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The induction of the primordial germ cells in the urodeles

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Summary

Xenoplastic recombinates of animal ectodermal caps with the ventral vegetative yolk mass of blastulae of stage 81/2–83/4 ofA. mexicanum, T. alpestris, T. cristatus carnifex andP. waltlii have demonstrated unambiguously that in the urodeles the primordial germ cells—together with other ventro-caudal mesodermal structures—develop from the animal ectodermal moiety of the blastula under an inductive influence emanating from the ventral vegetative yolk mass. Similar recombinates of3H-labeled and unlabeled ectodermal and endodermal components fully support this conclusion.

Recombinates of the ventral vegetative yolk mass with different regions of the animal ectodermal hemisphere show that primordial germ cells can be formed by any region of the animal ectodermal hemisphere, including those regions which in normal development will never form them. The number of primordial germ cells formed differs significantly among the various regions, that of the ventral peripheral region being the highest and that of the central, animal region the lowest. The capacity for primordial germ cell formation shows two increasing gradients, one animal-vegetative and the other dorse-ventral (in the peripheral zone). Although accurate measurements could not be made, there seems to be a relation between the number of primordial germ cells formed and the amount of ventro-caudal mesoderm induced.

The experiments, moreover, show that notochord differentiation largely or entirely suppresses primordial germ cell formation. Notochord differentiation shows a similar animalvegetative, but an opposite ventro-dorsal increase in frequency (in the peripheral zone) as compared with the capacity for primordial germ cell formation. The notochord-forming gradient in the peripheral regions is mainly due to the inductive action already exerted by the dorsal vegetative yolk mass in the intact blastula prior to isolation and recombination (see control explants). The ventro-dorsal decline in primordial germ cell formation in the peripheral regions is very probably due only to the inhibition of primordial germ cell formation by notochord differentiation (as an expression of dorsal mesoderm induction). Therefore, in the animal ectodermal moiety of the blastula there exists only an animal-vegetative gradient in mesodermal competence.

These results make it very likely that in urodeles the primordial germ cells do not arise from predetermined elements such as those demonstrated in anurans, but develop from common, totipotent animal ectodermal cells. The discrepancy in the mode of origin of the primordial germ cells between anurans and urodeles could be due only to pronounced differences in the time of appearance of the germinal cytoplasm (in anurans during oogenesis, in urodeles possibly during determination of the primordial germ cells within the ventro-caudal mesoderm).

The differences in site and mode of origin of the primordial germ cells between urodeles and anurans favor a dual phylogenetic origin of the two groups.

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References

  • Amanuma, A.: Effect of extirpation of the presumptive intermediate mesoderm upon the differentiation of the primordial germ cells. Zool. Mag. (Tokyo)66, 310–313 (1957) [Japanese; English summary]

    Google Scholar 

  • Amanuma, A.: On the role of the dorso-caudal endoderm in the formation of the primordial germ cells. J. Inst. Polytech., Osaka City Univ., Ser. D,9, 211–216 (1958)

    Google Scholar 

  • Asayama, S.: The developmental potiencies of the intermediate mesoderm ofTriturus pyrrhogaster when transplanted into orthotopic or heterotopic site in the body wall of another embryo. J. Inst. Polytech., Osaka City Univ., Ser. D,1, 13–28 (1950)

    Google Scholar 

  • Asayama, S.: Potency of lateral plate mesoderm relating to the formation of reproductive tissue. Zool. Mag. (Tokyo)70, 289–293 (1961) [Japanese, English summary]

    Google Scholar 

  • Asayama, S., Amanuma, A.: On the primordial germ cells of the secondary embryo induced by the organizer. Zool. Mag. (Tokyo)66, 279–283 (1957) [Japanese, English summary]

    Google Scholar 

  • Blackler, A. W.: The integrity of the reproductive cell line in the amphibia. Curr. Topics Develop. Biol.5, 71–87 (1970)

    Google Scholar 

  • Boterenbrood, E. C., Nieuwkoop, P. D.: The formation of the mesoderm in urodelean amphibians. V. Its regional induction by the endoderm. Wilhelm Roux' Archiv173, 319–332 (1973)

    Google Scholar 

  • Bounoure, L.: L'origine des cellules reproductrices et le problème de la ligne germinale. Paris: Gauthiers-Villars 1939

    Google Scholar 

  • Cambar, R.: L'uretère primaire de la grenouille se développe, en direction postérieure, à partir d'un blastème voisin du pronéphros: démonstration expérimentale. C. R. Soc. Biol. (Paris)146, 77 (1952)

    Google Scholar 

  • Capuron, A.: Analyse expérimentale de l'organogenèse uro-génitale d'embryons induits par la greffe de la lèvre dorsale du blastopore chez l'Amphibien UrodèlePleurodeles waltlii (Michah.). Ann. Embryol. Morphogen.1, 3–27 (1968)

    Google Scholar 

  • Capuron, A.: Mise en évidence de gonocytes dans divers territoires isolés au stade du bourgeon caudal et cultivés in vitro chezPheurodeles waltlii Michah. (Amphibien Urodèle). C. R. Acad. Sci. (Paris), Ser. D,274, 277–279 (1972)

    Google Scholar 

  • Czołowska, R.: Observations on the origin of the “germinal cytoplasm” inXenopus laevis. J. Embryol. exp. Morph.22, 229–251 (1969)

