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.

CHD5 is required for spermiogenesis and chromatin condensation

“…CHD5 may play different roles in different cell types, and so the suppression of cell growth and facilitating chromatin condensation are only two aspects of this protein’s chromatin-remodeling functions (Saito et al, 2010). There are many factors at work during chromatin condensation in elongating spermatids (Forgione et al, 2010; Kurtz et al, 2009; Steilmann et al, 2010), so it would be of great interest to identify the cofactor(s) that interact with CHD5 in these haploid cells. Additionally, elucidation of the chromatin element (histone, TP, protamine) ratios and their modification status (Awe and Renkawitz-Pohl, 2010; Song et al, 2011; Vigodner, 2011) would be of great help in understanding the role CHD5 plays in spermiogenesis.…”

Sperm ultrastructure of the spider crab Maja brachydactyla (Decapoda: Brachyura)

“…The chromatin is noncondensed and is organized into fibers of approximately 10 nm of diameter, similar to the size of a nucleosome (see the discussions by Kurtz et al, 2007;Martínez-Soler et al, 2007b). Indeed, the chromatin does not seem to be organized into superior structures such as the granules or fibers with a diameter of 20 nm or greater observed in other non-crustacean species (Gimenez-Bonafé et al, 2002;Martínez-Soler et al, 2007a;Kurtz et al, 2009b). However, the chromatin is not completely uniform throughout the nucleus, and the chromatin fibers seem to agglutinate in several more electron-dense areas, around the SO-complex and at the base of the lateral arms.…”

The shades of gray of the chromatin fiber

“…Rather, histone acetylated fibro‐granular structures of about 20 nm are present in the late mature spermatids before these fibers coalesce into the un‐acetylated electron‐dense chromatin of the sperm . According to these authors the granules “can contain four to six nucleosomes” . Such fibrogranular structures are reminiscent of the earlier described tetranucleosome structures that were visualized by crystallographic imaging of reconstituted chromatin.…”