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Models of Biological Pattern Formation and Their Application to the Early Development of Drosophila

  • Hans Meinhardt
Part of the NATO ASI Series book series (NSSB, volume 270)

Abstract

The complexity of a higher organism indicates that very many pattern forming reactions are at work that are coupled to each other in such a way that the final pattern can be generated with a high degree of reproducibility. Investigations of early development in Drosophila have provided us with much information about the molecular machinery on which development is based. About ten years ago, I proposed a model for pattern formation in early insect embryogenesis (Meinhardt, 1977). This model was based on a single morphogen gradient with a high point at the posterior pole of the egg. The gradient was assumed to be generated by short range auto catalysis and long range inhibition (Gierer and Meinhardt, 1972). This model was able to account for most of the experimental observations available at that time. More recently, this model of positional information has been complemented by a model for the hierarchical activation of gap-, pair rule and segment polarity genes (Meinhardt, 1985, 1986). In the meantime many additional genetic and molecular data have become available for Drosophila. Much of this new data supports the basic stipulations of these models, while some of it suggests modifications of these models. In this paper I will mention very briefly the basic ingredients of the models with reference to the Drosophila system and show of how these elements can be linked to obtain a reproducible pattern formation. This paper will be partially based on arguments previously put forward (Meinhardt, 1985,1986) and more recently updated (Meinhardt, 1988).

