The Caenorhabditis elegans lin-39, mab-5 and egl-5 Hox genes specify cell fates along the anterior-posterior body axis of the nematode during postembryonic development, but little is known about Hox gene functions during embryogenesis. Here, we show that the C. elegans labial-like gene ceh-13 is expressed in cells of many different tissues and lineages and that the rostral boundary of its expression domain is anterior to those of the other Hox genes. By transposon-mediated mutagenesis, we isolated a zygotic recessive ceh-13 loss-of-function allele, sw1, that exhibits an embryonic sublethal phenotype. Lineage analyses and immunostainings revealed defects in the organization of the anterior lateral epidermis and anterior body wall muscle cells. The epidermal and mesodermal identity of these cells, however, is correctly specified. ceh-13(sw1) mutant embryos also show fusion and adhesion defects in ectodermal cells. This suggests that ceh-13 plays a role in the anterior organization of the C. elegans embryo and is involved in the regulation of cell affinities.

Ahringer
J.
(
1996
)
Posterior patterning by the Caenorhabditis eleganseven-skipped homolog vab-7.
Genes Dev
10
,
1120
1130
Akam
M.
,
Averof
M.
,
Castelli-Gair
J.
,
Dawes
R.
,
Falciani
F.
,
Ferrier
D.
(
1994
)
The evolving role of Hox genes in arthropods.
Development
1994
,
209
215
Austin
J.
,
Kimble
J.
(
1989
)
Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans.
Cell
58
,
565
571
Brenner
S.
(
1974
)
The genetics of Caenorhabditis elegans.
Genetics
77
,
71
94
Burglin
T. R.
,
Ruvkun
G.
(
1993
)
The Caenorhabditis elegans homeobox gene cluster.
Curr. Opin. Genet. Dev
3
,
615
620
Carpenter
E. M.
,
Goddard
J. M.
,
Chisaka
O.
,
Manley
N. R.
,
Capecchi
M. R.
(
1993
).
Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain.
Development
118
,
1063
1075
Chisholm
A.
(
1991
)
Control of cell fate in the tail region of C. elegans by the gene egl-5.
Development
111
,
921
932
Chow
K. L.
,
Emmons
S. W.
(
1994
)
HOM-C/ Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail.
Development
120
,
2579
2592
Clark
S. G.
,
Chisholm
A. D.
,
Horvitz
H. R.
(
1993
)
Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39.
Cell
74
,
43
55
Costa
M.
,
Raich
W.
,
Agbunag
C.
,
Leung
B.
,
Hardin
J.
,
Priess
J. R.
(
1998
)
A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo.
J. Cell Biol
141
,
297
308
Cowing
D. W.
,
Kenyon
C.
(
1992
)
Expression of the homeotic gene mab-5 during Caenorhabditis elegans embryogenesis.
Development
116
,
481
490
Dolle
P.
,
Lufkin
T.
,
Krumlauf
R.
,
Mark
M.
,
Duboule
D.
,
Chambon
P.
(
1993
).
Local alterations of Krox-20 and Hox gene expression in the hindbrain suggest lack of rhombomeres 4 and 5 in homozygote null Hoxa-1 (Hox-1.6) mutant embryos.
Proc. Natl. Acad. Sci. USA
90
,
7666
7670
Duboule
D.
,
Morata
G.
(
1994
)
Colinearity and functional hierarchy among genes of the homeotic complexes.
Trends Genet
10
,
358
364
Finney
M.
,
Ruvkun
G.
(
1990
)
The unc-86 gene product couples cell lineage and cell identity in C. elegans.
Cell
63
,
895
905
Fire
A.
,
Xu
S.
,
Montgomery
M. K.
,
Kostas
S. A.
,
Driver
S. E.
,
Mello
C. C.
(
1998
)
Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.
Nature
391
,
806
811
Francis
G. R.
,
Waterston
R. H.
(
1985
)
Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization.
J. Cell Biol
101
,
1532
1549
Garcia-Fernandez
J.
,
Holland
P.
(
1994
)
Archetypal organization of the amphioxus Hox gene cluster.
Nature
370
,
563
566
Gavalas
A.
,
Studer
M.
,
Lumsden
A.
,
Rijli
F.
,
Chambon
R.
(
1998
)
Hoxa1 and hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch.
Development
125
,
1123
1136
Goddard
J. M.
,
Rossel
M.
,
Manley
N. R.
,
Capecchi
M. R.
(
1996
)
Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve.
Development
122
,
3217
3228
Goh
P.
,
Bogaert
T.
(
1991
)
Positioning and maintenance of embryonic body wall muscle attachments in C. elegans requires the mup-1 gene.
Development
111
,
667
681
Hirth
F.
,
Hartmann
B.
,
Reichert
H.
(
1998
)
Homeotic gene action in embryonic brain development of Drosophila.
Development
125
,
1579
1589
Hope
I.
(
1994
)
PES-1 is expressed during early embryogenesis in Caenorhabditis elegans and has homology to the fork head family of transcription factors.
Development
120
,
505
514
Hoppler
S.
,
Bienz
M.
(
1994
)
Specification of a single cell type by a Drosophila homeotic gene.
Cell
76
,
689
702
Hresko
M.
,
Williams
B.
,
Waterston
R.
(
1994
)
Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans.
J. Cell Biol
124
,
491
506
Hunter
C. P.
,
Kenyon
C.
(
1995
)
Specification of anteroposterior cell fates in Caenorhabditis elegans by Drosophila Hox proteins.
Nature
377
,
229
232
Hutter
H.
