After the onset of gastrulation, the Drosophila germband undergoes a morphological change in which its length along the anterior-posterior axis increases over two-and-a-half fold while its width along the dorsal-ventral axis simultaneously narrows. The behavior of individual cells during germband extension was investigated by epi-illumination and time-lapse video microscopy of living embryos. Cells intercalate between their dorsal and ventral neighbors during extension, increasing the number of cells along the anterior-posterior axis while decreasing the number of cells along the dorsal-ventral axis. Mutations that reduce segmental subdivision of the embryo along the anterior-posterior axis decrease both germband extension and its associated cell intercalation. In contrast, cell intercalation and germband extension are still detected in embryos that lack dorsal-ventral polarity. Characterization of germband extension and cell intercalation in mutant embryos with altered segmentation gene expression indicates that these processes are regionally autonomous and are dependent upon the establishment of striped expression patterns for certain pair-rule genes. Based on these observations, we propose a model for germband extension in which cell intercalation results from the establishment of adhesive differences between stripes of cells by pair-rule genes.

REFERENCES

Bejsovec
A.
,
Wieschaus
E.
(
1993
)
Segment polarity gene interactions modulate epidermal patterning in Drosophila embryos.
Development
119
,
501
517
Carroll
S. B.
,
Scott
M. P.
(
1985
)
Localization of the fushi tarazu protein during Drosophila embryogenesis.
Cell
43
,
47
57
Carroll
S. B.
,
Scott
M. P.
(
1986
)
Zygotically active genes that affect the spatial expression of the fushitarazu segmentation gene during early Drosophila embryogenesis.
Cell
45
,
113
126
Carroll
S. B.
,
Vavra
S. H.
(
1989
)
The zygotic control of Drosophila pair-rule gene expression. II. Spatial repression by gap and pair-rule gene products.
Development
107
,
673
683
Crews
S. T.
,
Thomas
J. B.
,
Goodman
C. S.
(
1988
)
The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product.
Cell
52
,
143
151
DiNardo
S.
,
Kuner
J. M.
,
Theis
J.
,
O'Farrell
P. H.
(
1985
)
Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein.
Cell
43
,
59
69
Driever
W.
,
Nusslein-Volhard
C.
(
1988
)
The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner.
Cell
54
,
95
104
Edgar
B. A.
,
O'Farrell
P. H.
(
1989
)
Genetic control of cell division patterns in the Drosophila embryo.
Cell
57
,
177
187
Ettensohn
C. A.
(
1985
)
Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells.
Dev. Biol
112
,
383
390
Foe
V. E.
(
1989
)
Mitotic domains reveal early commitment of cells in Drosophila embryos.
Development
107
,
1
22
Frasch
M.
,
Hoey
T.
,
Rushlow
C.
,
Doyle
H.
,
Levine
M.
(
1987
)
Characterization and localization of the even-skipped protein of Drosophila.
EMBO J
6
,
749
759
Frasch
M.
,
Levine
M.
(
1987
)
Complementary patterns of even-skipped and fushi tarazu expression involve their differential regulation by a common set of segmentation genes in Drosophila.
Genes Dev
1
,
981
995
Fristrom
D.
(
1988
)
The cellular basis of epithelial morphogenesis.
A review. Tissue & Cell
20
,
645
690
Gaul
U.
,
Jäckle
H.
(
1989
)
Analysis of maternal effect mutant combinations elucidates regulation and function of the overlap of hunchback and Kruppel gene expression in the Drosophila blastoderm embryo.
Development
107
,
651
662
Gergen
J. P.
,
Coulter
D.
,
Wieschaus
E.
(
1986
)
Segmental pattern and blastoderm cell identities.
Symp. Soc. Dev. Biol
43
,
195
220
Guthrie
S.
,
Prince
V.
,
Lumsden
A.
(
1993
)
Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts.
Development
118
,
527
538
Ingham
P.
,
Gergen
P.
(
1988
)
Interactions between the pair-rule genes runt, hairy, even-skipped and fushi tarazu and the establishment of periodic pattern in the Drosophila embryo.
Development
104
,
51
60
Ingham
P. W.
(
1988
)
The molecular genetics of embryonic pattern formation in Drosophila.
Nature
335
,
25
34
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
Jacobson
A. G.
,
Gordon
R.
(
1976
)
Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation.
J. Exp. Zool
197
,
191
246
Keller
R. E.
(
1978
)
Time lapse cinematographic analysis of superficial cell behavior during and prior to gastrulation in Xenopus laevis.
J. Morph
157
,
223
247
Keller
R.
(
1987
)
Cell rearrangement in morphogenesis.
Zool. Sci
4
,
763
779
Klingler
M.
,
Gergen
J. P.
(
1993
)
Regulation of runt transcription by Drosophila segmentation genes.
