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.
Highlights
Long arrays of tandemly repeated short DNA sequences are abundant in centromeres (Sun et al, 2003) and pericentromeric regions (Hoskins et al, 2007), and contribute to chromosome segregation and other heterochromatin functions (Dernburg et al, 1996; Ferree and Barbash, 2009)
This conclusion is supported by the results of RNase digestion experiments, which demonstrate that cycle 14 AAGAG RNA foci contain single-stranded RNA, and not R-loops or double-stranded RNA (Figure 1—figure supplement 3)
We demonstrate that AAGAG(n) satellite RNAs are transcribed from heterochromatic regions on multiple chromosomes, cluster into nuclear foci, associate with the earliest forms of heterochromatin in embryos, and persist throughout fly development
Summary
Long arrays of tandemly repeated short DNA sequences (known as satellites) are abundant in centromeres (Sun et al, 2003) and pericentromeric regions (Hoskins et al, 2007), and contribute to chromosome segregation and other heterochromatin functions (Dernburg et al, 1996; Ferree and Barbash, 2009). Satellite transcription and/or RNAs may promote centromere and heterochromatin functions (McNulty et al, 2017; Johnson et al, 2017; Velazquez Camacho et al, 2017; Shirai et al, 2017; Rosicet al., 2014). Given the emerging roles of non-protein coding RNAs (ncRNAs) in chromatin organization and other biological functions (Rinn and Chang, 2012), we investigated whether heterochromatic satellite transcripts are required for normal viability and development
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