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Rapid evolutionary diversification of the flamenco locus across simulans clade Drosophila species

Sarah Signor, Jeffrey Vedanayagam, Bernard Y. Kim, Filip Wierzbicki, Robert Kofler, View ORCID ProfileEric C. Lai
doi: https://doi.org/10.1101/2022.09.29.510127
Sarah Signor
1Biological Sciences, North Dakota State University, Fargo, North Dakota, USA
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  • For correspondence: sarah.signor@ndsu.edu
Jeffrey Vedanayagam
2Developmental Biology Program, Sloan-Kettering Institute, 430 East 67th St, ROC-10, New York, NY 10065, USA
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Bernard Y. Kim
3Department of Biology, Stanford University, Stanford, CA, USA
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Filip Wierzbicki
4Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria
5Vienna Graduate School of Population Genetics, Vienna, Austria
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Robert Kofler
4Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria
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Eric C. Lai
2Developmental Biology Program, Sloan-Kettering Institute, 430 East 67th St, ROC-10, New York, NY 10065, USA
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  • ORCID record for Eric C. Lai
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Abstract

Effective suppression of transposable elements (TEs) is paramount to maintain genomic integrity and organismal fitness. In D. melanogaster, flamenco is a master suppressor of TEs, preventing their movement from somatic ovarian support cells to the germline. It is transcribed by Pol II as a long (100s of kb), single-stranded, primary transcript, that is metabolized into Piwi-interacting RNAs (piRNAs) that target active TEs via antisense complementarity. flamenco is thought to operate as a trap, owing to its high content of recent horizontally transferred TEs that are enriched in antisense orientation. Using newly-generated long read genome data, which is critical for accurate assembly of repetitive sequences, we find that flamenco has undergone radical transformations in sequence content and even copy number across simulans clade Drosophilid species. D. simulans flamenco has duplicated and diverged, and neither copy exhibits synteny with D. melanogaster beyond the core promoter. Moreover, flamenco organization is highly variable across D. simulans individuals. Next, we find that D. simulans and D. mauritiana flamenco display signatures of a dual-stranded cluster, with ping-pong signals in the testis and/or embryo. This is accompanied by increased copy numbers of germline TEs, consistent with these regions operating as functional dual stranded clusters. Overall, the physical and functional diversity of flamenco orthologs is testament to the extremely dynamic consequences of TE arms races on genome organization, not only amongst highly related species, but even amongst individuals.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • An author was added, Figures 1 and 5 were revised.

Copyright 
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 November 17, 2022.
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Rapid evolutionary diversification of the flamenco locus across simulans clade Drosophila species
Sarah Signor, Jeffrey Vedanayagam, Bernard Y. Kim, Filip Wierzbicki, Robert Kofler, Eric C. Lai
bioRxiv 2022.09.29.510127; doi: https://doi.org/10.1101/2022.09.29.510127
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Rapid evolutionary diversification of the flamenco locus across simulans clade Drosophila species
Sarah Signor, Jeffrey Vedanayagam, Bernard Y. Kim, Filip Wierzbicki, Robert Kofler, Eric C. Lai
bioRxiv 2022.09.29.510127; doi: https://doi.org/10.1101/2022.09.29.510127

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