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JOURNAL ARTICLES
Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions
J.A. Williams, S.W. Paddock, S.B. Carroll
Development 1993 117: 571-584;
J.A. Williams
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S.W. Paddock
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S.B. Carroll
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Summary

The legs and wings of insects and vertebrates develop from secondary embryonic fields that arise after the primary body axes have been established. In order to understand how the insect imaginal wing field is patterned, we have examined in detail the temporal and spatial expression patterns of, and epistatic relationships between, four key regulatory genes that are specifically required for wing formation in Drosophila. The wingless protein, in a role surprisingly distinct from its embryonic segment polarity function, appears to be the earliest-acting member of the hierarchy and crucial for distinguishing the notum/wing subfields, and for the compartmentalization of the dorsal and ventral wing surfaces. The wingless product is required to restrict the expression of the apterous gene to dorsal cells and to promote the expression of the vestigial and scalloped genes that demarcate the wing primordia and act in concert to promote morphogenesis.

REFERENCES

    1. Baker N. E.
    (1988) Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila. Dev. Biol 125, 96–108
    OpenUrlCrossRefPubMedWeb of Science
    1. Baker N. E.
    (1988) Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102, 489–497
    OpenUrlAbstract
    1. Brower D. L.
    (1985) The sequential compartmentalization of Drosophila segments revisited. Cell 41, 361–364
    OpenUrlCrossRefPubMed
    1. Brower D. L.,
    2. Wilcox M.,
    3. Piovant M.,
    4. Smith R. J.,
    5. Reger L. A.
    (1984) Related cell surface antigens expressed with positional specificity in Drosophila imaginal discs. Proc. Natl.Acad. Sci. USA 81, 7485–7489
    OpenUrlAbstract/FREE Full Text
    1. Bryant S. V.,
    2. French V.,
    3. Bryant P. J.
    (1981) Distal regeneration and symmetry. Science 212, 993–1002
    OpenUrlAbstract/FREE Full Text
    1. Bryant S. V.,
    2. Gardiner D. M.
    (1992) Retinoic acid, local cell-cell interactions, and pattern formation in vertebrate limbs. Dev. Biol 152, 1–25
    OpenUrl
    1. Campbell S.,
    2. Inamdar M.,
    3. Rodrigues V.,
    4. Raghavan V.,
    5. Palazzolo M.,
    6. Chovnick A.
    (1992) The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila. Genes Dev 6, 367–379
    OpenUrlAbstract/FREE Full Text
    1. Cohen B.,
    2. McGriffin M. E.,
    3. Pfeifle C.,
    4. Segal D.,
    5. Cohen S. M.
    (1992) apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6, 715–729
    OpenUrlAbstract/FREE Full Text
    1. French V.,
    2. Bryant P. J.,
    3. Bryant S. V.
    (1976) Pattern regulation in epimorphic fields. Science 193, 969–981
    OpenUrlAbstract/FREE Full Text
    1. Garcia-Bellido A.,
    2. Ripoll P.,
    3. Morata G.
    (1976) Developmental compartmentalization in the dorsal mesothoracic disc of Drosophila. Dev. Biol 48, 132–147
    OpenUrlCrossRefPubMedWeb of Science
    1. Ghysen A.,
    2. O'Kane C.
    (1989) Neural enhancer-like elements as specific cell markers in Drosophila. Development 105, 35–52
    OpenUrlAbstract
    1. James A. A.,
    2. Bryant P.
    (1981) Mutations causing pattern deficiencies and duplications in the imaginal wing disc of Drosophilamelanogaster. Dev. Biol 85, 39–54
    OpenUrlCrossRefPubMedWeb of Science
    1. Lawrence P. A.,
    2. Morata G.
    (1976) Compartments in the wing of Drosophila: a study of the engrailed gene. Dev. Biol 50, 321–337
    OpenUrlCrossRefPubMedWeb of Science
