Abstract
Fish protamines are highly specialized molecules which are responsible for chromatin condensation during the last stages of spermatogenesis (spermiogenesis). However, not all fish contain protamines in their sperm nuclei; rather, there seems to be a random distribution of protamines within this group. The origin of this sporadic presence of protamines in the sperm and its significance have not yet been precisely determined. In this paper we have conducted an exhaustive survey of the literature available on the different types of nuclear protein composition of the sperm of teleost fish in order to try to correlate these data with what is presently known about the taxonomy of this group. The results of this analysis have allowed us to make the following observations. The divergence between protamines and histones has occurred several times during the evolution of the bony fish. However, the relative frequency of this divergence is almost negligible during the differentiation of genera and species (intrafamily variation) and is very small during the differentiation of families (interfamily variation). Nevertheless, the divergence is very noticeable among the different orders. It is therefore possible to conclude from all this that the sporadic distribution of protamines in bony fish is not a random event as initially believed. Furthermore, such a heterogeneous distribution of protamines cannot be easily accounted for by a mechanism of horizontal retroviral transmission through repeated and independent acquisition of a prot amine gene as has been recently proposed (Jankowski, Stater, Dixon (1986) J Mol Evol 23:1–10). Rather, it could possibly be explained by a repeated and independent loss of the expression of the protamine gene (or loss of the gene itself) which mainly occurred during the diversification of the orders of this group.
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Ando T, Watanabe S (1969) A new method for fractionation of protamines and the amino acid sequences of salmine and three components of iridine. Int J Protein Res 1:221–224
Ando T, Yamasaki M, Suzuki K (1973) Protamines. Isolation, characterization, structure and function. Springer-Verlag, Berlin
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
Balhorn R (1989) Mammalian protamines—structure and molecular interactions. In: Adolph KW (ed) Molecular biology of chromosome function. Springer-Verlag, New York, pp 366–395
Bellvé AR, McKay DJ, Renaux BS, Dixon GH (1988) Purification and characterization of mouse protamines P1 and P2. Amino acid reference of P2. Biochemistry 27:2890–2897
Black JA, Dixon GH (1967) Evolution of protamine: a further example of partial gene duplication. Nature 216:152–154
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. Plenum Press, New York, pp 139–167
Bretzel G (1972a) Über Thynnin, das Protamine des Thunfisches. Die Vollstaendige Aminosaurensequenz von Thynnin Y2. XI. Mitteilung über die Struktur der Untersuchsreike von E. Wald Schmidt-Leitz und Mitarbeitern. Hoppe Seyler's Z Physiol Chem 353:933–943
Bretzel G (1972b) Über Thynnin, das Protamin des Thunfisches. Die Sequenz der Komponente Y1. XII. Mitteilung über die Struktur der Protamine in der Untersunchgugsreike von E. Waldschmidt-Leitz und Mitarbeitern. Hoppe Seyler's Z Physiol Chem 353:1362–1364
Bretzel G (1973a) Über Thynnin, das Protamin des Thunfisches. Die Aminosauresequenz von Thynnin Z1. XIII. Mitteilung über die Struktur der Protamine in der Untersunchungsreike von E. Waldschmidt-Leitz und Mitarbeitern. Hoppe Seyler's Z Physiol Chem 354:312–320
Bretzel G (1973b) Über Thynnin, das Protamin des Thunfisches. Die Aminosauresequenz von Thynnin Z1. XIII. Mitteilung über die Struktur der Protamine in der Untersunchungsreike von E. Waldschmidt-Leitz und Mitarbeitern. Hoppe Seyler's Z Physiol Chem 354:543–549
Casas MT, Munoz-Guerra S, Subirana JP (1981) Preliminary report on the ultrastructure of chromatin in the histone containing spermatozoa of a teleost fish. Biol Cell 40:87–92
Chao H, Davies PL (1992) Amino acid sequence of the unique protamine from the yellow perch. FEBS Lett 299:166–168
Corzett M, Blacher R, Mazrimas JA, Balhorn R (1987) Analysis of hamster protamines—primary sequence and species distribution. J Cell Biol 105:151a
Daisley St L (1980) Protamine gene evolution in fish. PhD Thesis, Queens University, Kingston, Ontario
