Arthropod appendages are thought to have evolved as outgrowths from the body wall of a limbless ancestor. Snodgrass, in his Principles of Insect Morphology (1935), proposed that, during evolution, expansion of the body wall would originate the base of the appendages, or coxopodite, upon which the most distal elements that represent the true outer limb, or telopodite, would develop. The homeobox gene Distal-less (Dll), which is required in the Drosophila appendages for development of distal regions, has been proposed to promote formation of telopodite structures above the evolutionary ground-state of non-limb or body wall. Here, we present evidence that another homeobox gene, extradenticle (exd), which is required for appropriate development of the trunk and the proximal parts of the appendages, represents a coxopodite gene. We show that exd function is eliminated from the distal precursors in the developing limb and remains restricted to proximal precursors throughout development. This elimination is important because, when ectopically expressed, exd prevents distal development and gives rise to truncated appendages lacking distal elements. Moreover, the maintenance of exd expression during larval stages, contrary to Dll, does not require the hedgehog (hh) signaling pathway, suggesting that the proximal regions of the appendages develop independently of hh function. Finally, we show that in the crustacean Artemia, exd and Dll are expressed in comparable patterns as in Drosophila, suggesting a conserved genetic mechanism subdividing the arthropod limb.

Reference

Basler
K.
,
Struhl
G.
(
1994
)
Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
Nature
368
,
208
214
Botas
J.
(
1993
)
Control of morphogenesis and differentiation by HOM/Hox genes.
Curr. Opin. Cell Biol
5
,
1015
1022
Brand
A. H.
,
Perrimon
N.
(
1993
)
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
Development
118
,
401
415
Bryant
P. J.
(
1988
)
Localized cell death caused by mutations in a Drosophila gene coding for a transforming growth factor-homolog.
Dev. Biol
128
,
386
395
Bryant
P. J.
,
Schneiderman
H. A.
(
1969
)
Cell lineage, growth and determination in the imaginal leg discs in Drosophila melanogaster.
Dev.Biol
20
,
263
290
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
1123
Cohen
S. M.
,
Brönner
G.
,
Kuttner
F.
,
Jurgens
G.
,
Jäckle
H.
(
1989
)
Distal-less encodes a homeodomain protein required for limb development in Drosophila.
Nature
338
,
432
434
Cohen
S. M.
,
Jurgens
G.
(
1989
)
Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development.
EMBO J
8
,
2045
2055
Cohen
B.
,
Simcox
A. A.
,
Cohen
S. M.
(
1993
)
Allocation of the thoracic imaginal primordia in the Drosophila embryo.
Development
117
,
597
608
Díaz-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
Gavrieli
Y.
,
Sherma
Y.
,
Ben-Sasson
S.A.
(
1992
)
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
J. Cell Biol
119
,
493
501
González-Crespo
S.
,
Morata
G.
(
1995
)
Control of Drosophila adult pattern by extradenticle.
Development
121
,
2117
2125
González-Reyes
A.
,
Morata
G.
(
1990
)
The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products.
Cell
61
,
515
522
Grim
S.
,
Pflugfelder
G. O.
(
1996
)
Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless.
Science
271
,
1601
1604
Halder
G.
,
Callaerts
P.
,
Gehring
W.J.
(
1995
)
Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila.
Science
267
,
1788
1792
Lawrence
P. A.
,
Morata
G.
(
1994
)
Homeobox genes: Their function in Drosophila segmentation and pattern formation.
Cell,
78
,
181
189
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
Mann
R. S.
,
Chan
S.
(
1996
)
Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins.
Trends in Genetics
12
,
258
262
McGinnis
W.
,
Krumlauf
R.
(
1992
)
Homeobox genes and axial patterning.
Cell
68
,
283
302
Mohler
J.
(
1988
)
Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila.
Genetics
120
,
1061
1072
Panganiban
G.
,
Sebring
A.
,
Nagy
L.
,
Carroll
S.
(
1995
)
The development of crustacean limbs and the evolution of arthropods.
Science
270
,
1363
1366
Patel
N. H.
(
1994
)
Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes.
Meth. in Cell Biol
44
,
445
487
Peifer
M.
,
Wieschaus
E.
(
1990
)
Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity.
Genes Dev
4
,
1209
1223
Rauskolb
C.
,
Peifer
M.
,
Wieschaus
E.
(
1993
)
extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogene pbx1.
Cell
74
,
1101
1112
Rauskolb
C.
,
Smith
K. M.
,
Peifer
M.
,
Wieschaus
E.
(
1995
)
extradenticle determines segmental identities throughout Drosophila development.
Development
121
,
3663
3673
Röder
L.
,
Vola
C.
,
Kerridge
S.
(
1992
)
The role of the teashirt gene in trunk segmental identity in Drosophila.
Development
115
,
1017
1033
Tabata
T.
,
Kornberg
T.
(
1994
)
Hedgehog is a signalling protein with a key role in patterning Drosophila imaginal discs.
Cell
76
,
89
102
Wilder
E. L.
,
Perrimon
N.
(
1995
)
Dual functions of wingless in the Drosophila leg imaginal disc.
Development
121
,
477
488
Wilson
D. S.
,
Desplan
C.
(
1995
)
Cooperating to be different.
Curr. Biol
5
,
32
34
This content is only available via PDF.