Mech. Dev
43
,
3
19
Lawrence
P. A.
,
Johnston
P.
,
Macdonald
P.
,
Struhl
G.
(
1987
)
Borders of parasegments in Drosophila embryos are delimited by the fushi tarazu and even-skipped genes.
Nature
328
,
440
442
Lehmann
R.
,
Nusslein-Volhard
C.
(
1986
)
Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila.
Cell
47
,
141
152
Lehmann
R.
,
Nusslein-Volhard
C.
(
1987
)
hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo.
Dev. Biol
119
,
402
417
Lehmann
R.
(
1988
)
Phenotypic comparisons between maternal and zygoticgenes controlling the segmental pattern of the Drosophila embryo.
Development
104
,
17
27
Leptin
M.
,
Grunewald
B.
(
1990
)
Cell shape changes during gastrulation in Drosophila.
Development
104
,
73
84
Manoukian
A. S.
,
Krause
H. M.
(
1992
)
Concentration-dependent activities of the even-skipped protein in Drosophila embryos.
Genes Dev
6
,
1740
1751
Martinez Arias
A.
(
1985
)
The development of fused embryos of Drosophila melanogaster.
J. Embryol. Exp. Morphol
87
,
99
114
Merrill
P. T.
,
Sweeton
D.
,
Wieschaus
E.
(
1988
)
Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster.
Development
104
,
495
509
Nusslein-Volhard
C.
(
1979
)
Maternal effect mutations that alter the spatial coordinates of the embryo of Drosophila melanogaster.
Symp. Soc. Dev. Biol
37
,
185
211
Nusslein-Volhard
C.
,
Wieschaus
E.
(
1980
)
Mutations affecting segment number and polarity in Drosophila.
Nature
287
,
795
801
Nusslein-Volhard
C.
,
Frohnhofer
H. G.
,
Lehmann
R.
(
1987
)
Determination of anteroposterior polarity in Drosophila.
Science
238
,
1675
1681
Patel
N. H.
,
Martin
B. E.
,
Coleman
K. G.
,
Poole
S. J.
,
Ellis
M. C.
,
Kornberg
T. B.
,
Goodman
C. S.
(
1989
)
Expression of engrailed proteins in arthropods, annelids, and chordates.
Cell
58
,
955
968
Perrimon
N.
,
Mahowald
A. P.
(
1987
)
Multiple functions of segment polarity genes in Drosophila.
Dev. Biol
119
,
587
600
Rice
T. B.
,
Garen
A.
(
1975
)
Localized defects of blastoderm formation in maternal effect mutants of Drosophila.
Dev. Biol
43
,
277
286
Rickoll
W. L.
(
1976
)
Cytoplasmic continuity between embryonic cells and the primitive yolk sac during early gastrulation in Drosophila melanogaster.
Dev. Biol
49
,
304
310
Roth
S.
,
Hiromi
Y.
,
Godt
D.
,
Nusslein-Volhard
C.
(
1991
)
cactus, a maternal gene required for proper formation of the dorsal-ventral morphogen gradient in Drosophila embryos.
Development
112
,
371
388
Schupbach
T.
(
1987
)
Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster.
Cell
49
,
699
707
Simpson
P.
(
1983
)
Maternal-zygotic gene interactions during formation of the dorsal-ventral pattern in Drosophila embryos.
Genetics
105
,
615
632
St. Johnston
R. D.
,
Gelbart
W. M.
(
1987
)
decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo.
EMBO J
6
,
2785
2791
Steinberg
M. S.
(
1962
)
On the mechanism of tissue reconstruction by dissociated cells. III. Free energy relations and the reorganization of fused heteronomic tissue fragments.
Proc. Natl. Acad. sci. USA
48
,
1769
1776
Struhl
G.
,
Struhl
K.
,
Macdonald
P. M.
(
1989
)
The gradient morphogen bicoid is a concentration-dependent transcriptional activator.
Cell
57
,
1259
1273
Warga
R. M.
,
Kimmel
C. B.
(
1990
)
Cell movement during epiboly and gastrulation in zebrafish.
Development
108
,
569
580
Warrior
R.
,
Levine
M.
(
1990
)
Dose-dependent regulation of pair-rule stripes by gap proteins and the initiation of segment polarity.
Development
110
,
759
767
Wieschaus
E.
,
Nusslein-Volhard
C.
,
Kluding
H.
(
1984
)
Kruppel, a gene whose activity is required early in the zygotic genome for normal embryonic segmentation.
Dev. Biol
104
,
172
186
Zusman
S. B.
,
Wieschaus
E. F.
(
1985
)
Requirements for zygotic gene activity during gastrulation in Drosophila melanogaster.
Dev. Biol
111
,
359
371
This content is only available via PDF.