On the Evolution of Protamines in Bony Fish: Alternatives to the "retroviral Horizontal Transmission" Hypothesis

Overview

Journal J Mol Evol

Specialty Biochemistry

Date 1994 Sep 1

PMID 7932790

Citations 9

Authors

N Saperas

J Ausio

D Lloris

M Chiva

Affiliations

Soon will be listed here.

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 protamine 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.

Citing Articles

The protamines of the spider Steatoda sp. provide an example of liquid-liquid phase separation chromatin transitions during spermiogenesis.

Leyden M, Michalik P, Baruffaldi L, Mahmood S, Kalani L, Hunt D Development. 2024; 151(22).

PMID: 39465422 PMC: 11607694. DOI: 10.1242/dev.203134.

The protamines of the noble false widow spider provide an example of liquid-liquid phase separation chromatin transitions during spermiogenesis.

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PMID: 38895387 PMC: 11185589. DOI: 10.1101/2024.06.04.597381.

Protamines from liverwort are produced by post-translational cleavage and C-terminal di-aminopropanelation of several male germ-specific H1 histones.

DIppolito R, Minamino N, Rivera-Casas C, Cheema M, Bai D, Kasinsky H J Biol Chem. 2019; 294(44):16364-16373.

PMID: 31527083 PMC: 6827293. DOI: 10.1074/jbc.RA119.010316.

Differential gene susceptibility to sperm DNA damage: analysis of developmental key genes in trout.

Gonzalez-Rojo S, Fernandez-Diez C, Guerra S, Robles V, Herraez M PLoS One. 2014; 9(12):e114161.

PMID: 25479606 PMC: 4257556. DOI: 10.1371/journal.pone.0114161.

All roads lead to arginine: the squid protamine gene.

Lewis J, de Jong M, Bagha S, Tang A, Gilly W, Ausio J J Mol Evol. 2004; 58(6):673-80.

PMID: 15461424 DOI: 10.1007/s00239-004-2589-8.

References

Daisley S, Davies P . Divergence of protamine gene sequences in fish. Biochim Biophys Acta. 1982; 698(3):271-9. DOI: 10.1016/0167-4781(82)90157-9. View

Mann M, Risley M, Eckhardt R, Kasinsky H . Characterization of spermatid/sperm basic chromosomal proteins in the genus Xenopus (Anura, Pipidae). J Exp Zool. 1982; 222(2):173-86. DOI: 10.1002/jez.1402220209. View

Jankowski J, States J, DIXON G . Evidence of sequences resembling avian retrovirus long terminal repeats flanking the trout protamine gene. J Mol Evol. 1986; 23(1):1-10. DOI: 10.1007/BF02100993. View

Chao H, Davies P . Amino acid sequence of the unique protamine from yellow perch. FEBS Lett. 1992; 299(2):166-8. DOI: 10.1016/0014-5793(92)80239-d. View

Kasinsky H, Huang S, Mann M, Roca J, Subirana J . On the diversity of sperm histones in the vertebrates: IV. Cytochemical and amino acid analysis in Anura. J Exp Zool. 1985; 234(1):33-46. DOI: 10.1002/jez.1402340106. View

Krawetz S, Connor W, DIXON G . Cloning of bovine P1 protamine cDNA and the evolution of vertebrate P1 protamines. DNA. 1987; 6(1):47-57. DOI: 10.1089/dna.1987.6.47. View

Doolittle R, Feng D, Johnson M, McClure M . Relationships of human protein sequences to those of other organisms. Cold Spring Harb Symp Quant Biol. 1986; 51 Pt 1:447-55. DOI: 10.1101/sqb.1986.051.01.054. View

Black J, DIXON G . Evolution of protamine: a further example of partial gene duplication. Nature. 1967; 216(5111):152-4. DOI: 10.1038/216152a0. View

Maier W, Nussbaum G, Domenjoud L, Klemm U, Engel W . The lack of protamine 2 (P2) in boar and bull spermatozoa is due to mutations within the P2 gene. Nucleic Acids Res. 1990; 18(5):1249-54. PMC: 330441. DOI: 10.1093/nar/18.5.1249. View

10.

Dingwall C, Laskey R . Nuclear targeting sequences--a consensus?. Trends Biochem Sci. 1991; 16(12):478-81. DOI: 10.1016/0968-0004(91)90184-w. View

11.

Kennedy B, Davies P . Acid-soluble nuclear proteins of the testis during spermatogenesis in the winter flounder. Loss of the high mobility group proteins. J Biol Chem. 1980; 255(6):2533-9. View

12.

Bloch D . A catalog of sperm histones. Genetics. 1969; 61(1):Suppl:93-111. View

13.

Hoffmann J, CHANCE R, Johnson M . Purification and analysis of the major components of chum salmon protamine contained in insulin formulations using high-performance liquid chromatography. Protein Expr Purif. 1990; 1(2):127-33. DOI: 10.1016/1046-5928(90)90005-j. View

14.

Speckert W, Kennedy B, Daisley S, Davies P . Primary structure of protamine from the Northern pike Esox lucius. Eur J Biochem. 1983; 136(2):283-9. DOI: 10.1111/j.1432-1033.1983.tb07739.x. View

15.

Kadura S, Khrapunov S, Chabanny V, Berdyshev G . Changes in chromatin basic proteins during male gametogenesis of grass carp. Comp Biochem Physiol B. 1983; 74(2):343-50. DOI: 10.1016/0305-0491(83)90023-8. View

16.

Ando T, Watanabe S . A new method for fractionation of protamines and the amino acid sequences of salmine and three components of iridine. Int J Protein Res. 1969; 1(3):221-4. DOI: 10.1111/j.1399-3011.1969.tb01646.x. View

17.

Bretzel G . [Thynnin, the protamine of the tuna fish: the amino acid sequence of thynnin Z2. XIV. Communication on the structure of the protamines described by E. Waldschmidt-Leitz et al]. Hoppe Seylers Z Physiol Chem. 1973; 354(5):543-9. View

18.

Okamoto Y, Kuno K, Motohiro T, Nishi N, Muta E, Ota S . Primary structures of sardaines Z1 and Z2, protamines isolated from striped bonito (Sarda orientalis). J Biochem. 1992; 111(2):157-61. DOI: 10.1093/oxfordjournals.jbchem.a123730. View

19.

Moir R, DIXON G . Characterization of a protamine gene from the chum salmon (Oncorhynchus keta). J Mol Evol. 1988; 27(1):8-16. DOI: 10.1007/BF02099725. View

20.

McKay D, Renaux B, DIXON G . Human sperm protamines. Amino-acid sequences of two forms of protamine P2. Eur J Biochem. 1986; 156(1):5-8. DOI: 10.1111/j.1432-1033.1986.tb09540.x. View