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. Here we report that TART elements in Drosophila melanogaster and Drosophila virilis show species-specific innovations in promoter architecture that buffer loss of sequence exposed at chromosome ends. The two elements have evolved different ways to effect this protection. The D. virilis TART (TART(vir)) promoter is found in the 3' UTR of the element directly upstream of the element transcribed. Transcription starts within the upstream element so that a Tag of extra sequence is added to the 5' end of the newly transcribed RNA. This Tag provides expendable sequence to buffer end erosion of essential 5' sequence after the RNA is reverse transcribed onto the chromosome. In contrast, the D. melanogaster TART (TART(mel)) promoter initiates transcription deep within the 5' UTR, but the element is able to replace and extend the 5' UTR sequence by copying sequence from its 3' UTR, we believe while being reverse transcribed onto the chromosome end. Astonishingly, end-protection in TART(vir) and HeT-Amel are essentially identical (using Tags), whereas HeT-Avir is clearly protected from end erosion by an as-yet-unspecified program.