All insect legs are structurally similar, characterized by five primary segments. However, this final form is achieved in different ways. Primitively, the legs developed as direct outgrowths of the body wall, a condition retained in most insect species. In some groups, including the lineage containing the genus Drosophila, legs develop indirectly from imaginal discs. Our understanding of the molecular mechanisms regulating leg development is based largely on analysis of this derived mode of leg development in the species D. melanogaster. The current model for Drosophila leg development is divided into two phases, embryonic allocation and imaginal disc patterning, which are distinguished by interactions among the genes wingless (wg), decapentaplegic (dpp) and distalless (dll). In the allocation phase, dll is activated by wg but repressed by dpp. During imaginal disc patterning, dpp and wg cooperatively activate dll and also indirectly inhibit the nuclear localization of Extradenticle (Exd), which divide the leg into distal and proximal domains. In the grasshopper Schistocerca americana, the early expression pattern of dpp differs radically from the Drosophila pattern, suggesting that the genetic interactions that allocate the leg differ between the two species. Despite early differences in dpp expression, wg, Dll and Exd are expressed in similar patterns throughout the development of grasshopper and fly legs, suggesting that some aspects of proximodistal (P/D) patterning are evolutionarily conserved. We also detect differences in later dpp expression, which suggests that dpp likely plays a role in limb segmentation in Schistocerca, but not in Drosophila. The divergence in dpp expression is surprising given that all other comparative data on gene expression during insect leg development indicate that the molecular pathways regulating this process are conserved. However, it is consistent with the early divergence in developmental mode between fly and grasshopper limbs.

Abu-Shaar
M.
,
Mann
R. S.
(
1998
)
Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development.
Development
125
,
3821
3830
Aspland
S. E.
,
White
R. A. H.
(
1997
)
Nucleocytoplasmic localisation of extradenticle protein is spatially regulated throughout development in Drosophila.
Development
124
,
741
747
Baker
N.
(
1988
)
Embryonic and imaginal requirements for wingless, a segment-polarity gene in Drosophila.
Dev. Biol
125
,
96
108
Baker
N. E.
(
1987
)
Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in the embryos.
EMBO J
6
,
1765
1773
Chang
W. S.
,
Zachow
K. R.
,
Bentley
D.
(
1993
)
Expression of epithelial alkaline phosphatase in segmentally iterated bands during grasshopper limb morphogenesis.
Development
118
,
651
663
Cohen
B.
,
Simcox
A. A.
,
Cohen
S. M.
(
1993
)
Allocation of the imaginal primordia in the Drosophila embryo.
Development
117
,
597
608
Cohen
S. M.
(
1990
)
Specification of limb development in the Drosophila embryo by positional cues from the segmentation genes.
Nature
343
,
173
177
Cohen
S. M.
,
Bronner
G.
,
Kuttner
F.
,
Jurgens
G.
,
Jackle
H.
(
1989
)
Distal-less encodes a homeodomain protein required for limb development in Drosophila.
Nature
338
,
432
434
Couso
J.P.
,
Bate
M.
,
Martinez-Ariaz
A.
(
1993
)
A wingless-dependent polar coordinate system in Drosophila imaginal discs.
Science
259
,
484
489
de Celis
J. F.
,
Tyler
D. M.
,
de Celis
J.
,
Bray
S. J.
(
1998
)
Notch signalling mediates segmentation of the Drosophila leg.
Development
125
,
4617
4628
Diaz-Benjumea
F. J.
,
Cohen
B.
,
Cohen
S. M.
(
1994
)
Cell interactions between compartments establishes the proximal-distal axis of Drosophila legs.
Nature
372
,
175
179
Driever
W.
,
Nusslein-Volhard
C.
(
1988
)
The bicoid protein determines position in the Drosophila embryo in a concentration dependent manner.
Cell
54
,
95
104
Ferguson
E. L.
,
Anderson
K. V.
(
1992
)
Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo.
Cell
71
,
451
461
Gonzalez-Crespo
S.
,
Morata
G.
(
1996
)
Genetic evidence for the subdivision of the arthropod limb into coxopodite and telopodite.
Development
122
,
3921
3928
Goto
S.
,
Hayashi
S.
(
1997
)
Specification of the embryonic limb primordium by graded activity of Decapentaplegic.
Development
124
,
125
132
Goto
S.
,
Hayashi
S.
(
1999
)
Proximal to distal cell communication in the Drosophila leg provides a basis for an intercalary mechanism of limb patterning.
Development
126
,
3407
3413
Ito
K.
,
Awano
W.
,
Suzuki
K.
,
Hiromi
Y.
,
Yamamoto
D.
(
1997
)
The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells.
Development
124
,
761
771
Jiang
J.
,
Struhl
G.
(
1996
)
Complementary and mutually exclusiveactivities of decapentaplegic and wingless organize axial patterning during Drosophila leg development.
Cell
86
,
401
409
Kolodkin
A. L.
,
Matthes
D. J.
,
O'Conner
T. P.
,
Patel
N. H.
,
Admon
A.
,
Bentley
D.
,
Goodman
C. S.
(
1992
)
Fasciclin IV: sequence, expression, and function during growth cone guidance in the grasshopper embryo.
