Skip to main content
Log in

Fine structure of the photoreceptor of the ascidian tadpole during development

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The eye of the tadpole larva of Amaroucium constellatum consists of 15–20 photoreceptor cells, a single pigment cup cell, and three lens cells. Each photoreceptor cell during its development gives rise apically to a neck process and basally to an axon, which is thought to extend to the cerebral ganglion. At the tip of the neck a sensory cilium differentiates to produce the photoreceptor membranes. This process begins as a balloon-shaped evagination of the cell membrane above the ciliary basal body. This evagination infolds to form the presumptive photosensitive lamellae which increase in number, length, and regularity as the eye matures. Microvilli also arise from the tip of this cell and intermingle with the ciliary membranes. The neck process itself elongates, narrows, and becomes filled with microtubules during development. The pigment cell, initially long, flat, and electron lucent, develops into a cupshape. Its cytoplasm becomes packed with pigment granules, forming an effective light shield. The development of the lens cells involves formation of the lens vesicles and elongation of the cells into the lumen of the pigment cup. Differentiation of ascidian photoreceptor cells is compared with that of the vertebrate rod and cone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barnes, S. N.: The fine structure of the photoreceptor of the ascidian, Amaroucium constellatum. Biol. Bull. 137, 392 (1969)

    Google Scholar 

  • Barnes, S. N.: Fine structure of the photoreceptor and cerebral ganglion of the tadpole larva of Amaroucium constellatun (Verrill) (Subphylum: Urochordata; Class: Acsidiacea). Z. Zellforsch. 117, 1–16 (1971)

    Google Scholar 

  • Barnes, S. N.: Fine structure of the embryonic, larval, and metamorphic ascidian eye. Ph. D. thesis, University of Colorado (1972); also Dissert. Abstr. 33, 3429-B (1973)

  • Barnes, S. N., Gorman, A.L.F., McReynolds, J. S.: Fine structure and intracellular responses of photoreceptors of a pelagic tunicate, Salpa. Biol. Bull. 139, 414 (1970)

    Google Scholar 

  • Bell, A. L., Barnes, S. N., Anderson, K. L.: A fixation technique for electron microscopy which provides uniformly good preservation of the tissues of a variety of marine invertebrates. Biol. Bull. 137, 393 (1969)

    Google Scholar 

  • Bennett, H. S., Luft, J. H.: S-collidine as a basis for buffering fixatives. J. biophys. biochem. Cytol. 6, 113–114 (1959)

    Google Scholar 

  • Brandenburger, J. L., Woollacott, R. M., Eakin, R. M.: Fine structure of eyespots in tornarian larvae (Phylum: Hemichordata). Z. Zellforsch. 142, 89–102 (1973)

    Google Scholar 

  • Brightman, M. W-, Reese, T. S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969)

    Google Scholar 

  • Caley, D. W., Johnson, C., Liebelt, R. A.: The postnatal development of the retina in the normal and rodless CBA mouse: A light and electron microscopic study. Amer. J. Anat. 133, 179–212 (1972)

    Google Scholar 

  • Carasso, N.: Étude au microscope électronique de la morphogenèse du segment externe des cellules visuelles chez la Pleurodèle. C. R. Acad. Sci. (Paris) 248, 3058–3060 (1959)

    Google Scholar 

  • Cohen, A. I.: New evidence supporting the linkage to extracellular space of outer segment saccules of frog cones but not rods. J. Cell Biol. 37, 424–444 (1968)

    Google Scholar 

  • Cohen, A. I.: An ultrastructural analysis of the photoreceptors of the squid and their synaptic connections. III. Photoreceptor terminations in the optic lobes. J. comp. Neurol. 147, 399–426 (1973)

    Google Scholar 

  • Costello, D. P., Davidson, M. E., Eggers, A., Fox, M. H., Henley, C.: Methods for obtaining and handling marine eggs and embryos. Woods Hole, Massachusetts: Marine Biological Laboratory 1957

    Google Scholar 

  • DeRobertis, E.: Morphogenesis of retinal rods. J. biophys. biochem. Cytol. 2, Suppl., 209–218 (1956)

    Google Scholar 

  • DeRobertis, E., Lasansky, A.: Ultrastructure and chemical organization of photoreceptors. In: The structure of the eye (ed. G. K. Smelser), p. 29–49. New York: Academic Press 1961

    Google Scholar 

  • Dilly, P. N.: Electron microscope observations of the receptors in the sensory vesicle of the ascidian tadpole. Nature (Lond.) 191, 786–787 (1961)

    Google Scholar 

  • Dilly, P. N.: Studies on the receptors in the cerebral vesicle of the ascidian tadpole. 2. The ocellus. Quart. J. micr. Sci. 105, 13–20 (1964)

    Google Scholar 

  • Dixon, J. S., Cronly-Dillon, J. R.: The fine structure of the developing retina in Xenopus laevis. J. Embryol. exp. Morph. 28, 659–666 (1972)

