The Notch signalling pathway plays an important role during the development of the wing primordium, especially of the wing blade and margin. In these processes, the activity of Notch is controlled by the activity of the dorsal specific nuclear protein Apterous, which regulates the expression of the Notch ligand, Serrate, and the Fringe signalling molecule. The other Notch ligand, Delta, also plays a role in the development and patterning of the wing. It has been proposed that Fringe modulates the ability of Serrate and Delta to signal through Notch and thereby restricts Notch signalling to the dorsoventral boundary of the developing wing blade. Here we report the results of experiments aimed at establishing the relationships between Fringe, Serrate and Delta during wing development. We find that Serrate is not required for the initiation of wing development but rather for the expansion and early patterning of the wing primordium. We provide evidence that, at the onset of wing development, Delta is under the control of apterous and might be the Notch ligand in this process. In addition, we find that Fringe function requires Su(H). Our results suggest that Notch signalling during wing development relies on careful balances between positive and dominant negative interactions between Notch ligands, some of which are mediated by Fringe.

Brand
A.
,
Perrimon
N.
(
1993
)
Targeted expression as a means of altering cell fates and generating dominant phenotypes.
Development
118
,
401
415
Cohen
B.
,
McGuffin
M. E.
,
Pfeifle
C.
,
Segal
D.
,
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
Couso
J. P.
,
Bate
M.
,
Martinez-Arias
A.
(
1993
)
A wingless dependent polar coordinate system in Drosophila imaginal discs.
Science
259
,
484
489
Couso
J. P.
,
Knust
E.
,
Martinez-Arias
A.
(
1995
)
Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila.
Current Biol
5
,
1437
1448
de Celis
J. F.
,
Garcia Bellido
A.
(
1994
)
Roles of the Notch gene in Drosophila wing morphogenesis.
Mech. Dev
46
,
109
122
de Celis
J.
,
Garcia-Bellido
A.
,
Bray
S.
(
1996
)
Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc.
Development
122
,
359
369
deCelis
J.
,
Bray
S.
(
1997
)
Feedback mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing development.
Development
124
,
3241
3251
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
Doherty
D.
,
Feger
G.
,
Younger-Sheperd
S.
,
Jan
L. Y.
,
Jan
Y. N.
(
1996
)
Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation.
Genes Dev
10
,
421
434
Fleming
R. J.
,
Gu
Y.
,
Hukriede
N. A.
(
1997
)
Serrate -mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc.
Development
124
,
2973
2981
Huang
F.
,
Dambly-Chaudiere
C.
,
Ghysen
A.
(
1991
)
Emergence of sense organs in the wing disc of Drosophila.
Development
111
,
1087
1096
Irvine
K.
,
Wieschaus
E.
(
1994
)
fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development.
Cell
79
,
595
606
Jennings
B.
,
deCelis
J.
,
Delidakis
C.
,
Preiss
A.
,
Bray
S.
(
1995
)
Role of Notch and aechaete-scute complex in the expression of Enhancer of split bHLH proteins.
Development
121
,
3745
3752
Johansen
K.
,
Fehon
R.
,
Artavanis-Tsakonas
S.
(
1989
)
The Notch gene product is a glycoprotein expressed on the cell surface of both epidermal and neuronal precursor cell during Drosophila development.
J. Cell Biol
109
,
2427
2440
Kassis
J. A.
,
Noll
E.
,
Van Sickle
E.
,
Odenwald
W.
,
Perrimon
N.
(
1992
)
Altering the insertional specificity of a Drosophila transposable element.
Proc. Nat. Acad. Sci. USA
89
,
1919
1923
Kim
J.
,
Irvine
K. D.
,
Carroll
S. B.
(
1995
)
Cell recognition, signal induction, and symmetrical gene activation at the dorsal-ventral boundary of the developing Drosophila wing.
Cell
82
,
795
802
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.
,
Campos-Ortega
J. A.
(
1997
)
klumpfuss, a Drosophila gene encoding a member of the EGR family of transcription factors, is involved in bristle and leg development.
Development
124
,
3123
3134
Klein
T.
,
Brennan
K.
,
Martinez-Arias
A.
(
1997
)
An intrinsic dominant negative activity of Serrate that is modulated during wing development in Drosophila.
Dev. Biol
189
,
123
134
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.
,
Couso
J. P.
,
Martinez-Arias
A.
(
1998
)
Wing development and specification of dorsal cell fates in the absence of apterous in Drosophila.
Current Biology
8
,
417
420
Laufer
E.
,
Dahn
R.
,
Orozco
O.
,
Yeo
C.-Y.
,
Pisenti
J.
,
Henrique
D.
,
Abbott
U.
,
Fallon
J.
,
Tabin
C.
(
1997
)
Expression of Radical fringe in limb bud ectoderm regulates apical ectodermal ridge formation.
Nature
386
,
366
373
Micchelli
C.
,
Rulifson
E.
,
Blair
S.
(
1997
)
The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate.
Development
124
,
1485
1495
Neumann
C. J.
,
Cohen
S. M.
(
1996
)
A hirarchy of cross-regulationinvolving 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
Panin
V. M.
,
Papayannopolos
V.
,
Wilson
R.
,
Irvine
K. D.
(
1997
)
fringe modulates Notch-ligand interactions.
Nature
387
,
908
912
Rodriguez-Esteban
C.
,
Schwabe
J. W. R.
,
De La Pena
J.
,
Foys
B.
,
Eshelman
B.
,
Izpisua Belmonte
J. C.
(
1997
)
Radical fringe positions the apical ectodermanl rifge at the dorsoventral boundary of the vertebrate limb.
Nature
386
,
360
366
Schweisguth
F.
,
Posakony
J. W.
(
1992
)
Suppressor of Hairless, the Drosophila homolog of the Mouse recombination signal-binding protein gene, controls sensory organ cell fates.
Cell
69
,
1199
1212
Skeath
J. B.
,
Carroll
S. B.
(
1991
)
Regulation of achaete-scute gene expression ans sensory organ pattern formation in the Drosophila wing.
Genes Dev
5
,
984
995
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
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.
,
Paddock
S. W.
,
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
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
Yuan
Y.
,
Schultz
J.
,
Mlodzik
M.
,
Bork
P.
(
1997
)
Secreted fringe-like signalling molecules may be glycosyltransferases (letter).
Cell
88
,
9
11
Zecca
M.
,
Basler
K.
,
Struhl
G.
(
1996
)
Direct and long-range action of a Wingless morphogen gradient.
Cell
87
,
833
844
This content is only available via PDF.