Pattern Forming Reactions and the Generation of Primary Embryonic Axes

  • Hans Meinhardt
Chapter

Abstract

In his pioneering paper Turing [37] discovered a mechanism that allows the generation of patterns even when starting from more or less homogeneous itial situations. To account for essential steps in the early patterning of higher organisms, several extensions have to be made to overcome problems inherent in simple Turing reaction-diffusion type mechanisms:
  1. 1.

    The wavelength problem: Patterns generated by the Turing reaction diffusion mechanism have a characteristic wavelength. Upon growth a transition from a polar pattern into a symmetric and ultimately into a periodic pattern is expected. However, in many developing systems substantial growth is possible without losing the polar character. It is proposed that the maintenance of a polar pattern is accomplished by a feedback of the pattern on the ability of the cells to perform the patterning reaction, i.e., on their competence. Cells distant to a once formed organizing region lose the competence to form additional maxima, making the first formed maximum dominate.

     
  2. 2.

    The midline problem: The formation of a coordinate system for a bilaterally symmetric organism requires the formation of a midline, i.e., a reference line and not a reference point for the mediolateral patterning. The formation of a single straight line requires the cooperation of a spot like and a stripe-like system. In vertebrates the midline is formed by a local elongation under the influence of the organizer. ‘In contrast, in insects an inhibitory influence from a local dorsal organizer allows midline formation only ventrally.

     
  3. 3

    The left-right pattern: It is proposed that the midline signal induces the ‘left’ signal but higher levels of the midline signal repress the ‘left’ signal. Therefore, the ‘left’-signal has to escape from the midline to a lateral position. This mechanism needs only a minute asymmetry for a reproducible shift to the left. it accou if the systematic asymmetry L. lost.

     

Keywords

Polar Pattern Oral Opening Single Straight Line Spot System Germ Ring 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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References

