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Primordial germ cells and oocytes of Branchiostoma virginiae (Cephalochordata, Acrania) are flagellated epithelial cells: relationship between epithelial and primary egg polarity

Published online by Cambridge University Press:  26 September 2008

Jennifer E. Frick  and
Edward E. Ruppert
Jennifer E. Frick*
Affiliation:
Department of Biological Sciences, Clemson University, Clemson, South Carolina, USA
Edward E. Ruppert
Affiliation:
Department of Biological Sciences, Clemson University, Clemson, South Carolina, USA
*
Dr J.E. Frick, Department of Biological Sciences, Clemson University, Clemson, SC 29634 1903, USA. Tel: +1 (864) 656-3603. Fax: +1 (864) 656-0435. e-mail: jefrick@clemson.edu.
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Summary

Primordial germ cells (PGCs) are described from the gonad of c. 2 cm juvenile Branchiostoma virginiae; early oocytes (c. 10 μm) and enlarging, previtellogenic oocytes (c. 35 μm) are described from the ovary of c. 5 cm adults. The germinal epithelium of the juvenile gonad and adult ovary is composed of both germinal and somatic cells. In the juvenile, somatic cells retain contact with the basal lamina of the germinal epithelium though their perikarya may be displaced towards the lumen; the germinal epithelium is, therefore, a simple but pseudostratified epithelium. In the adult ovary, somatic cells may lose contact with the basal lamina and the epithelium appears to become stratified. PGCs and oocytes are identified as germ cells by the presence of nuage. PGCs and oocytes are polarised epithelial cells. They rest on a basal lamina, extend apically towards a lumen, form adhering junctions with neighbouring cells, and exhibit apical-basal polarity. PGCs and early oocytes have an apical flagellum with an associated basal body, accessory centriole, and one or more striated rootlet fibres. The flagellum is surrounded by a collar of microvilli. Once oocytes begin to enlarge and bulge basally into the connective tissue layer, the flagellum is lost, but the basal bodies and ciliary rootlets are present at the apex of 35 μm oocytes. Similarities of the oogenic pattern in cephalochordates and echinoderms indicate that the establishment of egg polarity in deuterostomes is influenced by the polarity of the germinal epithelium.

Keywords

AmphioxusAnimal-vegetal axisApical-basal polarityEgg axisEgg polarity
Type
Article
Information
Zygote , Volume 5 , Issue 2 , May 1997 , pp. 139 - 151
Copyright
Copyright © Cambridge University Press 1997