Daisley St L, Davies PL (1982) Divergence of protamine gene sequences in fish. Biochim Biophys Acta 698:271–279
Dingwall C, Laskey RA (1991) Nuclear targeting sequences—a consensus? Trends Bichem Sci 16:478–481
Doolittle RF (1986) Of urfs and orfs. A primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, CA, USA
Doolittle RF, Feng DF, Johnson MS, McClure MA (1986) Relationships of human protein sequences to those of other organisms. Cold Spring Harb Symp Quant Biol 51, Pt: 1:447–455
Hanover JA (1992) The nuclear pore: at the crossroads. FASEB J 6: 2288–2295
Hart JL (1973) Pacific fishes of Canada. Fisheries Research Board of Canada, Bulletin 180, Ottawa
Hoffmann JA, Chance RE, Johnson MG (1990) Purification and analysis of the major components of Chum salmon protamine contained in insulin formulations using high performance liquid chromatography. Protein Expr Purif 1:127–133
Jankowsky JM, States JC, Dixon GH (1986) Evidence of sequences resembling avian retrovirus long terminal repeats flanking the trout protamine. Gene J Mol Evol 23:1–10
Kadura SN, Khrapumor SN, Aleeksenko VR (1988) Three types of sperm proteins in eukaryotes (Russian). Ukr Biokim Zh 60:14–19
Kadura SN, Khrapunov SN, Chabanny, Berdyshev GD (1983) Changes in chromatin basic proteins during male gametogenesis of grass carp. Comp Biochem Physiol 74B:343–350
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
Kasinsky HE, Huang SY, Kwauk S, Mann M, Sweeney MAJ, Yee B (1978) On the diversity of sperm histones in the vertebrates. III. Electrophoretic variability of testis-specific histone patterns in Anura contrasts with relative constancy in Squamata. J Exp Zool 203:109–126
Kasinsky HE, Huang SY, Mann M, Roca J, Subirana JA (1985a) On the diversity of sperm histones in the vertebrates: IV. Cytochemical and amino acid analysis in Anura. J Exp Zool 234:33–46
Kasinsky HE, Mann M, Lemke M, Huang SY (1985b) Diversity of sperm basic chromosomal proteins in the vertebrates: a phylogenetic point of view. In: Reecks GR, Goodwin GH, Puigdoménech P (eds) Chromosomal proteins and gene expression. Plenum Press, New York, pp 335–352
Kennedy BP, Davies PL (1980) Acid-soluble nuclear proteins of the testis during spermatogenesis in the winter flounder: loss of the high mobility group proteins. J Biol Chem 255:2533–2539
Krawetz SA, Dixon GH (1988) Sequence similarities of the protamine genes: implications for regulation and evolution. J Mol Evol 27: 291–297
Krawetz SA, Connor W, Dixon GH (1987) Cloning of bovine P1 protamine cDNA and the evolution of vertebrate P1 protamines. DNA 6:47–57
Leim AH, Scott WB (1966) Fishes of the Atlantic coast of Canada. Fisheries Research Board of Canada, Bulletin 155, Ottawa
Lemke MJ (1985) Variability of testis-specific proteins in Gasterosteus aculeatus L. and related species. MSc thesis, University of British Columbia, Vancouver
Lindberg GU, Krasyukova ZV (1971) Fishes of the Sea of Japan and the adjacent areas of the Sea of Okhotsk and the Yellow Sea. Part 3. Teleostomi. XXIX. Perciformes. Academy of Sciences of the Union of Soviet Socialist Republics, Leningrad
Lindberg GU, Legeza MI (1969) Fishes of the Sea of Japan and the adjacent areas of the Sea of Okhotsk and the Yellow Sea. Part 2. Teleostomi. XII. Acipenseriformes—XXVIII. Polynemiformes. Academy of Sciences of the Union of Soviet Socialist Republics, Moskva-Leningrad
Maier WN, Nussbaum G, Domenjoud L, Klemm U, Engel W (1990) The lack of protamine 2 (P2) in boar and bull spermatozoa is due to mutations within the P2 gene. Nucleic Acids Res 18:1249–1254
Maitland PS, Linsell K (1980) Guía de los peces de agua dulce de Europa. Editorial Omega, Barcelona
Mann M, Risley MS, Eckhardt RA, Kasinsky HE (1982) Characterization of spermatid/sperm basic chromosomal proteins in the genus Xenopus (Anura, Pipidae). J Exp Zool 222:173–186
McKay DJ, Renaux BS, Dixon GH (1986a) Rainbow trout protamines. Amino acid sequences of six distinct proteins from a single testis. Eur J Biochem 158:361–366
McKay DJ, Renaux BS, Dixon GH (1986b) Human sperm protamines amino-acid sequences of two forms of protamine P2. Eur J Biochem 156:5–8
Moir RD (1987) Structure of several multigene families in salmonid fishes. PhD thesis, Department of Medical Science, University of Calgary, Alberta, Canada
Moir RD, Dixon GH (1988a) A repetitive DNA sequence in the salmonid fishes similar to a retroviral long repeat. J Mol Evol 27: 1–7
