Rows of cells that flank the parasegment boundary make up a signaling center within the epidermis of the Drosophila embryo. Signals emanating from these cells, encoded by hedgehog (hh) and wingless (wg), are shown to be required for all segment pattern dorsally. Wg activity is required for the differentiation of one cell type, constituting half the parasegment. The gene lines appears to act in parallel to the Wg pathway in the elaboration of this cell type. Hh activity is responsible for three other cell types in the parasegment. Some cell types are specified as Hh activity and interfere with the function of patched, analogous to patterning of imaginal discs. However, some pattern is independent of the antagonism of patched by Hh, and relies instead on novel interactions with lines. Lastly, we provide evidence that decapentaplegic does not mediate patterning by Hh in the dorsal epidermis.

Arora
K.
,
Levine
M. S.
,
O'Connor
M. B.
(
1994
)
The screw gene encodes a ubiquitously expressed member of the TGF-beta family required for specification of dorsal cell fates in the Drosophila embryo.
Genes Dev
8
,
2588
2601
Baker
N. E.
(
1987
)
Molecular cloning of sequences from wingless a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos.
EMBO J
6
,
1765
1773
Baker
N. E.
(
1988
)
Embryonic and imaginal requirements for wg, a segment polarity gene in Drosophila.
Dev. Biol
125
,
96
108
Basler
K.
,
Struhl
G.
(
1994
)
Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
Nature
368
,
208
214
Bejsovec
A.
,
Martinez Arias
A.
(
1991
)
Roles of wingless in patterning the larval epidermis of Drosophila.
Development
113
,
471
485
Bejsovec
A.
,
Wieschaus
E.
(
1993
)
Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos.
Development
119
,
501
517
Brand
A. H.
,
Perrimon
N.
(
1993
)
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
Development
118
,
401
415
Cabrera
C. V.
,
Alonso
M. C.
,
Johnston
P.
,
Phillips
R. G.
,
Lawrence
P. A.
(
1987
)
Phenocopies induced with antinsense RNA identify the wingless gene.
Cell
50
,
659
663
Campbell
G.
,
Weaver
T.
,
Tomlinson
A.
(
1993
)
Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless.
Cell
74
,
1113
23
Capdevila
J.
,
Estrada
M. P.
,
Sanchez
H. E.
,
Guerrero
I.
(
1994
)
The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development.
Embo Journal
13
,
71
82
Capdevila
J.
,
Guerrero
I.
(
1994
)
Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings.
EMBO J
13
,
4459
4468
Chakrabarti
A.
,
Matthews
G.
,
Colman
A.
,
Dale
L.
(
1992
)
Secretory and inductive properties of Drosophila wingless protein in Xenopus oocytes and embryos.
Development
115
,
355
369
Couso
J. P.
,
Bate
M.
,
Martinez Arias
A.
(
1993
)
A wingless-dependent polar coordinate system in Drosophila imaginal discs.
Science
259
,
484
–.
Couso
J. P.
,
Bishop
S. A.
,
Martinez Arias
A.
(
1994
)
The wingless signalling pathway and the patterning of the wing margin in Drosophila.
Development
120
,
621
636
Cumberledge
S.
,
Krasnow
M. A.
(
1993
)
Intercellular signalling in Drosophila segment formation reconstructed in vitro.
Nature
363
,
549
552
Diaz-Benjumea
F. J.
,
Cohen
B.
,
Cohen
S. M.
(
1994
)
Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs.
Nature
372
,
175
179
DiNardo
S.
,
Sher
E.
,
Heemskerk-Jongens
J.
,
Kassis
J. A.
,
O'Farrell
P. H.
(
1988
)
Two-tiered regulation of spatially patterned engrailed gene expression during drosophila embryogenesis.
Nature
332
,
604
609
Dougan
S. T.
,
DiNardo
S.
(
1992
)
wingless generates cell type diversity among engrailed expressing cells.
Nature
360
,
347
–.
Echelard
Y.
,
Epstein
D. P.
,
St-Jacques
B.
,
Shen
L.
,
Mohler
J.
,
McMahon
J. A.
,
McMahon
A. P.
(
1993
)
Sonic hedgehog, a member of a family of putative signaling molecules is implicated in the regulation of CNS polarity.
Cell
75
,
1417
1430
Fan
C. M.
,
Porter
J. A.
,
Chiang
C.
,
Chang
D. T.
,
Beachy
P. A.
,
Tessier
L. M.
(
1995
)
Long-range sclerotome induction by sonic hedgehog: direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway.
Cell
81
,
457
465
Fan
C. M.
,
Tessier-Lavigne
M.
(
1994
)
Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog.
Cell
79
,
1175
1186
Felsenfeld
A. L.
,
Kennison
J. A.
(
1995
)
Positional signaling by hedgehog in Drosophila imaginal disc development.
Development
121
,
1
10
Fietz
M. J.
,
Jacinto
A.
,
Taylor
A. M.
,
Alexandre
C.
