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

Abstract

The transposable elements HeT-A and TARTconstitute 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-Aproduces 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-Atranscripts 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 TARTsequence 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.

ACKNOWLEDGMENTS

We thank E. Lozovskaya and A. A. Hoffmann for Drosophila stocks, D. Nurminsky for assistance in screening the P1 phage library, and Ky Lowenhaupt for comments on the manuscript.

This work was supported by grants from the National Institutes of Health (GM 50315 and GM57006).