Cytoplasmic organization, nuclear migration, and nuclear division in the early syncytial Drosophila embryo are all modulated by the cytoskeleton. In an attempt to identify genes involved in cytoskeletal functions, we have examined a collection of maternal-effect lethal mutations induced by single P-element transposition for those that cause defects in nuclear movement, organization, or morphology during the syncytial embryonic divisions. We describe three mutations, grapes, scrambled, and nuclear-fallout, which define three previously uncharacterized genes. Females homozygous for these mutations produce embryos that exhibit extensive mitotic division errors only after the nuclei migrate to the surface. Analysis of the microfilament and microtubule organization in embryos derived from these newly identified mutations reveal disruptions in the cortical cytoskeleton. Each of the three mutations disrupts the actin-based pseudocleavage furrows and the cellularization furrows in a distinct fashion. In addition to identifying new genes involved in cytoskeletal organization, these mutations provide insights into cytoskeletal function during early Drosophila embryogenesis.

Bakken
A. H.
(
1973
)
A cytological and genetic study of oogenesis in Drosophila melanogaster.
Dev. Biol
33
,
100
122
Bier
E.
,
Vaessin
H.
,
Shepherd
S.
,
Lee
K.
,
McCall
S.
,
Barbel
S.
,
Ackerman
L.
,
Carretto
R.
,
Uemura
T.
,
Grell
E.
,
Jan
L. Y.
,
Jan
Y. N.
(
1989
)
Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector.
Genes Dev
3
,
1273
1287
Cooley
L.
,
Kelley
R.
,
Spradling
A.
(
1988
)
Insertional mutagenesis of the Drosophila genome with single P elements.
Science
239
,
1121
1128
Engels
W. R.
,
Preston
C. R.
,
Thompson
P.
,
Eggleston
W. B.
(
1986
)
In situ hybridization to Drosophila salivary chromosomes with biotinylated probes and alkaline phosphatase.
Focus
8
,
6
8
Erdelyi
M.
,
Szabad
J.
(
1989
).
Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. I. Mutations on the third chromosome.
Genetics
122
,
111
127
Foe
V. E.
,
Alberts
B. M.
(
1983
)
Studies of nuclear and cytoplasmic behavior during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis.
J. Cell Sci
61
,
31
70
Fryberg
E. A.
,
Goldstein
L. S. B.
(
1990
)
The Drosophila cytoskeleton.
Ann. Rev. Cell Biol
6
,
559
596
Gans
M.
,
Audit
C.
,
Masson
M.
(
1975
)
Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaster.
Genetics
81
,
683
704
Hatanaka
K.
,
Okada
M.
(
1991
)
Retarded nuclear migration in Drosophila embryos with aberrant F-actin reorganization caused by maternal mutations and by cytochalasin treatment.
Development
111
,
909
920
Hime
G.
,
Saint
R.
(
1992
)
Zygotic expression of the pebble locus is required for cytokinesis during the postblastoderm mitoses of Drosophila.
Development
114
,
165
171
Karpen
G. H.
,
Spradling
A. C.
(
1992
)
Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P-element insertional mutagenesis.
Genetics
132
,
737
757
Karr
T. L.
,
Alberts
B. M.
(
1986
)
Organization of the cytoskeleton in early Drosophila embryos.
J. Cell Biol
102
,
1494
1509
Karr
T. L.
(
1991
)
Intracellular sperm/egg interactions in Drosophila: A three-dimensional structural analysis of a paternal product in the developing egg.
Mech. Dev
34
,
101
111
Kellogg
D. R.
,
Mitchison
T. J.
,
Alberts
B. M.
(
1988
)
Behavior of microtubules and actin filaments in living Drosophila embryos.
Development
103
,
675
686
Kellogg
D. R.
,
Field
C. M.
,
Alberts
B. M.
(
1989
)
Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo.
J. Cell Biol
109
,
2977
2991
Merrill
P. T.
,
Sweeton
D.
,
Wieschaus
E.
(
1988
)
Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster.
Development
104
,
495
509
Miller
K.
,
Field
C. M.
,
Alberts
B. M.
(
1989
)
Actin binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatography.
J. Cell Biol
109
,
2963
2975
Minden
J. S.
,
Agard
D. A.
,
Sedat
J. W.
,
Alberts
B. M.
(
1989
)
Direct cell lineage analysis in Drosophila melanogaster by time lapse three dimensional optical microscopy of living embryos.
J. Cell Biol
109
,
505
516
Mitchison
T. J.
,
Sedat
J. W.
(
1983
)
Localization of antigenic determinants in whole Drosophila embryos.
Dev. Biol
99
,
261
264
Perrimon
N.
,
Mohler
D.
,
Engstrom
L.
,
Mahowald
A. P.
(
1986
)
X-linked female-sterile loci in Drosophila melanogaster.
Genetics
113
,
695
712
Perrimon
N.
,
Engstrom
L.