  1. 1.
    Adachi, H., Saijoh, Y., Mochida, K. Ohishi, S., Hashiguchi, H., Hirao, A., and Hamada, H. (1999).; Determination of left right, asymmetric expression of nodal by a left side-specific enhancer with sequence similarity to a lefty-2 enhancer. Genes Des. 13: 1589–1600.Google Scholar
  2. 2.
    Bard, J.B. and Lauder, 1. (1974). How’ well does Turing’s theory of morphogenesis’ work ? J. theor. Biol. 45: 501–531.CrossRefGoogle Scholar
  3. 3.
    Bisgrove; B.W:, Essner, J.J. and Yost, H.J. (1999): Regulation of midline development by antagonism of lefty-and nodal. Development 126:3253–3262.Google Scholar
  4. 4.
    Capdevila, J:,, Vogan, K.J., Tabin, C.J. and Izpisua Belmonte, J.C. (2000). Mechanisms of left-right determination in vertebrates. Cell 101: 9–21.Google Scholar
  5. 5.
    Chen, G., Handel, K. and ‘Roth, S. (2000): The maternal of-kappa b/dorsal gradient of tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. Development 127: 5145–5156.Google Scholar
  6. 6.
    Cheng, A’.M.S., Thisse,’B.,’ Thisse,’ C. and Wright, ‘C.V.E. (2000).’ The lefty-related factor xatv acts as a feedback inhibitor of nodal signaling in mesoderm induction and 1-r axis development in Xenopus. Development 127: 1049–1061.Google Scholar
  7. 7.
    Gierer, A., Berking, S, Bode, H., David, C.N.; Flick, K., Hansmann G., Schaller, H. and Trenkner, E. (1972). Regeneration of hydra from reaggregated cells. Nature New Biology 239: 98–101.Google Scholar
  8. 8.
    Gierer, A. and Meinhardt, H. (1972), A theory of biological pattern formation: Kybernetik 12:30–39. (available at http://www.eb.tuebingen.mpg.de/abt.4/meinhardt/theory.html) Google Scholar
  9. 9.
    Geees, A., Gee, L., Fisher, D.A. and Bode, H.R. (1996)., Conk-2, an nk-2 homeobox gene, has a role in patterning the basal end of the axis in hydra. Devi Biol. 180: 473–488.Google Scholar
  10. 10.
    Harland, R. and Gerhart, J. (1997). Formation and function of Spemanns orgy izer. Ann, Rev. Cell Der. Biol. 13: 611–667CrossRefGoogle Scholar
  11. 11.
    Hobmayer, B., Rentzsch, F., Kuhn, K., Happel, C,M., Cramer von Lâue,C., Snyder,P., Rothbacher,L. and Holstein,T,W. (2000). Wnt signalling molecules act in axis formation in the diploblastic metazoan hydra. Nature 407:186.189:Google Scholar
  12. 12.
    Hodges, A. (1983). Alan Turing: the enigma. Simon and Schuster, New YorkMATHGoogle Scholar
  13. 13.
    Keller, R., Danilchik,` M. (1988). Regional expression pattern and timing of convergence and extension during gastrulation of Xenopus laevis Development 103: 193–209Google Scholar
  14. Lacalli, T.C. and Harrison, L. G.’ (1978). The regulatory capacity of Turing’s model for morphogenesis, with application to slime moulds. J. theor. Biol. 70: 273–295.CrossRefGoogle Scholar
  15. 15.
    Levin, M. and.Mercola, M. (1998). Evolutionary conservation of mechanisms upstream of asymmetric Nodal expression: reconciling chick and Xenopus. Dev. Genetics 23: 185–193.Google Scholar
  16. 16.
    Levin. M. and Mercola, M. (1999). Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry,: in the node. Development 126:4703–4714:Google Scholar
  17. 17.
    Lohr. J.L. Danos, M.C., Groth, T. V. and Yost, H.J. (1998). Maintenance of asymmetric nodal expression in Xenopus laevis. Dev. Genetics 23: 194.Google Scholar
  18. 18.
    Meinhardt, H. (1982). Models of Biological Pattern Formation. Academic press, London (available at http://www.eb.tuebingen.mpg.de/abt.4/meinhardt/theory.html)Google Scholar
  19. 19.
    Meinhardt, H. (1989). Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. Development (Supplement):169–180_Google Scholar
  20. 20.
    Meinhardt, H. (1993). A model for pattern-formation of hypostome, tentacles; and foot in hydra: how to form structures close to each other, how to form them at a distance. Dev. Biol. 157: 321–333.Google Scholar
  21. 21.
    Meinhardt, H. (1994): Biological pattern-formation–new observations provide support for theoretical predictions.’BioEssays 16: 627–632.Google Scholar
  22. 22.
    Meinhardt, H. (2001). Organizer and axes formation as a self-organizing process. hit. J. Dev. Biol. 45:177–188.’Google Scholar
  23. 23.
    Meinhardt, H. (2002). The radial-symmetric hydra and the evolution of the bilateral body plan: an old body became a young brain. BaoEssays 24:185–191:Google Scholar
  24. 24.
    Meinhardt, H. (2003). The Algorithmic’ Beauty of Sea Shells (3rd enlarged edition) Springer, Heidelberg, New YorkGoogle Scholar
  25. 25.
    Meinhardt, H. and Gierer, A. (1980). Generation and regeneration of sequences, of structures during morphogenesis. J. theor..Biol. 85:429–450:Google Scholar
  26. 26.
    Meinhardt, H. and Gierer; A. (2000): Pattern formation by local self-activation and lateral inhibition. Bioessays 22: 753–760.Google Scholar
  27. 27.
    Müller, W. (1990). Ectopic head and foot formation in Hydra: Diacylglycerol-induced increase in positional values and assistance of the head in foot forma-tion. Differentiation 42: 131–143.Google Scholar
  28. 28.
    Nonaka, S., Shiratori, H., Saijoh, Y. and Hamada, H. (2002). Determiantion of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418: 96–99.CrossRefGoogle Scholar
  29. 29.
    Pera, E.M. and Kessel, M. (1998). Demarcation of ventral territories by the homeobox_ gene nkx2.’1 during early chick development. Dev. Genes Evol. 208: 168171.Google Scholar
  30. 30.
    Psychovos, D. and Stern, C.D. (1996): Restoration of the organizer after radical ablation of Hensen’s node and the anterior primitive streak an the chick embryo. Development 122: 3263–3273.Google Scholar
  31. 31.
    Roth, S., Neurnansilberberg, F.S.; Barcelo’, G. and Schupbach, T. (1995). Cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern-formation in Drosophila. Cell 81:967–978.Google Scholar
  32. 32.
    Saijoh, Y., Adachi, H., Sakuma, R., Yeo, C.Y., Yashiro, K., Watanabe, M., Hashiguchi, H., Mochida, K., ©hishi; S. and Kawabata, M. (2000). Left-right asymmetric expression of lefty2 and nodal is induced by a signaling pathway that includes the transcription factor FAST2. Molecular Cell 5: 35–47.Google Scholar
  33. 33.
    Schnakenberg, J. (1979). Simple chemical reaction system with limit cycle behavior. J. theor. Biol. 31: 389–400MathSciNetCrossRefGoogle Scholar
  34. 34.
    Schier, A.F. and Shen, M.M. (2000). Nodal signalling in vertebrate development. Nature 4: 385–389.CrossRefGoogle Scholar
  35. 35.
    Smith, J.C., Conlon, F.L., Saka, Y. and Tada, M. (2000). Xwntll and the regulation of gastrulation in Xenopus. Phil. Trans. R. Soc. Land. B 355: 923–930.CrossRefGoogle Scholar
  36. 36.
    Technau, U. and Bode, H.R. (1999). HyBral, a Brachyury homologue, acts during head formation in Hydra. Development 126: 999–1010.Google Scholar
  37. 37.
    Turing, A. (1952). The chemical basis of morphogenesis. Phil. Trans. R. Soc. Land. B. 237: 37–72.CrossRefGoogle Scholar
  38. 38.
    Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. theor. Biol. 25:1–47.:Google Scholar
  39. 39.
    Wu, L.H. and Lengyel, J.A. (1998). Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125: 2433–2442.Google Scholar
  40. 40.
    Zaffran, S., Das, G. and Frasch, M. (2000). The nk-2 horneobox gene scarecrow (scro) is expressed in pharynx, ventral nerve cord and brain of Drosophila embryos. Mech. Dev. 94: 237–241.Google Scholar

Copyright information

© Springer Japan 2003

Authors and Affiliations

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

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