Abstract
In most animals, the bulk of sperm DNA is packaged with sperm nuclear basic proteins (SNBPs), a diverse group of highly basic chromosomal proteins notably comprising mammalian protamines. The replacement of histones with SNBPs during spermiogenesis allows sperm DNA to reach an extreme level of compaction, but little is known about how SNBPs actually function in vivo. Mst77F is a Drosophila SNBP with unique DNA condensation properties in vitro, but its role during spermiogenesis remains unclear. Here, we show that Mst77F is required for the compaction of sperm DNA and the production of mature sperm, through its cooperation with protamine-like proteins Mst35Ba/b. We demonstrate that Mst77F is incorporated in spermatid chromatin as a precursor protein, which is subsequently processed through the proteolysis of its N-terminus. The cleavage of Mst77F is very similar to the processing of protamine P2 during human spermiogenesis and notably leaves the cysteine residues in the mature protein intact, suggesting that they participate in the formation of disulfide cross-links. Despite the rapid evolution of SNBPs, sperm chromatin condensation thus involves remarkably convergent mechanisms in distantly related animals.
Highlights
Spermiogenesis, the differentiation of post-meiotic spermatids into mature spermatozoa, generally involves major cellular reorganization events, such as the elimination of cytoplasm and the growth of a sperm flagellum [1]
We demonstrate that Male-specific transcript 77F (Mst77F) is required for the proper compaction of spermatid chromatin following the histone-to-protamine transition
The analysis of loss-of-function alleles of Mst77F demonstrates that this sperm nuclear basic proteins (SNBPs) is required for male fertility by allowing the proper organization of sperm chromatin following the histone-to-protamine transition
Summary
Spermiogenesis, the differentiation of post-meiotic spermatids into mature spermatozoa, generally involves major cellular reorganization events, such as the elimination of cytoplasm and the growth of a sperm flagellum [1]. Sperm DNA compaction is achieved through the replacement of nucleosomes with sperm nuclear basic proteins (SNBPs), such as the well-known mammalian protamines [2–4]. Drosophila is an excellent model for the study of sperm chromatin remodelling at the functional level, as the process shares several key features with the mammalian histone-to-protamine transition [5]. In Drosophila, as in most mammals, the vast majority of nucleosomes are replaced by SNBPs, with the notable exception of epigenetic determinants of sperm centromere identity [6–9]. Histones are transiently replaced with transition proteins before the final deposition of SNBPs [7,10]. The mechanism of de novo assembly of paternal nucleosomes at fertilization is remarkably conserved and involves the HIRA histone chaperone complex [12 –16]
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