    Google Scholar 

  • Dowling, J. E.: The organization of vertebrate visual receptors. In: Molecular organization and biological function (ed. J. M. Allen), p. 186–210. New York: Harper and Row 1967

    Google Scholar 

  • Dowling, J. E.: Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates. Proc. roy. Soc. B 170, 205–228 (1968)

    Google Scholar 

  • Dudley, P. L.: The fine structure and development of the nauplius eye of the copepod Doropygus seclusus Illg. Cellule 68, 6–42 (1969)

    Google Scholar 

  • Eakin, R. M.: Differentiation in the embryonic eye of Peripatus (Onychophora). 6th Int. Cong. E. M. 507–508 (1966)

  • Eakin, R. M.: Structure of invertebrate photoreceptors. In: Handbook of sensory physiology (ed. H. J. A. Dartnall), vol. VII/1, p. 625–684. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Eakin, R. M., Brandenburger, J. L.: Differentiation in the eye of a pulmonate snail Helix aspersa. J. Ultrastruct. Res. 18, 391–421 (1967)

    Google Scholar 

  • Eakin, R. M., Kuda, A.: Ultrastructure of sensory receptors in ascidian tadpoles. Z. Zellforsch. 112, 287–312 (1971)

    Google Scholar 

  • Eakin, R. M., Kuda, A.: Glycogen in lens of tunicate tadpole (Chordata: Ascidiacea). J. exp. Zool. 180, 267–270 (1972)

    Google Scholar 

  • Eakin, R. M., Westfall, J. A.: The development of photoreceptors in the stirnorgan of the treefrog, Hyla regilla. Embryologia (Nagoya) 6, 84–98 (1961)

    Google Scholar 

  • Eakin, R. M., Westfall, J. A.: Fine structure of photoreceptors in Amphioxus. J. Ultrastruct. Res. 6, 531–539 (1962)

    Google Scholar 

  • Eakin, R. M., Westfall, J. A.: Further observations on the fine structure of some invertebrate eyes. Z. Zellforsch. 62, 310–332 (1964)

    Google Scholar 

  • Eguchi, E., Naka, K., Kuwabara, M.: The development of the rhabdom and the appearance of the electrical response in the insect eye. J. gen. Physiol. 46, 143–157 (1962)

    Google Scholar 

  • Gorman, A.L.F., McReynolds, J. S., Barnes, S. N.: Photoreceptors in primitive chordates: Fine structure, hyperpolarizing potentials and evolution. Science 172, 1052–1054 (1971)

    Google Scholar 

  • Grave, C.: Amaroucium pellucidum (Leidy), form constellatum (Verrill). I. The activities and reactions of the tadpole larva. J. exp. Zool. 30, 239–257 (1920)

    Google Scholar 

  • Grave, C.: Amaroucium constellatum (Verrill). II. The structure and organization of the tadpole larva. J. Morph. 36, 71–101 (1921)

    Google Scholar 

  • Grave, C., Riley, G.: Development of the sense organs of the larva of Botryllus schlosseri. J. Morph. 57, 185–211 (1935)

    Google Scholar 

  • Gray, E. G.: Problems of interpreting the fine structure of vertebrate and invertebrate synapses. Int. Rev. gen. exp. Zool. 2, 139–170 (1966)

    Google Scholar 

  • Hollenberg, M. J., Spira, A. W.: Human retinal development: ultrastructure of the outer retina. Amer. J. Anat. 137, 357–386 (1973)

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961)

    Google Scholar 

  • Maser, M. D., Powell, T. E., Philpott, C. W.: Relationships among pH, osmolality, and concentration of fixative solutions. Stain Technol. 42, 175–182 (1967)

    Google Scholar 

  • Mast, S. O.: Reactions to light in the ascidians Amaroucium constellatum and Amaroucium pellucidum with special reference to photic orientation. J. exp. Zool. 34, 149–187 (1921)

    Google Scholar 

  • Minganti, A.: Ricerche istochimiche sulla localizzazione del territorio presuntivo degli organi sensoriali nella larva di Ascidie. Pubbl. Staz. Zool. Napoli 23, 52–57 (1951)

    Google Scholar 

  • Minganti, A.: Inhibition of melanogenesis in Phallusia embryos (Ascidians). Acta Embryol. Morph. exp. (Palermo) 1, 37–47 (1957)

    Google Scholar 

  • Moyer, F. H.: Development, structure, and function of the retinal pigmented epithelium. In: The retina: morphology, function and clinical characteristics (eds. B. R. Straatsma, M. O. Hall, R. A. Allen, F. Crescitelli), p. 1–30. Los Angeles: University of California Press 1969

    Google Scholar 

  • Mund, M. L., Rodrigues, M. M., Fine, B. S.: Pigmentation in the developing eye. Amer. J. Ophthal. 73, 167–182 (1972)

