Models of biological pattern formation: common mechanism in plant and animal development.

Earlier proposed models for primary pattern formation, for gene activation and for segmentation are summarized and compared with recent molecular-genetic observations. A model for head, foot, tentacle and bud formation in Hydra illustrates that complex patterns can be reliably generated. Stable cell determination requires autocatalytic (autoregulatory) genes. Segmentation in insects has been proposed to result from a reiteration of (at least three) cell states. Their patterning is achieved by a mutual activation of cell states that locally exclude each other. A model for accretion of new segments by proliferation at the posterior pole is proposed that accounts for the generation of a periodic and a sequential pattern in register with each other. The assumption of a process analogous to segmentation in plants can account for the initiation of leaves with an intrinsic polarity that eventually leads to the upper and lower leaf surfaces. The model accounts also for the formation of axillary buds in correct relation to a leaf and for the much smaller spacing of leaves within a whorl when compared with the spacing between two successive whorls along the shoot. It is concluded that the generation of complex structures in distantly related organisms may be based on similar mechanisms.

[1]  N. Patel,et al.  Expression of engrailed during segmentation in grasshopper and crayfish. , 1989, Development.

[2]  G. Struhl,et al.  Compartment boundarles and the control of Drosophila limb pattern by bedgebog protein , 1994 .

[3]  A Gierer,et al.  Generation and regeneration of sequence of structures during morphogenesis. , 1980, Journal of theoretical biology.

[4]  H. Meinhardt Cell determination boundaries as organizing regions for secondary embryonic fields. , 1983, Developmental biology.

[5]  Ken W. Y. Cho,et al.  Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid , 1991, Cell.

[6]  E. Lewis A gene complex controlling segmentation in Drosophila , 1978, Nature.

[7]  C. Nüsslein-Volhard,et al.  A gradient of bicoid protein in Drosophila embryos , 1988, Cell.

[8]  W. McGinnis,et al.  Autoregulation of a drosophila homeotic selector gene , 1988, Cell.

[9]  M. Levine,et al.  Autoregulation of a segmentation gene in Drosophila: combinatorial interaction of the even-skipped homeo box protein with a distal enhancer element. , 1991, Genes & development.

[10]  E. Coen,et al.  The war of the whorls: genetic interactions controlling flower development , 1991, Nature.

[11]  H. Meinhardt,et al.  Hierarchical Inductions of Cell States: A Model for Segmentation in Drosophila , 1986, Journal of Cell Science.

[12]  H. Meinhardt,et al.  Biological pattern formation: fmm basic mechanisms ta complex structures , 1994 .

[13]  M. Leptin twist and snail as positive and negative regulators during Drosophila mesoderm development. , 1991, Genes & development.

[14]  H. Saedler,et al.  Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. , 1995, Development.

[15]  Hans Meinhardt,et al.  The Algorithmic Beauty of Sea Shells , 1998, The Virtual Laboratory.

[16]  Simultaneous anterior and posterior regeneration and other growth phenomena in Maldanid polychaetes , 1951 .

[17]  M. Shankland Leech segmentation: cell lineage and the formation of complex body patterns. , 1991, Developmental biology.

[18]  R. Harland,et al.  Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center , 1991, Cell.

[19]  G. Martin,et al.  Why thumbs are up , 1995, Nature.

[20]  P. Ingham Segment polarity genes and cell patterning within the Drosophila body segment. , 1991, Current opinion in genetics & development.

[21]  P. Lawrence,et al.  Distribution of the wingless gene product in drosophila embryos: A protein involved in cell-cell communication , 1989, Cell.

[22]  L. Jaffe,et al.  Localization in the developing Fucus egg and the general role of localizing currents. , 1968, Advances in morphogenesis.

[23]  H. Bode,et al.  Development of the two-part pattern during regeneration of the head in hydra. , 1988, Development.

[24]  H. Meinhardt,et al.  Space-dependent cell determination under the control of morphogen gradient. , 1978, Journal of theoretical biology.

[25]  W. McGinnis,et al.  High-affinity binding sites for the Deformed protein are required for the function of an autoregulatory enhancer of the Deformed gene. , 1991, Genes & development.

