Mutations in the maternal-effect sterile gene mes-1 cause the offspring of homozygous mutant mothers to develop into sterile adults. Lineage analysis revealed that mutant offspring are sterile because they fail to form primordial germ cells during embryogenesis. In wild-type embryos, the primordial germ cell P4 is generated via a series of four unequal stem-cell divisions of the zygote. mes-1 embryos display a premature and progressive loss of polarity in these divisions: P0 and P1 undergo apparently normal unequal divisions and cytoplasmic partitioning, but P2 (in some embryos) and P3 (in most embryos) display defects in cleavage asymmetry and fail to partition lineage-specific components to only one daughter cell. As an apparent consequence of these defects, P4 is transformed into a muscle precursor, like its somatic sister cell D, and generates up to 20 body muscle cells instead of germ cells. Our results show that the wild-type mes-1 gene participates in promoting unequal germ-line divisions and asymmetric partitioning events and thus the determination of cell fate in early C. elegans embryos.

Reference

Adams
A. E. M.
,
Botstein
D.
,
Drubin
D. G.
(
1991
)
Requirement of yeast fimbrin for actin organization and morphogenesis in vivo.
Nature
354
,
404
408
Avery
L.
,
Horvitz
H. R.
(
1987
)
A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant.
Cell
51
,
1071
1078
Bardsley
A.
,
McDonald
K.
,
Boswell
R. E.
(
1993
)
Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on site of localization.
Development
119
,
207
219
Bossinger
O.
,
Schierenberg
E.
(
1992
)
Transfer and tissue-specific accumulation of cytoplasmic components in embryos of Caenorhabditis elegans and Rhabditis dolichura: in vivo analysis with a low-cost signal enhancement device.
Development
114
,
317
330
Boswell
R. E.
,
Mahowald
A. P.
(
1985
)
tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster.
Cell
43
,
97
104
Bowerman
B.
,
Eaton
B. A.
,
Priess
J. R.
(
1992
)
skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo.
Cell
68
,
1061
1075
Bowerman
B.
,
Draper
B. W.
,
Mello
C. C.
,
Priess
J. R.
(
1993
)
The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos.
Cell
74
,
443
452
Brenner
S.
(
1974
)
The genetics of Caenorhabditis elegans.
Genetics
77
,
71
94
Capowski
E. E.
,
Martin
P.
,
Garvin
C.
,
Strome
S.
(
1991
)
Identification of grandchildless loci whose products are required for normal germ-line development in the nematode Caenorhabditis elegans.
Genetics
129
,
1061
1072
Deppe
U.
,
Schierenberg
E.
,
Cole
T.
,
Krieg
C.
,
Schmitt
D.
,
Yoder
B.
,
von Ehrenstein
G.
(
1978
)
Cell lineages of the embryo of the nematode Caenorhabditis elegans.
Proc. Natl. Acad. Sci. USA
75
,
376
380
Ephrussi
A.
,
Dickinson
L. K.
,
Lehmann
R.
(
1991
)
oskar organizes the germ plasm and directs localization of the posterior determinant nanos.
Cell
66
,
37
50
Ephrussi
A.
,
Lehmann
R.
(
1992
)
Induction of germ cell formation by oskar.
Nature
358
,
387
392
Evans
T. C.
,
Crittenden
S. L.
,
Kodoyianni
V.
,
Kimble
J.
(
1994
)
Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo.
Cell
77
,
183
194
Fire
A.
,
Harrison
S. W.
,
Dixon
D.
(
1990
)
A modular set of lacZ fusionvectors for studying gene expression in Caenorhabditis elegans.
Gene
93
,
189
198
Fodor
A.
,
Deak
P.
(
1985
)
The isolation and genetic analysis of a Caenorhabditis elegans translocation (sZT1) strain bearing an X-chromosome balancer.
J. Genetics
64
,
143
157
Hay
B.
,
Ackerman
L.
,
Barbel
S.
,
Jan
L. Y.
,
Jan
Y. N.
(
1988
)
Identification of a component of Drosophila polar granules.
Development
103
,
625
640
Hill
D. P.
,
Strome
S.
(
1988
)
An analysis of the role of microfilaments in the establishment and maintenance of asymmetry in Caenorhabditis elegans zygotes.
Dev. Biol
125
,
75
84
Hill
D. P.
,
Strome
S.
