The establishment of the dorsal-ventral pattern in Drosophila embryos depends on a signal transduction process: a putative extracellular ligand released into the perivitelline space surrounding the embryo binds to the Toll receptor. Toll activation triggers the formation of the nuclear gradient of dorsal protein, the morphogen of the dorsal-ventral axis. Here, I analyse the dorsal protein distribution and the expression of zygotic dorsal-ventral genes in Toll- embryos that have been injected with wild-type cytoplasm under a variety of different injection conditions. Injections into two positions within a single embryo lead to the formation of two dorsal-ventral patterns in one embryo, allowing the analysis of interactions between pattern-forming processes. The results of single and double injections suggest that the spatial information for the embryonic dorsal-ventral axis is largely derived from spatial cues present in the extraembryonic compartment, which restrict the release of the putative Toll ligand. They argue against a Toll-dependent pattern-formation process employing local self-enhancement and lateral inhibition to enhance a weak initial asymmetry. The putative Toll ligand appears to originate from a ventrally restricted zone which extends along the entire anterior-posterior axis. Ligand diffusion or its graded release are required to determine the slope of the nuclear dorsal protein gradient. Both the Toll receptor and the putative ligand of Toll are in excess in wild-type embryos. Since spatial information for the embryonic dorsal-ventral axis is already present in the vitelline membrane or the perivitelline space, it is most likely generated during oogenesis. Oogenic pattern formation is also responsible for the perpendicular orientation the dorsal-ventral axis maintains with respect to the anterior-posterior axis.

REFERENCES

Anderson
K. V.
,
Jurgens
G.
,
Nusslein-Volhard
C.
(
1985
)
Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product.
Cell
42
,
779
789
Anderson
K.V.
,
Bokla
L.
,
Nusslein-Volhard
C.
(
1985
)
Establishment of dorsal-ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product.
Cell
42
,
791
798
Anderson
K. V.
,
Nusslein-Volhard
C.
(
1984
)
Information for the dorsal-ventral pattern of the Drosophila embryo is stored as maternal mRNA.
Nature
311
,
223
227
Casanova
J.
(
1991
)
Interaction between torso and dorsal, two elements of different transduction pathways in the Drosophila embryo.
Mechan. Dev
36
,
41
45
Chasan
R.
,
Anderson
K. V.
(
1989
)
The role of easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo.
Cell
56
,
391
400
Chasan
R.
,
Jin
Y.
,
Anderson
K. V.
(
1992
)
Activation of the easter zymogen is regulated by five other genes to define dorsal-ventral polarity in the Drosophila embryo.
Development
115
,
607
616
DeLotto
R.
,
Spierer
P.
(
1986
)
A gene required for the specification of dorsal-ventral pattern in Drosophila appears to encode a serine protease.
Nature
323
,
688
692
Frasch
M.
,
Hoey
T.
,
Rushlow
C.
,
Doyle
H.
,
Levine
M.
(
1987
)
1396Characterization and localization of the even-skipped protein in Drosophila embryogenesis.
EMBO J
6
,
749
759
Gierer
A.
,
Meinhardt
H.
(
1972
)
A theory of biological pattern formation.
Kybernetik
12
,
30
39
Govind
S.
,
Steward
R.
(
1991
)
Dorsoventral pattern formation in Drosophila: signal transduction and nuclear targeting.
Trends in Genet
7
,
119
125
Hashimoto
C.
,
Gertulla
S.
,
Anderson
K. V.
(
1991
)
Plasma membrane localization of the Toll protein in the syncytial Drosophila embryo: importance of transmembrane signaling for dorsal-ventral pattern formation.
Development
111
,
1021
1028
Hashimoto
C.
,
Hudson
K. L.
,
Anderson
K. V.
(
1988
)
The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein.
Cell
52
,
269
279
Horvitz
R. H.
,
Sternberg
P. W.
(
1991
)
Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva.
Nature
351
,
535
541
Ip
Y. T.
,
Kraut
R.
,
Levine
M.
,
Rushlow
C. A.
(
1991
)
The dorsal morphogen is a sequence-specific DNA-binding protein that interacts with a long-range repression element in Drosophila.
Cell
64
,
439
446
Jiang
J.
,
Kosman
D.
,
Ip
Y.T.
,
Levine
M.
(
1991
)
The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos.
Genes Dev
5
,
1881
1891
Kosman
D.
,
Ip
Y. T.
,
Levine
M.
,
Arora
K.
(
1991
)
Establishment of mesoderm-neuroectoderm boundary in the Drosophila embryo.
Science
254
,
118
122
Leptin
M.
(
1991
)
twist and snail as positive and negative regulators during Drosophila mesoderm development.
Genes Dev
5
,
1568
1576
Meinhardt
H.
