The early Caenorhabditis elegans embryo divides with a stereotyped pattern of cleavages to produce cells that vary in developmental potential. Differences in cleavage plane orientation arise between the anterior and posterior cells of the 2-cell embryo as a result of asymmetries in centrosome positioning. Mechanisms that position centrosomes are thought to involve interactions between microtubules and the cortex, however, these mechanisms remain poorly defined. Interestingly, in the early embryo the shape of the centrosome predicts its subsequent movement. We have used rhodamine-tubulin and live imaging techniques to study the development of asymmetries in centrosome morphology and positioning. In contrast to studies using fixed embryos, our images provide a detailed characterization of the dynamics of centrosome flattening. In addition, our observations of centrosome behavior in vivo challenge previous assumptions regarding centrosome separation by illustrating that centrosome flattening and daughter centrosome separation are distinct processes, and by revealing that nascent daughter centrosomes may become separated from the nucleus. Finally, we provide evidence that the midbody specifies a region of the cortex that directs rotational alignment of the centrosome-nucleus complex and that the process is likely to involve multiple interactions between microtubules and the cortex; the process of alignment involves oscillations and overshoots, suggesting a multiplicity of cortical sites that interact with microtubules.

REFERENCES

Albertson
D. G.
(
1984
).
Formation of the first cleavage spindle in nematode embryos.
Dev. Biol
101
,
61
72
Brenner
S.
(
1974
).
The genetics of Caenorhabditis elegans.
Genetics
77
,
71
94
Cheng
N. N.
,
Kirby
C. M.
,
Kemphues
K. J.
(
1995
).
Control of cleavage spindle orientation in Caenorhabditis elegans; the role of the genes par-2 and par-3.
Genetics
139
,
549
559
Dan
K.
(
1979
).
Studies on unequal cleavage in sea urchins: I. Migration of the nuclei to the vegetal pole.
Dev. Growth Differ
21
,
527
535
Dan
K.
,
Ito
S.
(
1984
).
Studies of unequal cleavage in Molluscs: I. Nuclear behavior and anchorage of a spindle pole to the cortex as revealed by isolation technique.
Dev. Growth Differ
26
,
249
262
Drewes
G.
,
Ebneth
A.
,
Preuss
U.
,
Mandelkow
E.-M.
,
Mandelkow
E.
(
1997
).
MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption.
Cell
89
,
297
308
Guo
S.
,
Kemphues
K. J.
(
1995
).
par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed.
Cell
81
,
611
620
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
Hird
S. N.
,
White
J. G.
(
1993
).
Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans.
J. Cell Biol
121
,
1343
1355
Hird
S. N.
(
1996
).
Cortical actin movements during the first cell cycle of the Caenorhabditis elegans embryo.
J. Cell Sci
109
,
525
533
Hyman
A. A.
,
White
J. G.
(
1987
).
Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans.
J. Cell Biol
105
,
2123
2135
Hyman
A. A.
(
1989
).
Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position.
J. Cell Biol
109
,
1185
1193
Kirby
C.
,
Kusch
M.
,
Kemphues
K. K.
(
1990
).
Mutations in the par genes of Caenorhabditis elegans affect cytoplasmic reorganization during the first cell cycle.
Dev. Biol
142
,
203
215
Laufer
J.
,
Bazzicapuso
P.
,
Wood
W. B.
(
1980
).
Segregation of development potential in early embryos of Caenorhabditis elegans.
Cell
19
,
569
577
Nigon
V.
,
Guerrier
P.
,
Monin
H.
(
1960
).
L'architecture polaire de l'ouef et les movements des constituants cellulaires au cours des premieres stapes du developpement chez quelques nematodes.
Bull. Biol. Fr. Belg
94
,
131
202
Paweletz
N.
,
Mazia
D.
,
Finze
E. M.
(
1984
).
The centrosome cycle in the mitotic cycle of sea urchin eggs.
Exp. Cell Res
152
,
47
65
Sammack
P. J.
,
Borisy
G. G.
(
1988
).
Detection of single fluoresecent microtubules and methods for determining their dynamics in living cells.
Cell Motil. Cytoskel
10
,
237
245
Shaw
S. L.
,
Yeh
E.
,
Maddox
P.
,
Salmon
E. D.
,
Bloom
K.
(
1997
).
Astral microtubule dynamics in yeast: a microtubule-based searching mechanism for spindle orientation and nuclear migration into the bud.
J. Cell Biol
139
,
985
994
Strome
S.
,
Wood
W. B.
(
1983
).
Generation of asymmetry and segregation of germline granules in early C. elegans embryos.
Cell
35
,
15
25
Waddle
J. A.
,
Cooper
J. A.
,
Waterston
R. H.
(
1994
).
Transient localized accumulation of actin in Caenorhabditis elegans blastomeres with oriented asymmetric divisions.
Development
120
,
2317
2328
White
J.
,
Strome
S.
(
1996
).
Cleavage plane specification in C. elegans: how to divide the spoils.
Cell
84
,
195
198
This content is only available via PDF.