The Two Drosophila Telomeric Transposable Elements Have Very Different Patterns of Transcription

Abstract

The transposable elements HeT-A and TART constitute the telomeres of Drosophila chromosomes. Both are non-long terminal repeat (LTR) retrotransposons, sharing the remarkable property of transposing only to chromosome ends. In addition, strong sequence similarity of their gag proteins indicates that these coding regions share a common ancestor. These findings led to the assumption that HeT-A and TART are closely related. However, we now find that these elements produce quite different sets of transcripts. HeT-A produces only sense-strand transcripts of the full-length element, whereas TART produces both sense and antisense full-length RNAs, with antisense transcripts in more than 10-fold excess over sense RNA. In addition, features of TART sequence organization resemble those of a subclass of non-LTR elements characterized by unequal terminal repeats. Thus, the ancestral gag sequence appears to have become incorporated in two different types of elements, possibly with different functions in the telomere. HeT-A transcripts are found in both nuclear and cytoplasmic cell fractions, consistent with roles as both mRNA and transposition template. In contrast, both sense and antisense TART transcripts are almost entirely concentrated in nuclear fractions. Also, TART open reading frame 2 probes detect a cytoplasmic mRNA for reverse transcriptase (RT), with no similarity to TART sequence 5 or 3 of the RT coding region. This RNA could be a processed TART transcript or the product of a "free-standing" RT gene. Either origin would be novel. The distinctive transcription patterns of both HeT-A and TART are conserved in Drosophila yakuba, despite significant sequence divergence. The conservation argues that these sets of transcripts are important to the function(s) of HeT-A and TART.Telomeres in Drosophila melanogaster are composed of multiple copies of two non-long terminal repeat (LTR) retrotransposons, HeT-A and TART, instead of the short DNA repeats generated by telomerase on the chromosome ends of most eukaryotes (13,24). Successive transpositions of HeT-A and TART yield arrays of repeats that are larger and more irregular than the repeats produced by telomerase. Nevertheless, these transpositions are, in some sense, equivalent to the telomeregenerating action of telomerase; both telomerase and the transposition of HeT-A and TART extend chromosome ends by RNA-templated additions of specific sequences.HeT-A and TART share two features that distinguish them from other known retrotransposable elements. Both transpose only to the ends of chromosomes (apparently to any chromosome end in D. melanogaster), and each contains a large segment of untranslated sequence (Fig. 1). We have recently shown that, for HeT-A, each of these distinguishing features is also conserved in related species (10), even when phylogenetic separation is great enough for the HeT-A sequences to have diverged by nearly 50%. HeT-A and TART also have some significant differences. TART encodes its own reverse transcriptase (RT); HeT-A does not. However, HeT-A...

Antisense Transcription of Retrotransposons in Drosophila: An Origin of Endogenous Small Interfering RNA Precursors

“…Because protein coding genes do not produce AS transcripts in Drosophila, mechanisms of AS transcription and downstream regulatory functions have not been fully elucidated. AS retroTn transcription of Drosophila telomere LTR retroTns has been observed previously (Danilevskaya et al 1999). Herein, we provide the first evidence of global AS transcription of LTR and non-LTR retroTns, and TIR DNA Tn families in Drosophila (Table 1 and Table S3).…”

Telomere maintenance in Drosophila: Rapid transposon evolution at chromosome ends

“…29 The transcription patterns of HeT-A and TART are quite different; TART produces much more antisense than sense transcripts, whereas HeT-A only produces sense-strand transcripts of the full-length element. 47,48 Moreover, they have two distinct patterns of expression in the germline. While TART transcripts only accumulate in nurse cells at late stages of oogenesis, HeT-A transcripts are detected in oocytes since the early stages.…”

Differential Maintenance of DNA Sequences in Telomeric and Centromeric Heterochromatin

“…Thus it is possible that the 39 region is conserved to direct transcription from this sequence. Northern blots show several transcripts ,1 kb in length with sequence homology to the 39 region (Danilevskaya et al 1999). Some of these RNAs are found only in males and might be products of the Y centromere.…”