We have used conditional wingless genotypes to dissect the role of this gene in late stages of wing disc development. One of these genotypes (wgIL/wg-lacZ) is simultaneously a reporter of wingless transcription and temperature-sensitive for wingless function, and has allowed us to define its pattern of transcription in the absence of wingless activity. The primordia of a subset of the bristles of the notum, which develop in or immediately adjacent to wingless-expressing cells, depend upon wingless activity. The time-course of this contribution and the effect on proneural gene expression together suggest that wingless may regulate the activity of products of the achaete-scute complex in proneural clusters. wingless activity is also required at the presumptive wing margin and is a necessary precondition for the change in proliferation pattern in this region. The involvement of wingless in transducing or mediating positional signals for spatial patterning in imaginal disc development is discussed.
Reference
Baker
N. E.
(1987
) Molecular cloning of wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos.
EMBO J
6
, 1765
–1773
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
103
, 289
–298
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
Cabrera
C. V.
, Alonso
M. C.
, Johnston
P.
, Phillips
R. G.
, Lawrence
P. A.
(1987
) Phenocopies induced with antisense RNA identify the wingless gene.
Cell
50
, 659
–663
Campuzano
S.
, Modolell
J.
(1992
) Patterning of the Drosophila nervous system: the achaete - scute gene complex.
Trends Gen
8
, 202
–208
Cubas
P.
, deCelis
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
DiNardo
S.
, Sher
E.
, Heemskerk-Jongens
J.
, Kassis
J.
, O'Farrell
P. H.
(1988
) Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis.
Nature
332
, 604
–609
Dougan
S.
, DiNardo
S.
(1992
) Drosophila wingless generates cell type diversity among engrailed expressing cells.
Nature
360
, 347
–350
Ellis
H. M.
, Soann
D. R.
, Posakony
J.
(1990
) extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins.
Cell
61
, 27
–38
Garrell
J.
, Modolell
J.
(1990
) The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a Helix-Loop-Helix protein.
Cell,
61
, 39
–48
Ghysen
A.
, Dambly-Chaudiere
C.
(1988
) From DNA to form: the achaete - scute complex.
Genes Dev
2
, 495
–501
Greenwald
I.
, Rubin
G.
(1992
) Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells.
Cell
68
, 271
–281
Hama
C.
, Ali
Z.
, Kornberg
T. B.
(1990
) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter.
Genes Dev
4
, 1079
–1093
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
Jan
Y. N.
, Jan
L. Y.
(1992
) Neuronal specification.
Current Opinion in Genetics & Development
2
, 608
–613
Kassis
J. A.
, Noll
E.
, Van Sickle
E. P.
, Odenwald
W. F.
, Perrimon
N.
(1992
) Altering the insertional specificity of a Drosophila transposable element.
Proc. Natn. Acad. Sci. USA
89
, 1919
–1923
Martin-Belmudo
M. D.
, Martinez
C.
, Rodriguiz
A.
, Jimenez
F.
(1991
) Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila.
Development
113
, 445
–454
Martinez-Arias
A.
, Baker
N. A.
, Ingham
P. W.
(1988
) Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo.
Development
103
, 157
–170
Murre
C.
, McCaw
P. S.
, Vaessin
H.
, Caudy
M.
, Jan
L. Y.
, Jan
Y. N.
, Cabrera
C. V.
, Buskin
J. N.
, Hauschka
S. D.
, 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
Nordemeer
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
Nusse
R.
, Varmus
H. E.
(1982
) Many tumours induced by the mouse438mammary tumor virus contain a provirus integrated in the same region of the host genome.
Cell
31
, 99
–109
Perrimon
N.
, Smouse
D.
(1989
) Multiple functions of a Drosophila homeotic gene, zeste - white3, during segmentation and neurogenesis.
Dev. Biol
135
, 287
–305
Phillips
R. G.
, Roberts
I. J. H.
, Ingham
P. W.
, Whittle
J. R. S.
(1990
) The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs.
Development
110
, 105
–114
Romani
S.
, Campuzano
S.
, Macagno
E. R. A.
, Modolell
J.
(1989
) Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development.
Genes Dev
3
, 997
–1007
Siegfried
E.
, Chou
T.-B.
, Perrimon
N.
(1992
) wingless signaling acts through zeste-white 3, the Drosophila homolog 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
Sporn
M. B.
, Roberts
A. B.
(1988
) Peptide growth factors are multifunctional.
Nature
332
, 217
–219
Usui
K.
, Kimura
K.-I.
(1992
) Sensory mother cells are selected from among mitotically quiescent cluster of cells in the wing disc of Drosophila.
Development
116
, 601
–610
Van Doren
M.
, Ellis
H. M.
, Posakony
J. W.
(1991
) The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete - scute protein complexes.
Development
113
, 245
–255
Wilcox
M.
, Smith
R. J.
(1977
) Regenerative interactions between Drosophila imaginal discs of different types.
Dev. Biol
60
, 287
–297
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