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References

Aizenstadt, T.B. & Gabaeva, N.S. (1987). The perinuclear bodies (nuage) in the developing germ cells of the lancelet Branchiostoma lanceolatum. Tsitologiya 29, 137–41. (In Russian with English summary.)Google Scholar
Aizenstadt, T.B., Gabaeva, N.S. & Gulyaev, D.V. (1990). Cytological study of lancelet oogenesis. 2. Oocyte growth and vitellogenesis in Branchiostoma lanceolatum. Ontogenez 21, 192–9. (In Russian with English summary.)Google Scholar
Al-Mukhtar, K.A.K. & Webb, A.C. (1971). An ultrastructural study of primordial germ cells, oogonia, and early oocytes in Xenopus laevis. J. Embryol. Exp. Morphol. 26, 195–217.Google ScholarPubMed
Boveri, T. (1892). Über die Bildungsstätte der Geschlechtsdrüsen und die Entstehung der Genitalkammern beim Amphioxus. Ant. Anz. 7, 170–81.Google Scholar
Boveri, T. (1901 a). Über die Polarität des Seeigel-Eis. Verh. Phys.-Med. Ges. Würzburg 34, 145–76.Google Scholar
Boveri, T. (1901 b). Die Polarität von Ovocyte, Ei, und Larve des Strongylocentrotus lividus. Zool. Jahrb. 14, 630–51. (+3 plates as Tafel 48–50).Google Scholar
Buss, L.W. (1987). The Evolution of Individuality. Princeton, NJ: Princeton University Press.Google Scholar
Cameron, R.A., Fraser, S.E., Britten, R.J. & Davidson, E.H. (1989). The oral-aboral axis of a sea urchin embryo is specified by first cleavage. Development 106, 641–7.CrossRefGoogle ScholarPubMed
Cerfontaine, P. (1906). Recherches sur le développement de l'amphioxus. Arch. Biol. Liège 22, 229–418. (+11 plates as Planches XII-XXII).Google Scholar
Coggins, L.W. (1973). An ultrastructural and radioautographic study of early oogenesis in the toad Xenopus laevis. J. Cell Sci. 12, 71–93.CrossRefGoogle ScholarPubMed
Conklin, E.G. (1932). The embryology of amphioxus. J. Morphol. 54, 69–151.CrossRefGoogle Scholar
Eckelbarger, K.J. & Larson, R.L. (1988). Ovarian morphology and oogenesis in Aurelia aurita (Scyphozoa: Semaeostomae): ultrastructural evidence of heterosynthetic yolk formation in a primitive metazoan. Mar. Biol. 100, 103–15.CrossRefGoogle Scholar
Eckelbarger, K.J. & Young, C.M. (1992). Ovarian ultrastructure and vitellogenesis in ten species of shallow-water and bathyal sea cucumbers (Echinodermata: Holothuroidea). J. Mar. Biol. Assoc. U.K. 72, 759–81.CrossRefGoogle Scholar
Eddy, E.M. (1975). Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43, 229–80.Google Scholar
Frick, J.E. & Ruppert, E.E. (1996). Primordial germ cells of Synaptula hydriformis (Holothuroidea; Echinodermata) are epithelial flagellated-collar cells: their apical-basal polarity becomes primary egg polarity. Biol. Bull. 191, 168–77.CrossRefGoogle ScholarPubMed
Frick, J.E., Ruppert, E.E. & Wourms, J.P. (1996). Morphology of the ovotestis of Synaptula hydriformis (Holothuroidea, Apoda): an evolutionary model of oogenesis and the origin of egg polarity in echinoderms. Invert. Biol. 115, 46–66.CrossRefGoogle Scholar
Gabaeva, N.S. & Aizenstadt, T.B. (1990). Cytological study of lancelet oogenesis. 1. Ovary structure and transformation of germinal epithelium in Branchiostoma lanceolatum. Ontogenez 21, 185–91. (In Russian with English summary.)Google Scholar
Gard, D.L. (1995). Axis formation during amphibian oogenesis: reevaluating the role of the cytoskeleton. Curr. Top. Dev. Biol. 30, 215–52.Google Scholar
Gerhart, J., Black, S., Gimlich, R. & Scharf, S. (1983). Control of polarity in the amphibian egg. In Time, Space, and Pattern in Embryonic Development, ed. Jeffery, W.R. & Raff, R.A., pp. 261–86. New York: A.R. Liss.Google Scholar
Gerhart, J., Danilchik, M., Doniach, T., Roberts, S., Rowning, B. & Stewart, R. (1989). Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107, 37–51.CrossRefGoogle ScholarPubMed
González-Reyes, A. & St Johnston, D. (1994). Role of oocyte position in establishment of anterior-posterior polarity in Drosophila. Science 266, 639–42.CrossRefGoogle ScholarPubMed
