Genomic organization of the Drosophila telomere retrotransposable elements

Abstract

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 3Ј 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. The sharp distinction between the distribution of telomeric elements and that of other transposable elements suggests that chromatin structure is important in telomere element localization. Measurements reported here show (1) D. melanogaster telomeres are very long, in the size range reported for inbred mouse strains (averaging 46 kb per chromosome end in Drosophila stock 2057). As in organisms with telomerase, their length varies depending on genotype. There is also slight under-replication in polytene nuclei. (2) Surprisingly, the relationship between the number of HeT-A and TART elements is not stochastic but is strongly correlated across stocks, supporting the idea that the two elements are interdependent. Although currently assembled portions of the HeT-A/TART arrays are from the most-proximal part of long arrays, ∼61% of the total HeT-A sequence in these regions consists of intact, potentially active elements with little evidence of sequence decay, making it likely that the content of the telomere arrays turns over more extensively than has been thought.

Drosophila telomeres: an exception providing new insights

“…The stochastic nature of transposition coupled with the end replication problem predicts that individual elements in the array will be variably 5′ truncated. Both of these predictions are observed (58)(59)(60). An important prerequisite in this telomere elongation mechanism is the generation of transcripts from the HTT elements in spite of 5′ truncations.…”

“…The 4R telomere may be an exception in that it lacks TAS and, instead, has a 5.4 kb "transition zone" that consists of a scramble of HTT elements and other non-telomeric transposons between the uninterrupted HTT array and the last gene (58,60). These observations are not surprising given the rapid turnover of telomeric sequences near the chromosome terminus.…”

Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

“…[25][26][27] In agreement with this mechanism of transposition, the elements appear randomly mixed in head-to-tail arrays and frequently truncated at the 5' end. [27][28][29][30] Full-length elements, likely master copies, are found at these arrays and, in several cases, two full-length elements occur within an array of three tandem elements implying the occurrence of three successive retrotransposition events. This transpositional behavior would allow the existence of master copies at telomeres.…”

Adapting to life at the end of the line

“…The elements transcribed to produce new transpositions are all located in telomere arrays and therefore at risk of loss in this dynamic environment. 12 Telomere arrays are very long so it would appear that elements located in the more proximal regions have been there for telomerase and the reverse transcriptase of non-LTR elements are closely related. 17 Although the Drosophila repeats (complete retrotransposons) are much longer and more complex than telomerase repeats, the length of Drosophila telomere arrays is similar to those of other multicellular eukaryotes.…”