Summary
A hypothesis is presented which explains the segregation of germ cells from somatic cells, and the subsequent determination of both cell types with a single mechanism. This hypothesis is in part based on that of Meinhardt (1977) and can be summarized as follows: In the newly fertilized egg, the action of a sink in the pole plasm leads to the formation of an anterior-posterior gradient of an inhibitor. The concentration of this inhibitor in the posterior 20% of the egg is below that needed to repress synthesis of an activator. When, during the nuclear division stage, nuclei enter this posterior region, synthesis of the activator begins. As the activator is autocatalytic, this leads to the formation of a peak of activator in this region; and since the activator also catalyses the synthesis of the inhibitor, a peak of inhibitor is formed in the same place. The inhibitor then diffuses anteriorly through the periplasm, forming a posterior-anterior gradient. The presence of this inhibitor in the periplasm causes the nuclei that enter the periplasm to form blastoderm cells and to take up particular segmental states appropriate to their position, while those that remain in the yolk-containing plasm develop into vitellophages. The action of the sink in the pole plasm is postulated to result in the formation of the pole cells, and subsequently to direct some of these into forming cells of the germ-line.
Similar content being viewed by others
References
Achtelig M, Krause G (1971) Experimente am ungefurchten Ei vonPimpla turionellae L (Hymenoptera) zur Funktionasanalyse des Oosombereichs. Wilhelm Roux's Archives 167:164–182
Beams HW, Kessel RG (1974) The problem of germ cell determinants. Int Rev Cytol 39:413–479
Cavallin M (1971) La ‘polyembryonie substitutive’ et le problème de l'origine de la lignée germinale chez le Phasme Carausius morosus Br. CR Acad Sci Ser D: 272:462
Counce SJ (1963) Developmental morphology of polar granules inDrosophila. Including observations on the pole cell behavior and distribution during embryogenesis. J Morphol 112:129–146
Counce SJ (1972) The causal analysis of insect embryogenesis. In: Counce, SJ, Waddington, CH (eds) Developmental systems: Insects, Vol II. Academic Press, New York, pp 1–156
Counce SJ, Ede DA (1957) The effect on embryogenesis of a sexlinked female-sterility factor inDrosophila melanogaster. J Embryol Exp Morphol 5:404–421
Deak II (in press) Positional information and determination duringDrosophila embryogenesis. In: Buckingham ME (ed) Development and differentiation. CRC Press, Florida
Deak II (1980) A model linking segmentation, compartmentalization and regeneration inDrosophila development. J Theor Biol 84, in press
Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229–280
Fielding CF (1967) Developmental genetics of the mutantgrandchildless ofDrosophila subobscura. J Embryol Exp Morphol 17:375–384
Franz D (1972) Der Einfluß des Abstands zwischen verlagertem Hinterpolmaterial und Eioberfläche auf das embryonale Segmentmuster von Euscelis plebejus. Staatsexamenarbeit, Fak f Biologie der Universität Freiburg i Br
Gehring WJ (1976) Developmental genetics ofDrosophila. Annu Rev Genet 10:209–252
Geigy R (1931) Action de l'ultra-violet sur le pôle germinal dans l'oeuf deDrosophila melanogaster (castration et mutabilité) Rev Suisse Zool 38:187–288
Hegner RW (1914) Studies on germ-cells. J Morphol. 25:375–510
Illmensee K, Mahowald AP, Loomis MR (1976) The ontogeny of germ plasm during oogenesis inDrosophila. Dev Biol 49:40–65
Johson RT, Rao PN (1971) Nucleocytoplasmic interaction in the achievement of nuclear synchrony in DNA synthesis and mitosis in multinucleate cells. Biol Rev Cambridge Philos Soc 46:97
Kalthoff K (1971) Position of targets and period of competence for UV-induction of the malformation double abdomen in the egg of Smittia spec. (Dipt, Chir) Wilhelm Roux's Archives 168:63–84
Kalthoff K, Hanel P, Zissler D (1977) A morphogenetic determinant in the anterior pole of an insect egg (Smittia spec., Chironomidae, Diptera). Localisation by combined centrifugation and UV irradiation. Dev Biol 55:285–305
Kauffman SA (1977) Chemical patterns, compartments and binary epigenetic code inDrosophila. Am Zool 17:631–648
Kauffman SA, Shymko RM, Trabert K (1978) Control of sequential compartment formation inDrosophila. Science 199:259–270
Kaufmann BP (1940) The nature of hybrid sterility. — Abnormal development in eggs of hybrids betweenDrosophila miranda andDrosophila subobscura. J Morphol 66:197–213
