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From DNA transcription to visible structure: What the development of multicellular animals teaches us

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This article is concerned with the problem of the relation between the genetic information contained in the DNA and the emergence of visible structure in multicellular animals. The answer is sought in a reappraisal of the data of experimental embryology, considering molecular, cellular and organismal aspects. The presence of specific molecules only confers a tissue identity on the cells when their concentration exceeds the ‘threshold of differentiation’. When this condition is not fulfilled the activity of the genes that code for the specific molecules in question only confers on them a histogenetic potency, i.e. the capacity to form the corresponding tissue in further development (or to transdifferentiate to that tissue). The progressive restriction of histogenetic potencies during development reflects the irreversible repression of more and more genes. The establishment of a given tissue identity under the influence of an inducing tissue (or a morphogenetic hormone) is only possible when the cells have acquired the competence to respond. Tissue differentiation proceeds progressively during development thanks to the cytoplasmic ‘memory’ that cells retain collectively (or sometimes individually) of the items of information successively registered by their ancestors cells. The increasing complexity of visible structure emerging during development results only from the progression of tissue differentiation. This involves continual exchange of information among the cells and leads to (1) cell displacements and rearrangements, particularly during organogenesis and (2) extreme diversification of cell individualities within tissues, particularly during postembryonic growth. A mutation (just as a teratogenic factor) evokes an anomaly that is localized in both space and time because it alters a certain aspect of cell behaviour (particularly cell surface adhesiveness or mitotic activity) at the time when this is involved in the establishment of a particular structural trait. Neither the organization of the adult nor the modalities of development are encoded in the DNA. The automatic concatenation of cell interactions in the embryo and the structural amplification it entails is conditioned by the specific biochemical composition of the cytoplasm of the egg and by the heterogeneous distribution of its inclusions.

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References

  1. Akers, R.M., Philips, C.R. and Wessels, N.K. (1986). Expression of an epidermal antigen used to study tissue induction in the early Xenopus laevis embryo. - Science 231: 613–616.

    Google Scholar 

  2. Ashby, W.R. (1958). Requisite variety and its implication for the controls of complex systems. - Cybernetica 1: 83–89.

    Google Scholar 

  3. Beljanski, M. (1983). The Regulation of DNA Replication and Transcriptions. - Monogr. Exp. Biol. Med. 8: 189 p., Bâle, Karger.

    Google Scholar 

  4. Boussios, T., Condon, M.R. and Bertles, J.F. (1985). Ontogeny of hamster hemoglobins in yolk-sac erythroid cells in vivo and in culture. - Proc. Nat. Acad. Sci. U.S.A. 28: 2794–2798.

    Google Scholar 

  5. Byrne, J., Warburton, D., Kline, J., Blanc, W. and Stein, Z. (1985). Morphology of early fetal deaths and their chromosomal characteristics. - Teratology 32: 297–315.

    Google Scholar 

  6. Caplan, A.I. and Ordahl, C.P. (1978). Irreversible gene repression model for control of development. - Science 201: 120–130.

    Google Scholar 

  7. Chandebois, R. (1976). Cell sociology: a way of reconsidering the current concepts of morphogenesis. - Acta biotheor. 25: 71–102.

    Google Scholar 

  8. Chandebois, R. (1977). Cell sociology and the problem of position effect: pattern formation, origin and role of gradients. - Acta biotheor. 26: 203–238.

    Google Scholar 

  9. Chandebois, R. (1980). Cell sociology and the problem of automation in the development of pluricellular animals. - Acta biotheor. 29: 1–35.

    Google Scholar 

  10. Chandebois, R. (1981). The problem of automation in animal development: confrontation of the concept of cell sociology with biochemical data. - Acta biotheor. 30: 143–169.

    Google Scholar 

  11. Chandebois, R. and Faber, J. (1983). Automation in Animal Development. A new Theory derived from the Concept of Cell Sociology. - Monogr. Dev. Biol. 16: Bâle, Karger.

    Google Scholar 

  12. Chandebois, R. and Brunet, C. (in press). The origin of abnormality in a human simelian foetus as elucidated by our knowledge of vertebrate development. - Teratology.

  13. Clark, W.R. and Rutter, W.J. (1967). Levels of regulation during the ontogeny of insulin in the rat embryo. - Fed. Proc. 26: p. 603.

    Google Scholar 

  14. Clayton, R.M. (1979). Regulatory factors for lens fibre formation in cell culture. I. Possible requirement for pre-existing levels of crystallin mRNA. Ophthalmic Res. 11: 324–328.

    Google Scholar 

  15. Clayton, R.M. (1982). Cellular and molecular aspects of differentiation and transdifferentiation of ocular tissues in vitro.- In M.M. Yeoman and D.E.S. Truman, eds., Differentiation in Vitro, 83–120.- Cambridge: Cambridge University Press.

