RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster
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.
- Authors:
-
[1];
[2];
[3];
[3];
[4]
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Irvine, CA (United States)
- National Univ. of Ireland, Galway (Ireland)
- Univ. of California, Berkeley, CA (United States);
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Institutes of Health (NIH); National Science Foundation (NSF); Science Foundation Ireland–Health Research Board–Wellcome Trust (SFI-HRB-WT); Science Foundation Ireland –President of Ireland Young Research Award (SFI-PIYRA)
- OSTI Identifier:
- 1591826
- Grant/Contract Number:
- [AC02-05CH11231; RO1 GM117420; 00105/Z/12/Z; K99 GM121868; 13/YI/2187]
- Resource Type:
- Accepted Manuscript
- Journal Name:
- eLife
- Additional Journal Information:
- [ Journal Volume: 8]; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; cell biology; chromosomes and gene expression; satellite RNA; heterochromatin; non-coding RNA; spermatogenesis; histone-protamine exchange; repetitive RNA
Citation Formats
Mills, Wilbur Kyle, Lee, Yuh Chwen G., Kochendoerfer, Antje M., Dunleavy, Elaine M., and Karpen, Gary H. RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster. United States: N. p., 2019.
Web. doi:10.7554/eLife.48940.
Mills, Wilbur Kyle, Lee, Yuh Chwen G., Kochendoerfer, Antje M., Dunleavy, Elaine M., & Karpen, Gary H. RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster. United States. doi:10.7554/eLife.48940.
Mills, Wilbur Kyle, Lee, Yuh Chwen G., Kochendoerfer, Antje M., Dunleavy, Elaine M., and Karpen, Gary H. Tue .
"RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster". United States. doi:10.7554/eLife.48940. https://www.osti.gov/servlets/purl/1591826.
@article{osti_1591826,
title = {RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster},
author = {Mills, Wilbur Kyle and Lee, Yuh Chwen G. and Kochendoerfer, Antje M. and Dunleavy, Elaine M. and Karpen, Gary H.},
abstractNote = {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.},
doi = {10.7554/eLife.48940},
journal = {eLife},
number = ,
volume = [8],
place = {United States},
year = {2019},
month = {11}
}
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