    Google Scholar 

  • Nakao, T.: On the fine structure of the Amphioxus photoreceptor. Tohoku J. exp. Med. 82, 349–369 (1964)

    Google Scholar 

  • Nilsson, S.E.G.: Receptor cell outer segment development and ultrastructure of the disk membranes in the retina of the tadpole (Rana pipiens). J. Ultrastruct. Res. 11, 581–620 (1964)

    Google Scholar 

  • Ochs, S.: Fast transport of materials in the mammalian nerve fibers. Science 176, 252–260 (1972)

    Google Scholar 

  • Olney, J.: An E. M. study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Invest. Ophthal. 7, 250–268 (1968)

    Google Scholar 

  • Palade, G. E.: A study of fixation for electron microscopy. J. exp. Med. 95, 285–298 (1952)

    Google Scholar 

  • Reynolds, E.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)

    Google Scholar 

  • Richardson, K. C., Jarett, L., Finke, E. H.: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960)

    Google Scholar 

  • Röhlich, P.: Formation of the brush border by fusion of vesicles. Proc. 5th Int. Cong. E. M. 2, LL-5 (1962)

    Google Scholar 

  • Sabatini, D. E., Bensch, K., Barrnett, R. J.: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963)

    Google Scholar 

  • Satir, P., Gilula, N. B.: The fine structure of membranes and intercellular communication in insects. Ann. Rev. Entomol. 18, 143–166 (1973)

    Google Scholar 

  • Schwartz, W. J.: A septate-like contact in the rat retina. J. Neurocytol. 2, 85–89 (1973)

    Google Scholar 

  • Scott, F. M. Sister: The developmental history of Amaruocium constellatum. I. Early embryonic development. Biol. Bull. 88, 126–138 (1945)

    Google Scholar 

  • Scott, F. M. Sister: The developmental history of Amaroucium constellatum. II. Organogenesis of the larval action system. Biol. Bull. 91, 66–80 (1946)

    Google Scholar 

  • Sjöstrand, F. S.: Electron microscopy of the retina. In: The structure of the eye (ed. G. K. Smelser), p 1–28. New York: Academic Press 1961

    Google Scholar 

  • Sörensen, S. P. L.: Ergänzung zu der Abhandlung: Enzymstudien II: Über die Messung und die Bedeutung der Wasserstoffionenkonzentration bei enzymatischen Prozessen. Biochem. Z. 22, 352–356 (1909)

    Google Scholar 

  • Takuyasu, K., Yamada, E.: The fine structure of the retina studied with the electron microscope. IV. Morphogenesis of outer segments. J. biophys. biochem. Cytol. 6, 225–230 (1959)

    Google Scholar 

  • Tilney, L. G., Porter, K. R.: Studies on the microtubules in Heliozoa. II. The effect of low temperature on the formation and maintenance of the axopodia. J. Cell Biol. 34, 327–343 (1967)

    Google Scholar 

  • Waddington, C. H., Perry, M. M.: The ultra-structure of the developing eye of Drosophila. Proc. roy. Soc. B 153, 155–178 (1960)

    Google Scholar 

  • Watson, M. L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958)

    Google Scholar 

  • Weidman, T. A., Kuwabara, T.: Postnatal development of the rat retina. An electron microscope study. Arch. Ophthal. 79, 470–484 (1968)

    Google Scholar 

  • Weidman, T. A., Kuwabara, T.: Development of the rat retina. Invest. Ophthal. 8, 60–69 (1969)

    Google Scholar 

  • Welsch, U.: Die Feinstruktur der Josephschen Zellen im Gehirn von Amphioxus. Z. Zellforsch. 86, 252–261 (1968)

    Google Scholar 

  • Whittaker, J. R.: An analysis of melanogenesis in differentiating pigment cells of ascidian embryos. Develop. Biol. 14, 1–39 (1966)

    Google Scholar 

  • Yamada, E., Ishikawa, T.: Some observations on the submicroscopic morphogenesis of the human retina. In: The structure of the eye (ed. J. Rohen), vol. II, p. 5–16 Stuttgart: F. K. Schattauer 1965

    Google Scholar 

  • Young, R. W.: The renewal of photoreceptor cell outer segments. J. Cell Biol. 33, 61–72 (1967)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This investigation was supported in part by NIH Grants number GM01981, RR06084, and EY00443.1 wish to acknowledge Dr. A. L. Bell for his assistance during this investigation, Drs. S. W. Smith, T. H. Goldsmith, and R. Wehner for critical reading of the manuscript, and Jeri Cohen for technical assistance.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barnes, S.N. Fine structure of the photoreceptor of the ascidian tadpole during development. Cell Tissue Res. 155, 27–45 (1974). https://doi.org/10.1007/BF00220282

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00220282

Key words

Navigation