    Google Scholar 

  16. Clayton, R.M. (1982). The molecular basis for competence, determination and transdifferentiation: a hypothesis. In R.M. Clayton, ed., Stability and Switching in Cellular Differentiation, 23–38.- New York: Plenum.

    Google Scholar 

  17. Clayton, R.M., Thomson, I. and de Pomerai, D.I. (1979). Relationship between crystallin mRNA expression in retina cells and their capacity to re-differentiate into lens cells.- Nature 282: 628–629.

    Google Scholar 

  18. Cohen, J. (1979). Maternal constraints on development. In D.R. Newth and M. Balls, eds., Maternal Effects in Development, 1–28.- Cambridge: Cambridge University Press.

    Google Scholar 

  19. Cuny, R. and Malacinski, G.M. (1986). Axolotl retina and lens development: mutual tissue stimulation and autonomous failure in the eyeless mutant retina.- J. Embryol. Exp. Morphol. 96: 151–170.

    Google Scholar 

  20. De Pomerai, D.I., Pritchard, D.J. and Clayton, R.M. (1977). Biochemical and immunological studies of lentoid formation in cultures of embryonic chick neural retina and day old chick lens epithelium.- Dev. Biol. 60: 416–427.

    Google Scholar 

  21. Ede, D.A. (1972). Cell behaviour and embryonic development.- Inter. J. Neuroscience 3: 165–174.

    Google Scholar 

  22. Ellison, M.L., Ambrose, E.J. and Easty, G.C. (1969). Chondrogenesis in chick embryo somites to in vitro.- J. Embryol. Exp. Morphol. 21: 331–340.

    Google Scholar 

  23. Elsdale, T. and Pearson, M. (1979). Somitogenesis in amphibia. II. Origins in early embryogenesis of two factors involved in somite specification.- J. Embryol. Exp. Morphol. 53: 245–267.

    Google Scholar 

  24. Flickinger, R.A. (1962). Sequential gene action, protein synthesis and cellular differentiation.- Int. Rev. Cytol. 13: 75–98.

    Google Scholar 

  25. Flickinger, R.A. (1976). The effect of growth rate on differentiation of chick embryo limb bud mesenchyme in organ culture.- Exp. Cell Res. 99: 449–453.

    Google Scholar 

  26. Frenster, J.H. and Herstein, P.R. (1973). RNA in gene expression. In M.C. Niu and S.J. Segal, eds., The Role of DNA in Reproduction and Development, 330–338.- Amsterdam: North-Holland.

    Google Scholar 

  27. Fujimoto, H. and Yanagisawa, K.O. (1983). Defects in the archenteron of mouse embryos homozygous for the 7-mutation.- Differentiation 25: 44–47.

    Google Scholar 

  28. Goodwin, B.C. (1985). What are the causes of morphogenesis? BioEssays 3: 32–36.

    Google Scholar 

  29. Grunz, H. (1977). Differentiation of the four animal and the four vegetal blastomeres of the eight-cell-stage of Triturus alpestris.- Roux's Arch. Dev. Biol. 181: 267–277.

    Google Scholar 

  30. Grunz, H. (1985). Change in the differentiation pattern of Xenopus laevis ectoderm by the variation of the incubation time and concentration of the vegetalizing factor.- Roux's Arch. Dev. Biol. 192: 130–137.

    Google Scholar 

  31. Gurdon, J.B. (1973). Gene expression during cell differentiation. In J.J. Heard and O.E. Lowenstein, eds., Oxford Biology Readers, 2–16.- Oxford: Oxford University Press.

    Google Scholar 

  32. Gurdon, J.B. (1987). Embryonic induction -molecular prospects.- Development 99: 285–306.

    Google Scholar 

  33. Hadorn, E. (1966). Konstanz, Wechsel und Typus der Determination und Differenzierung in Zellen aus männlichen Genitalanlagen von Drosophila melanogaster nach Dauer-kultur in vivo.- Dev. Biol. 13: 424–509.

    Google Scholar 

  34. Harris, A.K., Stopak, D. and Warner, P. (1984). Generation of spatially periodic patterns by a mechanical alternative to the Turing model.- J. Embryol. Exp. Morphol. 80: 1–20.

    Google Scholar 

  35. Hillman, H. (1976). Towards a classification of evidence in biological and medical research in respect of its validity.- Acta biotheor. 25: 153–162.

    Google Scholar 

  36. Hillman, N., Sherman, M.I. and Graham, C. (1972). The effect of spatial arrangement on cell determination during mouse development.- J. Embryol. Exp. Morphol. 28: 263–278.

    Google Scholar 

  37. Ho, M.W. & Saunders, P.T. (dy1982). The epigenetic approach to the evolution of organisms — with notes on its relevance to social and cultural evolution.- In H.C. Plotkin, ed., Learning, Development and Culture, 343-361. John Wiley and Sons.