(
1990
)
Brief cytochalasin-induced disruption of microfilaments during a critical interval in 1-cell C. elegans embryos alters the partitioning of developmental instructions to the 2-cell embryo.
Development
108
,
159
172
Hutter
H.
,
Schnabel
R.
(
1994
)
glp-1 and inductions establishing embryonic axes in C. elegans.
Development
120
,
2051
2064
Kemphues
K. J.
,
Priess
J. R.
,
Morton
D. G.
,
Cheng
N.
(
1988
)
Identification of genes required for cytoplasmic localization in early C. elegans embryos.
Cell
52
,
311
320
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.
(
1991
)
The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo.
Development
112
,
679
691
Lehmann
R.
(
1992
)
Germ-plasm formation and germ-cell determination in Drosophila.
Curr. Opin. Genet. Dev
2
,
543
549
Lillie
S. H.
,
Brown
S. S.
(
1994
)
Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae.
J. Cell Biol
125
,
825
842
McKim
K. S.
,
Howell
A. M.
,
Rose
A. M.
(
1988
)
The effects of translocations on recombination frequency in Caenorhabditis elegans.
Genetics
120
,
987
1001
Mello
C. C.
,
Draper
B. W.
,
Krause
M.
,
Weintraub
H.
,
Priess
J. R.
(
1992
)
The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos.
Cell
70
,
163
176
Mello
C. C.
,
Draper
B. W.
,
Priess
J. R.
(
1994
)
The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo.
Cell
77
,
95
106
Miller
D. M.
,
Ortiz
I.
,
Berliner
G. C.
,
Epstein
H. F.
(
1983
)
Differential localization of two myosins within nematode thick filaments.
Cell
34
,
477
490
Morton
D. G.
,
Roos
J. M.
,
Kemphues
K. J.
(
1992
)
par-4, a gene required for cytoplasmic localization and determination of specific cell types in Caenorhabditis elegans embryogenesis.
Genetics
130
,
771
790
Okkema
P. G.
,
Harrison
S. W.
,
Plunger
V.
,
Aryana
A.
,
Fire
A.
(
1993
)
Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans.
Genetics
135
,
385
404
Palmer
R. E.
,
Sullivan
D. S.
,
Huffaker
T.
,
Koshland
D.
(
1992
)
Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae.
J. Cell Biol
119
,
583
593
Priess
J. R.
,
Schnabel
H.
,
Schnabel
R.
(
1987
)
The glp-1 locus and cellular interactions in early C. elegans embryos.
Cell
51
,
601
611
Priess
J. R.
,
Thomson
J. N.
(
1987
)
Cellular interactions in early C. elegans embryos.
Cell
48
,
241
250
Schnabel
R.
(
1994
)
Autonomy and nonautonomy in cell fate specification of muscle in the Caenorhabditis elegans embryo: a reciprocal induction.
Science
263
,
1449
1452
Strome
S.
,
Wood
W. B.
(
1982
)
Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans.
Proc. Natl. Acad. Sci. USA
79
,
1558
1562
Strome
S.
,
Wood
W. B.
(
1983
)
Generation of asymmetry andsegregation of germ-line granules in early C. elegans embryos.
Cell
35
,
15
25
Strome
S.
(
1993
)
Determination of cleavage planes.
Cell
72
,
3
6
Sulston
J. E.
,
Horvitz
H. R.
(
1977
)
Post-embryonic cell lineages of the nematode, Caenorhabditis elegans.
Dev. Biol
56
,
110
156
Sulston
J. E.
,
White
J. G.
(
1980
)
Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans.
Dev. Biol
78
,
577
597
Sulston
J. E.
,
Schierenberg
E.
,
White
J. G.
,
Thomson
J. N.
(
1983
)
The embryonic cell lineage of the nematode Caenorhabditis elegans.
Dev. Biol
100
,
64
119
Wang
C.
,
Lehmann
R.
(
1991
)
Nanos is the localized posterior determinant in Drosophila.
Cell
66
,
637
647
Wilson
J. E.
,
Macdonald
P. M.
(
1993
)
Formation of germ cells in Drosophila.
Curr. Opin. Genet. Dev
3
,
562
565
Wolf
N.
,
Priess
J.
,
Hirsh
D.
(
1983
)
Segregation of germline granules in early embryos of Caenorhabditis elegans: an electron microscopic analysis.
J. Embryol. Exp. Morph
73
,
297
306
Yochem
J.
,
Greenwald
I.
(
1989
)
glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins.
Cell
58
,
553
563
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