In Drosophila, the Hox gene Ultrabithorax (Ubx) specifies the development of two different metameres--parasegment 5, which is entirely thoracic, and parasegment 6, which includes most of the first abdominal segment. Here we investigate how a single Hox gene can specify two such different morphologies. We show that, in the early embryo, cells respond similarly to UBX protein in both parasegments. The differences between parasegments 5 and 6 can be explained by the different spatial and temporal pattern of UBX protein expression in these two metameres. We find no evidence for multiple threshold responses to different levels of UBX protein. We examine in particular the role of Ubx in limb development. We show that UBX protein will repress limb primordia before 7 hours, when Ubx is expressed in the abdomen, but not later, when UBX is first expressed in the T3 limb primordium. The regulation of one downstream target of UBX, the Distalless gene, provides a model for this transition at the molecular level.

Reference

Akam
M. E.
(
1983
)
The location of Ultrabithorax transcripts in Drosophila tissue sections.
EMBO J
2
,
2075
2084
Artero
R. D.
,
Akam
M.
,
Perez-Alonso
M.
(
1992
)
Oligonucleotide probes detect splicing variants in situ in Drosophila embryos.
Nucleic Acid Res
20
,
5687
5690
Beachy
P. A.
,
Helfand
S. L.
,
Hogness
D. S.
(
1985
)
Segmental distribution of Bithorax complex proteins during Drosophila development.
Nature
313
,
545
551
Bender
W.
,
Akam
M.
,
Karch
F.
,
Beachy
P. A.
,
Peifer
M.
,
Spierer
P.
,
Lewis
E.B.
,
Hogness
D. S.
(
1983
)
Molecular genetics of the Bithorax complex in Drosophila melanogaster.
Science
221
,
23
29
Blochinger
K.
,
Bodmer
R.
,
Jan
L. Y.
,
Jan
Y. N.
(
1990
)
Patterns of expression of Cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos.
Genes Dev
4
,
1322
1331
Busturia
A.
,
Vernos
I.
,
Macías
A.
,
Casanova
J. A.
,
Morata
G.
(
1990
)
Different forms of Ultrabithorax proteins generated by alternative splicing are functionally equivalent.
EMBO J
9
,
3551
3555
Carroll
S. B.
,
DiNardo
S.
,
O'Farrell
P. H.
,
White
R. A.
,
Scott
M. P.
(
1988
)
Temporal and spatial relationships between segmentation and homeotic gene expression in Drosophila embryos: distributions of the fushi tarazu, engrailed, Sex combs reduced, Antennapedia, and Ultrabithorax proteins.
Genes Dev
2
,
350
60
Castelli-Gair
J.
,
Greig
S.
,
Micklem
G.
,
Akam
M.
(
1994
)
Dissecting the temporal requirements for homeotic gene function.
Development
120
,
1983
1995
Cohen
S. M.
(
1990
)
Specification of limb development in the Drosophila embryo by positional cues from segmentation genes.
Nature
343
,
173
177
Cohen
B.
,
Simcox
A. A.
,
Cohen
S. M.
(
1993
)
Allocation of the thoracic imaginal primordia in the Drosophila embryo.
Development
117
,
597
608
Cohen
S. M.
,
Jurgens
G.
(
1989
)
Proximal-distal pattern fomation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development.
EMBO J
8
,
2045
2055
Dambly-Chaudiere
C.
,
Ghysen
A.
(
1987
)
Independent subpatterns ofsense organs require independent genes of the achaete-scute complex in Drosophila larvae.
Genes Dev
1
,
297
306
Dambly-Chaudiere
C.
,
Jamet
E.
,
Burri
M.
,
Bopp
D.
,
Basler
K.
,
Hafen
E.
,
Dumont
N.
,
Spielmann
P.
,
Ghysen
A.
,
Noll
M.
(
1992
)
The paired box gene pox neuro: a determinant of poly-innervated sense organs in Drosophila.
Cell
69
,
159
172
Duncan
I.
(
1987
)
The Bithorax complex.
Ann. Rev. Genet
21
,
285
319
Gibson
G.