  38. Horder, T.J. (1983). Embryological bases of evolution. In B.C. Goodwin, N. Holder and C.G. Wylie, eds., Development and Evolution, 316–352.- Cambridge, Cambridge University Press.

    Google Scholar 

  39. Hsiao, T.H. and Hsiao, C. (1979). Ecdysteroids in the ovary and the egg of the greater wax moth.- J. Insect Physiol. 25: 45–52.

    Google Scholar 

  40. Jackson, I.J., Schofield, P. and Hogan, B. (1985). A mouse homoeo box gene is expressed during embryogenesis and in adult kidney.- Nature 317: 745–748.

    Google Scholar 

  41. Jacob, F. and Monod, J. (1961). On the regulation of gene activity. Cold Spring Harbor Symp. Quant. Biol. 26: 193–211.

    Google Scholar 

  42. Jacobs-Cohen, R.J., Spiegelman, M. and Bennett, D. (1983). Abnormalities of cells and extracellular matrix of 7/7 embryos.- Differentiation 25: 48–55.

    Google Scholar 

  43. Jacobson, A.G. (1966). Inductive processes in embryonic development.- Science 152: 25–34.

    Google Scholar 

  44. Koshland, D.E. Jr. and Kirtley, M.E. (1967). Protein structure in relation to cell dynamics and differentiation. In M. Locke, ed., Major Problems in Developmental Biology, 217–249.- New York: Academic Press.

    Google Scholar 

  45. Lash, J.W. (1963). Tissue interaction and specific metabolic responses: Chondrogenic induction and differentiation. In M. Locke, ed., Cytodifferentiation and Macromolecular Syntheses, 235–260.- New York: Academic Press.

    Google Scholar 

  46. Lash, J.W. (1967). Differential behaviour of anterior and posterior embryonic chick somites in vitro.- J. Exp. Zool. 165: 47–55.

    Google Scholar 

  47. Lee, L.W. and Gerhart, J.C. (1973). Dependence of transdetermination frequency on the developmental stage of cultured imaginal discs of Drosophila melanogaster.- Dev. Biol. 35: 62–82.

    Google Scholar 

  48. Lewin, R. (1984). Why is development so illogical? Science 224: 1327–1329.

    Google Scholar 

  49. Lopashov, G.V. (1977). Levels in stabilisation of cell differentiation and its experimental transformation. Differentiation 9: 131–137.

    Google Scholar 

  50. Lopashov, G.V. and Stroeva, O.G. (1961). Morphogenesis of the vertebrate eye.- Adv. Morphog. 1: 331–337.

    Google Scholar 

  51. Løvtrup, S. (1981). The epigenetic utilization of the genomic message. In G.G.E. Scudder and J.L. Reveal, eds., Evolution Today, Proceedings of the 2nd International Congress of Systematic and Evolutionary Biology, 145–161.

  52. McGinnis, W., Garber, R.L., Wirz, J., Kuroiwa, A. and Gehring, W.J. (1984). A homologous protein-coding sequence in Drosophila homoeotic genes and its conservation in other metazoans.- Cell 37: 403–408.

    Google Scholar 

  53. Mifune (1957). cit. by Dalcq, A.M. (1960). Germinal organisation and induction phenomena. In W.W. Novinski, ed., Fundamental Aspects of Normal and Malignant Growth, 305–494.- Amsterdam, Elsevier.

    Google Scholar 

  54. Minelli, A. (1971). Memory, morphogenesis and behaviour.- Scientia. September–October issue: 1–9.

  55. Müller, G. (1985). Experimental reestablishment of ancestral patterns in the chick limb. In J. Mlíkovsky, and V.J.A. Novák, eds., Evolution and Morphogenesis, 439–446.- Praha, Academia.

    Google Scholar 

  56. Nieuwkoop, P.D. (1963). Pattern formation in artificially activated ectoderm (Rana pipiens and Ambystoma punctatum). Dev. Biol. 7: 255–279.

    Google Scholar 

  57. Nieuwkoop, P.D. (1969). The formation of the mesoderm in urodelean amphibians. I. Induction by the endoderm.- Arch. Entwicklungsmech. Org. (Wilhelm Roux) 162: 341–373.

    Google Scholar 

  58. Nieuwkoop, P.D. (1973). The ‘organisation center’ of the amphibian embryo: its origin, spatial organization and morphogenetic action.- Adv. Morphog. 10: 1–39.

    Google Scholar 

  59. Nieuwkoop, P.D., Johnen, A.G. and Albers, B. (1985). The Epigenetic Nature of Early Chordate Development. Inductive interaction and competence.- Developmental and Cell Biology Monographs, vol. 16.- Cambridge: Cambridge University Press, 373 p.

