Drosophila imaginal discs are divided into units called compartments. Cells belonging to the same compartment are related by lineage and express a characteristic set of ‘selector genes’. The borders between compartments act as organizing centres that influence cell growth within compartments. Thus, in the cells immediately anterior to the anterior-posterior compartment boundary the presence of the hedgehog product causes expression of decapentaplegic, which, in turn, influences the growth and patterning of the wing disc. The normal growth of the disc requires that posterior-specific genes, such as hedgehog and engrailed are not expressed in cells of the anterior compartment. Here we show that hedgehog can activate engrailed in the anterior compartment and that both hedgehog and engrailed are specifically repressed in anterior cells by the activity of the neurogenic gene groucho. In groucho mutant discs, hedgehog and engrailed are expressed at the dorsoventral boundary of the anterior compartment, leading to the ectopic activation of decapentaplegic and patched and to a localised increase in cell growth associated with pattern duplications. The presence of engrailed in the anterior compartment causes the transformation of anterior into posterior structures.
Reference
Artavanis-Tsakonas
S.
, Deledakis
C.
, Fehon
R. G.
(1991
) The Notch locus and the cell biology of neuroblast segregation.
Annu. Rev. Cell Biol
7
, 427
–452
Basler
K.
, Struhl
G.
(1994
) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
Nature
368
, 208
–214
Bate
C. M.
, Martinez Arias
A.
(1991
) The embryonic origin of imaginal discs in Drosophila.
Development
112
, 755
–761
Blair
S. S.
(1992
) engrailed expression in the anterior lineage compartment of the developing wing blade of Drosophila.
Development
115
, 21
–33
Blair
S. S.
(1992
) shaggy (zeste-white 3) and the formation of supernumerary bristle precursors in the developing wing blade of Drosophila.
Dev. Biol
152
, 263
–278
Blair
S. S.
(1993
) Mechanism of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila.
Development
119
, 339
–351
Blair
S. S.
, Brower
D. L.
, Thomas
J. B.
, Zabortink
M.
(1994
) The role of the apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila.
Development
120
, 1805
–1815
Blochinger
K.
, Jan
L. Y.
, Jan
Y. N.
(1993
) Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila.
Development
117
, 441
–450
Brower
D. L.
(1986
) engrailed expression in Drosophila imaginal discs.
EMBO J
5
, 2649
–2656
Busturia
A.
, Morata
G.
(1988
) Ectopic expression of homeotic genes caused by the elimination of the Polycomb gene in Drosophila imaginal epidermis.
Development
104
, 713
–720
Capdevila
J.
, Estrada
M. P.
, Sanchez-Herrero
E.
, Guerrero
I.
(1994
) The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development.
EMBO J
13
, 71
–82
Capdevila
J.
, Guerrero
I.
(1994
) Targeted expression of the signaling melecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings.
EMBO J
13
, 4459
–4468
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
de Celis
J. F.
, Garcia-Bellido
A.
(1994
) Roles of the Notch gene in Drosophila wing morphogenesis.
Mech. Dev
46
, 109
–122
Diaz-Benjumea
F.
, Cohen
S. M.
(1993
) Interactions between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila.
Cell
75
, 741
–752
Eaton
S.
, Kornberg
T. B.
(1990
) Repression of ci-D in posterior compartments by engrailed.
Genes Dev
4
, 1068
–1077
Felsenfeld
A. L.
, Kennison
J. A.
(1995
) Positional signalling by hedgehog in Drosophila imaginal disc development.
Development
121
, 1
–10
Garcia-Bellido
A.
, Ripoll
P.
, Morata
G.
(1973
) Developmental compartimentalisation of the wing disc of Drosophila.
Nature New Biol
245
, 251
–253
Garcia-Bellido
A.
, Santamaria
P.
(1972
) Developmental analysis of the wing disc in the mutant engrailed of Drosophila melanogaster.
Genetics
72
, 87
–104
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
Hartley
D. A.
, Preiss
A.
