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Reactivation of a somatic errantivirus and germline invasion in Drosophila ovaries

Author

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  • Marianne Yoth

    (iGReD, Université Clermont Auvergne, CNRS, INSERM, Faculté de Médecine)

  • Stéphanie Maupetit-Méhouas

    (iGReD, Université Clermont Auvergne, CNRS, INSERM, Faculté de Médecine)

  • Abdou Akkouche

    (iGReD, Université Clermont Auvergne, CNRS, INSERM, Faculté de Médecine)

  • Nathalie Gueguen

    (iGReD, Université Clermont Auvergne, CNRS, INSERM, Faculté de Médecine)

  • Benjamin Bertin

    (LIMAGRAIN EUROPE, Centre de recherche)

  • Silke Jensen

    (iGReD, Université Clermont Auvergne, CNRS, INSERM, Faculté de Médecine)

  • Emilie Brasset

    (iGReD, Université Clermont Auvergne, CNRS, INSERM, Faculté de Médecine)

Abstract

Most Drosophila transposable elements are LTR retrotransposons, some of which belong to the genus Errantivirus and share structural and functional characteristics with vertebrate endogenous retroviruses. Like endogenous retroviruses, it is unclear whether errantiviruses retain some infectivity and transposition capacity. We created conditions where control of the Drosophila ZAM errantivirus through the piRNA pathway was abolished leading to its de novo reactivation in somatic gonadal cells. After reactivation, ZAM invaded the oocytes and severe fertility defects were observed. While ZAM expression persists in the somatic gonadal cells, the germline then set up its own adaptive genomic immune response by producing piRNAs against the constantly invading errantivirus, restricting invasion. Our results suggest that although errantiviruses are continuously repressed by the piRNA pathway, they may retain their ability to infect the germline and transpose, thus allowing them to efficiently invade the germline if they are expressed.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41733-5
    DOI: 10.1038/s41467-023-41733-5
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    References listed on IDEAS

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    1. Yoshinori Kawamura & Kuniaki Saito & Taishin Kin & Yukiteru Ono & Kiyoshi Asai & Takafumi Sunohara & Tomoko N. Okada & Mikiko C. Siomi & Haruhiko Siomi, 2008. "Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells," Nature, Nature, vol. 453(7196), pages 793-797, June.
    2. Edward J. Grow & Ryan A. Flynn & Shawn L. Chavez & Nicholas L. Bayless & Mark Wossidlo & Daniel J. Wesche & Lance Martin & Carol B. Ware & Catherine A. Blish & Howard Y. Chang & Renee A. Reijo Pera & , 2015. "Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells," Nature, Nature, vol. 522(7555), pages 221-225, June.
    3. Paulo Navarro-Costa & Alicia McCarthy & Pedro Prudêncio & Christina Greer & Leonardo G. Guilgur & Jörg D. Becker & Julie Secombe & Prashanth Rangan & Rui G. Martinho, 2016. "Early programming of the oocyte epigenome temporally controls late prophase I transcription and chromatin remodelling," Nature Communications, Nature, vol. 7(1), pages 1-15, November.
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    Cited by:

    1. 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.

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