RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster

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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.

Data availability

All generated data are included within manuscript

The following previously published data sets were used

1. Brown
(2014) Diversity and dynamics of the Drosophila transcriptome
Nature, 12962.

https://www.nature.com/articles/nature12962#s1

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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.

"This ORCID iD identifies the author of this article:" 0000-0002-4842-4190
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.

"This ORCID iD identifies the author of this article:" 0000-0002-0081-7892
Antje M Kochendoerfer

Centre for Chromosome Biology, National University of Ireland Galway, Galway, Ireland

Competing interests
The authors declare that no competing interests exist.
Elaine Dunleavy

Centre for Chromosome Biology, National University of Ireland Galway, Galway, Ireland

Competing interests
The authors declare that no competing interests exist.
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.

"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.

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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.