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Diversification and collapse of a telomere elongation mechanism

Bastien Saint-Leandre, Son C. Nguyen, Mia T. Levine
doi: https://doi.org/10.1101/445429
Bastien Saint-Leandre
1Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104.
2Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, 19104.
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Son C. Nguyen
2Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, 19104.
3Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104.
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Mia T. Levine
1Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104.
2Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, 19104.
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  • For correspondence: m.levine@sas.upenn.edu
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Abstract

In virtually all eukaryotes, telomerase counteracts chromosome erosion by adding repetitive sequence to terminal ends. Drosophila melanogaster instead relies on specialized retrotransposons that insert preferentially at telomeres. This exchange of goods between host and mobile element—wherein the mobile element provides an essential genome service and the host provides a hospitable niche for mobile element propagation—has been called a ‘genomic symbiosis’. However, these telomere-specialized, ‘jockey’ family elements may actually evolve to selfishly over-replicate in the genomes that they ostensibly serve. Under this intra-genomic conflict model, we expect rapid diversification of telomere-specialized retrotransposon lineages and possibly, the breakdown of this tenuous relationship. Here we report data consistent with both predictions. Searching the raw reads of the 15-million-year-old ‘melanogaster species group’, we generated de novo jockey retrotransposon consensus sequences and used phylogenetic tree-building to delineate four distinct telomere-associated lineages. Recurrent gains, losses, and replacements account for this striking retrotransposon lineage diversity. Moreover, an ancestrally telomere-specialized element has ‘escaped,’ residing now throughout the genome of D. rhopaloa. In D. biarmipes, telomere-specialized elements have disappeared completely. De novo assembly of long-reads and cytogenetics confirmed this species-specific collapse of retrotransposon-dependent telomere elongation. Instead, telomere-restricted satellite DNA and DNA transposon fragments occupy its terminal ends. We infer that D. biarmipes relies instead on a recombination-based mechanism conserved from yeast to flies to humans. Combined with previous reports of adaptive evolution at host proteins that regulate telomere length, telomere-associated retrotransposon diversification and disappearance offer compelling evidence that intra-genomic conflict shapes Drosophila telomere evolution.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 18, 2018.
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Diversification and collapse of a telomere elongation mechanism
Bastien Saint-Leandre, Son C. Nguyen, Mia T. Levine
bioRxiv 445429; doi: https://doi.org/10.1101/445429
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Diversification and collapse of a telomere elongation mechanism
Bastien Saint-Leandre, Son C. Nguyen, Mia T. Levine
bioRxiv 445429; doi: https://doi.org/10.1101/445429

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