    Google Scholar 

  • Harrison, R. G.: Harrison stages and description of the normal development of the spotted salamander,Ambystoma punctatum (Linn.). In: Organization and development of the embryo, S. Wilens, ed. p. 44–66. New Haven-London: Yale University Press 1969

    Google Scholar 

  • Humphrey, R. R.: The primordial germ cells ofHemidactylium and other Amphibia. J. Morph. Physiol.41, 1–43 (1925)

    Google Scholar 

  • Humphrey, R. R.: Extirpation of the primordial germ cells inAmbystoma; its effect upon the development of the gonad. J. exp. Zool.49, 363–399 (1927)

    Google Scholar 

  • Humphrey, R. R.: The developmental potencies of the intermediate mesoderm ofAmbystoma when transplanted into ventro-lateral sites in other embryos: the primordial germ cells of such grafts and their role in the development of a gonad. Anat. Rec.40, 67–90 (1928)

    Google Scholar 

  • Humphrey, R. R.: The early position of the primordial germ cells in Urodeles; evidence from experimental studies. Anat. Rec.42, 301–314 (1929)

    Google Scholar 

  • Kalt, M. R.: Germ cell development and premeiotic rRNA amplification inXenopus laevis. J. Cell Biol.55, 128a (1972)

    Google Scholar 

  • Kocher-Becker, U., Tiedemann, H.: Induction of mesodermal and endodermal structures and primordial germ cells inTriturus ectoderm by a vegetalizing factor from chick embryos. Nature. (Lond.)233, 65–66 (1971)

    Google Scholar 

  • Kopriwa, B. M., Leblond, C. P.: Improvements in the coating technique of radioautography. J. Histochem. Cytochem.10, 269–284 (1962)

    Google Scholar 

  • Kotani, M.: On the formation of the primordial germ cells from the presumptive ectoderm ofTriturus gastrulae. J. Inst. Polytech., Osaka City Univ., Ser. D,8, 145–158 (1957)

    Google Scholar 

  • Kotani, M.: The formation of germ cells after extirpation of the presumptive lateral mesoderm ofTriturus gastrulae. J. Inst Polytech., Osaka City Univ., Ser. D,9, 195–208 (1958)

    Google Scholar 

  • Leikola, A.: The mesodermal and neural competence isolated gastrula ectoderm studied by heterogenous inductors. Ann. Zool. Soc. Zool. Bot. Fenn. Vanamo25, 1–50 (1963)

    Google Scholar 

  • Leikola, A.: On the loss of mesodermal competence ofTriturus gastrula ectoderm in vivo. Experientia (Basel)21, 458–459 (1965)

    Google Scholar 

  • Nakamura, D., Matsuzawa, T.: Differentiation capacity of the marginal zone in the morula and blastula ofTriturus pyrrhogaster. Embryologia (Nagoya)9, 223–237 (1967)

    Google Scholar 

  • Nieuwkoop, P. D.: Experimental investigations on the origin and determination of the germ cells, and on the development of the lateral plates and germ ridges in Urodeles. Arch. néerl. Zool.8, 1–205 (1947)

    Google Scholar 

  • Nieuwkoop, P. D.: The formation of the mesoderm in urodelean amphibians. I. Induction by the endoderm. Wilhelm Roux' Archiv162, 341–373 (1969a)

    Google Scholar 

  • Nieuwkoop, P. D.: The formation of the mesoderm in urodelean amphibians. II. The origin of the dorso-ventral polarity of the mesoderm. Wilhelm Roux' Archiv163, 298–315 (1969b)

    Google Scholar 

  • Nieuwkoop, P. D.: The formation of the mesoderm in urodelean amphibians. III. The vegetalizing action of the Li-ion. Wilhelm Roux' Archiv166, 105–123 (1970)

    Google Scholar 

  • Nieuwkoop, P.D.: The “organization center” of the amphibian embryo: its origin, spatial organization, and morphogenetic action. Advanc. Morphogen.10, 1–39 (1973)

    Google Scholar 

  • Nieuwkoop, P. D., Ubbels, G. A.: The formation of the mesoderm in urodelean amphibians. IV. Qualitative evidence for the purely “ectodermal” origin of the entire mesoderm and of pharyngeal endoderm. Wilhelm Roux' Archiv169, 185–199 (1972)

    Google Scholar 

  • O'Connor, R. J.: Experiments on the development of the pronephric duct. J. Anat. (Lond.)73, 145–155 (1938)

    Google Scholar 

  • Schechtman, A. M.: Experiments on anus formation in a frog egg. Proc. Soc. exp. Biol. (N.Y.)41, 48–50 (1939)

    Google Scholar 

  • Siegel, S.: Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill 1956

    Google Scholar 

  • Smith, L. D.: A test of the capacity of presumptive somatic cells to transform into primordial germ cells in the Mexican axolotl. J. exp. Zool.156, 229–242 (1964)

    Google Scholar 

  • Sukirno, S. S.: Developmental capacities of the blastula in the anuranXenopus laevis (Daud.). Thesis, Bandung, Indonesia (1970)

  • Williams, M. A., Smith, L. D.: Ultrastructure of the “germinal plasm” during maturation and early cleavage inR. pipiens. Develop. Biol.25, 568–580 (1971)

    Google Scholar 

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Sutasurja, L.A., Nieuwkoop, P.D. The induction of the primordial germ cells in the urodeles. W. Roux' Archiv f. Entwicklungsmechanik 175, 199–220 (1974). https://doi.org/10.1007/BF00582092

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