    1. Masucci J. D.,
    2. Miltenberger R. J.,
    3. Hoffman F. M.
    (1990) Pattern-specific expression of the Drosophiladecapentaplegic gene in imaginal disks is regulated by 3cis-regulatory elements. Genes Dev 4, 2011–2023
    OpenUrlAbstract/FREE Full Text
    1. Meinhart H.
    (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev. Biol 96, 375–385
    OpenUrlCrossRefPubMedWeb of Science
    1. Nusse R.,
    2. Varmus H. E.
    (1992) Wnt genes. Cell 69, 1073–1087
    OpenUrlCrossRefPubMedWeb of Science
    1. O'Brochta D. A.,
    2. Bryant P. J.
    (1985) A zone of non-proliferatingcells at a lineage restriction boundary in Drosophila. Nature 313, 138–141
    OpenUrlCrossRefPubMed
    1. Peifer M.,
    2. Bejsovec A.
    (1992) Knowing your neighbors: Cell interactions determine intrasegmental patterning in Drosophila. Trends Genet 8, 243–249
    1. Peifer M.,
    2. Rauskolb C.,
    3. Williams M.,
    4. Riggleman B.,
    5. Wieschaus E.
    (1991) The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation. Development 111, 1029–1044
    OpenUrlAbstract/FREE Full Text
    1. Phillips R. G.,
    2. Roberts I. J. H.,
    3. Ingham P. W.,
    4. Whittle J. R. S.
    (1990) The Drosophila segment polarity gene patched is involved in a positional-signaling mechanism in imaginal discs. Development 110, 105–114
    OpenUrlAbstract
    1. Posakony L. M.,
    2. Raftery L. A.,
    3. Gelbart W. M.
    (1990) Wing formation in Drosophilamelanogaster requires decapentaplegic gene function along the anterior-posterior boundary. Mech. Devel 33, 69–82
    OpenUrlCrossRefPubMed
    1. Rijsewijk F.,
    2. Schuermann M.,
    3. Waganaar E.,
    4. Panen P.,
    5. Weigel D.,
    6. Nusse R.
    (1987) The Drosophila homologue of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657
    OpenUrlCrossRefPubMedWeb of Science
    1. Schubiger G.,
    2. Schubiger M.
    (1978) Distal transformation in Drosophila leg imaginal disc fragments. Dev. Biol 67, 286–296
    OpenUrlCrossRefPubMedWeb of Science
    1. Simcox A. A.,
    2. Roberts I. J. H.,
    3. Hersperger E.,
    4. Gribbin M. C.,
    5. Shearn A.,
    6. Whittle J. R. S.
    (1989) Imaginal discs can be recovered from cultered embryos mutant for the segment polarity genes engrailed, naked -and patched but not from wingless. Development 107, 715–722
    OpenUrlAbstract/FREE Full Text
    1. Skeath J. B.,
    2. Carroll S. B.
    (1991) Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev 5, 984–995
    OpenUrlAbstract/FREE Full Text
    1. Stevens M. E.,
    2. Bryant P. J.
    (1985) Apparent genetic complexity generated by developmental thresholds: the apterous locus in Drosophila melanogaster. Genetics 110, 281–297
    OpenUrlAbstract/FREE Full Text
    1. Van den Heuvel M.,
    2. Nusse R.,
    3. Johnston P.,
    4. Lawrence P. A.
    (1989) Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell 59, 739–749
    OpenUrlCrossRefPubMedWeb of Science
    1. Whittle J. R. S.
    (1990) Pattern formation in imaginal discs. Seminars in Cell Biol 1, 241–252
    OpenUrlPubMed
    1. Williams J. A.,
    2. Bell J. B.
    (1988) Molecular organization of the vestigial region in Drosophila melanogaster. EMBOJ 7, 1355–1363
    OpenUrlPubMedWeb of Science
    1. Williams J. A.,
    2. Bell J. B.,
    3. Carroll S. B.
    (1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5, 2481–2495
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions
J.A. Williams, S.W. Paddock, S.B. Carroll
Development 1993 117: 571-584;
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JOURNAL ARTICLES
Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions
J.A. Williams, S.W. Paddock, S.B. Carroll
Development 1993 117: 571-584;

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