The eye-antennal imaginal discs of Drosophila melanogaster form the head capsule of the adult fly. Unlike the limb primordia, each eye-antennal disc gives rise to morphologically and functionally distinct structures. As a result, these discs provide an excellent model system for determining how the fates of primordia are specified during development. In this study, we investigated how the adjacent primordia of the compound eye and dorsal head vertex are specified. We show that the genes wingless (wg) and orthodenticle (otd) are expressed throughout the entire second instar eye-antennal disc, conferring a default fate of dorsal vertex cuticle. Activation of decapentaplegic (dpp) expression in the posterior eye disc eliminates wg and otd expression, thereby permitting eye differentiation. We also demonstrate that otd is activated by wg in the vertex primordium. Finally, we show that early activation of dpp depends on hedgehog (hh) expression in the eye anlage prior to morphogenetic furrow formation.

REFERENCES

Basler
K.
,
Struhl
G.
(
1994
)
Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
Nature
368
,
208
214
Blackman
R. K.
,
Sanicola
M.
,
Raftery
L. A.
,
Gillevet
T.
,
Gelbart
W. M.
(
1991
)
An extensive 3cis-regulatory region directs the imaginal disk expression of decapentaplegic, a menber of the TGF-b family in Drosophila.
Development
111
,
657
665
Blair
S. S.
,
Brower
D. L.
,
Thomas
J. B.
,
Zavortink
M.
(
1994
)
The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila.
Development
120
,
1805
1815
Brook
W. J.
,
Cohen
S. M.
(
1996
)
Antagonistic interactions between Wingless and Decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg.
Science
273
,
1373
1377
Burke
R.
,
Basler
K.
(
1996
)
Hedgehog-dependent patterning in the Drosophila eye can occur in the absence of Dpp signaling.
Dev. Biol
179
,
360
368
Chanut
F.
,
Heberlein
U.
(
1997
)
Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina.
Development
124
,
559
567
Diaz-Benjumea
F. J.
,
Cohen
B.
,
Cohen
S.
(
1994
)
Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs.
Nature
372
,
175
179
Diaz-Benjumea
F. J.
,
Cohen
S. M.
(
1993
)
Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila.
Cell
75
,
741
752
Garcia-Bellido
A.
,
Ripoll
P.
,
Morata
G.
(
1973
)
Developmental compartimentalization of the wing disc of Drosophila.
Nature New Biol
245
,
251
253
Haynie
J. L.
,
Bryant
P. J.
(
1986
)
Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster.
J. Exp. Zool
237
,
293
308
Heberlein
U.
,
Wolff
T.
,
Rubin
G.M.
(
1993
)
The TGF-homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina.
Cell
75
,
913
926
Heslip
T. R.
,
Theisen
H.
,
Walker
H.
,
Marsh
J. L.
(
1997
)
SHAGGY and DISHEVELLED exert opposite effects on wingless and decapentaplegic expression and on positional identity in imaginal discs.
Development
124
,
1069
1078
Itoh
K.
,
Sokol
S. Y.
(
1997
)
Graded amounts of Xenopus dishevelled specify discrete anteroposterior cell fates in prospective ectoderm.
Mech. Dev
61
,
113
125
Itoh
K.
,
Tang
T. L.
,
Neel
B. G.
,
Sokol
S. Y.
(
1995
)
Specific modulation of ectodermal cell fates in Xenopus embryos by glycogen synthase kinase.
Development
121
,
3979
88
Jiang
J.
,
Struhl
G.
(
1996
)
Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development.
Cell
86
,
401
409
Johnston
L. A.
,
Schubiger
G.
(
1996
)
Ectopic express of wingless in imaginal discs interferes with decapentaplegic expression a0nd alters cell determination.
Development
122
,
3519
3529
Klingensmith
J.
,
Nusse
R.
,
Perrimon
N.
(
1994
)
The Drosophila segment polarity gene dishevelled encodes a novel protein required for esponse to the wg signal.
Genes Dev
8
,
118
130
Kornberg
T.
,
Siden
I.
,
O'Farrell
P.
,
Simon
M.
(
1985
)
The engrailed locus of Drosophila: In situ localization of transcripts reveals compartment-specific expression.
Cell
40
,
43
53
Lee
J. J.
,
Ekker
S. C.
,
Von Kessler
D. P.
,
Porter
J. A.
,
Sun
B. I.
,
Beachy
P. A.
(
1994
)
Autoproteolysis in hedgehog protein biogenesis.
Science
266
,
1528
1537
Lee
J. J.
,
von Kessler
D. P.
,
Parks
S.
,
Beachy
P. A.
(
1992
)
Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog.
Cell
71
,
33
50
Ma
C.
,
Moses
K.
(
1995
)
wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye.
Development
121
,
2279
2289
Ma
C.
,
Zhou
Y.
,
Beachy
P. A.
,
Moses
K.
(
1993
)
The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye.
Cell
75
,
927
938
Masucci
J. D.
,
Miltenberger
R. J.
,
Hoffmann
F. M.
(
1990
)
Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal discs is regulated by 3cis-regulatory elements.
Genes Dev
4
,
2011
2023
Morata
G.
,
Lawrence
P. A.
(
1975
)
Control of compartment development by the engrailed gene in Drosophila.
Nature
255
,
614
617
Morata
G.
