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Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus

Author

Listed:
  • Jasper Lopik

    (University of Cambridge, Li Ka Shing Centre)

  • Azad Alizada

    (University of Cambridge, Li Ka Shing Centre)

  • Maria-Anna Trapotsi

    (University of Cambridge, Li Ka Shing Centre)

  • Gregory J. Hannon

    (University of Cambridge, Li Ka Shing Centre)

  • Susanne Bornelöv

    (University of Cambridge, Li Ka Shing Centre)

  • Benjamin Czech Nicholson

    (University of Cambridge, Li Ka Shing Centre)

Abstract

The PIWI-interacting RNA (piRNA) pathway prevents endogenous genomic parasites, i.e. transposable elements, from damaging the genetic material of animal gonadal cells. Specific regions in the genome, called piRNA clusters, are thought to define each species’ piRNA repertoire and therefore its capacity to recognize and silence specific transposon families. The unistrand cluster flamenco (flam) is essential in the somatic compartment of the Drosophila ovary to restrict Gypsy-family transposons from infecting the neighbouring germ cells. Disruption of flam results in transposon de-repression and sterility, yet it remains unknown whether this silencing mechanism is present more widely. Here, we systematically characterise 119 Drosophila species and identify five additional flam-like clusters separated by up to 45 million years of evolution. Small RNA-sequencing validated these as bona-fide unistrand piRNA clusters expressed in somatic cells of the ovary, where they selectively target transposons of the Gypsy family. Together, our study provides compelling evidence of a widely conserved transposon silencing mechanism that co-evolved with virus-like Gypsy-family transposons.

Suggested Citation

  • Jasper Lopik & Azad Alizada & Maria-Anna Trapotsi & Gregory J. Hannon & Susanne Bornelöv & Benjamin Czech Nicholson, 2023. "Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42787-1
    DOI: 10.1038/s41467-023-42787-1
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    References listed on IDEAS

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    1. Marianne Yoth & Stéphanie Maupetit-Méhouas & Abdou Akkouche & Nathalie Gueguen & Benjamin Bertin & Silke Jensen & Emilie Brasset, 2023. "Reactivation of a somatic errantivirus and germline invasion in Drosophila ovaries," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Felipe Karam Teixeira & Martyna Okuniewska & Colin D. Malone & Rémi-Xavier Coux & Donald C. Rio & Ruth Lehmann, 2017. "piRNA-mediated regulation of transposon alternative splicing in the soma and germ line," Nature, Nature, vol. 552(7684), pages 268-272, December.
    3. Peter Refsing Andersen & Laszlo Tirian & Milica Vunjak & Julius Brennecke, 2017. "A heterochromatin-dependent transcription machinery drives piRNA expression," Nature, Nature, vol. 549(7670), pages 54-59, September.
    4. Cynthia Dennis & Emilie Brasset & Arpita Sarkar & Chantal Vaury, 2016. "Export of piRNA precursors by EJC triggers assembly of cytoplasmic Yb-body in Drosophila," Nature Communications, Nature, vol. 7(1), pages 1-12, December.
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