The margin of the wing of Drosophila is defined and patterned from a stripe of cells expressing the wingless (wg) gene that is established during the third larval instar in the developing wing blade. The expression of the genes cut and achaete in a small domain in the prospective wing margin region reflects the activity of wg and probably mediate its function. Our results indicate that, in the wing margin, the wingless signal requires the activity of at least three genes: armadillo (arm), dishevelled (dsh) and shaggy (sgg) and that the functional relationship between these genes and wg is the same as that which exist during the patterning of the larval epidermis. These observations indicate that arm, dsh and sgg encode elements of a unique ‘wingless signalling pathway’ that is used several times throughout development.
REFERENCES
Adler
P.
(1992
) The genetic control of tissue polarity in Drosophila.
Bioessays
14
, 735
–741
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
Bejsovec
A.
, Martinez Arias
A.
(1991
) Roles of wingless in patterning the larval epidermis of Drosophila.
Development
113
, 471
–485
Bloechinger
K.
, Bodmer
R.
, Jack
J.
, Jan
L. Y.
, Jan
Y. N.
(1988
) Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila.
Nature
333
, 629
–635
Bourouis
M.
, Moore
P.
, Ruel
L.
, Grau
Y.
, Heitzler
P.
, Simpson
P.
(1990
) An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc2 subfamily.
EMBO J
9
, 2877
–2884
Campuzano
S.
, Modolell
J.
(1992
) Patterning of the Drosophila nervous system: the achaete-scute gene complex.
Trends Genet
8
, 202
–208
Cohen
S.
(1990
) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes.
Nature
343
, 173
–177
Couso
J. P.
, Bate
M.
, Martinez Arias
A.
(1993
) A wingless -dependent polar coordinate system in Drosophila imaginal discs.
Science
259
, 484
–489
Cubas
P.
, de Celis
J. F.
, Campuzano
S.
, Modolell
J.
(1991
) Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc.
Genes Dev
5
, 996
–1008
Cubas
P.
, Modolell
J.
(1992
) The extramacrochaetae gene provides information for sensory organ patterning.
EMBO J
11
, 3385
–3393
Dominguez
M.
, Campuzano
S.
(1993
) asense, a member of the Drosophila achaete-scute complex, is a proneural and neural differentiation gene.
EMBO J
12
, 2049
–2060
Dougan
S.
, DiNardo
S.
(1992
) Drosophilawingless generates cell diversity using engrailed expressing cells.
Nature
360
, 347
–349
Fristrom
D.
(1969
) Cellular degeneration in the production of some mutant phenotypes in Drosophila melanogaster.
Molec. Gen. Genet
103
, 363
–379
González
F.
, Swales
L.
, Bejsovec
A.
, Skaer
H.
, Martinez Arias
A.
(1991
) Secretion and movement of the wingless protein in the Drosophila embryo.
Mech. Dev
35
, 43
–54
Hartenstein
V.
, Posakony
J. W.
(1990
) A dual function of the Notch gene in Drosophila sensillum development.
Dev. Biol
142
, 13
–30
Ingham
P.
(1991
) Segment polarity genes and cell patterning within the Drosophila body segment.
Curr. Op. Genet. Dev
1
, 261
–267
Ingham
P. W.
, Martinez Arias
A.
(1992
) Boundaries and fields in early embryos.
Cell
68
, 221
–235
Jack
J.
, DeLotto
Y.
(1992
) Effect of wing scalloping mutations on cut expression and sense organ differentiation in the Drosophila wing margin.
Genetics
131
, 353
–363
Jack
J.
, Dorsett
D.
, DeLotto
Y.
, Liu
S.
(1991
) Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer.
Development
113
, 735
–747
Klingensmith
J.
, Noll
E.
, Perrimon
N.
(1989
) The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death.
Dev. Biol
134
, 130
–145
Moon
R.
(1993
) In pursuit of the functions of the Wnt family of developmental regulators: insights from Xenopus laevis.
BioEssays
15
, 91
–97
Murre
C.
, McCaw
P. S.
, Vassin
H.
, Caudy
M.
, Jan
L. Y.
, Jan
Y. L.
, Cabrera
C. V.
, Lassar
A. B.
, Weintraub
H.
, Baltimore
D.
(1989
) Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence.
Cell
58
, 537
–544
Noordermeer
J.
, Johnston
P.
, Rijsewijk
F.
, Nusse
R.
, Lawrence
P. A.
(1992
) The consequences of ubiquitous expression of the wingless gene in the Drosophila embryo.
Development
116
, 711
–719
O'Brochta
, Bryant
P.
(1985
) A zone of non-proliferating cells at a lineage restriction boundary in Drosophila.
Nature
313
, 138
–141
Patel
N.
, Schafer
B.
, Goodman
C.
, Holmgren
R.
(1989
) The role of segment polarity genes during Drosophila neurogenesis.
Genes Dev
3
, 890
–904
Peifer
M.
, Bejsovec
A.
(1992
) Knowing your neighbours: cell interactions determine intrasegmental patterning in Drosophila.
Trends Genet
8
, 243
–249
Peifer
M.
, Rauskolb
C.
, Williams
M.
, Riggleman
R.
, Wieschaus
E.
(1991
) The segment polaity gene armadillo interacts with the wingless signalling pathway in both embryonic and adult pattern formation.
Development
11
, 1029
–1045
Peifer
M.
, McCrea
P. D.
, Green
K. J.
, Wieschaus
E.
, Gumbiner
B. M.
(1992
) The vertebrate adhesive junction proteins-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties.
J. Cell Biol
118
, 681
–691
Perrimon
N.
, Mahowald
A. P.
(1987
) Multiple functions of segment polarity genes in Drosophila.
Dev. Biol
119
, 587
–600
Perrimon
N.
, Smouse
D.
(1989
) Multiple functions of a Drosophila homeotic gene zeste white 3 during segmentation and neurogenesis.
Dev. Biol
135
, 287
–305
Phillips
R. G.
, Whittle
J. R. S.
(1993
) wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development.
Development
118
, 427
–438
Rijsewijk
F.
, Schuermann
M.
, Wagenaar
E.
, Parren
P.
, Weigel
D.
, 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
Rodriguez
I.
, Hernandez
R.
, Modolell
J.
, Ruiz-Gomez
M.
(1990
) Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia.
EMBO J
9
, 3583
–3592
Siegfried
E.
, Chou
T.
, Perrimon
N.
(1992
) wingless signalling acts through zeste-white 3, the Drosophila homologue of glycogen synthase kinase 3, to regulate engrailed and establish cell fate.
Cell
71
, 1167
–1179
Skeath
J. B.
, Carroll
S. B.
(1991
) Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing.
Genes Dev
5
, 984
–995
Tsukamoto
A.
, Grosschedl
R.
, Guzman
R.
, Parslow
T.
, Varmus
H.
(1988
) Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice.
Cell
55
, 619
–625
van den Heuvel
M.
, Klingensmith
J.
, Perrimon
N.
, Nusse
R.
(1993
) Cell patterning in the Drosophila segment: engrailed and wingless antigen distributions in segment polarity mutant embryos.
Development
1993
, 105
–144
Williams
J. A.
, Paddock
S.
, Carroll
S. B.
(1993
) Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions.
Development
117
, 571
–584
Woodget
J. R.
(1991
) A common denominator linking glycogen metabolism, nuclear oncogenes and development.
Trends Biochem. Sci
26
, 177
–187
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