of the Y chromosome >13 MYA, providing a unique opportunity to compare the structural evolution of this retrotransposon in two contexts. We find that these retrotransposon arrays, both heterochromatic, are maintained quite differently, resulting in sequence organizations that apparently reflect different roles in the two chromosomal environments.

Evolution of species-specific promoter-associated mechanisms for protecting chromosome ends by Drosophila Het-A telomeric transposons.

The non-LTR retrotransposons forming Drosophila telomeres constitute a robust mechanism for telomere maintenance, one which has persisted since before separation of the extant Drosophila species. These elements in D. melanogaster differ from nontelomeric retrotransposons in ways that give insight into general telomere biology.

Gag proteins of Drosophila telomeric retrotransposons: collaborative targeting to chromosome ends.

TAHRE, the least abundant of the three retrotransposons forming telomeres in Drosophila melanogaster, has high sequence similarity to the gag gene and untranslated regions of HeT-A, the most abundant telomere-specific retrotransposon. Despite TAHRE's apparent evolutionary relationship to HeT-A, we find TAHRE Gag cannot locate to telomere-associated "Het dots" unless collaborating with HeT-A Gag. TAHRE Gag is carried into nuclei by HeT-A or TART Gag, but both TART and TAHRE Gags need HeT-A Gag to localize to Het dots.

Drosophila telomeres: A variation on the telomerase theme.

In Drosophila, the role of telomerase is carried out by three specialized retrotransposable elements, HeT-A, TART and TAHRE. Telomeres contain long tandem head-to-tail arrays of these elements. Within each array, the three elements occur in random, but polarized, order.

Following the chromosome path to the garden of the genome.

I have been fascinated by chromosomes for longer than I care to mention; their beautiful structure, cell-type-specific changes in morphology, and elegant movements delight me. Shortly before I began graduate study, the development of nucleic acid hybridization made it possible to compare two nucleic acids whether or not their sequences were known. From this stemmed a progression of development in tools and techniques that continues to enhance our understanding of how chromosomes function.

Intracellular targeting of telomeric retrotransposon Gag proteins of distantly related Drosophila species.

The retrotransposons that maintain telomeres in Drosophila melanogaster have unique features that are shared across all Drosophila species but are not found in other retrotransposons. Comparative analysis of these features provides insight into their importance for telomere maintenance in Drosophila. Gag proteins encoded by HeT-A(mel) and TART(mel) are efficiently and cooperatively targeted to telomeres in interphase nuclei, a behavior that may facilitate telomere-specific transposition.

Genomic organization of the Drosophila telomere retrotransposable elements.

The emerging sequence of the heterochromatic portion of the Drosophila melanogaster genome, with the most recent update of euchromatic sequence, gives the first genome-wide view of the chromosomal distribution of the telomeric retrotransposons, HeT-A, TART, and Tahre. As expected, these elements are entirely excluded from euchromatin, although sequence fragments of HeT-A and TART 3 untranslated regions are found in nontelomeric heterochromatin on the Y chromosome. The proximal ends of HeT-A/TART arrays appear to be a transition zone because only here do other transposable elements mix in the array.

RNA interference has a role in regulating Drosophila telomeres.

Unlike many other organisms, Drosophila maintains its telomeres by the transposition of retrotransposons to chromosome ends. Recent work shows that proteins in the RNA interference pathway specifically regulate the expression of these retrotransposons and frequency of transposition in germline cells, but do not affect retrotransposon expression or telomere function in the soma.

Comparison of dot chromosome sequences from D. melanogaster and D. virilis reveals an enrichment of DNA transposon sequences in heterochromatic domains.

Background: Chromosome four of Drosophila melanogaster, known as the dot chromosome, is largely heterochromatic, as shown by immunofluorescent staining with antibodies to heterochromatin protein 1 (HP1) and histone H3K9me. In contrast, the absence of HP1 and H3K9me from the dot chromosome in D. virilis suggests that this region is euchromatic.

Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres.

Telomere molecular biology is far more complex than originally thought. Understanding biological systems is aided by study of evolutionary variants, and Drosophila telomeres are remarkable variants. Drosophila lack telomerase and the arrays of simple repeats generated by telomerase in almost all other organisms; instead, Drosophila telomeres are long tandem arrays of two non-LTR retrotransposons, HeT-A and TART.

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

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.

Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group.

Telomeres of most animals, plants, and unicellular eukaryotes are made up of tandem arrays of repeated DNA sequences produced by the enzyme telomerase. Drosophila melanogaster has an unusual variation on this theme; telomeres consist of tandem arrays of sequences produced by successive transpositions of two non-LTR retrotransposons, HeT-A and TART. To explore the phylogenetic distribution of these variant telomeres, we have looked for TART homologues in a distantly related Drosophila species, virilis.

The promoter of the heterochromatic Drosophila telomeric retrotransposon, HeT-A, is active when moved into euchromatic locations.

The Drosophila telomeric retrotransposon, HeT-A, is found only in heterochromatin; therefore, its promoter must function in this chromatin environment. Studies of position effect variegation suggest that promoters of heterochromatic genes are very different from euchromatic promoters, but this idea has not been tested with isolated promoter sequences. The HeT-A promoter is the first heterochromatin promoter to be isolated and it is of interest to investigate its activity when removed from telomeric heterochromatin.

Gag proteins of the two Drosophila telomeric retrotransposons are targeted to chromosome ends.

Drosophila telomeres are formed by two non-LTR retrotransposons, HeT-A and TART, which transpose only to chromosome ends. Successive transpositions of these telomeric elements yield arrays that are functionally equivalent to the arrays generated by telomerase in other organisms. In contrast, other Drosophila non-LTR retrotransposons transpose widely through gene-rich regions, but not to ends.

Coevolution of the telomeric retrotransposons across Drosophila species.

As in other eukaryotes, telomeres in Drosophila melanogaster are composed of long arrays of repeated DNA sequences. Remarkably, in D. melanogaster these repeats are produced, not by telomerase, but by successive transpositions of two telomere-specific retrotransposons, HeT-A and TART.