How mammals pack their sperm: a variant matter

Abstract

Producing competent gametes is essential for transmitting genetic information throughout generations. Spermatogenesis is a unique example of rearrangements of genome packaging to ensure fertilization. After meiosis, spermatids undergo drastic morphological changes, perhaps the most dramatic ones occurring in their nuclei, including the transition into a protamine-packaged genome. In this issue of Genes & Development, Montellier and colleagues (pp. 1680–1692) shed new light on the molecular mechanisms regulating this transition by ascribing for the first time a function to a histone variant, TH2B, in the regulation of this process.

Chromatin remodelling during male gametophyte development

“…Packaging of the mammalian paternal genome as protamine‐associated DNA also involves testis‐specific histone variants, which mark specific regions of the genome to facilitate its compaction and reorganisation (Rousseaux et al ., ; Boussouar et al ., ). Several testis‐specific histone variants have been described in animals that provide the means to dynamically rearrange chromatin during each stage of spermatogenesis (Boskovic and Torres‐Padilla, ). In mice, the testis‐specific histone H2B variant TH2B orchestrates the final events of protamine exchange by promoting nucleosome instability to favour protamine packaging of sperm DNA (Montellier et al ., ).…”

“…Subtle phenotypes are often observed in histone knock‐out studies and it is speculated that inherent buffering systems can sometimes mask functional heterogeneity (Drabent et al ., ; Lin et al ., ; Brown, ; Maze et al ., ). Because SCs are integral to species propagation, it is perhaps unsurprising that compensatory mechanisms exist and emphasises the plasticity and resourcefulness of the germline (Boskovic and Torres‐Padilla, ). The fact that H3.10 is under direct regulatory control of DUO1 suggests a role in shaping the chromatin landscape to facilitate germline fate specification and to remove epigenetic marks typical of somatic cells.…”

Timing in the Testis

“…Like space travelers who must jettison weight in order to achieve escape velocity for a journey into orbit (Weir, 2014), they condense both cytoplasm and chromatin. In this process, DNA becomes wrapped in a condensed, toroidal structure around protamines, and heterochromatin is found only in a few regions (largely near the centromeres and telomeres) that preserve histones (Boskovic and Torres-Padilla, 2013). The drastic reduction of gene expression likely includes a suspension of clock gene transcription.…”

Ultrastructure of spermiogenesis and the distribution of spermatozoal nuclear histones in the Japanese mantis shrimp, Oratosquilla oratoria (Crustacea: Stomatopoda)

“…SBNPs have been identified in the sponge Neofibularia nolitangere , in which only canonical histones are present (Ausió, Van Veghel, Gomez, & Barreda, ). Several histone variants, such as the H3.3, H2A.X, and H2B variants, have been confirmed as being crucial for sperm DNA packaging in vertebrates and marine invertebrates (Boskovic & Torrespadilla, ; Török et al, ; Török & Gornik, ; Zini, Zhang, & Gabriel, ). We speculated that mantis shrimp sperm may present a nucleosome chromatin structure in the presence of histones H2A, H2B, H3, and H4 in the nucleus.…”