Spermiogenic nuclear protein transitions and chromatin condensation. Proposal for an ancestral model of nuclear spermiogenesis

Abstract

We have chosen three species (Sparus aurata, Dicentrarchus labrax, and Monodonta turbinata) that represent different transition patterns in the composition and structure of spermiogenic nuclei. The transition patterns of these species are representative of spermiogenesis in a large number of animal species. We analyze: (a) nuclear protein exchange; (b) chromatin condensation pattern; and (c) histone acetylation during spermiogenic development. In the simplest spermiogenesis histones and nucleosomes remain in mature sperm. Chromatin of spermatids is organized into 20 nm granules, simultaneous with a nuclear volume reduction. The granules coalesce in the final stage of spermiogenesis. Granular chromatin is correlated with acetylation of histones H3 and H4, whereas final coalescence is associated with histone deacetylation. We also studied two other spermiogenesis where a basic protein substitutes histones. Each species has a very different substituting protein. One has a typical protamine of 34 amino acids; the other has a sperm nuclear basic proteins (SNBP) of 106 amino acids. In both, the structural transitions and histone acetylation pattern are similar: in early spermiogenesis chromatin is organized into 20 nm granules, and histones are significantly acetylated, while the nuclear volume decreases. Subsequently, acetylated histones are displaced by the protamine or SNBP. Histone substitution causes chromatin remodelling and additional reduction in nuclear volume. We analyze these three cases together with earlier works and propose that the formation of 20 nm granules containing acetylated H3 and H4 accomplishes the minimum functional requirement to be considered the most evolutionarily ancestral chromatin conformation preceding condensation in animal spermiogenesis.