The vestigial (vg) gene of Drosophila plays a central role in the development and patterning of the wing: loss of vestigial results in failures in wing development and ectopic expression of vestigial leads to the development of ectopic wings. The wing-specific regulation of vestigial is mediated through two enhancers: (1) the Boundary Enhancer (vgBE) is early acting and becomes restricted to the wing margin, and (2) the Quadrant Enhancer (vgQE), acts later and is responsible for the expression of vestigial in the developing wing blade. These enhancers receive regulatory inputs from three signalling pathways: wingless, decapentaplegic and Notch/Suppressor of Hairless. Our experiments show that the vestigial gene product is also an input in the regulation of vestigial expression. In particular, Vestigial provides an important input for the regulation of the activity of the vgQE acting in concert with Wingless and Decapentaplegic. Our results suggest how interactions between vgBE and the vgQE mediated by Vestigial can explain the interactions between the wing margin and the wing blade during the growth of the wing. We further show that Vestigial and Notch collaborate with Wingless to subdivide and pattern the wing blade. These results lead us to propose a general role for Wingless during development in which it stabilizes cell fate decisions that have been implemented by other molecules.

Brand
A.
,
Perrimon
N.
(
1993
)
Targeted expression as a means of altering cell fates and generating dominant phenotypes.
Development
118
,
401
415
Campbell
S.
,
Inamdar
M.
,
Rodrigues
V.
,
Raghavan
V.
,
Palazzolo
M.
,
Chovnick
A.
(
1991
)
The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila.
GenesDev
6
,
367
379
Couso
J. P.
,
Bishop
S. A.
,
Martinez-Arias
A.
(
1994
)
The wingless signalling pathway and the patterning of the wing margin.
Development
120
,
621
636
Couso
J. P.
,
Knust
E.
,
Martinez-Arias
A.
(
1995
)
Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila.
Current Biology
5
,
1437
1448
Diaz-Benjumea
F. J.
,
Cohen
S. M.
(
1995
)
Serrate signals through Notch to establish a wingless -dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing.
Development
121
,
4215
4225
Echelard
Y.
,
Epstein
D. J.
,
St-Jacques
B.
,
Shen
L.
,
Mohler
J.
,
McMahon
J.
,
McMahon
A. P.
(
1993
)
Sonic Hedgehog, a member of a family of putative signalling molecules, is implicated in the regulation of CNS polarity.
Cell
75
,
1417
1430
Gorfinkiel
N.
,
Morata
G.
,
Guerrero
I.
(
1997
)
The homeobox gene Distal-less induces ventral appendage development in Drosophila.
Genes Dev
11
,
2259
2271
Hoppler
S.
,
Moon
R. T.
(
1998
)
BMP-2/4 and Wnt-8 cooperatively pattern the Xenopus mesoderm.
Mech. Dev
71
,
1190129
–.
Hoppler
S.
,
Brown
J.
,
Moon
R.
(
1996
)
Expression of a dominant negative Wnt blocks induction of MyoD in Xenopus embryos.
Genes Dev
10
,
2805
2817
Kim
J.
,
Johnson
K.
,
Chen
H. J.
,
Carrol
S.
,
Laughton
A.
(
1997
)
Drosophila Mad binds to DNA and directly mediates activation of vestigial by Dcapentaplegic.
Nature
388
,
304
308
Kim
J.
,
Sebring
A.
,
Esch
J. J.
,
Kraus
M. E.
,
Vorwerk
K.
,
Magee
J.
,
Carroll
S. B.
(
1996
)
Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene.
Nature
382
,
133
138
Klein
T.
,
Martinez-Arias
A.
(
1998
)
Different spatial and temporal interactions between Notch, wingless and vestigial specify proximal and distal pattern elements of the wing in Drosophila.
Dev Biol
194
,
196
212
Klein
T.
,
Martinez-Arias
A.
(
1998
)
Interactions among Delta, Serrate and Fringe modulate Notch activity during Drosophila wing development.
Development,
125
,
2951
2962
Klein
T.
,
Couso
J. P.
,
Martinez-Arias
A.
(
1998
)
Wing development and specification of dorsal cell fates in the absence of apterous in Drosophila.
Current Biol
8
,
417
420
Lecuit
T.
,
Cohen
S.
(
1997
)
Proaximal-distal axis formation in the Drosophila leg.
Nature
388
,
139
145
Neumann
C.
,
Cohen
S. M.
(
1996
)
Long-range action of Wingless organizes the dorsal-ventral axis ot the Drosophila wing.
Development
124
,
871
880
Neumann
C. J.
,
Cohen
S. M.
(
1996
)
A hirarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing.
Development
122
,
3477
3485
Ng
M.
,
Diaz-Benjumea
F.
,
Vincent
J. P.
,
Wu
J.
,
Cohen
S. M.
(
1996
)
Specification of the wing by localized expression of wingless protein.
Nature
381
,
316
318
Riddle
R.
,
Johnson
R.
,
Laufer
E.
,
Tabin
C.
(
1993
)
Sonic hedgehog mediates the polarizing activity of the ZPA.
Cell
75
,
1401
1416
Simpson
P.
,
Lawrence
P.
,
Machat
F.
(
1981
)
Clonal analysis of two wing scalloping mutants in Drosophila.
Dev. Biol
84
,
206
211
Speicher
S. A.
,
Thomas
U.
,
Hinz
U.
,
Knust
E.
(
1994
)
The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginal discs: control of cell proliferation.
Development
120
,
535
544
Staehling-Hampton
K.
,
Hoffmann
F. M.
(
1994
)
Ectopic decapentaplegic in the Drosophila midgut alters the expression of five homeotic genes, dpp and wingless, causing morphological defects.
Dev. Biol
164
,
502
512
Struhl
G.
,
Basler
K.
(
1993
)
Organizing activity of Wingless protein in Drosophila.
Cell
72
,
527
540
Tautz
D.
,
Pfeiffle
C.
(
1989
)
A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchbach.
Chromosoma
98
,
81
85
Wilder
B.
,
Perrimon
N.
(
1995
)
Dual functions of wingless in the leg imaginal disc of Drosophila.
Development
121
,
477
488
Williams
J. A.
,
Bell
J. B.
,
Carroll
S. B.
(
1991
)
Control of Drosophila wing and haltere development by the nuclear vestigial gene product.
Genes Dev
5
,
2481
2495
Williams
J. A.
,
Paddock
S. W.
,
Carroll
S. B.
(
1993
)
Pattern formation in a secondary field: A hirarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions.
Development
117
,
571
584
Williams
J. A.
,
Paddock
S. W.
,
Vorwerk
K.
,
Carroll
S. B.
(
1994
)
Organization of wing formation and induction of a wing patterning gene at the dorsal/ ventral compartment boundary.
Nature
368
,
299
305
Wolpert
L.
(
1969
)
Positional information and the spatial pattern of cellular differentiation.
J. Theor. Biol
25
,
1
47
Zecca
M.
,
Basler
K.
,
Struhl
G.
(
1995
)
Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing.
Development
121
,
2265
2278
Zecca
M.
,
Basler
K.
,
Struhl
G.
(
1996
)
Direct and long-range action of a Wingless morphogen gradient.
Cell
87
,
833
844
Zhang
J.
,
Carthew
R. W.
(
1998
)
Interactions between Wingless and Dfz2 during Drosophila wing development.
Development
125
,
3075
3085
This content is only available via PDF.