Genetic and Developmental Approaches to Understanding Determination in Early Development

  • Kenneth D. Konrad
  • Anthony P. Mahowald

Abstract

In this paper we review experimental evidence relating to the stage of determination of blastoderm cells of the Drosophila melanogaster embryo. Cellular ablation studies and clonal analysis reveal that the ectodermal precursors of both the larva and adult are determined for segmental identity at blastoderm. The adult ectodermal precursors, however, are not determined for specific structures within segments. This situation is not clear with respect to larval epidermal precursors. In contrast, cellular transplantation studies indicate that mesodermal and endodermal precursors of both the larva and adult are undetermined with respect to segmental identity or tissue specificity at blastoderm. We also review the maternal influence on cellular determination as revealed by maternal effect mutations. Many of these mutations exert an effect on the developmental fate of most or all of the blastoderm cells. These global effects may be produced through a disruption of gradients of maternal determinative gene products. Observations from a developmental analysis of a maternal effect mutation disrupting dorsal-ventral polarity reveals that maternal information may also be involved in the cell interactions required for gastrulation. Other maternal effect mutations appear to affect the developmental fate of a more limited portion of the blastoderm surface. Maternal effect mutations of either class can exhibit a strict maternal effect or a varying degree of rescuability by the paternal genome.

Keywords

Fibril Pyrimidine Nash Acetylcholinesterase 

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References

  1. Anderson, D. (1966). The comparative embryology of the Diptera. Ann. Rev. Ent. 11:23–46.CrossRefGoogle Scholar
  2. Anderson, K. and Nusslein-Volhard, C. (1982). Genetic control of dorsal-ventral polarity in the Drosophila embryo. Biology of the Cell 45:400.Google Scholar
  3. Anderson, K.V. and Nusslein-Volhard, C. (1983). Genetic analysis of dorsal-ventral embryonic pattern in Drosophila. In “Primers in Developmental Biology,” G. Malacinski and S. Bryant (eds.). MacMillan Press, in press.Google Scholar
  4. Baker, B. (1973). The maternal and zygotic control of development by cinnamon, a new mutant in Drosophila melanogaster. Develop. Biol. 33:429–440.CrossRefGoogle Scholar
  5. Capdevila, M.P. and Garcia-Bellido, A. (1981). Genes involved in the activation of the bithorax complex of Drosophila. Wilhelm Roux’ Arch. 190:339–350.CrossRefGoogle Scholar
  6. Crick, F.H.C. and Lawrence, P.A. (1975). Compartments and polyclones in insect development. Science 189:340–347.CrossRefGoogle Scholar
  7. Counce, S.J. (1956a). Studies on female-sterility genes in Drosophila melanogaster: I. The effects of the gene deep orange on embryonic development. Z. VererbLehre 87:443–461.CrossRefGoogle Scholar
  8. Counce, S.J. (1956b). Studies on female-sterility genes in Drosophila melanogaster: II. The effects of the gene fused on embryonic development. Z. VererbLehre 87:462–481.CrossRefGoogle Scholar
  9. Davidson, E.H. (1976). Gene Activity in Early Development. Academic Press, New York.Google Scholar
  10. Denell, R.E. and Frederick, R.D. (1983). Homeosis in Drosophila: A description of the Polycomb lethal syndrome. Dev. Biol., in press.Google Scholar
  11. Gans, M., Audit, C., Masson, M. (1975). Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaster. Genetics 81: 683–704.Google Scholar
  12. Garcia-Bellido, A., Lawrence, P.A., and Morata, G. (1973). Developmental compartmentalization of the wing disk of Drosophila. Nature New Biol. 245:251–253.CrossRefGoogle Scholar
  13. Haynie, J.L. and Bryant, P.J. (1977). The effects of X-rays on the proliferation dynamics of cells in the imaginai wing disk of Drosophila melanogaster. Wilhelm Roux’ Arch. 183:85–100.CrossRefGoogle Scholar