Mahowald AP (1971) Polar granules ofDrosophila. III. The continuity of polar granules during the life cycle ofDrosophila. J Exp Zool 176:329–344
Mahowald AP (1972) Oogenesis. In: Counce SJ, Waddington CH (eds)Developmental systems: Insects, Vol I. Academic Press, New York, pp 1–47
Mahowald AP (1977) The germ plasm ofDrosophila: an experimental system for the analysis of determination. Am Zool 17, 551–563
Meinhardt H (1977) A model of pattern formation in insect embryogenesis. J Cell Sci 23:117–139
Meinhardt H (1978) Space-dependent cell determination under the control of a morphogen gradient. J Theor Biol 74:307–321
Okada M, Kleinman IA, Schneiderman HA (1974) ChimericDrosophila adults produced by transplantation of nuclei into specific regions of fertilized eggs. Dev Biol 39:286–294
Poulson DF (1947) The pole cells ofDiptera, their fate and significance. Proc Natl Acad Sci USA 6:182–184
Poulson DF (1950) Histogenesis, organogenesis and differentiation in the embryo ofDrosophila melanogaster Meigen. In: Demerec M (ed) Biology ofDrosophila. Wiley, New York, pp 168–274
Rabinowitz M (1941) Studies on the cytology and early embryology of the egg ofDrosophila melanogaster J Morphol 69:1–49
Sander K (1960) Analyse des ooplasmatischen Reaktionssystems vonEuscelis plebejus Fall. (Cicadina) durch Isolieren und Kombinieren von Keimteilen. II. Mit.: Die Differenzierungsleistungen nach Verlagern von Hinterpolmaterial. Wilhelm Roux's Archives 151:660–707
Sander K (1975) Pattern specification in the insect embryo. In: Ciba Found Symp 29 (New Series): 241–263
Sander K (1976) Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol 12:125–238
Schubiger G, Wood WJ (1977) Determination during early embryogenesis inDrosophila melanogaster. Am Zool 17:565–576
Scriba MEL (1964) Beeinflussung der frühen Embryonalentwicklung vonDrosophila melanogaster durch Chromosomenaberrationen. Zool Jahrb Abt Anat Ontog Tiere 81:435–490
Seidel F (1924) Die Geschlechtsorgane in der embryonalen Entwicklung vonPyrrhocoris apterus L. Z Morphol Oekol Tiere 1:429–506
Seidel F (1926) Die Determinierung der Keimanlage bei Insekten. Biol Zentralbl 46:321–343
Seidel F (1929) Untersuchungen über das Bildungsprinzip der Keimanlagen im Ei der LibellePlatycnemis pennipes. Wilhelm Roux's Archives 119:322–440
Seidel F (1931) Die Reaktionsfolge im Determinationsgeschehen des Libellenkeims. Verh Dtsch Zool Ges (Zool Anz Suppl 5) 33:193–200
Seidel F, Bock E, Krause G (1940) Die Organisation des Insekteneies. Naturwissenschaften 28:433–446
Sonnenblick BP (1941) Germ cell movements and sex differentiation of the gonads in theDrosophila embryo. Proc Natl Acad Sci USA 27:484–489
Thierry-Mieg DJ (1976) Study of a temperature-sensitive mutantgrandchildless-like inDrosophila melanogaster. J Microsc Biol Cell 25:1–6
Turner FR, Mahowald AP (1976) Scanning electron microscopy ofDrosophila embryos. I. The structure of the egg envelope and the formation of the cellular blastoderm. Dev Biol 50:95–108
Vogel O (1977) Regionalisation of segment-forming capacities during early embryogenesis in Drosophila melanogaster. Wilhelm Roux's Archives 182:9–32
Wieschaus E, Szabad J (1979) The development and function of the female germ line inDrosophila melanogaster: A cell lineage study. Dev Biol 68:29–46
Wolf R, Krause G (1971) Die Ooplasmabewegungen während der Furchung von Pimpla turionellae L. (Hymenoptera), eine Zeitrafferfilmanalyse. Wilhelm Roux's Archives 167:266–287
Yajima H (1960) Studies on embryonic determination of the harlequin-fly,Chironomus dorsalis. I. Effects of centrifugation and of its combination with constriction and puncturing. J Embryol Exp Morphol 8:198–215
Zalokar M, Erk I (1976) Division and migration of nuclei during early embryogenesis ofDrosophila melanogaster. J Microsc Biol Cell 25:97–106
Author information
Authors and Affiliations
Additional information
Dr. Ilan Deak had submitted this paper shortly before his untimely death. The editors decided to publish his thoughts as expressed by him. However, with the consent of his friends and collaborators, some paragraphs reviewing earlier data were cut out, and deviating opinions were added as footnotes
Rights and permissions
About this article
Cite this article
Deak, I.I. Embryogenesis inDrosophila: Can a single mechanism explain the developmental segregation of germ-line and somatic cells and their subsequent determination?. Wilhelm Roux' Archiv 188, 179–185 (1980). https://doi.org/10.1007/BF00849046
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00849046