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An ultrastructural analysis of early fertilization in the sand dollar, Echinarachnius parma

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Summary

The morphology of gametes of a representative echinoid, Echinarachnius parma were investigated ultrastructurally with particular emphasis on gamete interaction during fertilization. The acrosomal region of the spermatozoon is characterized by the presence of two components: an acrosomal vesicle and periacrosomal materials. The acrosomal vesicle, which is completely bounded by a limiting membrane, is surrounded by periacrosomal materials. Nuclear and mitochondrial regions of the spermatozoon are also described briefly. The ovum is surrounded by two extraneous coats: an outer jelly layer and an inner vitelline envelope. Pigment cells are present within the outer jelly layer. Ooplasmic organelles and inclusions including cortical granules and the female pronucleus are described.

Spermatozoa undergo the acrosomal reaction in the vicinity of mature ova. Events of acrosomal reaction, including dehiscence of the acrosomal vesicle and acrosomal tubule formation, are described and summarized schematically. Acrosomal vesicle contents remain adherent to the outer surface of the tubule membrane. Primary binding of the spermatozoon to the surface of the ovum is accomplished by the establishment of morphological continuity between this extracellular coat and the vitelline envelope of the ovum. It is suggested that the species specificity of fertilization resides in this primary binding of gametes. Membrane fusion, between the tip of the acrosomal tubule and the colemma, follows primary binding and cytoplasmic continuity of the gametes is thereby established. It is concluded that the early events of fertilization in Echinarachnius parma generally conform to the Hydroides-Saccoglossus pattern of the Colwins (1967).

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References

  • Afzelius, B. A.: The fine structure of sea urchin spermatozoa as revealed by the electron microscope. Z. Zellforsch. 42, 134–148 (1955)

    Google Scholar 

  • Afzelius, B. A., Murray, A.: The acrosomal reaction of spermatozoa during fertilization or treatment with egg water. Exp. Cell Res. 12, 325–337 (1957)

    Google Scholar 

  • Aketa, K.: Physiological studies on the sperm surface component responsible for sperm-egg bonding in sea urchin fertilization. I. Effect of spermbinding protein on the fertilizing capability of sperm. Exp. Cell Res. 80, 439–441 (1973)

    Google Scholar 

  • Anderson, E.: Oocyte differentiation in the sea urchin, Arbacia punctulata, with particular reference to the origin of cortical granules and their participation in the cortical reaction. J. Cell Biol. 37, 514–539 (1968)

    Google Scholar 

  • Anderson, W. A.: Cytochemistry of sea urchin gametes. II. Ruthenium red staining of gamete membranes of sea urchins. J. Ultrastruct. Res. 24, 322–333 (1968)

    Google Scholar 

  • Bernstein, M. H.: Normal and reactive morphology of sea urchin spermatozoa. Exp. Cell Res. 27, 197–209 (1962)

    Google Scholar 

  • Colwin, A. L., Colwin, L. H.: Morphology of fertilization: acrosome filament formation and sperm entry. In: The beginnings of embryonic development (Tyler, A., von Borstel, R. C. and Metz, C. B., eds.), p. 135–168, Washington, D. C.: Am. Assoc. Advanc. Sci. 1957

    Google Scholar 

  • Colwin, A. L., Colwin, L. H.: Fine structure of the spermatozoon of Hydroides hexagonus (Annelida), with special reference to the acrosomal region. J. biophys. biochem. Cytol. 10, 211–230 (1961a)

    Google Scholar 

  • Colwin, L. H., Colwin, A. L.: Changes in the spermatozoon of Hydroides hexagonus (Annelida) I. Passage of the acrosomal region through the vitelline membrane. J. biophys. biochem. Cytol. 10, 231–254 (1961b)

    Google Scholar 

  • Colwin, A. L., Colwin, L. H.: Changes in the spermatozoon of Hydroides hexagonus (Annelida). II. Incorporation with the egg. J. biophys. biochem. Cytol. 10, 255–274 (1961c)

    Google Scholar 

  • Colwin, A. L., Colwin, L. H.: Role of the gamete membranes in fertilization in Saccoglossus kowalevskii (Enteropneusta). I. The acrosomal region and its changes in early stages of fertilization. J. Cell Biol. 19, 477–500 (1963a)

    Google Scholar 

  • Colwin, L. H., Colwin, A. L.: Role of the gamete membranes in fertilization in Saccoglossus kowalevskii. II. Zygote formation by gamete membrane fusion. J. Cell Biol. 19, 501–518 (1963b)

    Google Scholar 

  • Colwin, A. L., Colwin, L. H.: Role of the gamete membranes in fertilization. In: Cellular membranes in development (Locke, M., ed.), 22nd Symp. Soc.study Dev. Growth, p. 233–279. New York: Academic Press 1964

    Google Scholar 

  • Colwin, A. L., Colwin, L. H., Philpott, D. E.: Electron microscope studies of early stages of sperm penetration in Hydroides hexagonus (Annelida) and Saccoglossus kowalevskii (Enteropneusta). J. Biophys. biochem. Cytol. 3, 489–502 (1957)

