Abstract
Drosophila chromosomes are elongated by retrotransposon attachment, a process poorly understood. Here we characterized a mutation affecting the HipHop telomere-capping protein. In mutant ovaries and the embryos that they produce, telomere retrotransposons are activated and transposon RNP accumulates. Genetic results are consistent with that this hiphop mutation weakens the efficacy of HP1-mediated silencing while leaving piRNA-based mechanisms largely intact. Remarkably, mutant females display normal fecundity suggesting that telomere de-silencing is compatible with germline development. Moreover, unlike prior mutants with overactive telomeres, the hiphop stock does not over-accumulate transposons for hundreds of generations. This is likely due to the loss of HipHop’s abilities both to silence transcription and to recruit transposons to telomeres in the mutant. Furthermore, embryos produced by mutant mothers experience a checkpoint activation, and a further loss of maternal HipHop leads to end-to-end fusion and embryonic arrest. Telomeric retroelements fulfill an essential function yet maintain a potentially conflicting relationship with their Drosophila host. Our study thus showcases a possible intermediate in this arm race in which the host is adapting to over-activated transposons while maintaining genome stability. Our results suggest that the collapse of such a relationship might only occur when the selfish element acquires the ability to target non-telomeric regions of the genome. HipHop is likely part of this machinery restricting the elements to the gene-poor region of telomeres. Lastly, our hiphop mutation behaves as a recessive suppressor of PEV that is mediated by centric heterochromatin, suggesting its broader effect on chromatin not limited to telomeres.
Highlights
Transposable elements (TEs) are omnipresent in eukaryotic genomes
Transposons are selfish elements that multiply by inserting extra copies of themselves into the host genome
Active transposons threaten the stability of the host genome, while the host responses by transcriptionally silencing the selfish elements or targeting their
Summary
Transposable elements (TEs) are omnipresent in eukaryotic genomes. They are primarily viewed as a threat to the host organism as TE insertions can disrupt gene expression and function, or induce secondary genome instability as a result of illegitimate recombination. The presence of certain TEs is beneficial to the host, and one of the best examples concerns telomeres in the model of Drosophila, where chromosome ends are populated by telomere specific retrotransposons. HeT-A has a single open-reading-frame (orf) encoding a Gag-like protein (Orf1p) but lacks the accompanying orf, encoding the reverse transcriptase found in typical non-LTR elements This suggests that HeT-A lacks the ability to transpose on its own. In our earlier study [5], we showed that the Orf1p protein from HeT-A is present in the nucleus of somatic cells in S phase, and forms large spherical structures that are attached to one and sometimes multiple chromosome ends. We speculated that HeT-A Sphere represents an intermediate in the molecular events leading to HeT-A transpositions
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