Neuron
9
,
831
845
Lecuit
T.
,
Cohen
S. M.
(
1997
)
Proximal-distal axis formation in the Drosophila leg.
Nature
388
,
139
145
Masucci
J. D.
,
Miltenberger
R. J.
,
Hoffman
F. M.
(
1990
)
Pattern specific expression of the decapentaplegic gene in the imaginal discs is regulated by 3cis regulatory elements.
Genes Dev
4
,
2011
2023
Maxton-Kuchenmeister
J.
,
Handel
K.
,
Schmidt-Ott
U.
,
Roth
S.
,
Jäckle
H.
(
1999
)
Toll homolog expression in the beetle Tribolium suggests a different mode of dorsoventral patterning than in Drosophila embryos,.
Mechanisms of Development
83
,
107
114
Morata
G.
,
Sanchez-Herrero
E.
(
1999
)
Patterning mechanisms in the body trunk and the appendages of Drosophila. [Review].
Development
126
,
2823
2828
Nagy
L. M.
,
Carroll
S.
(
1994
)
Conservation of wingless patterning functions in the short-germ embryos of Triboliumcastaneum.
Nature
367
,
460
463
Newfeld
S. J.
,
Gelbart
W. M.
(
1995
)
Identification of two Drosophila TGF-family members in the grasshopper Schistocerca americana.
J. Mol. Evol
41
,
155
160
Niwa
N.
,
Saitoh
M.
,
Ohuchi
H.
,
Yoshioka
H.
,
Noji
S.
(
1997
)
Correlation between Distal-less expression patterns and structures of appendages in development of the two-spotted cricket, Gryllus bimaculatus.
Zool. Sci
14
,
115
125
Palopoli
M. F.
,
Patel
N. H.
(
1998
)
Evolution of the interaction between Hox genes and a downstream target.
Curr. Biol
8
,
587
590
Panganiban
G.
,
Nagy
L.
,
Carroll
S.
(
1994
)
The role of the Distal-less gene in the development and evolution of insect limbs.
Curr. Biol
4
,
671
675
Panganiban
G.
,
Sebring
A.
,
Nagy
L.M.
,
Carroll
S.
(
1995
)
The development of crustacean limbs and the evolution of arthropods.
Science
270
,
1363
1366
Panganiban
G.
,
Irvine
S.M.
,
Lowe
C.
,
Roehl
H.
,
Corley
L.S.
,
Sherbon
B.
,
Grenier
J.K.
,
Fallon
J.F.
,
Kimble
J.
,
Walker
M.
,
Wray
G.A.
,
Swalla
B.J.
,
Martindale
M.Q.
,
Carroll
S.B.
(
1997
)
The origin and evolution of animal appendages.
Proc. Natl. Acad. Sci. USA
94
,
5162
5166
Patel
N. H.
,
Kornberg
T. B.
,
Goodman
C. S.
(
1989
)
Expression of engrailed during segmentation in grasshopper and crayfish.
Development
107
,
201
212
Penton
A.
,
Hoffmann
F.
(
1996
)
Decapentaplegic restricts the domain of wingless during Drosophila limb patterning.
Nature
382
,
162
164
Rauskolb
C.
,
Irvine
K.
(
1999
)
Notch-mediated segmentation and growth control of the Drosophila leg.
Dev. Biol
210
,
339
350
Raz
E.
,
Shilo
B.
(
1993
)
Establishment of ventral cell fates in the Drosophila embryonic ectoderm requires DER, the EGF receptor homolog.
Genes Dev
7
,
1937
1948
Sanicola
M.
,
Sekelsky
J.
,
Elson
S.
,
Gelbart
W.
(
1995
)
Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed.
Genetics
139
,
745
756
Singer
M. A.
,
Hortsch
M.
,
Goodman
C. S.
,
Bentley
D.
(
1992
)
Annulin, a protein expressed at limb segment boundaries in the grasshopper embryo, is homologous to protein cross-linking transglutaminases.
Dev. Biol
154
,
143
159
Staehling-Hampton
K.
,
Jackson
P. D.
,
Clark
M. J.
,
Brand
A. H.
,
Hoffmann
F. M.
(
1994
)
Specificity of Bone Morphogenetic Protein-related factors: Cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A.
Cell Growth Differ
5
,
585
593
Theisen
H.
,
Haerry
T.
,
O'Connor
M.
,
Marsh
J.
(
1996
)
Developmental territories created by mutual antagonism between Wingless and Decapentaplegic.
Development
122
,
3939
3948
Truman
J. W.
,
Riddiford
L. M.
(
1999
)
The origins of insect metamorphosis.
Nature
401
,
447
452
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
Wolff
C.
,
Schroder
R.
,
Schulz
C.
,
Tautz
D.
,
Klingler
M.
(
1998
)
Regulation of the Tribolium homologues of caudal and hunchback in Drosophila: evidence for maternal gradient systems in a short germ embryo.
Development
125
,
3645
3654
Wu
J.
,
Cohen
S. M.
(
1999
)
Proximodistal axis formation in the Drosophila leg: subdivision into proximal and distal domains by Homothorax and Distal-less.
Development
126
,
109
117
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