,
Mahowald
A. P.
(
1989
)
Zygotic lethals with specific maternal-effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome.
Genetics
121
,
333
352
Planques
V.
,
Warn
A.
,
Warn
R. M.
(
1991
)
The effects of microinjection of rhodamine-phallodin on mitosis and cytokinesis in early stage Drosophila embryos.
Exp. Cell Res
192
,
557
566
Postner
M. A.
,
Miller
K. G.
,
Weischaus
E.
(
1992
)
Maternal-effect mutations of the sponge locus affect cytoskeletal rearrangements in Drosophila melanogaster embryos.
J. Cell Biol
119
,
11205
1218
Rabinowitz
M.
(
1941
)
Studies on the cytology and early embryology of the egg of Drosophila melanogaster.
J. Morphol
69
,
1
49
Rice
T. B.
,
Garen
A.
(
1975
)
Localized defects of blastoderm formation in maternal-effect mutants of Drosophila.
Dev. Biol
43
,
277
286
Rose
L. S.
,
Wieschaus
E.
(
1992
)
The Drosophila cellularization gene nullo produces a blastoderm-specific transcript whose levels respond to the nucleocytoplasmic ratio.
Genes Dev
6
,
1255
1268
Sandler
L.
(
1977
)
Evidence for a set of closely linked autosomal genes that interact with sex-chromosome heterochromatin in Drosophila melanogaster.
Genetics
86
,
567
582
Schupbach
T.
,
Wieschaus
E.
(
1989
)
Female sterile mutations on thesecond chromosome of Drosophila melanogaster. I. Maternal-effect mutations.
Genetics
121
,
101
117
Schweisguth
F.
,
Lepesant
J. A.
,
Vincent
A.
(
1990
)
The serendipity alpha gene encodes a membrane associated protein required for the cellularization of the Drosophila embryo.
Genes Dev
4
,
922
931
Simpson
L.
,
Wieschaus
E.
(
1990
)
Zygotic activity of the nullo-locus is required to stabilize the actin-myosin network during cellularization in Drosophila.
Development
110
,
851
863
St. Johnston
D.
,
Beuchle
D.
,
Nusslein-Volhard
C.
(
1991
)
staufen, a gene required to localize maternal RNAs in the Drosophila egg.
Cell
66
,
51
63
Stafstrom
J. P.
,
Staehelin
L. A.
(
1984
)
Dynamics of the nuclear envelope and nuclear pore complexes during mitosis in the Drosophila embryo.
European Journal of Cell Biology
34
,
179
189
Sullivan
W.
(
1987
)
Independence of fushi tarazu expression with respect to cellular density in Drosophila embryos.
Nature
327
,
164
167
Sullivan
W.
,
Minden
J. M.
,
Alberts
B. M.
(
1990
)
daughterless-abo-like, a Drosophila maternal-effect mutation that exhibits abnormal centrosome separation during the late blastoderm divisions.
Development
110
,
311
323
Szabad
J.
,
Erdelyi
M.
,
Hoffmann
G.
,
Szidonya
J.
,
Wright
T. R. F.
(
1989
)
Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. II. Mutations on the second chromosome.
Genetics
122
,
823
835
Theurkauf
W.
(
1992
)
Behavior of structurally divergent alpha-tubulin isotypes during Drosophila embryogenesis: evidence for post-translational regulation of isotype abundance.
Dev. Biol
154
,
204
217
Turner
R. R.
,
Mahowald
A. P.
(
1977
)
Scanning electron microscopy of Drosophila melanogaster embryogenesis. I. The structure of the egg envelope and the formation of the cellular blastoderm.
Dev. Biol
50
,
95
108
Warn
R. M.
,
Magrath
R.
,
Webb
S.
(
1984
)
Distribution of F-actin during cleavage of the Drosophila syncytial blastoderm.
J. Cell Biol
98
,
156
162
Warn
R. M.
,
Smith
L.
,
Warn
A.
(
1985
)
Three distinct distributions of F-actin occur during the divisions of polar surface caps to produce pole cells in Drosophila embryos.
J. Cell Biol
100
,
1010
1015
Warn
R. M.
,
Warn
A.
(
1986
)
Microtubule arrays present during the syncytial and cellular blastoderm stages of the early Drosophila embryo.
Exp. Cell Res
163
,
201
210
Warn
R. N.
,
Flegg
L.
,
Warn
A.
(
1987
)
An investigation of microtubule organization and functions in living Drosophila embryos by injection of a fluorescently labeled antibody against tyrosinated tubulin.
J. Cell Biol
105
,
1721
1730
Wieschaus
E.
,
Sweeton
D.
(
1988
)
Requirements of X-linked zygotic gene activity during cellularization of early Drosophila embryos.
Development
104
,
483
493
Zalokar
M.
,
Audit
C.
,
Erk
I.
(
1975
)
Developmental defects of female-sterile mutants of Drosophila melanogaster.
Dev. Biol
47
,
419
432
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