Short-range interaction between dorsal and ventral (D and V) cells establishes an organizing center at the DV compartment boundary that controls growth and specifies cell fate along the dorsal-ventral axis of the Drosophila wing. The secreted signaling molecule Wingless (Wg) is expressed by cells at the DV compartment boundary and has been implicated in mediating its long-range patterning activities. Here we show that Wg acts directly, at long range, to define the expression domains of its target genes, Distal-less and vestigial. Expression of the Achaete-scute genes, Distal-less and vestigial at different distances from the DV boundary is controlled by Wg in a concentration-dependent manner. We propose that Wg acts as a morphogen in patterning the D/V axis of the wing.
REFERENCES
REFERENCES
Axelrod
J. D.
, Matsuno
K.
, Artavanis-Tsakonas
S.
, Perrimon
N.
(1996
) Interaction between wingless and Notch signaling pathways mediated by Dishevelled.
Science
271
, 1826
–1832
Basler
K.
, Edlund
T.
, Jessell
T. M.
, Yamada
T.
(1993
) Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGF-family member.
Cell
73
, 687
–702
Basler
K.
, Struhl
G.
(1994
) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
Nature
368
, 208
–214
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
) Mechanisms 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.
(1994
) A role for the segment polarity gene shaggy-zeste white 3 in the specification of regional identity in the developing wing of Drosophila.
Dev Biol
162
, 229
–244
Brook
W. J.
, Cohen
S.M.
(1996
) Antagonistic interactionsbetween Wingless and Decapentaplegic responsible for dorsal-ventral pattern in the Drosophila leg.
Science
273
, 1373
–1377
Burke
R.
, Basler
K.
(1996
) Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing.
Development
122
, 2261
–2269
Capdevila
J.
, Guerrero
I.
(1994
) Targeted expression of the signalling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings.
EMBO J
13
, 4459
–4468
Cohen
B.
, Simcox
A. A.
, Cohen
S. M.
(1993
) Allocation of the thoracic imaginal disc primordia in the Drosophila embryo.
Development
117
, 597
–608
Couso
J. P.
, Bishop
S.
, Martinez Arias
A.
(1994
) The wingless signalling pathway and the patterning of the wing margin in Drosophila.
Development
120
, 621
–636
Couso
J. P.
, Knust
E.
, Martinez Arias
A.
(1995
) Serrate and wingless in Drosophila wing development.
Curr. Biol
5
, 1437
–1448
Diaz-Benjumea
F. J.
, Cohen
B.
, Cohen
S. M.
(1994
) Cell interactions between compartments establishes the proximal-distal axis of Drosophila limbs.
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
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
Fan
C. M.
, Porter
J. A.
, Chiang
C.
, Chang
D. T.
, Beachy
P. A.
, Tessier-Lavigne
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
Ghysen
A.
, O'Kane
C.
(1989
) Neural enhancer-like elements as markers of cell lineage.
Development
105
, 35
–52
Green
J. B. A.
, Smith
J. C.
(1992
) Responses of embryonic Xenopus cells to activin and FGF are separated by multiple dose thresholds and correspond to distinct axes of the mesoderm.
Cell
71
, 731
–739
Gurdon
J. B.
, Harger
P.
, Mitchell
A.
, Lemaire
P.
(1994
) Activin signalling and response to a morphogen gradient.
Nature
371
, 487
–492
Gurdon
J. B.
, Mitchell
A.
, Mahoney
D.
(1995
) Direct and continuous assessment by cells of their position in a morphogen gradient.
Nature
376
, 520
–521
Heemskerk
J.
, DiNardo
S.
(1994
) Drosophila hedgehog acts as a morphogen in cellular patterning.
Cell
76
, 449
–460
Hoppler
S.
, Bienz
M.
(1995
) Two different thresholds of wingless signalling with distinct developmental consequences in the Drosophila midgut.
EMBO J
14
, 5016
–5026
Ingham
P. W.
, Fietz
M. J.
(1995
) Quantitative effects of hedgehog and decapentaplegic activity on the patterning of the Drosophila wing.
Curr. Biol
5
, 432
–440
Irvine
K.
, Wieschaus
E.
(1994
) fringe, a boundary specific signalling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development.
Cell
79
, 595
–606
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 by Drosophila vestigial gene.
Nature
382
, 133
–138
Klingensmith
J.
, Nusse
R.
, Perrimon
N.
(1994
) The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal.
Genes Dev
8
, 118
–130
Lawrence
P. A.
, Struhl
G.