(
1989
)
Models for positional signaling with application to the dorsoventral patterning of insects and segregation into different cell types.
Development
107
,
169
180
Meinhardt
H.
,
Gierer
A.
(
1980
)
Generation and regeneration of sequences of structures during morphogenesis.
J. Theor. Biol
85
,
429
450
Pan
D.
,
Huang
J.-D.
,
Courey
A. J.
(
1991
)
Functional analysis of the Drosophilatwist promotor reveals a dorsal -binding ventral activator region.
Genes Dev
5
,
1892
1901
Rao
Y.
,
Vaessin
H.
,
Jan
L. Y.
,
Jan
Y.-N.
(
1991
)
Neuroectoderm in Drosophila embryos is dependent on the mesoderm for positioning but not for formation.
Genes Dev
5
,
1577
1588
Ray
R. P.
,
Arora
K.
,
Nusslein-Volhard
C.
,
Gelbart
W.
(
1991
)
The control of cell fate along the dorsal-ventral axis of the Drosophila embryo.
Development
113
,
35
54
Roth
S.
,
Stein
D.
,
Nusslein-Volhard
C.
(
1989
)
A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo.
Cell
59
,
1189
1202
Rushlow
C. A.
,
Frasch
M.
,
Doyle
H.
,
Levine
M.
(
1987
)
Maternal regulation of zerknullt: a homeobox gene controlling differentiation of dorsal tissues in Drosophila.
Nature
330
,
583
586
Rushlow
C. A.
,
Han
K.
,
Manley
J. L.
,
Levine
M.
(
1989
)
The graded distribution of the dorsal morphogen is initiated by selective nuclear transport in Drosophila.
Cell
59
,
1165
1177
Santamaria
P.
,
Nusslein-Volhard
C.
(
1983
)
Partial rescue of dorsal, a maternal effect mutation affecting the dorso-ventral pattern of the Drosophila embryo, by the injection of wild-type cytoplasm.
EMBO J
2
,
1695
1699
Schneider
D. S.
,
Hudson
K. L.
,
Lin
T.-Y.
,
Anderson
K. V.
(
1991
)
Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo.
Genes Dev
5
,
797
807
Sprenger
F.
,
Nuusslein-Volhard
C.
(
1992
)
Torso receptor activity is regulated by a diffusible ligand produced at the extracellular terminal regions of the Drosophila egg.
Cell
71
,
987
1001
Sprenger
F.
,
Stevens
M.L.
,
Nusslein-Volhard
C.
(
1989
)
The Drosophila gene torso encodes a putative receptor tyrosine kinase.
Nature
338
,
478
483
Stein
D.
,
Nusslein-Volhard
C.
(
1992
)
Multiple extracellular activities in Drosophila egg perivitelline fluid are required for establishment of embryonic dorsal-ventral polarity.
Cell
68
,
429
440
Stein
D.
,
Roth
S.
,
Vogelsang
E.
,
Nusslein-Volhard
C.
(
1991
)
The polarity of the dorsoventral axis in the Drosophila embryo is defined by an extracellular signal.
Cell
65
,
725
735
Stevens
L.
,
Frohnhöfer
H.
,
Klingler
M.
,
Nusslein-Volhard
C.
(
1990
)
Localized requirement for torsolike expression in follicle cells for the development of terminal anlagen of the Drosophila embryo.
Nature
346
,
660
663
Steward
R.
(
1989
)
Relocalization of the dorsal protein from the cytoplasm to the nucleus correlates with its function.
Cell
59
,
1179
1188
Steward
R.
,
Zusman
S. B.
,
Huang
L. H.
,
Schedl
P.
(
1988
)
The dorsal protein is distributed in a gradient in early Drosophila embryos.
Cell
55
,
487
495
St Johnston
R. D.
,
Nusslein-Volhard
C.
(
1992
)
The origin of pattern and polarity in the Drosophila embryo.
Cell
68
,
1
20
Thisse
C.
,
Perrin-Schmitt
F.
,
Stoetzel
C.
,
Thisse
B.
(
1991
)
Sequence-specific transactivation of the Drosophila twist gene by the dorsal gene product.
Cell
65
,
1
20
Thisse
B.
,
Stoetzel
C.
,
Gorostiza-Thisse
C.
,
Perrin-Schmitt
F.
(
1988
)
Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos.
EMBO J
7
,
2175
2183
Thomas
J. B.
,
Crews
S. T.
,
Goodman
C. S.
(
1988
)
Molecular genetics of the single-minded locus: A gene involved in the development of the Drosophila nervous system.
Cell
52
,
133
141
Van der Meer
J. M.
(
1977
)
Optical clean and permanent whole mount preparations for phase-contrast microscopy of cuticular structures of insect larvae.
Dros. Info. Serv
52
,
160
–.
This content is only available via PDF.