,
Ingham
P. W.
(
1995
)
Secretion of the amino-terminal fragment of the Hedgehog protein is necessary and sufficient for hedgehog signaling in Drosophila.
Curr. Biol
5
,
643
650
Francis
P. H.
,
Richardson
M. K.
,
Brickell
P. M.
,
Tickle
C.
(
1994
)
Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb.
Development
120
,
209
218
Gonzalez
F.
,
Swales
L.
,
Bejsovec
A.
,
Skaer
H.
,
Martinez Arias
A.
(
1991
)
Secretion and movement of wingless protein in the epidermis of the Drosophila embryo.
Mech. Dev
35
,
43
54
Heberlein
U.
,
Singh
C. M.
,
Luk
A. Y.
,
Donohoe
T. J.
(
1995
)
Growth and differentiation in the Drosophila eye coordinated by hedgehog [see comments].
Nature
373
,
709
11
Heemskerk
J.
,
DiNardo
S.
(
1994
)
Drosophila hedgehog acts as a morphogen in cellular patterning.
Cell
76
,
449
460
Heemskerk
J.
,
DiNardo
S.
,
Kostriken
R.
,
O'Farrell
P. H.
(
1991
)
Multiple modes of engrailed regulation in the progression towards cell fate determination.
Nature
352
,
404
410
Hidalgo
A.
(
1994
)
Three distinct roles for the engrailed gene in Drosophila wing development.
Curr. Biol
4
,
1087
1098
Hooper
J. E.
,
Scott
A. M. P.
(
1989
)
The Drosophila patched gene encodes a putative membrane protein required for segmental patterning.
Cell
59
,
751
765
Ingham
P. W.
(
1993
)
Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo.
Nature
366
,
560
562
Ingham
P. W.
,
Hidalgo
A.
(
1993
)
Regulation of wingless transcription in the Drosophila embryo.
Development
117
,
283
291
Ingham
P.
,
Taylor
A.
,
Nakano
Y.
(
1991
)
Role of the Drosophila patched gene in positional signalling.
Nature
353
,
184
187
Irish
V. F.
,
Gelbart
W. M.
(
1987
)
The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo.
Genes Dev
1
,
868
879
Jackson
P. D.
,
Hoffmann
F. M.
(
1994
)
Embryonic expression patterns of the Drosophila decapentaplegic gene: separate regulatory elements control blastoderm expression and lateral ectodermal expression.
Dev. Dynam
199
,
28
44
Jiang
J.
,
Struhl
G.
(
1995
)
Protein kinase A and hedgehog signaling in Drosophila limb development.
Cell
80
,
563
572
Kassis
J. A.
,
Noll
E.
,
VanSickle
E. P.
,
Odenwald
W. F.
,
Perrimon
N.
(
1992
)
Altering the insertional specificity of a Drosophila transposable element.
Proc. Natl. Acad. Sci. USA
89
,
1919
1923
Krauss
S.
,
Concordet
J.-P.
,
Ingham
P. W.
(
1993
)
A functionally conserved homolog of the Drosophila segment polarity gene hedgehog is expressed in tissues with polarising activity in zebrafish embryos.
Cell
75
,
1431
1444
Lawrence
P. A.
,
Johnston
P.
,
Macdonald
P.
,
Struhl
G.
(
1987
)
Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and evenskipped genes.
Nature
328
,
440
442
Lee
J. J.
,
von Kessler
D. P.
,
Parks
S.
,
Beachy
P. A.
(
1992
)
Secreton and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog.
Cell
71
,
33
50
Lee
J. J.
,
Ekker
S. C.
,
von
K. D.
,
Porter
J. A.
,
Sun
B. I.
,
Beachy
P. A.
(
1994
)
Autoproteolysis in hedgehog protein biogenesis [see comments].
Science
266
,
1528
1537
Lepage
T.
,
Cohen
S. M.
,
Diaz
B. F.
,
Parkhurst
S. M.
(
1995
)
Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning [see comments].
Nature
373
,
711
715
Li
W.
,
Ohlmeyer
J. T.
,
Lane
M. E.
,
Kalderon
D.
(
1995
)
Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development.
Cell
80
,
553
62
Lohs-Schardin
M.
,
Cremer
C.
,
Nusslein-Volhard
C.
(
1979
)
A fate map of the larval epidermis of Drosophila melanogaster: Localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser beam.
Dev. Biol
73
,
239
255
Marti
E.
,
Bumcrot
D. A.
,
Takada
R.
,
McMahon
A. P.
(
1995
)
Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants [see comments].
Nature
375
,
322
5
Martinez Arias
A.
,
Baker
N. E.
,
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
McMahon
A. P.
,
Joyner
A. L.
,
Bradley
A.
,
McMahon
J. A.
(
1992
).
The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1- mice results from stepwise deletion of engrailed -expressing cells by 9.5 days postcoitum.
Cell
69
,
581
595
McMahon
A. P.
,
Moon
R. T.
(
1989
)
Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis.
Cell
58
,
1075
1084
Mohler
J.
