1. Cell Biology
  2. Chromosomes and Gene Expression
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RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster

  1. Wilbur Kyle Mills
  2. Grace Yuh Chwen Lee
  3. Antje M Kochendoerfer
  4. Elaine Dunleavy
  5. Gary H Karpen  Is a corresponding author
  1. University of California, Berkeley, United States
  2. National University of Ireland Galway, Ireland
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Cite this article as: eLife 2019;8:e48940 doi: 10.7554/eLife.48940

Abstract

Tandemly-repeated DNAs, or satellites, are enriched in heterochromatic regions of eukaryotic genomes and contribute to nuclear structure and function. Some satellites are transcribed, but we lack direct evidence that specific satellite RNAs are required for normal organismal functions. Here, we show satellite RNAs derived from AAGAG tandem repeats are transcribed in many cells throughout Drosophila melanogaster development, enriched in neurons and testes, often localized within heterochromatic regions, and important for viability. Strikingly, we find AAGAG transcripts are necessary for male fertility, and that AAGAG RNA depletion results in defective histone-protamine exchange, sperm maturation and chromatin organization. Since these events happen late in spermatogenesis when the transcripts are not detected, we speculate that AAGAG RNA in primary spermatocytes 'primes' post-meiosis steps for sperm maturation. In addition to demonstrating essential functions for AAGAG RNAs, comparisons between closely related Drosophila species suggest that satellites and their transcription evolve quickly to generate new functions.

Article and author information

Author details

  1. Wilbur Kyle Mills

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4842-4190
  2. Grace Yuh Chwen Lee

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0081-7892
  3. Antje M Kochendoerfer

    Centre for Chromosome Biology, National University of Ireland Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  4. Elaine Dunleavy

    Centre for Chromosome Biology, National University of Ireland Galway, Galway, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  5. Gary H Karpen

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    GHKarpen@lbl.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1534-0385

Funding

National Institutes of Health (RO1 GM117420)

  • Gary H Karpen

National Science Foundation (Graduate Research Fellowship)

  • Wilbur Kyle Mills

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

Reviewing Editor

  1. Howard Y Chang, Stanford University, United States

Publication history

  1. Received: May 31, 2019
  2. Accepted: November 3, 2019
  3. Accepted Manuscript published: November 5, 2019 (version 1)

Copyright

© 2019, Mills 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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