    Google Scholar 

  60. Owens, E.M. and Solursh, M. (1983). Accelerated maturation of limb bud mesenchyme by the Brachypod H mouse mutation.- Differentiation 24: 145–148.

    Google Scholar 

  61. Perlman, S.M., Ford, P.J. and Rosbach, M.M. (1977). Presence of tadpole and adult globin RNA sequences in oocytes of Xenopus laevis.- Proc. Nat. Acad. Sci. U.S.A. 74: 3835–3839.

    Google Scholar 

  62. Ranzi, S. (1980). On RNA action in differentiation: Induction and differentiation of somites in chick embryo. In R.G. McKinnell, M.A. Di Berardino, M. Blumenfeld and R.D. Bergad, eds., Differentiation and neoplasia. Results and Problems in Cell Differentiation, vol. 11, 191–195.- Berlin: Springer Verlag.

    Google Scholar 

  63. Sang, J.H. (1984). Genetics and Development.- London: Longman Group Ltd.

    Google Scholar 

  64. Saunders, J.W. Jr. and Fallon, J.F. (1967). Cell death in morphogenesis. In M. Locke, ed., Major Problems in Developmental Biology. 25th Growth Symp., 289–314.- New York: Academic Press.

    Google Scholar 

  65. Saxén, L., Koskimies, O., Lahtii, A., Miettinen, H., Rapola, J. and Wartiovaara, J. (1968). Differentiation of kidney mesenchyme in an experimental model system.- Adv. Morphog. 7: 251–293.

    Google Scholar 

  66. Scherrer, K. (1980). Cascade regulation. A model of integrative control of gene expression in eukaryotic cells and organisms. In G.M. Kolodny, ed., Eukaryotic Gene Regulation, 58–129. CRC, Inc.

  67. Scott, M.P. (1985). Molecules and puzzles from the antennapedia homoeotic gene complex of Drosophila.- Trends in Genetics 1: 74–79.

    Google Scholar 

  68. Sengel, P. (1971). The organogenesis and arrangement of cutaneous appendages in birds.- Adv. Morphog. 9: 181–230.

    Google Scholar 

  69. Slîpka, J. and Novák, V.J.A. (1985). Evolution and interrelations of the endocrine system in both invertebrates and vertebrates. In J. Mlîkovský and V.J.A. Novák, eds., Evolution and Morphogenesis, 493–505.- Praha: Academia.

    Google Scholar 

  70. Stephens, T.D., Vasan, N.S. and Lash, J.W. (1980). Extracellular matrix synthesis in the chick embryo lateral plate prior to and during limb outgrowth.- J. Embryol. Exp. Morphol. 59: 71–87.

    Google Scholar 

  71. Tamarin, A., Crawley, A., Lee, J. and Tickle, C. (1984). Analysis of upper beak defects in chicken embryos following treatment with retinoic acid.- J. Embryol. Exp. Morph. 84: 105–123.

    Google Scholar 

  72. Townes, P.L. and Holtfreter, J. (1955). Directed movements and selective adhesion of embryonic amphibian cells.- J. Exp. Zool. 128: 53–120.

    Google Scholar 

  73. Tuckett, F. and Morriss-Kay, G.M. (1985). The kinetic behaviour of the cranial neural epithelium during neurulation in the rat.- J. Embryol. Exp. Morph. 85: 111–119.

    Google Scholar 

  74. Waddington, C.H. (1956). Principles of Embryology. London: Allen & Unwin.

    Google Scholar 

  75. Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation.- J. Theor. Biol. 25: 1–47.

    Google Scholar 

  76. Yamada, T. (1967). Cellular synthetic activities in induction of tissue transformation. In A.V.S. de Reuck and J. Krugel, eds., Cell Differentiation, CIBA Fdn. Symp., 116–130.- Boston: Little Brown and Company.

    Google Scholar 

  77. Zemek, K., Mlíkovský, J. and Socha, R. (1985). Multilevel system of heredity and its ontogenetic and phylogenetic consequences. In J. Mlíkovský and V.J.A. Novák, eds., Evolution and Morphogenesis, 75–87.- Praha: Academia.

    Google Scholar 

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  1. Laboratoire de Morphogénétique animale, Université d'Aix-Marseille 1, Centre de Saint Charles, Place Victor Hugo, F-13331, Marseille Cedex 3, France

    Rosine Chandebois

  2. Hubrecht Laboratory, Netherlands Institute for Developmental Biology, Uppsalalaan 8, 3584, CT Utrecht, Netherlands

    Jacob Faber

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Chandebois, R., Faber, J. From DNA transcription to visible structure: What the development of multicellular animals teaches us. Acta Biotheor 36, 61–119 (1987). https://doi.org/10.1007/BF00049353

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