,
Gehring
W. J.
(
1988
)
Head and thoracic transformations caused by ectopic expression of Antennapedia during Drosophila development.
Development
102
,
657
675
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
González-Reyes
A.
,
Urquía
N.
,
Gehring
W.
,
Struhl
G.
,
Morata
G.
(
1990
)
Are cross regulatory interactions between homeotic genes functionally significant?.
Nature
344
,
78
80
Hafen
E.
,
Levine
M.
,
Gehring
W. J.
(
1984
)
Regulation of Antennapedia transcript distribution by the Bithorax complex in Drosophila.
Nature
307
,
287
289
Heuer
J. G.
,
Kaufman
T. C.
(
1992
)
Homeotic genes have specific funcional roles in the establishment of the Drosophila embryonic peripheral nervous system.
Development
115
,
35
47
Irvine
K. D.
,
Helfand
S. L.
,
Hogness
D. S.
(
1991
)
The large upstream control region of the Drosophila homeotic gene Ultrabithorax.
Development
111
,
407
424
Irvine
K. D.
,
Botas
J.
,
Jha
S.
,
Mann
R. S.
,
Hogness
D. S.
(
1993
)
Negative autoregulation by Ultrabithorax controls the level and pattern of its expression.
Development
117
,
387
399
Kaufman
T. C.
,
Lewis
R.
,
Wakimoto
B.
(
1980
)
Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homeotic gene complex in polytene chromosome interval 84 A-B.
Genetics
94
,
115
133
Keilin
D.
(
1911
)
Sur certaines organes sensitifs constants chez les larves de Dipteres et leur signification probable. C.R. Hebd. Seances Acad.
Sci
153
,
977
979
Kelsh
R.
,
Weinzierl
R. O. J.
,
White
R. A. H.
,
Akam
M.
(
1994
)
Homeotic gene expression in the locust Schistocerca: an antibody that detects conserved epitopes in Ultrabithorax and abdominal-A proteins.
Dev. Genet
15
,
19
31
Kornfeld
K.
,
Saint
R. B.
,
Beachy
P. A.
,
Harte
P. J.
,
Peattie
D. A.
,
Hogness
D. S.
(
1989
)
Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila.
Genes Dev
3
,
243
258
Lawrence
P. A.
,
Morata
G.
(
1994
)
Homeobox genes: their function in Drosophila segmentation and pattern formation.
Cell
78
,
181
189
Lewis
E. B.
(
1978
)
A gene complex controlling segmentation in Drosophila.
Nature
276
,
565
570
Lopez
A. J.
,
Hogness
D. S.
(
1991
)
Immunochemical dissection of the Ultrabithorax homeoprotein family in Drosophila melanogaster.
Proc. Nat. Acad. Sci.USA
88
,
9924
9928
Mann
R. S.
(
1994
)
engrailed -mediated repression of Ultrabithorax is necessary for the parasegment 6 identity in Drosophila.
Development
120
,
3205
3212
Mann
R. S.
,
Hogness
D. S.
(
1990
)
Functional dissection of Ultrabithorax proteins in D. melanogaster.
Cell
60
,
597
610
Martínez Arias
A.
,
Lawrence
P. A.
(
1985
)
Parasegments and compartments in the Drosophila embryo.
Nature
313
,
639
642
Martínez Arias
A.
,
White
R. A. H.
(
1988
)
Ultrabithorax and engrailed expression in Drosophila embryos mutant for segmentation genes of the pair-rule class.
Development
102
,
325
338
Morata
G.
,
Kerridge
S.
(
1981
)
Sequential functions of the bithorax complex in Drosophila.
Nature
290
,
778
781
Muller
J.
,
Bienz
M.
(
1991
)
Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo.
EMBO J
10
,
3147
3155
O'Connor
M. B.
,
Binari
R.
,
Perkins
L. A.
,
Bender
W.
(
1988
)
Alternative RNA products from the Ultrabithorax domain of the bithorax complex.
EMBO J
7
,
435
445
O'Hara
E.
,
Cohen
B.
,
Cohen
S. M.
,
McGinnis
W.
(
1993
)
Distal-les is a downstream gene of Deformed required for ventral maxillary identity.