  14. Illmensee, K. (1978). Drosophila chimeras and the problem of determination. In “Genetic Mosaics and Cell Differentiation,” W.J. Gehring (ed.), pp. 51–69. Springer-Verlag, New York.Google Scholar
  15. Jimenez, G. and Campos-Ortega, J.A. (1982). Maternal effects of zygotic mutants affecting early neurogenesis in Drosophila. Wilhelm Roux’ Arch. 191191–201.Google Scholar
  16. Kaufman, T.C. and Wakimoto, B.T. (1982). Genes that control high-level developmental switches. In “Evolution and Development,” J.T. Bonner (ed.), pp. 189–205, Dahlem Konferenzen. Springer-Verlag, New York.CrossRefGoogle Scholar
  17. Komorowska, B. (1980). L’effet d’une mutation de sterilite femelle sur la cephalogenese de Drosophila melanogaster pendant la vie embryonnaire. Thesis, University of P. and M. Curie.Google Scholar
  18. Konrad, K.D., Goralski, T.J., Turner, F.R., and Mahowald, A.P. (1982). Maternal effect mutation affecting gastrulation. J. Cell Biol. 95:159a.Google Scholar
  19. Lawrence, P.A. (1981). The cellular basis of segmentation in insects. Cell 26:3–10.CrossRefGoogle Scholar
  20. Lawrence, P.A. (1982). Cell lineage of the thoracic muscles of Drosophila. Cell 29:493–503.CrossRefGoogle Scholar
  21. Lawrence, P.A. and Brower, D.L. (1982). Myoblasts from Drosophila wing disks can contribute to developing muscles throughout the fly. Nature 295:55–57.CrossRefGoogle Scholar
  22. Lawrence, P.A. and Johnston, P. (1982). Cell lineage of the Drosophila abdomen: The epidermis, oonocytes, and ventral muscles. J. Embryol. Exp. Morph. 72:197–208.Google Scholar
  23. Lawrence, P.A. and Morata, G. (1977). The early development of mesothoracic compartments in Drosophila. Dev. Biol. 56:40–51.CrossRefGoogle Scholar
  24. Lehmann, R., Dietrich, U., Jimenez, F., and Campos-Ortega, J.A. (1981). Mutations of early neurogenesis in Drosophila. Wilhelm Roux’ Arch. 190:226–229.CrossRefGoogle Scholar
  25. Lohs-Schardin, M. (1982). Dicephalic—A Drosophila mutant affecting polarity in follicle organization and embryonic patterning. Wilhelm Roux’ Arch. 191:28–36.CrossRefGoogle Scholar
  26. Lohs-Schardin, M., Cremer, C., and Nusslein-Volhard, C. (1979a). A fate map for the larval epidermis of Drosophila melanogaster: Localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Develop. Biol. 73:239–255.CrossRefGoogle Scholar
  27. Lohs-Schardin, M., Sander, K., Cremer, C., Cremer, T., and Zorn, C. (1979b). Localized ultraviolet laser microbeam irradiation of early Drosophila embryos: Fate maps based on location and frequency of adult defects. Develop. Biol. 68:533–545.CrossRefGoogle Scholar
  28. Mahowald, A.P. (1977). The germ plasm of Drosophila: An experimental system for the analysis of determination. Amer. Zool. 17:551–563.Google Scholar
  29. Mahowald, A.P. and Boswell, R.E. (1983). Germ plasm and germ cell development in invertebrates. In “Current Problems in Germ Cell Differentiation,” McLaren and Wylie (eds.). Cambridge Press, in press.Google Scholar
  30. Mohler, J.D. (1977). Developmental genetics of the Drosophila egg: I. Identification of 59 sex-linked cistrons with maternal effects on embryonic development. Genetics 85:259–272.Google Scholar
  31. Norby, S. (1973). The biochemical genetics of rudimentary mutants of Drosophila melanogaster. Hereditas. 73:11–16.CrossRefGoogle Scholar
  32. Nusslein-Volhard, C. (1977). Genetic analysis of pattern formation in the embryo of Drosophila melanogaster. Characterization of the maternal-effect mutant bicaudal. Wilhelm Roux’ Arch. 183:249–268.CrossRefGoogle Scholar
  33. Nusslein-Volhard, C. (1979). Maternal effect mutations that alter the spatial coordinates of the embryo of Drosophila melanogaster. In “Spatial Determinants of Development,” S. Subtelny and I. Konigberg (eds.), pp. 185–211. Academic Press, New York.Google Scholar
  34. Nusslein-Volhard, C., Lohs-Schardin, M., Sander, K., and Cremer, C. (1980). A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature 283:474–476.CrossRefGoogle Scholar