[26]  D. Brower,et al.  Allelic interactions at the engrailed locus of Drosophila: engrailed protein expression in imaginal discs. , 1989, Developmental biology.

[27]  S. Carroll,et al.  Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing drosophila wing , 1995, Cell.

[28]  C. Waddington,et al.  Studies on the Nature of the Amphibian Organization Centre. III.--The Activation of the Evocator , 1936 .

[29]  N E Baker,et al.  Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos , 1987, The EMBO journal.

[30]  M. Locke,et al.  THE CUTICULAR PATTERN IN AN INSECT, RHODNIUS PROLIXUS STAL , 1959 .

[31]  H. Meinhardt Models of biological pattern formation , 1982 .

[32]  H. Meinhardt 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. , 1993, Developmental biology.

[33]  R. Kosher,et al.  Wnt-5a and Wnt-7a are expressed in the developing chick limb bud in a manner suggesting roles in pattern formation along the proximodistal and dorsoventral axes , 1993, Mechanisms of Development.

[34]  H. Meinhardt,et al.  A model for pattern formation on the shells of molluscs , 1987 .

[35]  C. Nüsslein-Volhard,et al.  Mutations affecting segment number and polarity in Drosophila , 1980, Nature.

[36]  C. Tabin,et al.  Sonic hedgehog mediates the polarizing activity of the ZPA , 1993, Cell.

[37]  R. Moon,et al.  Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. , 1993, Genes & development.

[38]  P. Ingham,et al.  Regulation of wingless transcription in the Drosophila embryo. , 1993, Development.

[39]  W. Gelbart,et al.  Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary , 1990, Mechanisms of Development.

[40]  L. Wolpert Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[41]  P. Nieuwkoop The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. , 1973, Advances in morphogenesis.

[42]  Jean-Paul Vincent,et al.  It takes three to distalize , 1994, Nature.

[43]  S. Carroll,et al.  Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary , 1994, Nature.

[44]  D. Summerbell,et al.  Positional signalling and specification of digits in chick limb morphogenesis , 1975, Nature.

[45]  C. Pfeifle,et al.  apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. , 1992, Genes & development.

[46]  C. Nüsslein-Volhard,et al.  The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner , 1988, Cell.

[47]  G. Stent,et al.  Embryonic development of the hirudinid leech Hirudo medicinalis: structure, development and segmentation of the germinal plate. , 1982, Journal of embryology and experimental morphology.

[48]  H. Meinhardt,et al.  A boundary model for pattern formation in vertebrate limbs. , 1983, Journal of embryology and experimental morphology.

[49]  E. Wieschaus,et al.  fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development , 1994, Cell.

[50]  H. Meinhardt Pattern formation in biology: a comparison of models and experiments , 1992 .

[51]  Alexander F. Schier,et al.  Direct homeodomain–DNA interaction in the autoregulation of the fushi tarazu gene , 1992, Nature.

[52]  R. Chandebois Histogenesis and morphogenesis in planarian regeneration. , 1976, Monographs in developmental biology.

[53]  A. Hudson,et al.  Phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus , 1995 .

[54]  A. Gierer Generation of biological patterns and form: some physical, mathematical, and logical aspects. , 1981, Progress in biophysics and molecular biology.

[55]  F. Karch,et al.  A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. , 1990, The EMBO journal.

[56]  Nipam H. Patel,et al.  Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles , 1994, Nature.

[57]  A. Gierer,et al.  Regeneration of hydra from reaggregated cells. , 1972, Nature: New biology.

[58]  Wolfgang Driever,et al.  The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo , 1989, Nature.

[59]  H. Meinhardt The threefold subdivision of segments and the initiation of legs and wings in insects , 1986 .

[60]  Michael J. Pankratz,et al.  Gradients of Krüppel and knirps gene products direct pair-rule gene stripe patterning in the posterior region of the drosophila embryo , 1990, Cell.

[61]  S. Cohen,et al.  Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila , 1993, Cell.

[62]  J. Gurdon,et al.  Direct and continuous assessment by cells of their position in a morphogen gradient , 1995, Nature.

[63]  H. Meinhardt Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. , 1989, Development.

[64]  T. Mohandas,et al.  Complementary homeo protein gradients in developing limb buds. , 1989, Genes & development.