We have undertaken electron micrographic reconstruction of the Caenorhabditis elegans hermaphrodite uterus and determined the correspondence between cells defined by their lineage history and differentiated cell types. In this organ, many cells do not move during morphogenesis and the cell lineage may function to put cells where they are needed. Differentiated uterine cell types include the toroidal ut cells that make structural epithelium, and specialized utse and uv cells that make the connection between the uterus and the vulva. A cell fate decision in which the anchor cell (AC) induces adjacent ventral uterine intermediate precursor cells to adopt the pi fate, rather than the ground state rho, has profound consequences for terminal differentiation: all pi progeny are directly involved in making the uterine-vulval connection whereas all rho progeny contribute to ut toroids or the uterine-spermathecal valve. In addition to specifying certain uterine cell fates, the AC also induces the vulva. Its multiple inductions thereby function to coordinate the connection of an internal to an external epithelium. The AC induces the pi cells and ultimately fuses with a subset of their progeny. This is an example of reciprocal cell-cell interaction that can be studied at single cell resolution. The AC is thus a transitory cell type that plays a pivotal role in organizing the morphogenesis of the uterine-vulval connection.

Reference

Albertson
D. G.
,
Thomson
J. N.
(
1976
)
The pharynx of Caenorhabditis elegans.
Phil. Trans. R. Soc. Lond. B. Biol. Sci
274
,
299
325
Albertson
D. G.
(
1984
)
Formation of the first cleavage spindle in nematode embryos.
Dev. Biol
101
,
61
72
Aroian
R. V.
,
Koga
M.
,
Mendel
J. E.
,
Ohshima
Y.
,
Sternberg
P. W.
(
1990
)
The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily.
Nature
348
,
693
699
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
Brenner
S.
(
1974
)
The genetics of Caenorhabditis elegans.
Genetics
77
,
71
94
Evans
T. C.
,
Crittendon
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
Greenwald
I. S.
,
Sternberg
P. W.
,
Horvitz
H. R.
(
1983
)
The lin-12 locus specifies cell fates in Caenorhabditis elegans.
Cell
34
,
435
444
Grobstein
C.
(
1955
)
Induction interaction in the development of the mouse metanephros.
J. Exp. Zool
130
,
319
340
Grobstein
C.
(
1956
)
Trans-filter induction of tubules in mouse metanephrogenic mesenchyme.
Exp. Cell Res
10
,
424
440
Henderson
S. T.
,
Gao
D.
,
Lambie
E. J.
,
Kimble
J.
(
1994
)
lag-2 mayencode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans.
Development
120
,
2913
2924
Hill
R. J.
,
Sternberg
P. W.
(
1992
)
The lin-3 gene encodes an inductive signal for vulval development in C. elegans.
Nature
358
,
470
476
Hirsh
D.
,
Oppenheim
D.
,
Klass
M.
(
1976
)
Development of the reproductive system of Caenorhabditis elegans.
Dev. Biol
49
,
200
219
Katz
W. S.
,
Hill
R. J.
,
Clandinin
T. R.
,
Sternberg
P. W.
(
1995
)
Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates.
Cell
82
,
297
307
Kimble
J.
,
Hirsh
D.
(
1979
)
Post-embryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans.
Dev. Biol
70
,
396
417
Kimble
J.
(
1981
)
Lineage alterations after ablation of cells in the somatic gonad of Caenorhabditis elegans.
Dev. Biol
87
,
286
300
Kimble
J. E.
,
White
J. G.
(
1981
)
On the control of germ cell development in Caenorhabditis elegans.
Dev. Biol
81
,
208
219
Newman
A. P.
,
White
J. G.
,
Sternberg
P. W.
(
1995
)
The C. elegans lin-12 gene mediates induction of ventral uterine specialization by the anchor cell.
Development
121
,
263
271
Podbilewicz
B.
,
White
J.
(
1994
)
Cell fusions in the developing epithelia of C. elegans.
Dev. Biol
161
,
408
424
Roberts
D. J.
,
Johnson
R. L.
,
Burke
A. C.
,
Nelson
C. E.
,
Morgan
B. A.
,
Tabin
C.
(
1995
)
Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut.
Development
121
,
3163
3174
Seydoux
G.
,
Greenwald
I.
(
1989
)
Cell autonomy of lin-12 function in a cell fate decision in C. elegans.
Cell
57
,
1237
1245
Sternberg
P. W.
,
Horvitz
H. R.
(
1986
)
Pattern formation during vulval development in Caenorhabditis elegans.
Cell
44
,
761
772
Strome
S.
(
1983
)
Generation of asymmetry and segregation of germ-line granules in early Caenorhabditis elegans embryos.
Cell
35
,
15
25
Sulston
J.
,
Horvitz
H. R.
(
1977
)
Postembryonic 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
Tabin
C.
(
1995
)
The initiation of the limb bud: growth factors, Hox genes, and retinoids.
Cell
80
,
671
674
Tax
F. E.
,
Yeargers
J. J.
,
Thomas
J. H.
(
1994
)
Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila.
Nature
368
,
150
154
Thomas
J. H.
,
Stern
M. J.
,
Horvitz
H. R.
(
1990
)
Cell interactions coordinate the development of the C. elegans egg-laying system.
Cell
62
,
1041
1052
White
J. G.
,
Southgate
E.
,
Thomson
J. N.
,
Brenner
S.
(
1976
)
The structure of the ventral nerve cord of Caenorhabditis elegans.
Phil. Trans. R. Soc. Lond. B Biol. Sci
275
,
327
348
White
J. G.
,
Southgate
E.
,
Thomson
J. N.
,
Brenner
S.
(
1986
)
The structure of the nervous system of the nematode Caenorhabditis elegans.
Phil. Trans. Roy. Soc., Lond. B
314
,
1
340
Wilkinson
H. A.
,
Fitzgerald
K.
,
Greenwald
I.
(
1994
)
Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision.
Cell
79
,
1187
1198
Wylie
A. H.
,
Kerr
J. F. R.
,
Currie
A. R.
(
1980
)
Cell death: the significance of apoptosis.
Int. Rev. Cytol
68
,
251
306
Yochem
J.
,
Weston
K.
,
Greenwald
I.
(
1988
)
C. eleganslin-12 encodes a transmembrane protein similar to DrosophilaNotch and yeast cell cycle gene products.
Nature
335
,
547
550
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