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On the dispersion of imaginal progenitor cells in the Drosophila blastoderm

Published online by Cambridge University Press:  14 April 2009

Robert J. Wyman  and
David G. King
Robert J. Wyman
Affiliation:
Department of Biology, Yale University, New Haven, Connecticut 06520
David G. King
Affiliation:
Department of Biology, Yale University, New Haven, Connecticut 06520
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Summary

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The number of blastoderm cells in Drosophila whose descendants form adult structures has frequently been estimated from genetic mosaics. Data from somatic recombination (method I) and gynandromorph (method II) mosaics both yield very low estimates, e.g. about 10–20 progenitor cells for the eye and antenna, wing or leg.

In gynandromorphs the mosaic dividing line has a random orientation on the blastoderm. In the 6000 cell blastoderm it should be very unlikely that the mosaic dividing line passes through any small patch of only 10–20 cells. Yet it has been reported that 10–25% of eye/antenna, wing or leg disks in gynandromorphs are mosaic. Thus the frequency of mosaicism data seems to be in contradiction to the progenitor population estimates. Similar discrepancies are found in the data for other adult structures.

In this paper we derive a formula for estimating the number of cells in a blastoderm patch from the frequency with which the gynandromorph dividing line passes through it (method III). In a second method (method IV) we use the maximum distances inside the progenitor areas on a fate map to estimate the progenitor patch size. These two estimates agree closely with each other. We find, e.g. that 50–100 cells are in the patches from which the eye/antenna, wing or leg disks derive.

We examine a number of possible explanations for why the first two estimates are so much smaller than the last two. The former estimates refer to the number of progenitor cells which actually have descendants in the adult structure; the latter estimates refer to the total patch area in which the progenitor cells sit. With the present information the most reasonable conclusion is that the progenitor cells for the adult structures are dispersed among other cells which have different developmental fates. If confirmed by experiment, this result has many implications for the process of determination.

Type
Research Article
Information
Genetics Research , Volume 31 , Issue 3 , June 1978 , pp. 273 - 286
Copyright
Copyright © Cambridge University Press 1978