,
Lawrence
P. A.
(
1979
)
Development of the eye-antenna imaginal disc of Drosophila.
Dev. Biol
70
,
355
371
Morimura
S.
,
Maves
L.
,
Chen
Y.
,
Hoffman
F. M.
(
1996
)
decapentaplegic overexpression affects Drosophila wing and leg imaginal disc development and wingless expression.
Dev. Biol
177
,
136
151
Penton
A.
,
Hoffman
M.
(
1996
)
Decapentaplegic restricts the domain of wingless during limb patterning.
Nature
382
,
162
165
Raftery
L. A.
,
Twombly
V.
,
Wharton
K.
,
Gelbart
W. M.
(
1995
)
Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila.
Genetics
139
,
231
254
Ready
D. F.
,
Hanson
T. E.
,
Benzer
S.
(
1976
)
Development of the Drosophila retina, a neurocrystalline lattice.
Dev. Biol
53
,
217
240
Royet
J.
,
Finkelstein
R.
(
1995
)
Pattern formation in Drosophila head development: the role of the orthodenticle homeobox gene.
Development
121
,
3561
3572
Royet
J.
,
Finkelstein
R.
(
1996
)
hedgehog, wingless, and orthodenticle specify adult head development in Drosophila.
Development
122
,
1849
1858
Rubenstein
J. L. R.
,
Martinez
S.
,
Shimamura
K.
,
Puelles
L.
(
1994
)
The embryonic vertebrate forebrain: the prosomeric model.
Science
266
,
578
580
Ruel
L.
,
Pantesco
V.
,
Lutz
Y.
,
Simpson
P.
,
Bourouis
M.
(
1993
)
Functional significance of a family of protein kinases encoded at the shaggy locus in Drosophila.
EMBO J
12
,
1657
1669
Sanicola
M.
,
Sekelsky
J. S. E.
,
Gelbart
W. M.
(
1995
)
Drawing a stripe in Drosophila imaginal discs: negative regulation of decapentaplegic and patched expression by engrailed.
Genetics
139
,
745
756
Sekelsky
J. J.
,
Newfeld
S. J.
,
Raftery
L. A.
,
Chartoff
E. H.
,
Gelbart
W. M.
(
1995
)
Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster.
Genetics
139
,
1347
1358
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
Siegfried
E.
,
Perrimon
N.
(
1994
)
Drosophila wingless: a paradigm for the function and mechanisms of Wnt signaling.
BioEssays
16
,
395
404
Spencer
F. A.
,
Hoffmann
F. M.
,
Gelbart
W. M.
(
1982
)
decapentaplegic; a gene complex affecting morphogenesis in Drosophila melanogaster.
Cell
28
,
451
461
St. Johnston
R. D.
,
Hoffman
F. M.
,
Blackman
R. K.
,
Segal
R.
,
Grimaila
R. W.
,
Padgett
H. A.
,
Gelbart
W. M.
(
1990
)
The molecular organization of the decapentaplegic gene in Drosophila melanogaster.
Genes Dev
4
,
1114
1127
Tabata
T.
,
Kornberg
T. B.
(
1994
)
Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs.
Cell
76
,
89
102
Tabata
T.
,
Schwartz
C.
,
Gustavson
E.
,
Ali
Z.
,
Kornberg
T. B.
(
1995
)
Creating a Drosophila wing de novo: the role of engrailed and the compartment borber hypothesis.
Development
122
,
3359
3369
Theisen
H.
,
Purcell
J.
,
Bennett
M.
,
Kansagara
D.
,
Syed
A.
,
Marsh
J. L.
(
1994
)
dishevelled is required during wingless signaling to establish both cell polarity and cell identity.
Development
120
Tickle
C.
(
1995
).
Vertebrate limb development.
Curr. Opin. Genet. Dev
5
,
478
484
Tomlinson
A.
,
Ready
D. F.
(
1987
)
Neuronal differentiation in the Drosophila ommatidium.
Dev. Biol
120
,
366
376
Treisman
J.
,
Rubin
G. M.
(
1995
)
wingless inhibits morphogenetic furrow movement in the Drosophila eye disc.
Development
121
,
3519
3527
van den Heuvel
M.
,
Harryman-Samos
C.
,
Klingensmith
J.
,
Perrimon
N.
,
Nusse
R.
(
1993
)
Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein.
EMBO J
12
,
5293
5302
Vincent
J.-P.
,
Girdham
C. H.
,
O'Farrell
P. H.
(
1994
)
A cell-autonomous, ubiquitous marker for the analysis of Drosophila genetic mosaics.
Dev. Biol
164
,
328
331
Wiersdorff
V.
,
Lecuit
T.
,
Cohen
S. M.
,
Mlodzik
M.
(
1996
)
Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye.
Development
122
,
2153
2162
Wieschaus
E.
,
Perrimon
N.
,
Finkelstein
R.
(
1992
)
orthodenticle activity is required for the development of medial structures in the larval and adult epidermis of Drosophila.
Development
115
,
801
811
Xu
T.
,
Rubin
G. M.
(
1993
)
Analysis of genetic mosaics in developing and adult Drosophila tissues.
Development
117
,
1223
1237
Zecca
M.
,
Basler
K.
,
Struhl
G.
(
1995
)
Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing.
Development
121
,
2265
2278
This content is only available via PDF.