(1996
) Morphogens, compartments and pattern: lessons from Drosophila?.
Cell
85
, 951
–961
Lecuit
T.
, Brook
W. J.
, Ng
M.
, Calleja
M.
, Sun
H.
, Cohen
S. M.
(1996
) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing.
Nature
381
, 387
–393
Nellen
D.
, Burke
R.
, Struhl
G.
, Basler
K.
(1996
) Direct and long-range action of a Dpp morphogen gradient.
Cell
85
, 357
–368
Neumann
C. J.
, Cohen
S. M.
(1996
) Distinct mitogenic and cell fate specification functions of wingless in different regions of the wing.
Development
122
, 1781
–1789
Neumann
C. J.
, Cohen
S. M.
(1996
) A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing.
Development
122
, 3477
–3485
Neumann
C. J.
, Cohen
S. M.
(1996
) Sternopleural is a regulatory mutation of wingless with both dominant and recessive effects on larval development of Drosophila melanogaster.
Genetics
142
, 1147
–1155
Ng
M.
, Diaz-Benjumea
F. J.
, Vincent
J.-P.
, Wu
J.
, Cohen
S. M.
(1996
) Specification of the wing primordium in Drosophila.
Nature
381
, 316
–319
Noordermeer
J.
, Klingensmith
J.
, Perrimon
N.
, Nusse
R.
(1994
) dishevelled and armadillo act in the Wingless signalling pathway in Drosophila.
Nature
367
, 80
–83
Orsulic
S.
, Peifer
M.
(1996
) An in vivo structure-function study of armadillo, the-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and wingless signaling.
J. Cell Biol
134
, 1283
–1301
Peifer
M.
(1993
) The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction.
J. Cell Sci
105
, 993
–1000
Peifer
M.
, Rauskolb
C.
, Williams
M.
, Riggleman
B.
, Wieschaus
E.
(1991
) The segment polarity gene armadillo Interacts with the wingless signaling pathway in both embryonic and adult pattern formation.
Development
111
, 1029
–1043
Perrimon
N.
, Mahowald
A. P.
(1987
) Multiple functions of segment polarity genes in Drosophila.
Dev. Biol
119
, 587
–600
Phillips
R.
, Whittle
J. R. S.
(1993
) wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development.
Development
118
, 427
–438
Riddle
R. D.
, Johnson
R. L.
, Laufer
E.
, Tabin
C.
(1993
) sonic hedgehog mediates the polarizing activity of the ZPA.
Cell
75
, 1401
–1416
Roelink
H.
, Porter
J. A.
, Chiang
C.
, Tanabe
Y.
, Chang
D. T.
, Beachy
P.
, Jessell
T. M.
(1995
) Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis.
Cell
81
, 445
–455
Rulifson
E. J.
, Blair
S. S.
(1995
) Notch regulates wingless expression and is not required for reception of the paracrine wingless signal during wing margin neurogenesis in Drosophila.
Development
121
, 2813
–2824
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.
, Wilder
E.
, Perrimon
N.
(1994
) Components of wingless signalling in Drosophila.
Nature
376
, 76
–80
Skeath
J. B.
, Carroll
S. B.
(1991
) Regulation of Achaete-Scute gene expression and sensory organ pattern formation in the Drosophila wing.
Genes Dev
5
, 984
–995
Struhl
G.
, Basler
K.
(1993
) Organizing activity of wingless protein in Drosophila.
Cell
72
, 527
–540
Tabata
T.
, Kornberg
T.
(1994
) Hedgehog is a signalling protein with a key role in patterning Drosophila imaginal discs.
Cell
76
, 89
–102
Theisen
H.
, Purcell
J.
, Bennett
M.
, Kansagara
D.
, Syed
A.
, Marsh
J. L.
(1994
) dishevelled is required during wingless signalling to establish both cell polarity and cell identity.
Development
120
, 347
–360
van den Heuvel
M.
, Nusse
R.
, Johnston
P.
, Lawrence
P. A.
(1989
) Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication.
Cell
59
, 739
–749
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
Wilder
E. L.
, Perrimon
N.
(1995
) Dual functions of wingless in the Drosophila leg imaginal disc.
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 thedeveloping 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. Theoret. Biol
25
, 1
–47
Yanagawa
S.-I.
, van Leeuwen
F.
, Wodarz
A.
, Klingensmith
J.
, Nusse
R.
(1995
) The Dishevelled protein is modified by Wingless signaling in Drosophila.
Genes Dev
9
, 1087
–1097
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.
© 1997 by Company of Biologists
1997
