Heterochromatin-dependent transcription of satellite DNAs in the Drosophila melanogaster female germline

  1. Xiaolu Wei  Is a corresponding author
  2. Danna G Eickbush
  3. Iain Speece
  4. Amanda M Larracuente  Is a corresponding author
  1. University of Rochester, United States

Abstract

Large blocks of tandemly repeated DNAs-satellite DNAs (satDNAs)-play important roles in heterochromatin formation and chromosome segregation. We know little about how satDNAs are regulated, however their misregulation is associated with genomic instability and human diseases. We use the Drosophila melanogaster germline as a model to study the regulation of satDNA transcription and chromatin. Here we show that complex satDNAs (>100-bp repeat units) are transcribed into long noncoding RNAs and processed into piRNAs (PIWI interacting RNAs). This satDNA piRNA production depends on the Rhino-Deadlock-Cutoff complex and the transcription factor Moonshiner—a previously-described non-canonical pathway that licenses heterochromatin-dependent transcription of dual-strand piRNA clusters. We show that this pathway is important for establishing heterochromatin at satDNAs. Therefore, satDNAs are regulated by piRNAs originating from their own genomic loci. This novel mechanism of satDNA regulation provides insight into the role of piRNA pathways in heterochromatin formation and genome stability.

Data availability

Sequencing data generated in this study have been deposited in NCBI Sequence Read Archive (SRA) under project accession PRJNA647441. Published sequencing data used in this study are from NCBI SRA database, and the full list of accession numbers can be found in Supplementary File 1.

The following data sets were generated

Article and author information

Author details

  1. Xiaolu Wei

    Biomedical Genetics, University of Rochester, Rochester, United States
    For correspondence
    xiaolu_wei@urmc.rochester.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9952-3757
  2. Danna G Eickbush

    Biology, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Iain Speece

    Biology, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Amanda M Larracuente

    Biology, University of Rochester, Rochester, United States
    For correspondence
    alarracu@bio.rochester.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5944-5686

Funding

National Institutes of Health (R35 GM119515)

  • Amanda M Larracuente

University of Rochester (Stephen Biggar and Elisabeth Asaro fellowship)

  • Amanda M Larracuente

University of Rochester (Messersmith Fellowship)

  • Xiaolu Wei

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Publication history

  1. Received: August 22, 2020
  2. Accepted: July 8, 2021
  3. Accepted Manuscript published: July 13, 2021 (version 1)
  4. Version of Record published: July 29, 2021 (version 2)

Copyright

© 2021, Wei et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Xiaolu Wei
  2. Danna G Eickbush
  3. Iain Speece
  4. Amanda M Larracuente
(2021)
Heterochromatin-dependent transcription of satellite DNAs in the Drosophila melanogaster female germline
eLife 10:e62375.
https://doi.org/10.7554/eLife.62375

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