Positional information and the spatial pattern of cellular differentiation,*

https://doi.org/10.1016/S0022-5193(69)80016-0Get rights and content

The problem of pattern is considered in terms of how genetic information can be translated in a reliable manner to give specific and different spatial patterns of cellular differentiation. Pattern formation thus differs from molecular differentiation which is mainly concerned with the control of synthesis of specific macromolecules within cells rather than the spatial arrangement of the cells. It is suggested that there may be a universal mechanism whereby the translation of genetic information into spatial patterns of differentiation is achieved. The basis of this is a mechanism whereby the cells in a developing system may have their position specified with respect to one or more points in the system. This specification of position is positional information. Cells which have their positional information specified with respect to the same set of points constitute a field. Positional information largely determines with respect to the cells' genome and developmental history the nature of its molecular differentiation. The specification of positional information in general precedes and is independent of molecular differentiation. The concept of positional information implies a co-ordinate system and polarity is defined as the direction in which positional information is specified or measured. Rules for the specification of positional information and polarity are discussed. Pattern regulation, which is the ability of the system to form the pattern even when parts are removed, or added, and to show size invariance as in the French Flag problem, is largely dependent on the ability of the cells to change their positional information and interpret this change. These concepts are applied in some detail to early sea urchin development, hydroid regeneration, pattern formation in the insect epidermis, and the development of the chick limb. It is concluded that these concepts provide a unifying framework within which a wide variety of patterns formed from fields may be discussed, and give new meaning to classical concepts such as induction, dominance and field. The concepts direct attention towards finding mechanisms whereby position and polarity are specified, and the nature of reference points and boundaries. More specifically, it is suggested that the mechanism is required to specify the position of about 50 cells in a line, relatively reliably, in about 10 hours. The size of embryonic fields is, surprisingly, usually less than 50 cells in any direction.

References (79)

  • GoodwinB. et al.

    J. Theoret. Biol.

    (1969)
  • GustafsonT. et al.

    Int. Rev. Cytol.

    (1963)
  • HadornE.
  • JacobF. et al.
  • JacobsonM.
  • JacobsonM.

    Devl Biol.

    (1968)
  • SaundersJ.W. et al.

    Devl Biol.

    (1963)
  • TokunagaC. et al.

    Devl Biol.

    (1965)
  • UrsprungH.
  • WaddingtonC.H.
  • ZwillingE.

    Adv. Morphogen.

    (1961)
  • AmprinoR.
  • ApterM.J.

    Cybernetics and Development

    (1966)
  • BerrillN.J.

    Growth, Development and Pattern

    (1961)
  • BohnH.

    Zool. Anz.

    (1967)
  • BrowneE.

    J. exp. Biol.

    (1909)
  • BryantP.J. et al.

    Devl Biol.

    (1969)
  • BulloughW.

    The Evolution of Differentiation

    (1967)
  • ChildC.M.

    Patterns and Problems of Development

    (1941)
  • ClarksonS.G.

    Ph.D. Thesis, University of London

    (1967)
  • ClarksonS.G. et al.

    Nature, Lond.

    (1967)
  • DalcqA.M.

    Form and Causality in Early Development

    (1938)
  • DavidsonM.E. et al.

    J. exp. Zool.

    (1948)
  • FurshpanE.J. et al.
  • GustafsonT.
  • GustafsonT. et al.

    Biol. Rev.

    (1967)
  • HampéA.

    J. Embryol. exp. Morph.

    (1958)
  • HicklinJ. et al.

    Nature, Lond.

    (1969)
  • HoltfreterJ. et al.
  • HörstadiusS.

    Wilhelm Roux Arch. EntwMech. Org.

    (1936)
  • HörstadiusS.

    Biol. Rev.

    (1939)
  • HuxleyJ.S. et al.

    The Elements of Experimental Embryology

    (1934)
  • KienyM.

    J. Embryol. exp. Morph.

    (1964)
  • KroegerH.

    Wilhelm Roux Arch. EntwMech. Org.

    (1959)
  • KroegerH.

    Naturwissenschaften

    (1960)
  • LamertonL.F. et al.

    Progr. Biophys. Mol. Biol.

    (1968)
  • LawrenceP.A.

    J. exp. Biol.

    (1966)
  • LederbergJ.
  • LockeM.

    Adv. Morphogen.

    (1966)
  • Cited by (2199)

    View all citing articles on Scopus

    This work was first presented at the 3rd Serbelloni Meeting on Theoretical Biology, Easter, 1968 (see Wolpert, 1969).

    *

    This work is supported by The Nuffield Foundation. I am grateful for the helpful discussion, comments and criticisms provided by Dr Brian Goodwin, Dr Morrel Cohen, Dr David Gingell, Dr David Garrod and Dr Peter Lawrence.

    View full text