Development
117
,
847
856
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
Ray
R. P.
,
Arora
C.
,
Nusslein-Volhard
C.
,
Gelbart
W.
(
1991
)
Thecontrol of cell fate along the dorsal-ventral axis of the Drosophila embryo.
Development
113
,
35
54
Sánchez-Herrero
E.
,
Vernos
I.
,
Marco
R.
,
Morata
G.
(
1985
)
Genetic organisation of the Drosophila Bithorax complex.
Nature
313
,
108
113
Sato
T.
,
Denell
R. E.
(
1985
)
Homoeosis in Drosophila: anterior and posterior transformations of Polycomb lethal embryos.
Dev. Biol
110
,
53
64
Simon
J.
,
Chiang
A.
,
Bender
W.
,
Shimell
M. J.
,
O'Connor
M.
(
1993
)
Elements of the Drosophila Bithorax complex that mediate repression by Polycomb group products.
Dev. Biol
158
,
131
144
Simon
J.
,
Peifer
M.
,
Bender
W.
,
O'Connor
M. O.
(
1990
)
Regulatory elements of the Bithorax complex that control expression along the anterior-posterior axis.
EMBO J
9
,
3945
3956
Smolik-Utlaut
S. M.
(
1990
)
Dosage requirements of Ultrabithorax and bithoraxoid in the determination of segment identity in Drosophila melanogaster.
Genetics
124
,
357
66
St. Johnston
D.
,
Gelbart
W.
(
1987
)
Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo.
EMBO J
6
,
2785
2791
Struhl
G.
(
1981
)
A homeotic mutation transforming leg to antenna in Drosophila.
Nature
292
,
635
638
Struhl
G.
(
1982
)
Genes controlling segmental specification in the Drosophila thorax.
Proc. Natl. Acad. Sci. USA
79
,
7380
7384
Struhl
G.
,
White
R. A. H.
(
1985
)
Regulation of the Ultrabithorax gene of Drosophila by the other Bithorax complex genes.
Cell
43
,
507
519
Subramaniam
V.
,
Bomze
H. M.
,
Lopez
A. J.
(
1994
)
Functional differences between Ultrabithorax protein isoforms in Drosophila melanogaster—evidence from elimination, substitution and ectopic expression of specific isoforms.
Genetics
136
,
979
991
Tautz
D.
,
Pfeifle
C.
(
1989
)
A non-radioactive in situ hybridizationmethod for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
Chromosoma
98
,
81
85
Tiong
S.
,
Bone
L. M.
,
Whittle
J. R.
(
1985
)
Recessive lethal mutations within the bithorax complex in Drosophila.
Mol. Gen. Genet
200
,
335
42
Vachon
G.
,
Cohen
B.
,
Pfeifle
C.
,
McGuffin
M. E.
,
Botas
J.
,
Cohen
S. M.
(
1992
)
Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through target gene Distal-less.
Cell
71
,
437
450
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
Wakimoto
B. T.
,
Kaufman
T. C.
(
1981
)
Analysis of larval segmentation in lethal genotypes associated with the Antennapedia gene complex in Drosophilamelanogaster.
Dev. Biol
81
,
51
64
Wang
B. B.
,
Muller-Immergluck
M. M.
,
Austin
J.
,
Robinson
N. T.
,
Chisholm
A.
,
Kenyon
C.
(
1993
)
A homeotic gene cluster patterns the anteroposterior body axis of C. elegans.
Cell
74
,
29
42
White
R. A. H.
,
Wilcox
M.
(
1984
)
Protein products of the Bithorax complex in Drosophila.
Cell
39
,
163
171
Zeng
W.
,
Andrew
D. J.
,
Mathies
L. D.
,
Horner
M. A.
,
Scott
M. P.
(
1993
)
Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity.
Development
118
,
339
352
Zhang
C.-C.
,
Muller
J.
,
Hoch
M.
,
Jäckle
H.
,
Bienz
M.
(
1991
)
Target sequences for hunchback in a control region conferring Ultrabithorax expression boundaries.
Development
113
,
1171
1179
This content is only available via PDF.