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References

  1. Baker, N.E. (1987). Molecular cloning of sequences from wingless a segment polarity gene in Drosophila the spatial distribution of a transcript in embryos. Embo J, 6, 1765–1774.PubMedPubMedCentralGoogle Scholar
  2. Baker, N.E. (1988). Localization of transcripts from the wingless gene in whole Drosophila embryos. Development 103, 289–298.PubMedGoogle Scholar
  3. Bohn, H. (1970). Interkalare Regeneration und segmentale Gradienten bei den Extremitäten von Leucophaea-Larven (Blattari). I. Femur und Tibia. Wilhelm Roux’ Archiv 165, 303–341.Google Scholar
  4. Bohn, H. (1974). Extent and properties of the regeneration field in the larval legs of cockroaches (Leucophaea maderae). I. Extirpation experiments. J. Embryol. exp. Morph. Vol.31, 3, 557–572.PubMedGoogle Scholar
  5. Bull, A.L. (1966). Bicaudal, a Genetic Factor which Affects the Polarity of the Embryo in Drosophila melanogaster. J. Exp. Zool. 161, 221–242.CrossRefGoogle Scholar
  6. Carroll, S.B. and Scott, M.P. (1986). Zygotically active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis. Cell, 45, 113–126.CrossRefGoogle Scholar
  7. Driever, W. and Nüsslein-Volhard, C. (1989). The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 337, 138–143.CrossRefGoogle Scholar
  8. Edgar, B.A., Schubiger, G. and Odell, G.M. (1989). A genetic switch, based on negative regulation, sharpens stripes in Drosophila ernbryos. Dev. Genetics 10, 124–142.CrossRefGoogle Scholar
  9. Garcia-Bellido, A., Ripoll, P. and Morata, G. (1973). Developmental compartmentalization of the wing disk of Drosophila. Nature New Biol. 245, 251–253.CrossRefGoogle Scholar
  10. Gaul, U. and Jackie, H. (1987). Pole region-dependent repression of the Drosophila gap gene Krüppel by maternal gene products. Cell 51, 549–555.CrossRefGoogle Scholar
  11. Gierer, A. (1981). Generation of biological patterns and form: Some physical, mathematical, and logical aspects. Prog. Biophys. molec. Biol. 37, 1–47.Google Scholar
  12. Gierer, A. and Meinhardt, H. (1972). A theory of biological pattern formation. Kybernetik 12, 30–39.CrossRefGoogle Scholar
  13. Gierer, A. and Meinhardt, H. (1974). Biological pattern formation involving lateral inhibition. Lectures on Mathematics in the Life Sciences 7, 163–183.Google Scholar
  14. Goodwin, B.C. and Kauffman, S.A. (1990). Spatial harmonics and pattern specification in early Drosophila development. 1. Bifurcation sequences and gene expression. J. theor. Biol. 144, 303–319.CrossRefGoogle Scholar
  15. Goto, T., Macdonald, P. and Maniatis, T. (1989). Early and late periodic patterns of even skipped expression are controlled by distinct regulatory elements that respond to different spatial cues. Cell, 57, 413–422.CrossRefGoogle Scholar
  16. Hafen, E., Kuroiwa, A. and Gehring, W.J. (1984). Spatial distribution of transcripts from the segmentation gene fushi tarazu during Drosophila embryonic development. Cell, 37, 833–842.CrossRefGoogle Scholar
  17. Harding, K., Hoey, T., Warrior, R. and Levine, M. (1989). Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila. Embo J, 8, 1205–1212.PubMedPubMedCentralGoogle Scholar
  18. Harding, K., Rushlow, C., Doyle, H.J., Hoey, T. and Levine, M. (1986). Cross-regulatory interactions among pair-rule genes in Drosophila. Science 233, 953–959.CrossRefGoogle Scholar
  19. Hiromi, Y. and Gehring, W.J. (1987). Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50, 963–974.CrossRefGoogle Scholar
  20. Hooper, J.E. and Scott, M.P. (1989). The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 59, 751–765.CrossRefGoogle Scholar
  21. Howard, K. and Ingham, P. (1986). Regulatory Interactions between the Segmentation Genes fushi tarazu, hairy, and engrailed in the Drosophila Blastoderm. Cell 44, 949–957.CrossRefGoogle Scholar
  22. Howard, K., Ingham, P. and Rushlow, C. (1988). Region-specific alleles of the Drosophila segmentation gene hairy. Genes & Development 2, 1037–1046.CrossRefGoogle Scholar
  23. Howard, K., Ingham, P. and Rushlow, C. (1988). Region-specific alleles of the Drosophila segmentation gene hairy. Genes Dev, 2, 1037–1046.CrossRefGoogle Scholar
  24. Ingham, P. (1988). The molecular genetics of embryonic pattern formation in Drosophila. Nature 335, 25–34.CrossRefGoogle Scholar
  25. Kalthoff, K. and Sander, K. (1968). Der Entwicklungsgang der Missbildung “Doppelabdomen” im partiell UV-bestrahlten Ei von Smittia parthenogenetica. Wilhelm Roux’ Archiv 161, 129–146.Google Scholar
  26. Knipple, D.C., Scifert, E., Rosenberg, U.B., Preiss, A. and Jackie, H. (1985). Spatial and temporal pattern of Krüppel gene expression in early Drosophila development. Nature 317, 40 – 44.CrossRefGoogle Scholar
  27. Kornberg, T.I., Siden, I., O’Farell, P. and Simon, M. (1985). The engrailed locus of Drosophila: In-situ hybridisation of transcripts reveals compartment-specific expression. Cell 40, 45–53.CrossRefGoogle Scholar
  28. Lacalli, T.C. (1990). Modeling the Drosophila pair-rule pattern by reaction diffusion — gap input and pattern control in a 4- morphogen system. J Theor Bioll 44, 171–194.CrossRefGoogle Scholar
  29. Lacalli, T.C., Wilkinson, D.A. and Harrison, L.G. (1988). Theoretical aspects of stripe formation in relation to Drosophila segmentation. Development 104, 105–113.PubMedGoogle Scholar
  30. Lohs-Schardin, M., Cremer, C. and Nüsslein-Volhard, C. (1979). A fate map for the larval epidermis of Drosophila melanogaster: Localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Dev. Biol. 73, 239 – 255.CrossRefGoogle Scholar
  31. Martinez-Arias, A., Baker, N.E. and Ingham, P.W. (1988). Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103, 151–170.Google Scholar
  32. Martinez-Arias, A. and Lawrence, P.A. (1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639–642.CrossRefGoogle Scholar
  33. Meinhardt, H. (1976). Morphogenesis of lines and nets. Differentiation 6, 117–123.CrossRefGoogle Scholar
  34. Meinhardt, H. (1977). A model of pattern formation in insect embryogenesis. J. Cell Sci. 23, 117–139.Google Scholar