    Google Scholar 

  • Colwin, L. H., Colwin, A. L.: Membrane fusion in relation to sperm-egg association. In: Fertilization. Comparative morphology, biochemistry and immunology (Netz, C. B., Monroy, A., eds.), p. 237–293. New York: Academic Press 1967

    Google Scholar 

  • Colwin, L. H., Colwin, A. L., Summers, R. G.: The acrosomal region and the beginning of fertilization in the holothurian, Thyone briareus. In: The functional anatomy of the spermatozoon (Afzelius, B., ed.). Oxford: Pergamon Press 1974. In press

    Google Scholar 

  • Costello, D. P., Davidson, M. E., Eggers, A., Fox, M. H., Henley, C.: Methods for obtaining and handling marine eggs and embryos. M.B.L. Woods Hole, Mass. 1957

    Google Scholar 

  • Dan, J. C.: Studies on the acrosome. I. Reaction to egg-water and other stimuli. Biol. Bull. 103, 54–66 (1952)

    Google Scholar 

  • Dan, J. C.: The acrosome reaction. Int. Rev. Cytol. 5, 365–393 (1956)

    Google Scholar 

  • Dan, J. C.: Acrosome reaction and lysins. In.: Fertilization. Comparative morphology, biochemistry and immunology (Metz, C. B. and Monroy, A., eds.), p. 237–293. New York: Academic Press 1967

    Google Scholar 

  • Dan, J. C.: Morphogenetic aspects of acrosome formation and reaction. In: Advances in morphogenesis, vol. 8 (Abercrombie, M., Brachet, J., King, T. J., eds.), p. 1–39. New York: Academic Press 1970

    Google Scholar 

  • Dan, J. C., Kakizawa, Y., Kushida, H., Fujita, K.: Acrosomal triggers. Exp. Cell Res. 72, 60–68 (1972)

    Google Scholar 

  • Dan, J. C., Kushida, H., Ohori, Y.: Formation of the acrosomal process in echinoderm spermatozoa. Proc. 5th Intern. Congr. Electron Microscopy, Philadelphia (Breese, S., ed.), p. YY-12. New York: Academic Press 1962

    Google Scholar 

  • Dan, J. C., Ohori, Y., Kushida, H.: Studies on the acrosome. VII. Formation of the acrosomal process in sea urchin spermatozoa. J. Ultrastruct. Res. 11, 508–524 (1964)

    Google Scholar 

  • Endo, Y.: Changes in the cortical layer of sea urchin eggs at fertilization as studied with the electron microscope. I. Clypeaster japonicus. Exp. Cell Bes. 25, 383–397 (1961)

    Google Scholar 

  • Franklin, L. E.: Morphology of gamete membrane fusion and of sperm entry into oocytes of the sea urchin. J. Cell Biol. 25, 81–100 (1965)

    Google Scholar 

  • Franklin, L. E.: Fertilization and the role of the acrosomal region in non-mammals. Biol. Reprod. Suppl. 2, 159–176 (1970)

    Google Scholar 

  • Hagström, B. E.: Studies on polyspermy in sea urchins. Arch. Zool. 10, 307–315 (1956)

    Google Scholar 

  • Harvey, E. B., Anderson, T. F.: The spermatozoon and fertilization membrane of Arbacia punctulata as shown by the electron microscope. Biol. Bull. 85, 151–156 (1943)

    Google Scholar 

  • Hinegardner, R. T.: Echinoderms. In: Methods in developmental biology (Wilt, F. H and Wessels, N. K., eds.), p. 139–155. New York: Thomas Y. Crowell Comp. 1967

    Google Scholar 

  • Inoue, S., Hardy, J. P.: Fine structure of the fertilization membranes of sea urchins embryos. Exp. Cell Res. 68, 259–272 (1971)

    Google Scholar 

  • Jessen, H., Behnke, O., Wingstrand, K. G., Rostgaard, J.: Actin-like filaments in the acrosomal apparatus of spermatozoa of a sea urchin. Exp. Cell Res. 80, 47–55 (1973)

    Google Scholar 

  • Longo, F. J.: Fertilization: A comparative ultrastructural review. Biol. Reprod. 9, 149–215 (1973)

    Google Scholar 

  • Longo, F. J., Anderson, E.: The fine structure of pronuclear development and fusion in the sea urchin, Arbacia punctulata. J. Cell Biol. 39, 339–368 (1968)

    Google Scholar 

  • Longo, F. J., Anderson, E.: Sperm differentiation in the sea urchins, Arbacia punctulata and Strongylocentrotus purpuratus. J. Ultrastruct. Res. 27, 486–509 (1969)

    Google Scholar 

  • Longo, F. J., Anderson, E.: The effects of nicotine on fertilization in the sea urchin. Arbacia punctulata. J. Cell Biol. 46, 308–325 (1970)