References

REFERENCES

(1)Baker, W. K. (1967). A clonal system of differential gene activity in Drosophila. Developmental Biology 16, 1–17.CrossRefGoogle ScholarPubMed
(2)Bakken, A. H. (1973). A cytological and genetic study of oogenesis in Drosophila melanogaster. Developmental Biology 33, 100–122.CrossRefGoogle ScholarPubMed
(3)Becker, H. J. (1957). Über Rontgenmosaikflecken und Defectmutationen am Auge von Drosophila und die Entwicklungsphysiologie des Auges. Zeitschrift für Induktive Abstammungs – und Vererbungslehre 88, 333–373.Google Scholar
(4)Bryant, P. J. (1970). Cell lineage relationships in the imaginal wing disc of Drosophila melanogaster. Developmental Biology 22, 389–411.CrossRefGoogle ScholarPubMed
(5)Bryant, P. J. & Schneiderman, H. A. (1969). Cell lineage, growth and determination in the imaginal leg discs of Drosophila melanogaster. Developmental Biology 20, 263–290.CrossRefGoogle ScholarPubMed
(6)Chan, L. N. & Gehring, W. (1971). Determination of blastoderm cells in Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 68, 2217–2221.CrossRefGoogle ScholarPubMed
(7)Gans, M., Audit, C. & Masson, M. (1975). Isolation and characterization of sex-linked female-sterile mutants in Drosophila melanogaster. Genetics 81, 683–704.CrossRefGoogle ScholarPubMed
(8)Garcia-Bellido, A. & Merriam, J. R. (1969). Cell lineage of the imaginal discs in Drosophila gynandromorphs. Journal of Experimental Zoology 170, 61–75.CrossRefGoogle ScholarPubMed
(9)Garcia-Bellido, A. & Merriam, J. R. (1971 a). Parameters of the wing imaginal disc development of Drosophila melanogaster. Developmental Biology 24. 61–87.CrossRefGoogle ScholarPubMed
(10)Garcia-Bellido, A. & Merriam, J. R. (1971 b). Clonal parameters of tergite development in Drosophila. Developmental Biology 26, 264–276.CrossRefGoogle ScholarPubMed
(11)Gehring, W. J., Wieschaus, E. & Hollinger, M. (1976). The use of ‘normal’ and ‘transformed’ gynandromorphs in mapping the primordial germ cells and the gonadal mesoderm in Drosophila. Journal of Embryology and Experimental Morphology 35, 607–616.Google ScholarPubMed
(12)Geigy, R. (1931). Erzeugung rein imaginaler Defekte durch ultraviolette Eibstrahlung bei Drosophila melanogaster. Wilhelm Roux Archiv für Entwicklungsmechanik der Organismen 125, 406–447.CrossRefGoogle Scholar
(13)Guerra, M., Postlethwaite, J. H. & Schneiderman, H. A. (1963). The development of the imaginal abdomen of Drosophila melanogaster. Developmental Biology 32, 361–372.CrossRefGoogle Scholar
(14)Haynie, J. L. & Bryant, P. J. (1977). The effects of x-rays on the proliferation dynamics of cells in the imaginal wing disc of Drosophila melanogaster. Wilhelm Roux's Archives of Developmental Biology 183, 85–100.CrossRefGoogle Scholar
(15)Hotta, Y. & Benzer, S. (1973). Mapping of behaviour in Drosophila mosaics. In Genetic Mechanisms of Development (ed. Ruddle, F.), pp. 129–167. New York: Academic Press.CrossRefGoogle Scholar
(16)Illmensee, K. & Mahowald, A. P. (1974). Transplantation of posterior polar plasm in Drosophila. Induction of germ cell at the anterior pole of the eggs. Proceedings of the National Academy of Sciences, U.S.A. 71, 1016–1020.CrossRefGoogle Scholar
(17)Janning, W. (1974). Entwicklungsgenetische Untersuchungen an Gynandern von Drosophila melanogaster. II. Der morphogenetische Anlageplan. Wilhelm Roux Archiv für Entwicklungsmechanik der Organismen 174. 349–359.CrossRefGoogle Scholar
(18)Kankel, D. R. & Hall, J. C. (1976). Fate mapping of nervous system and other internal tissues in genetic mosaics of Drosophila melanogaster. Developmental Biology 48, 1–24.CrossRefGoogle ScholarPubMed
(19)Lawrence, P. A., Green, S. M. & Johnston, P. (1973). Compartmentalization and growth of the Drosophila abdomen. Journal of Embryology and Experimental Morphology 43, 233–245.Google Scholar
(20)Lawrence, P. A. & Morata, G. (1977). The early development of mesothoracic compartments in Drosophila. Developmental Biology 56, 40–51.CrossRefGoogle ScholarPubMed
(21)Madhavan, M. M. & Schneiderman, H. A. (1977). Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development of Drosophila melanogaster. Wilhelm Roux's Archives of Developmental Biology 183, 269–305.CrossRefGoogle Scholar
(22)Nissani, M. & Lipow, C. (1977). A method for estimating the number of blastoderm cells which give rise to Drosophila imaginal discs. Theoretical and Applied Genetics 49, 3–8.CrossRefGoogle ScholarPubMed
(23)Parks, H. B. (1936). Cleavage patterns in Drosophila and mosaic formation. Annals of the Entomological Society of America 29, 350–392.CrossRefGoogle Scholar
(24)Postlethwaite, J. H. & Schneiderman, H. A. (1971 a). A clonal analysis of development in Drosophila melanogaster: Morphogenesis, determination, and growth in the wild-type antenna. Developmental Biology 24, 477–519.CrossRefGoogle Scholar
(25)Postlethwaite, J. H. & Schneiderman, H. A. (1971 b). Pattern formation and determination in the antenna of the homoeotic mutant Antennapedia of Drosophila melanogaster. Developmental Biology 25, 606–640.CrossRefGoogle Scholar
(26)Rice, T. B. (1973). Isolation and characterization of maternal effect mutants: An approach to the study of early determination in Drosophila melanogaster. Ph.D. thesis, Yale University, New Haven, Conn.Google Scholar
(27)Ripoll, P. (1972). The embryonic organization of the imaginal wing disk of Drosophila melanogaster. Wilhelm Roux Archiv für Entwicklungsmechanik der Organismen 169, 200–215.CrossRefGoogle Scholar
(28)Sonnenblick, B. P. (1950). The early embryology of Drosophila melanogaster. In Biology of Drosophila (ed. Demerec, M.). New York: Wiley.Google Scholar
(29)Steiner, E. (1976). Establishment of compartments in the developing leg imaginal discs of Drosophila melanogaster. Wilhelm Roue's Archives of Developmental Biology 180, 9–30.CrossRefGoogle Scholar
(30)Stern, C. (1940). The prospective significance of imaginal discs in Drosophila. Journal of Morphology 67, 107–122.CrossRefGoogle Scholar
(31)Sturtevant, A. H. (1929). The claret mutant type of Drosophila simulans: A study of chromosome elimination and of cell-lineage. Zeitschrift für Wissenschaftliche Zoologie 135, 323–356.Google Scholar
(32)Turner, F. R. & Mahowaid, A. P. (1976). Scanning electron microscopy of Drosophila embryogenesis. I. The structure of the egg envelopes and the formation of the cellular blastoderm. Developmental Biology 50, 95–108.CrossRefGoogle ScholarPubMed
(33)Wieschaus, E. (1974). Clonal analysis of early development in Drosophila melanogaster. Appendix I. Thesis, Yale University, New Haven, Conn.Google Scholar
(34)Wieschaus, E. & Gehring, W. (1976 a). Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Developmental Biology 50, 249–263.CrossRefGoogle ScholarPubMed
(35)Wieschaus, E. & Gehring, W. (1976 b). Gynandromorph analysis of the thoracic disc primordia in Drosophila melanogaster. Wilhelm Roux's Archives of Developmental Biology 180, 31–46.CrossRefGoogle Scholar
(36)Zalokar, M., Audit, C. & Erk, I. (1975). Developmental defects of female-sterile mutants of Drosophila melanogaster. Developmental Biology 47, 419–432.CrossRefGoogle ScholarPubMed
(37)Zalokar, M. & Erk, I. (1976). Division and migration of nuclei during early embryogenesis of Drosophila melanogaster. Journal de Microscopie et de Biologie Cellulaire 25, 97–107.Google Scholar