  35. Meinhardt, H. (1978). Space-dependent Cell Determination under the control of a morphogen gradient. J. theor. Biol.74, 307–321.CrossRefGoogle Scholar
  36. Meinhardt, H. (1980). Cooperation of Compartments for the Generation of Positional Information. Z. Naturiorsch. 35c, 1086–1091.Google Scholar
  37. Meinhardt, H. (1982). Models of biological pattern formation. Academic Press, London.Google Scholar
  38. Meinhardt, H. (1982). The Role of Compartmentalization in the activation of particular control genes and in the generation of proximo- distal positional information in appendages. Amer.Zool. 22, 209–220.CrossRefGoogle Scholar
  39. Meinhardt, H. (1983a). A boundary model for pattern formation in vertebrate limbs. J. Embryol exp. Morph. 76, 115–137.PubMedGoogle Scholar
  40. Meinhardt, H. (1983b). Cell determination boundaries as organizing regions for secondary embryonic fields. Devi. Biol 96, 375–385.CrossRefGoogle Scholar
  41. Meinhardt, H. (1984). Models for positional signalling, the threefold subdivision of segments and the pigmentation pattern of molluscs. J. Embryol. exp. Morph. 83,(Supplement) 289–311.PubMedGoogle Scholar
  42. Meinhardt, H. (1985). Mechanisms of Pattern Formation During Development of Higher Organisms: A Hierarchial Solution of a Complex Problem. Ber. Bunsenges. Phys. Chem. 89, 691–699.CrossRefGoogle Scholar
  43. Meinhardt, H. (1986). Hierarchical inductions of cell states: a model for segmentation in Drosophila. J. Cell Sci. Suppl.4, 357–381.CrossRefGoogle Scholar
  44. Meinhardt, H. (1986). The threefold subdivision of segments and the initiation of legs and wings in insects. Trends Genetics 2, 36–41.CrossRefGoogle Scholar
  45. Meinhardt, H. (1988). Models for maternally supplied positional information and the activation of segmentation genes in Drosophila embryogenesis. In: Development 104, (Supplement), 95–110.Google Scholar
  46. Meinhardt, H. and Gierer, A. (1980). Generation and regeneration of sequences of structures during morphogenesis. J. theor. Biol. 85, 429–450.CrossRefGoogle Scholar
  47. Nagorcka, B.N. (1989). Wavelike isomorphic prepatterns in development. J. Theoretical Biol. 137, 127–162.CrossRefGoogle Scholar
  48. Nakano, Y., Guerrero, L, Hidalgo, A., Taylor, A., Whittle, J.R.S. and Ingham, P.W. (1989). A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature 341, 508–513.CrossRefGoogle Scholar
  49. Nüsslein-Volhard, C. (1977). Genetic analysis of pattern formation in the embryo of Drosophila melanogaster. Wilhelm Roux’s Archives 183, 249–268.CrossRefGoogle Scholar
  50. Nüsslein-Volhard, C., Frohnhöfer, H.G. and Lehmann, R. (1987). Determination of anteroposterior polarity in Drosophila. Science 238, 1675–1681.CrossRefGoogle Scholar
  51. Nüsslein-Volhard, C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801.CrossRefGoogle Scholar
  52. Nüsslein-Volhard, C., Wieschaus, E. and Kluding, H. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux’s Arch. Dev. Biol. 183, 267–282.CrossRefGoogle Scholar
  53. Pankratz, E., Scifert, E., Gerwin, N., Billi, B., Nauber, N. and Jackie, H. (1990). Gradients of Krüppel and knirps gene products direkt pair rule gene stripe patterning in the posterior regions of the Drosophila embryo. Cell, 61, 309–316.CrossRefGoogle Scholar
  54. Pankratz, M.J., Jackie, H., Scifert, E. and Hoch, M. (1989). Krüppel requirement for knirps enhancement reflects overlapping gap gene activities in the Drosophila embryo. Nature 341, 337–340.CrossRefGoogle Scholar
  55. Rijsewijk, F., Schuermann, M., Wagenaar, E., Parren, P., Weigel, D. and Nüsse, R. (1987). The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657.CrossRefGoogle Scholar
  56. Sander, K. (1959). Analyse des ooplasmatischen Reaktionssystems von Euscelis plebejus Fall. (Cicadina) durch Isolieren und Kombinieren von Keimteilen. I. Mitt.: Die Differenzierungsleistungen vorderer und hinterer Eiteile. Wilhelm Roux’ Archiv 151, 430–497.CrossRefGoogle Scholar
  57. Sander, K. (1960). Analyse des ooplasmatischen Reaktionssystems von Euscelis Plebejus Fall (Cicadina) durch Isolieren und Kombinieren von Keimteilen. IL Mitteilung: Die Differenzierungsleistungen nach Verlagern von Hinterpolmaterial. Wilhelm Roux’ Archiv 151, 660–707.CrossRefGoogle Scholar
  58. Sander, K. (1976). Specification of the basic body pattern in insect embryogenesis. Adv. Ins. Physiol.12, 125–238.CrossRefGoogle Scholar
  59. Sullivan, W. (1987). Independence of fushi tarazu expression with respect to cellular density in Drosophila embryos. Nature 327, 164–167.CrossRefGoogle Scholar
  60. Tautz, D., Lehmann, R., Schnuerch, H., Schuh, R., Scifert, E., Kienlin, A., Jones, K. and Jackie, H. (1987). Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes. Nature 327, 383–389.CrossRefGoogle Scholar
  61. Tautz, D., Tautz, C., Webb, D. and Dover, G.A. (1987). Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. Implications for molecular coevolution in multigene families. J. Mol. Biol. 195, 525–542.CrossRefGoogle Scholar
  62. Treisman, J. and Desplan, C. (1989). The products of the Drosophila gap genes hunchback and Krüppel bind to the hunchback promoters. Nature 341, 335–337.CrossRefGoogle Scholar
  63. Turing, A. (1952). The chemical basis of morphogenesis. Phil. Trans. B. 237, 37–72.CrossRefGoogle Scholar
  64. Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. theoret. Biol. 25, 1–47.CrossRefGoogle Scholar
  65. Yajima, H. (1960). Studies on embryonic determination of the harlequin-fly, Chironomous dorsalis. J. Embryol. exp. Morph. 8, 198–215.PubMedGoogle Scholar
  66. van der Meer, J.M. and Miyamoto, D.M. (1984). The specification of metameric order in the insect Callosobruchus maculatus Fabr. (Coleoptera). II. The effects of temporary constriction on segment number. Roux’s Arch Dev Biol 193, 326–338.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Hans Meinhardt
    • 1
  1. 1.Max-Planck-Institut für EntwicklungsbiologieTübingenGermany

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