Abstract
ABSTRACTDuring spermiogenesis, haploid spermatids undergo extensive chromatin remodeling events in which histones are successively replaced by more basic protamines to generate highly compacted chromatin. Here we show for the first time that H3K79 methylation is a conserved feature preceding the histone-to-protamine transition in Drosophila melanogaster and rat. During Drosophila spermatogenesis, the Dot1-like methyltransferase Grappa (Gpp) is primarily expressed in canoe stage nuclei. The corresponding H3K79 methylation is a histone modification that precedes the histone-to-protamine transition and correlates with histone H4 hyperacetylation. When acetylation was inhibited in cultured Drosophila testes, nuclei were smaller and chromatin was compact, Gpp was little synthesized, H3K79 methylation was strongly reduced, and protamines were not synthesized. The Gpp isoform Gpp-D has a unique C-terminus, and Gpp is essential for full fertility. In rat, H3K79 methylation also correlates with H4 hyperacetylation but not with active RNA polymerase II, which might point towards a conserved function in chromatin remodeling during the histone-to-protamine transition in both Drosophila and rat.
Highlights
IntroductionThe transition from a nucleosomal histone-based structure to a protamine-based structure is a highly conserved, unique event in most invertebrates and vertebrates, including Drosophila and humans (reviewed by Barckmann et al, 2013; Braun, 2001; Oliva, 2006; Rathke et al, 2014)
During spermatogenesis, the transition from a nucleosomal histone-based structure to a protamine-based structure is a highly conserved, unique event in most invertebrates and vertebrates, including Drosophila and humans
We found that the H3K79 methyltransferase Grappa (Gpp) is expressed in canoe stage nuclei during spermiogenesis and that H3K79 methylation is a conserved histone modification that precedes histone removal both in Drosophila and rat
Summary
The transition from a nucleosomal histone-based structure to a protamine-based structure is a highly conserved, unique event in most invertebrates and vertebrates, including Drosophila and humans (reviewed by Barckmann et al, 2013; Braun, 2001; Oliva, 2006; Rathke et al, 2014). Received 3 December 2013; Accepted 3 March 2014 called spermiogenesis, somatic histones that build the nucleosomal structure are first replaced by testis-specific histone variants. These histone variants are replaced by small transition proteins, which in turn are replaced by highly basic and much smaller protamines, resulting in highly compacted chromatin with a doughnut-like structure (Braun, 2001; Kimmins and Sassone-Corsi, 2005; Sassone-Corsi, 2002). Analogous to the situation in mammals, histones in Drosophila are replaced stepwise by transition-like proteins and protamines (Jayaramaiah Raja and Renkawitz-Pohl, 2005; Rathke et al, 2007; Rathke et al, 2010)
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