(
1988
)
Requirements for hedgehog a segmental polarity gene in patterning larval and adult cuticle of drosophila.
Genetics
120
,
1061
1072
Mohler
J.
,
Vani
K.
(
1992
)
Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila.
Devel
115
,
957
971
Nakano
Y.
,
Guerrero
I.
,
Hidalgo
A.
,
Taylor
A.
,
Whittle
J. R. S.
,
Ingham
P. W.
(
1989
)
A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched.
Nature
341
,
508
513
Nusse
R.
,
Varmus
H. E.
(
1992
)
Wnt genes.
[Review]. Cell
69
,
1073
1087
Nusslein-Volhard
C.
,
Wieschaus
E.
(
1980
)
Mutations affecting segment number and polarity in Drosophila.
Nature
287
,
795
801
Padgett
R. W.
,
St. Johnston
R. D.
,
Gelbart
W. M.
(
1987
)
A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming frowth factor-β family.
Nature
325
,
81
84
Pan
D.
,
Rubin
G. M.
(
1995
)
cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal discs.
Cell
80
,
543
552
Patel
N. H.
,
Martin-Blanco
E.
,
Coleman
K. G.
,
Poole
S. J.
,
Ellis
M. C.
,
Kornberg
T. B.
,
Goodman
C. S.
(
1989
)
Expression of engrailed proteins in arthropods annelids and chordates.
Cell
58
,
955
968
Porter
J. A.
,
von
K. D.
,
Ekker
S. C.
,
Young
K. E.
,
Lee
J. J.
,
Moses
K.
,
Beachy
P. A.
(
1995
)
The product of hedgehog autoproteolytic cleavage active in local and long-range signalling.
Nature
374
,
363
366
Riddle
R.
,
Johnson
R. L.
,
Laufer
E.
,
Tabin
C.
(
1993
)
Sonic hedgehog mediates the polarizing activity of the ZPA.
Cell
75
,
1401
1416
Rijsewijk
F.
,
Scheurmann
M.
,
Wagenaar
E.
,
Parren
P.
,
Weigel
D.
,
Nusse
R.
(
1987
)
The Drosophila homolog of the mouse mammary oncogene int −1 is identical to the segment polarity gene wingless.
Cell
50
,
649
657
Roelink
H.
,
Augsburger
A.
,
Heemskerk
J.
,
Korzh
V.
,
Norlin
S.
,
Ruiz
i.
,
Altaba
A.
,
Tanabe
Y.
,
Placzek
M.
,
Edlund
T.
,
Jessell
T. M.
, et al. 
(
1994
)
Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord.
Cell
76
,
761
775
Staehling-Hampton
K.
,
Hoffmann
F. M.
,
Baylies
M. K.
,
Rushton
E.
,
Bate
M.
(
1994
)
dpp induces mesodermal gene expression in Drosophila.
Nature
372
,
783
786
Struhl
G.
,
Basler
K.
(
1993
)
Organizing activity of wingless protein in Drosophila.
Cell
72
,
527
540
Strutt
D. I.
,
Wiersdorff
V.
,
Mlodzik
M.
(
1995
)
Regulation of furrow progression in the Drosophila eye by cAMP-dependent protein kinase A [see comments].
Nature
373
,
705
709
Tabata
T. S. E.
,
Kornberg
T. B.
(
1992
)
The Drosophila hedgehog 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 signalling protein with a key role in patterning Drosophila imaginal discs.
Cell
76
,
89
102
Tautz
D.
,
Peifle
C.
(
1989
)
A non-radioactive in situ hybridization method for localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
Chromosoma
98
,
81
85
van den Heuvel
M.
,
Nusse
R.
,
Johnston
P.
,
Lawrence
P.
(
1989
)
Distribution of the wingless gene product in Drosophila embryos: A protein involved in cell-cell communication.
Cell
59
,
739
749
van der Meer
S.
(
1977
)
Optical clean and permanent whole mountpreparation for phase contrast microscopy of cuticular structures of insect larvae.
Dros. Inf. Serv
52
,
160
161
Wharton
K. A.
,
Ray
R. P.
,
Gelbart
W. M.
(
1993
)
An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo.
Development
117
,
807
822
Wharton
K. A.
,
Thomsen
G. H.
,
Gelbart
W. M.
(
1991
)
Drosophila 60A gene, another transforming growth factor beta family member, is closely related to human bone morphogenetic proteins.
Proc. Nat. Acad. Sci. USA
88
,
9214
9218
Wieschaus
E.
,
Riggleman
R.
(
1987
)
Autonomous requirements for the segment polarity gene armadillo during Drosophila embryogenesis.
Cell
49
,
177
184
Wilder
E.
,
Perrimon
N.
(
1995
)
Dual functions of wingless in the Drosophila leg imaginal disc.
Development
121
,
477
488
Zecca
M.
,
Basler
K.
,
Struhl
G.
(
1995
)
Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing.
Development
121
,
2265
2278
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