González-Reyes, A., Elliott, H. & St Johnston, D. (1995). Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654–8.Google Scholar
Guraya, S.S. (1983). Cephalochordata. In Reproductive Biology of Invertebrates, vol. 1, Oogenesis, Oviposition, and Oosorption, ed. Adiyodi, K.G. & Adiyodi, R.G., pp. 735–52. Chichester: Wiley.Google Scholar
Hay, E.D. (1990). Epithelial-mesenchymal transitions. Semin. Dev. Biol. 1, 347–56.Google Scholar
Henry, J.J., Klueg, K.M. & Raff, R.A. (1992). Evolutionary dissociation between cleavage, cell lineage and embryonic axes in sea urchin embryos. Development 114, 931–8.Google Scholar
Hirakow, R. & Kajita, N. (1990). An electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: cleavage. J. Morphol. 203, 331–44.Google Scholar
Hirakow, R. & Kajita, N. (1991). Electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: the gastrula. J. Morphol. 207, 37–52.CrossRefGoogle ScholarPubMed
Holland, N.D. & Holland, L.Z. (1989). Fine structural Study of the cortical reaction and formation of the egg coats in a lancelet (=amphioxus), Branchiostoma floridae (Phylum Chordata: Subphylum Cephalochordata = Acrania). Biol. Bull. 176, 111–22.CrossRefGoogle Scholar
Holland, N.D. & Holland, L.Z. (1991). The fine structure of the growth stage oocytes of a lancelet (= amphioxus), Branchiostoma lanceolatum. Invert. Reprod. Dev. 19, 107–22.CrossRefGoogle Scholar
Holland, N.D. & Holland, L.Z. (1992). Early development in the lancelet (= amphioxus) Branchiostoma floridae from sperm entry through pronuclear fusion: presence of vegetal pole plasm and lack of conspicuous ooplasmic segregation. Biol. Bull. 182, 77–96.CrossRefGoogle ScholarPubMed
Hörstadius, S. (1973). Experimental Embryology of Echinoderms. Oxford: Clarendon Press.Google Scholar
Houk, M.S. & Hinegardner, R.T. (1980). The formation and early differentiation of sea urchin gonads. Biol. Bull. 159, 280–94.CrossRefGoogle Scholar
Jenkinson, J.W. (1911). On the origin of the polar and bilateral structure of the egg of the sea urchin. Arch. Entwicklungsmech. Organ. 32, 699–716.Google Scholar
Kalthoff, K. (1976). Specification of the antero-posterior body pattern in insect eggs. In Insect Development, ed. Lawrence, P.A., pp. 53–75. Oxford: Blackwell Scientific.Google Scholar
Kato, K.H., Washitani-Nemoto, S., Hino, A. & Nemoto, S. (1990). Ultrastructural studies on the behavior of centrioles during meiosis of starfish oocytes. Dev. Growth Differ. 32, 41–9.Google Scholar
Kessel, R.G. (1968). Electron microscope studies on developing oocytes of a coelenterate medusa with special reference to vitellogenesis. J. Morphol. 126, 211–48.CrossRefGoogle Scholar
Klymkowsky, M.W. & Karnovsky, A. (1994). Morphogenesis and the cytoskeleton: studies of the Xenopus embryo. Dev. Biol. 165, 372–83.CrossRefGoogle ScholarPubMed
Langerhans, P. (1876). Zur Anatomie des Amphioxus lanceolatus. Arch. Mikrosk. Anat. 12, 290–348. (+4 plates as Tafel XII-XV).CrossRefGoogle Scholar
Larkman, A.U. (1981). An ultrastructural investigation of the early stages of oocyte differentiation in Actinia fragacea (Cnidaria; Anthozoa). Int. J. Invert. Reprod. 4, 147–67.CrossRefGoogle Scholar
Larkman, A.U. (1983). An ultrastructural study of oocyte growth within the endoderm and entry into the mesoglea in Actinia fragacea (Cnidaria, Anthozoa). J. Morphol. 178, 155–77.Google Scholar
Larkman, A.U. (1984). The fine structure of mitochondria and the mitochondrial cloud during oogenesis on the sea anemone Actinia. Tissue Cell 16, 393–404.Google Scholar
Maruyama, Y.K., Nakaseko, Y. & Yagi, S. (1985). Localization of cytoplasmic determinants responsible for primary mesenchyme formation and gastrulation in the unfertilized egg of the sea urchin Hemicentrotus pulcherrimus. J. Exp. Zool. 236, 155–63.CrossRefGoogle Scholar
Neidert, L. & Leiber, A. (1903). Über Bau und Entwicklung der weiblichen Geschlechtsorgane des Amphioxus lanceolatus. Zool. Jahrb. 18, 187–226. (+5 plates as Tafel 15–19).Google Scholar
