Abstract
We have analyzed the chromosomal protein composition of the sperm from several species belonging to three different classes (Hydrozoa, Scyphozoa, Anthozoa) of the phylum Cnidaria. In every instance, the sperm nuclear basic proteins (SNBPs) were found to consist of one to two major protein fractions that belong to the histone H1 family, as can be deduced from their amino acid composition and solubility in dilute perchloric acid, and the presence of a trypsin-resistant core. In those species where mature spawned sperm could be obtained, we were able to show that these proteins completely replace the somatic histones from the stem cells that are present at the onset of spermatogenesis. The presence of a highly specialized histone H1 molecule in the sperm of this phylum provides support for the idea that the protamine-like proteins (PL) from higher groups in the phylogenetic tree (and possibly protamines as well) may all have evolved from a primitive histone H1 ancestor.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- SNBPs:
-
sperm nuclear basic proteins
- PL:
-
protamine-like protein
- HPLC:
-
high-performance liquid chromatography
- TFA:
-
trifluoroacetic acid
- PAGE:
-
polyacrylamide gel electrophoresis
- PCA:
-
perchloric acid
References
Ausio J (1986) Structural variability and compositional homology of the protamine-like components of the sperm from bivalve molluscs. Comp Biochem Physiol 85B:439–449
Ausio J (1988) An unusual cysteine-containing histone H1-like protein and two protamine-like proteins are the major nuclear proteins of the sperm of the bivalve molluscMacoma nasuta. J Biol Chem 263:10141–10150
Ausio J (1992a) Presence of a highly specific histone H1-like protein in the chromatin of the sperm of the bivalve mollusks. Mol Cell Biochem 115:163–172
Ausio J (1992b) Purification and biochemical characterization of the nuclear sperm-specific proteins of the bivalve mollusksAgriodesma saxicola andMytilimeria nuttalli. Biol Bull 182:31–40
Ausio J (1995) Histone H1 and the evolution of the nuclear sperm-specific proteins. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoal taxonomy and phylogeny. Paris: Memoires de Muséum National d'Histoire Naturelle 166:447–462
Ausio J, Subirana JA (1982) A high molecular weight nuclear basic protein from the bivalve molluskSpisula solidissima. J Biol Chem 257:2802–2805
Ausio J, Toumadje A, McParland R, Becker RR, Johnson WC Jr, van Holde KE (1987) Structural characterization of the trypsin resistant core in the nuclear sperm-specific protein fromSpisula solidissima. Biochemistry 26:975–982
Bloch DP (1969) A catalog of sperm histones. Genetics (Suppl) 61:93–111
Bloch DP (1976) Histones of sperm. In: King RC (ed) Handbook of genetics, vol 5. New York: Plenum, pp 139–167
Carlos S, Hunt DF, Rocchini C, Amott DP, Ausio J (1993a) Post-translational cleavage of a histone H1-like protein in the sperm ofMytilus. J Biol Chem 268:195–199
Carlos S, Jutglar L, Borrell I, Hunt DF, Ausio J (1993b) Sequence and characterization of a sperm-specific histone H1-like protein ofMytilus californianus. J Biol Chem 268:185–194
Cole RD (1984) A minireview of microheterogeneity of H1 histone and its possible significance. Anal Biochem 136:24–30
Isenberg I (1978) Histones. In: Busch H (ed) The cell nucleus, vol 4, part A. Academic Press, New York, pp 435–154
Kasinsky HE (1989) Specificity and distribution of sperm basic proteins. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and other basic nuclear proteins. CRC Press, Boca Ratón, FL, pp 73–163
Laverack MS, Dando J (1979) Lecture notes on invertebrate zoology, 2nd ed. Blackwell Scientific, Oxford, p 30
Mayes ELV, Johns EW (1982) Accumulated data. In: Johns EW (ed) The HMG chromosomal proteins. Academic Press, New York, pp 223–247
Neelin JM (1968) Variability in cell-specific and common histones of avian erythrocytes. Can J Biochem 46:241–247
Rozov SM, Gorel FL, Kozlova SV, Berdnikov VA (1986) Histone H1 of the jellyfishRhizostoma pulmo: homology with avian histone H5. Mol Biol 20:163–170 (English translation, Mol Biol 20:136–142)
Saperas N, Chiva M, Ausio J (1992) Purification and characterization of the protamines and related proteins form the sperm of a tunicate,Styela plicata. Comp Biochem Physiol 103B:969–974
Saperas N, Chiva M, Ribes E, Kasinsky HE, Rosenberg E, Youson JH, Ausio J (1994a) Chromosomal proteins of the sperm of a cephalochordate (Branchiostoma floridae) and an agnathan (Petromyzon marinus): compositional variability of the nuclear sperm proteins in deuterostomes. Biol Bull 186:101–114
Saperas N, Ausio J, Domenec L, Chiva M (1994b) On the evolution of protamines in bony fish: alternatives to the “retroviral horizontal transmission” hypothesis. J Mol Evol 39:282–295
Subirana JA, Cozculluela C, Palau J, Unzeta M (1973) Protamines and other basic proteins from spermatozoa of molluscs. Biochim Biophys Acta 317:364–379
van Holde KE (1988) Chromatin. Springer Verlag, New York, p 1
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rocchini, C., Marx, R.M., Schnorr von Carosfeld, J. et al. Replacement of nucleosomal histones by histone H1-like proteins during spermiogenesis in Cnidaria: Evolutionary implications. J Mol Evol 42, 240–246 (1996). https://doi.org/10.1007/BF02198850
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02198850