    Google Scholar 

  • Longo, F. J., Schuel, H.: An ultrastructural examination of polyspermy induced by soyabean trypsin inhibitor in the sea urchin. Develop. Biol. 34, 187–199 (1973)

    Google Scholar 

  • Luft, J. H.: Ruthenium Red and Violet. I. Chemistry, purification, and methods for use for electron microscopy and mechanism of action. Anat. Rec. 171, 347–368 (1965a)

    Google Scholar 

  • Luft, J. H.: Ruthenium Red and Violet. II. Fine structural localization in animal tissues. Anat. Rec. 171, 369–416 (1965b)

    Google Scholar 

  • Marshall, R. D., Luykx, P.: Observations on the centrioles of the sea urchin spermatozoon. Develop. Growth Diff. 14, 311–323 (1973)

    Google Scholar 

  • Millonig, G.: Fine structural analysis of the cortical reaction in the sea urchin egg: after normal fertilization and after electric induction. J. submicr. Cytol. 1, 69–84 (1969)

    Google Scholar 

  • Pasteels, J. J.: Aspects structuraux de la fécondation vue au microscope électronique. Arch. Biol. (Liège) 76, 463–509 (1965)

    Google Scholar 

  • Rothschild, L.: Sea urchin spermatozoa. Endeavor 15, 79–86 (1956a)

    Google Scholar 

  • Rothschild, L.: The fertilizing spermatozoon. Discovery 18, 64–65 (1956b)

    Google Scholar 

  • Schuel, H., Wilson, W. L., Chen, K., Lorand, L.: A trypsin-like proteinase localized in cortical granules isolated from unfertilized sea urchin eggs by zonal centrifugation. Role of the enzyme in fertilization. Develop. Biol. 34, 175–186 (1973)

    Google Scholar 

  • Stambaugh, R., Buckley, B. S.: Histochemical subcellular localization of the acrosomal proteinase effecting dissolution of the zona pellucida using fluorescein-labeled inhibitors. Fertil. Steril. 23, 348–352 (1972)

    Google Scholar 

  • Summers, R. G., Colwin, L. H., Colwin, A. L., Turner, R.: Fine structure of the acrosomal region in Spermatozoa of two echinoderms, Ctenodiscus (starfish) and Thyone (holothurian). Biol. Bull. 141, 404 (1971)

    Google Scholar 

  • Summers, R. G., Hylander, B. L., Colwin, A. L., Colwin, L. H.: Functional anatomy of the echinoderm sperm and its interaction with the egg at fertilization. Amer. Zool. (1974). In press

  • Takashima, R., Takashima, T.: Electron microscope observations on the fertilization phenomenon of sea urchins with special reference to the acrosomal filament. Tokushima J. exp. Med. 6, 334–340 (1960)

    Google Scholar 

  • Tegner, M. J., Epel, D.: Sea urchin sperm-egg interaction studied with the scanning electron microscope. Science 179, 685–688 (1973)

    Google Scholar 

  • Tilney, L. G., Hatano, S., Ishikawa, H., Mooseker, M. S.: The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J. Cell Biol. 59, 109–126 (1973)

    Google Scholar 

  • Tilney, L. G., Hatano, S., Mooseker, M. S.: Actin in starfish sperm: its localization and function in the acrosomal process. J. Cell Biol. 55, 261a (1972)

  • Tyler, A.: Properties of fertilizin and related substances of eggs and sperm of marine animals. Amer. Naturalist 83, 195–219 (1949)

    Google Scholar 

  • Vacquier, V. D., Epel, D., Douglas, L. A.: Sea urchin eggs release protease activity at fertilization. Nature (Lond.) 237, 34–36 (1972)

    Google Scholar 

  • Vacquier, V. D., Tegner, M. J., Epel, D.: Protease activity establishes the block against polyspermy in sea urchins eggs. Nature (Lond.) 240, 352–353 (1972)

    Google Scholar 

  • Vacquier, V. D., Tegner, M. J., Epel, D.: Protease released from sea urchin eggs at fertilization alters the vitelline layer and aids in preventing polyspermy. Exp. Cell Res. 80, 111–119 (1973)

    Google Scholar 

  • Wolpert, L., Mercer, E. H.: An electron microscope study of fertilization of the sea urchin egg Psammechinus miliaris. Exp. Cell Res. 22, 45–55 (1961)

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, University of Maine, Orono, Maine, USA

    R. G. Summers & B. L. Hylander

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  1. R. G. Summers
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  2. B. L. Hylander
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The authors wish to acknowledge the technical assistance of Dr. Paul Rusanowski. This work was supported by N.S.F. Grant GB 37967 and by N.S.F. Grant GV 24157 to Dr. John Dearborn.

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Summers, R.G., Hylander, B.L. An ultrastructural analysis of early fertilization in the sand dollar, Echinarachnius parma . Cell Tissue Res. 150, 343–368 (1974). https://doi.org/10.1007/BF00220142

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