Nielsen, C. (1995). Animal Evolution: Interrelationships of the Living Phyla. New York: Oxford University Press.Google Scholar
Okada, T. & Yamamoto, M. (1993). Identification of early oogenetic cells in the solitary ascidians, Ciona savignyi and Ciona intestinalis: an immunoelectron microscopic study. Dev. Growth Differ. 35, 495–506.Google Scholar
Remane, A. (1963). The evolution of the Metazoa from colonial flagellates vs plasmodial ciliates. In The Lower Metazoa, vol. 2, ed. Dougherty, E.C., pp. 23–32. Berkeley: University of California Press.Google Scholar
Reverberi, G. (1966). L'uovo ovarico di Amfiosso al microscopio elettronico. Arch. Zool. Ital. 51, 903–15. (+16 plates as Tav. LXXXIV-XCIX).Google Scholar
Reverberi, G. (1971). Amphioxus. In Experimental Embryology of Marine and Fresh-water Invertebrates, ed. Reverberi, G., pp. 551–72. Amsterdam: North-Holland.Google Scholar
Reverberi, G. & De Leo, G. (1972). The oocyte of amphioxus examined by the electron microscope. Acta Embryol. Exp. [1972], 65–84.Google Scholar
Rieger, R. (1976). Monociliated epidermal cells in Gastrotricha: significance for concepts of early metazoan evolution. Z. Zool. Syst. Evolut.-forsch. 14, 198–26.CrossRefGoogle Scholar
Ruppert, E.E. (1997). Cephalochordata (Acrania). In Microscopic Anatomy of Invertebrates, vol. 15, Hemichordata, Chaetognatha and the Invertebrate Chordates, ed. Harrison, F.W. & Ruppert, E.E.. New York: Wiley-Liss. In press.Google Scholar
Ruppert, E.E. & Barnes, R.D. (1994). Invertebrate Zoology, 6th edn. Philadelphia: W.B. Saunders.Google Scholar
Salvini-Plawen, L.v. (1978). On the origin and evolution of the lower Metazoa. Z. Zool. Syst. Evolut.-forsch. 16, 40–88.CrossRefGoogle Scholar
Schroeder, T.E. (1980). Expressions of the prefertilization polar axis in sea urchin eggs. Dev. Biol. 79, 428–43.Google Scholar
Schroeder, T.E. (1985). Cortical expressions of polarity in the starfish oocyte. Dev. Growth Differ. 27, 311–21.CrossRefGoogle ScholarPubMed
Schroeder, T.E. & Otto, J.J. (1991). Snoods: a periodic network containing cytokeratin in the cortex of starfish oocytes. Dev. Biol. 114, 240–7.Google Scholar
Simons, K. & Fuller, S.D. (1985). Cell surface polarity in epithelia. Annu. Rev. Cell Biol. 1, 243–88.CrossRefGoogle ScholarPubMed
Smiley, S. (1988). The dynamics of oogenesis and the annual ovarian cycle of Stichopus californicus (Echinodermata: Holothuroidea). Biol. Bull. 175, 79–93.Google Scholar
Tyler, P.A., Eckelbarger, K. & Billett, D.S.M. (1994). Reproduction in Bathyplotes natans (Holothuroidea: Synallactidae) from bathyal depths in the northeast and western Atlantic. J. Mar. Biol. Assoc. U.K. 74, 383–402.CrossRefGoogle Scholar
Vincent, J.-P. & Gerhart, J.C. (1987). Subcortical rotation in Xenopus eggs: an early step in embryonic axis specification. Dev. Biol. 123, 526–39.Google Scholar
Vincent, J.-P., Oster, G.F. & Gerhart, J.C. (1986). Kinematics of gray crescent formation in Xenopus eggs: the displacement of subcortical cytoplasm relative to the egg surface. Dev. Biol. 113, 484–500.Google Scholar
Welsch, U. & Fang, Y.Q. (1996). The reproductive organs of Branchiostoma. Israel J. Zool. 42, 183–212.Google Scholar
Welsch, U. & Storch, V. (1976). Comparative Animal Cytology and Histology. Seattle: University of Washington Press.Google Scholar
Wickstead, J.H. (1975). Chordata: Acrania (Cephalochordata). In Reproduction of Marine Invertebrates, vol. 2, Entoprocts and Lesser Coelomates, ed. Giese, A.C. & Pearse, J.S., pp. 283–319. New York: Academic Press.CrossRefGoogle Scholar
Wilson, E.B. (1896). The Cell in Development and Inheritance, 1st edn. New York: Macmillan.Google Scholar
Wourms, J.P. (1987). Oogenesis. In Reproduction of Marine Invertebrates, vol. 9, General Aspects: Seeking Unity in Diversity, ed. Giese, A.C., Pearse, J.S. & Pearse, V.B., pp. 49–178. Pacific Grove, CA: Boxwood Press.Google Scholar
Zarnik, B. (1905). Über Zellenauswanderungen in der Leber und im Mitteldarm von Amphioxus. Anat. Anz. 27, 433–49.Google Scholar