In which taxa did H1 linker histones appear in the course of evolution? Detailed comparative analysis of the histone H1 and histone H1-related sequences available to date suggests that the origin of histone H1 can be traced to bacteria. The data also reveal that the sequence corresponding to the 'winged helix' motif of the globular structural domain, a domain characteristic of all metazoan histone H1 molecules, is evolutionarily conserved and appears separately in several divergent lines of protists. Some protists, however, appear to have only a lysine-rich basic protein, which has compositional similarity to some of the histone H1-like proteins from eubacteria and to the carboxy-terminal domain of the H1 linker histones from animals and plants. No lysine-rich basic proteins have been described in archaebacteria. The data presented in this review provide the surprising conclusion that whereas DNA-condensing H1-related histones may have arisen early in evolution in eubacteria, the appearance of the sequence motif corresponding to the globular domain of metazoan H1s occurred much later in the protists, after and independently of the appearance of the chromosomal core histones in archaebacteria.

Despite their relatively arginine-rich composition, protamines exhibit a high degree of structural variation. Indeed, the primary structure of these histone H1-related sperm nuclear basic proteins (SNBPs) is not random and is the depository of important phylogenetic information. This appears to be the result of their fast rate of evolution driven by positive selection. The way by which the protein variability participates in the transitions that lead to the final highly condensed chromatin organization of spermatozoa at the end of spermiogenesis is not clearly understood. In this paper we focus on the transient chromatin/nucleoplasm patterning that occurs in either a lamellar step or an inversion step during early and mid-spermiogenesis. This takes place in a small subset of protamines in internally fertilizing species of vertebrates, invertebrates and plants. It involves "complex" protamines that are processed, replaced, or undergo side chain modification (such as phosphorylation or disulfide bond formation) during the histone-to-protamine transition. Characteristic features of such patterning, as observed in TEM photomicrographs, include: constancy of the dominant pattern repeat distance λ(m) despite dynamic changes in developmental morphology, bicontinuity of chromatin and nucleoplasm, and chromatin orientation either perpendicular or parallel to the nuclear envelope. This supports the hypothesis that liquid - liquid phase separation by the mechanism of spinodal decomposition may be occurring during spermiogenesis in these species. Spinodal decomposition involves long wave fluctuations of the local concentration with a low energy barrier and thus differs from the mechanism of nucleation and growth that is known to occur during spermiogenesis in internally fertilizing mammals.

During spermiogenesis in some internally fertilizing molluscs and insects, the post-meiotic spermatid nucleus develops via a sequence of complex patterns of the nuclear contents (chromatin and nucleoplasm) on the way to final chromatin condensation. We have examined the TEM data on these sequences for three species: Philaenus spumarius(a homopteran insect), Murex brandaris (a gastropod mollusc), and Eledone cirrhosa(a cephalopod mollusc). For each of these, spatially quantitative study reveals a constant spacing between pattern repeats through changes from granular to fibrillar to lamellar pattern, followed finally by a shrinkage of the spacing. Therefore we distinguish a "patterning" stage followed by a "condensation" stage. The former appears to demand a dynamic explanation, because there is no sign of structural connections to establish the part of the spacing that crosses the nucleoplasm. We consider types of dynamic mechanism, and show that for "nanostructural" dimensions (tens of nanometers as pattern spacing) reaction-diffusion dynamics are quite inappropriate, but that separation of two fluid phases by a mechanism similar to what is known as "spinodal decomposition" is a very attractive possibility.

Spermatid/sperm basic chromosomal proteins from 17 species and subspecies of the genus Xenopus (Anura, Pipidae) were compared. Electrophoresis on acetic acid/urea/Triton X-100 polyacrylamide gels revealed that each Xenopus species with a diploid chromosome number of 36, 72, or 108 showed multiple, diverse spermatid/sperm-specific basic chromatin proteins with mobilities greater than the somatic histones. The numbers and mobilities of these proteins were characteristic of each Xenopus species and each subspecies of Xenopus laevis. Cytochemical tests revealed that the sperm basic nuclear proteins of these Xenopus species and subspecies were rich in arginine and lysine and contained more arginine than the nuclear proteins of somatic cells. X. tropicalis (2n = 20) and X. sp. n. (Zaire) displayed spermatid/sperm-specific basic chromatin proteins which migrated within the histone H1 region of acetic acid/urea/Triton X-100 polyacrylamide gels. Cytochemically the sperm nuclei of these species resembled those of somatic cells. These observations suggest that spermatid/sperm basic nuclear proteins can be used as molecular markers for individual species and subspecies of the genus Xenopus.

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