Moir RD, Dixon GH (1988b) Characterization of a protamine gene from the Chum salmon (Oucorhynchus keta). J Mol Evol 27:8–16
Moyle PB, Cech JJ Jr (1982) Fishes: an introduction to ichthyology. Prentice-Hall, Englewood Cliffs, NJ
Muñoz-Guerra S, Azorin F, Casas MT, Marcet X, Maristany MA, Roca J, Subirana JA (1982) Structural organization of sperm chromatin from the fish Carassius auratus. Exp Cell Res 137:47–53
Nandi AK, Chandhuri A, Mandal RK (1979) Nature and evolutionary significance of basic proteins in fish spermatozoa. Indian J Biochem Biophys 16:6–10
Nelson JS (1984) Fishes of the world, 2nd ed. John Wiley and Sons, New York
Okamoto Y, Kuno K, Motohiro T, Nishi N, Muta E, Ota S (1992) Primary structures of sardaines Z1 and Z2, protamines isolated from striped bonito (Sarda orientalis). J Biochem 111:157–161
Okamoto Y, Muta E, Ota S (1987) Primary structures of M6 and M7 of mugiline β (Mugil japonicas). J Biochem 101:1017–1024
Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histone-to-protamine replacement reaction. Progr Nucleic Acid Res Mol Biol 40:25–94
Pirhonen A, Valtonen P, Linnala-Kankkunen A, Heiskanen N, Haenpaa P (1990) Primary structures of two protamine P2 variants (St2a and St2b) from stallion spermatozoa. Biochem Biophys Acta 1039:177–180
Poccia DL (1991) Sp histones and chromatin structure in male germ line nuclei and male pronuclei of the sea urchin. In: Baccetti B (ed) Comparative spermatology 20 years after, vol 75. Serono Symposia Publications from Raven Press, pp 61–65
Poccia DL, Green GR (1992) Packaging and unpackaging the sea urchin sperm genome. Trends Biochem Sci 17:223–227
Saperas N (1992) Distribució i caracterizació de les proteïmes espermàtiques bàsiques en peixos, agnats i procordats. PhD thesis, Universitat Politècnica de Catalunya, Barcelona, Spain
Saperas N, Chiva M, Ausio J (1992) Purification and characterization of the protamines and related proteins from the sperm of a tunicate, Styela plicata. Comp Biochem Physiol 106B:9690–9974
Saperas N, Chiva M, Ribes E, Kasinsky H, Rosenberg H, Youson JH, Ausio J (1994) Chromosomal proteins of the sperm of a Cephalochordate (Branchiostoma floridae) and an Agnathan (Petromyzon marinus). Compositional variability of the nuclear sperm proteins of deuterostomes. Biol Bull 186:101–114
Saperas N, Lloris D, Chiva M (1993b) Sporadic appearance of histones, histone-like proteins, and protamines in sperm chromatin of bony fish. J Exp Zool 265:575–586
Saperas N, Ribes E, Buesa C, Garcia-Hegardt F, Chiva M (1993c) Differences in chromatin condensation during spermatogenesis in two species of fish with distinct protamines. J Exp Zool 265:185–194
Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Fisheries Research Board of Canada, Bulletin 184, Ottawa
Speckert W, Kennedy B, Daisley St L, Davies P (1983) Primary structure of protamine from the northern pike Esox lucius. Eur J Biochem 136:283–289
Stanker LH, McKeown C, Balhorn R, Lee C, Mazrimas J, Goralka M, Wyrobek A (1992) Immunological evidence for a P2 protamine precursor in mature rat sperm. Mol Reprod Dev 33:481–488
van Holde KE (1988) Chromatin. Springer Verlag, Berlin
von Holt C, De Groot P, Schwager S, Brandt WF (1984) The structure of sea urchin histones and considerations on their function. In: Stein GS, Stein JL, Marzluff WF (eds) Histone genes: structure, organization and regulation. John Wiley, New York, pp 65–105
Whitehead PIP (1985) Clupeoid fishes of hte world (Suborder clupeoidei). Part 1, Chirocentridae, Clupeidae and Pristigasteridae. FAO Species Catalogue, vol 7. FAO Fisheries Synopsis No. 125, Rome
Whitehead PIP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) (1984–86) Fishes of the Northeastern Atlantic and the Mediterranean, 3 vols. UNESCO, Paris
Yulikova EP, Evseenko LK, Baratova L, Belyamova LP, Rybin VK, Silaev AB (1976) The primary structure of sturine B, a protamine from Caspian sturgeon. Bioorg Khim 2:1613–1618
Yulikova EP, Rybin VK, Silaev AB (1979) The primary structure of stellin A. Bioorg Khim 5:5–10
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Saperas, N., Ausio, J., Lloris, D. et al. On the evolution of protamines in bony Fish: Alternatives to the “Retroviral horizontal transmission” hypothesis. J Mol Evol 39, 282–295 (1994). https://doi.org/10.1007/BF00160152
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DOI: https://doi.org/10.1007/BF00160152