  35. Nusslein-Volhard, C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801.CrossRefGoogle Scholar
  36. Nusslein-Volhard, C., Wieschaus, E., and Jurgens, G. (1982). Segmentation in Drosophila, a genetic analysis (Segmentierung in Drosophila, Eine genetische Analyse). In “Veshandlungen des deutschen Zoologischen Gesellschaft.” Guster Fischer Verlag, in press.Google Scholar
  37. Poulson, D.F. (1940). The effects of certain X-chromosome deficiencies on the development of Drosophila melanogaster. J. Exp. Zool. 83:271–325.CrossRefGoogle Scholar
  38. Poulson, D.F. (1950). Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster Meigen. In “Biology of Drosophila,” M. Demerec (ed.), pp. 168–274. Wiley, New York.Google Scholar
  39. Rice, T.B. (1973). Isolation and characterization of maternal-effect mutants: an approach to the study of early determination in Drosophila melanogaster. Ph.D. Dissertation, Yale University, New Haven, 147 pp.Google Scholar
  40. Rice, T.B. and Garen, A. (1975). Localized defects of blastoderm formation in maternal effect mutants of Drosophila. Develop. Biol. 43:277–286.CrossRefGoogle Scholar
  41. Romans, P., Hodgetts, R.B., and Nash, D. (1976). Maternally influenced embryonic lethality: Allele specific genetic rescue at female fertility locus in Drosophila melanogaster. Can. J. Genet. Cytol. 18:773–781.Google Scholar
  42. Shannon, M.P. (1972). Characterization of the female-sterile mutant almondex of Drosophila melanogaster. Genetica 43:244–256.CrossRefGoogle Scholar
  43. Shannon, M.P. (1973). The development of eggs produced by the female-sterile mutant almondex of Drosophila melanogaster. J. Exp. Zool. 183:383–400.CrossRefGoogle Scholar
  44. Schubiger, G., Moseley, R.C., and Wood, W.J. (1977). Interaction of different egg parts in determination of various body regions in Drosophila melanogaster. PNAS 74:2050–2053.CrossRefGoogle Scholar
  45. Schubiger, G. and Newman Jr., S.M. (1982). Determination in Drosophila embryos. Amer. Zool. 22:47–55.Google Scholar
  46. Simcox, A.A. and Sang, J.H. (1983). When does determination occur in Drosophila embryos? Develop. Biol., in press.Google Scholar
  47. Struhl, G. (1981). A gene product required for correct initiation of segmental determination in Drosophila. Nature 293:36–41.CrossRefGoogle Scholar
  48. Struhl, B. and Brower, D. (1982). Early role of the esc + gene product in the determination of segments in Drosophila. Cell 31: 285–292.CrossRefGoogle Scholar
  49. Turner, F.R. and Mahowald, A.P. (1976). Scanning electron microscopy of Drosophila embryogenesis: I. The structure of the egg envelopes and the formation of the cellular blastoderm. Devel. Biol. 50:95–108.CrossRefGoogle Scholar
  50. Underwood, E.M., Caulton, J.H., Allis, C.D., and Mahowald, A.P. (1980a). Developmental fate of pole cells in Drosophila melanogaster. Devel. Biol. 77:303–314.CrossRefGoogle Scholar
  51. Underwood, E.M., Turner, F.R., and Mahowald, A.P. (1980b). Analysis of cell movements and fate mapping during early embryogenesis in Drosophila melanogaster. Dev. Biol. 74:286–301.CrossRefGoogle Scholar
  52. Wieschaus, E. and Gehring, W. (1976). Clonal analysis of primordial disk cells in the early embryo of Drosophila melanogaster. Devel. Biol. 50:249–263.CrossRefGoogle Scholar
  53. Wieschaus, E. and Szabad, J. (1979). The development and function of the female germ line in Drosophila melanogaster: A cell lineage study. Dev. Biol. 68:29–46.CrossRefGoogle Scholar
  54. Wright, T.R.F. (1970). The genetics of embryogenesis in Drosophila. Adv. in Genetics 15:262–395.Google Scholar
  55. Zalokar, M., Audit, C., and Erk, I. (1975). Developmental defects of female-sterile mutants of Drosophila melanogaster. Devel. Biol. 47:419–432.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Kenneth D. Konrad
    • 1
  • Anthony P. Mahowald
    • 1
  1. 1.Developmental Biology Center, Department of Developmental Genetics and AnatomyCase Western Reserve UniversityClevelandUSA

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