, Artavanis-Tsakonas
S.
(1988
) A deduced gene product from the Drosophila neurogenic locus Enhancer of split shows homology to mammalian G-proteinsubunit.
Cell
55
, 785
–795
Hidalgo
A.
(1994
) Three distinct roles for the engrailed gene in Drosophila wing development.
Curr. Biol
12
, 1087
–1098
Ingham
P. W.
, Hidalgo
A.
(1993
) Regulation of wingless transcription in the Drosophila embryo.
Development
117
, 283
–291
Jennings
B.
, Preiss
A.
, Delidakis
C.
, Bray
S.
(1994
) The Notch signalling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo.
Development
120
, 3537
–3548
Karlsson
J.
(1981
) The distribution of regenerative potential in the wing disc of Drosophila.
J. Embryol. Exp. Morphol
61
, 303
–316
Lawrence
P. A.
, Struhl
G.
(1982
) Further studies of the engrailed phenotype in Drosophila.
EMBO J
1
, 827
–833
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
, 3305
–3317
Lieber
T.
, Kidd
S.
, Alcamo
E.
, Corvin
V.
, Young
M. W.
(1993
) Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei.
Genes Dev
7
, 949
–1965
Paroush
Z.
, Finley
R.
, Kidd
T.
, Wainwright
S.
, Ingham
P.
, Brent
R.
, Ish-Horowick
D.
(1994
) groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with Hairy-related bHLH proteins.
Cell
79
, 805
–815
Posakony
L. G.
, Raftery
L. A.
, Gelbart
W. M.
(1991
) Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary.
Mech. Dev
33
, 69
–82
Preiss
A.
, Hartley
D. A.
, Artavanis-Tsakonas
S.
(1988
) The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Drosophila.
EMBO J
7
, 3917
–3927
Raftery
L. A.
, Sanicola
M.
, Blackman
R. K.
, Gelbart
W. M.
(1991
) The relationships of decapentaplegic and engrailed expression in Drosophila imaginal discs: do these genes mark the anterior-posterior compartment boundary?.
Development
113
, 27
–33
Ruiz-Gomez
M.
, Ghysen
A.
(1993
) The expression and role of a proneural gene, achaete, in the development of the larval nervous system of Drosophila.
EMBO J
12
, 1121
–1130
Sanicola
M.
, Sekelsky
J.
, Elson
S.
, Gelbart
W. M.
(1995
) Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed.
Genetics
139
, 745
–756
Schrons
H.
, Knust
E.
, Campos-Ortega
J. A.
(1992
) The Enhancer of split complex and adjacent genes in the 96F region of Drosophila melanogaster are required for segregation of neural and epidermal progenitor cells.
Genetics
132
, 481
–503
Schubiger
M.
, Palka
J.
(1987
) Changing spatial patterns of DNA replication in the developing wing of Drosophila.
Dev. Biol
123
, 145
–153
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
Simpson
P.
, El Messal
M.
, Moscoso del Prado
J.
, Ripoll
P.
(1988
) Stripes of positional homologies across the wing blade of Drosophila melanogaster.
Development
103
, 391
–401
Tabata
T.
, Eaton
S.
, Kornberg
T.
(1992
) The Drosophilahedhehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation.
Genes Dev
6
, 2635
–2645
Tabata
T.
, Kornberg
T. B.
(1994
) Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs.
Cell
76
, 89
–102
Tong
S. Y. K.
, Russell
M. A.
(1990
) Clonal analysis of segmental and compartmental homoeotic transformations in polycomb mutants of Drosophila melanogaster.
Dev. Biol
2
, 306
–318
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
This content is only available via PDF.
© 1995 by Company of Biologists
1995
-JournalMeeting.png?versionId=3773)
(update)-ImmuneSI.png?versionId=3773)
-GSWorkshop.png?versionId=3773)
(update)-InPreprints.png?versionId=3773)
-FocalPlaneNetworkLaunch.png?versionId=3773)