,
Schnabel
R.
(
1994
)
glp-1 and inductions establishing embryonic axes in C. elegans.
Development
120
,
2051
2064
Kenyon
C.
,
Austin
J.
,
Costa
M.
,
Cowing
D.
,
Harris
J.
,
Honigberg
L.
,
Hunter
C.
,
Maloof
J.
,
Muller-Immergluck
M.
,
Salser
S.
, et al. 
(
1997
)
The dance of the Hox genes: patterning the anteroposterior body axis of Caenorhabditis elegans.
Cold Spring Harb. Symp. Quant. Biol
62
,
293
305
Labouesse
M.
,
Hartwieg
E.
,
Horvitz
H. R.
(
1996
)
The Caenorhabditis elegans LIN-26 protein is required to specify and/or maintain all non-neuronal ectodermal cell fates.
Development
122
,
2579
2588
Lawrence
P.
,
Morata
G.
(
1994
)
Homeobox genes: their function in Drosophila segmentation and pattern formation.
Cell
78
,
181
189
Maduro
M.
,
Pilgrim
D.
(
1995
)
Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system.
Genetics
141
,
977
988
Mark
M.
,
Lufkin
T.
,
Vonesch
J. L.
,
Ruberte
E.
,
Olivo
J. C.
,
Dolle
P.
,
Gorry
P.
,
Lumsden
A.
,
Chambon
P.
(
1993
)
Two rhombomeres are altered in Hoxa-1 mutant mice.
Development
119
,
319
338
McGinnis
W.
,
Krumlauf
R.
(
1992
)
Homeobox genes and axial patterning.
Cell
68
,
283
302
Merrill
V. K.
,
Diederich
R. J.
,
Turner
F. R.
,
Kaufman
T. C.
(
1989
)
A genetic and developmental analysis of mutations in labial, a gene necessary for proper head formation in Drosophilamelanogaster.
Dev. Biol
135
,
376
391
Miller
D. D.
,
Ortiz
I.
,
Berliner
G. C.
,
Epstein
H. F.
(
1983
)
Differential localization of two myosins within nematode thick filaments.
Cell
34
,
477
490
Moerman
D. G.
,
Hutter
H.
,
Mullen
G. P.
,
Schnabel
R.
(
1996
)
Cell autonomous expression of perlecan and plasticity of cell shape in embryonic muscle of Caenorhabditis elegans.
Dev. Biol
173
,
228
242
Podbilewicz
B.
,
White
J. G.
(
1994
)
Cell fusions in the developing epithelial of C. elegans.
Dev. Biol
161
,
408
424
Priess
J. R.
,
Hirsh
D. I.
(
1986
)
Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo.
Dev. Biol
117
,
156
173
Prince
V.
,
Joly
L.
,
Ekker
M.
,
Ho
R.
(
1998
)
Zebrafish hox genes: genomic organization and modified colinear expression patterns in the trunk.
Development
125
,
407
420
Salser
S. J.
,
Kenyon
C.
(
1992
)
Activation of a C. elegans Antennapedia homologue in migrating cells controls their direction of migration.
Nature
355
,
255
258
Schaller
D.
,
Wittmann
C.
,
Spicher
A.
,
Muller
F.
,
Tobler
H.
(
1990
)
Cloning and analysis of three new homeobox genes from the nematode Caenorhabditis elegans.
Nucleic Acids Res
18
,
2033
2036
Schnabel
R.
,
Hutter
H.
,
Moerman
D.
,
Schnabel
H.
(
1997
)
Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification.
Dev. Biol
184
,
234
265
Sharkey
M.
,
Graba
Y.
,
Scott
M.
(
1997
)
Hox genes in evolution: protein surfaces and paralog groups.
Trends Genet
13
,
145
151
Studer
M.
,
Lumsden
A.
,
Ariza
M. L.
,
Bradley
A.
,
Krumlauf
R.
(
1996
)
Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1.
Nature
384
,
630
634
Sulston
J.
,
Du
Z.
,
Thomas
K.
,
Wilson
R.
,
Hillier
L.
,
Staden
R.
,
Halloran
N.
,
Green
P.
,
Thierry-Mieg
J.
,
Qiu
L.
, et al. 
(
1992
)
The C. elegans genome sequencing project: a beginning.
Nature
356
,
37
41
Sulston
J.
,
Schierenberg
E.
,
White
J.
,
Thomson
J.
(
1983
)
The embryonic cell lineage of the nematode Caenorhabditis elegans.
Dev. Biol
100
,
64
119
TheSequencing Consortium
(
1998
)
Genome sequence of the nematode C. elegans: a platform for investigating biology.
Science
282
,
2012
2018
Wang
B. B.
,
Muller-Immergluck
M.
,
Austin
J.
,
Robinson
N. T.
,
Chisholm
A.
,
Kenyon
C.
(
1993
)
A homeotic gene cluster patterns the anteroposterior body axis of C. elegans.
Cell
74
,
29
42
Williams
B. D.
,
Waterston
R. H.
(
1994
)
Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations.
J. Cell Biol
124
,
475
490
Wittmann
C.
,
Bossinger
O.
,
Goldstein
B.
,
Fleischmann
M.
,
Kohler
R.
,
Brunschwig
K.
,
Tobler
H.
,
Muller
F.
(
1997
)
The expression of the C. elegans labial -like Hox gene ceh-13 during early embryogenesis relies on cell fate and on anteroposterior cell polarity.
Development
124
,
4193
4200
Zwaal
R. R.
,
Broeks
A.
,
van Meurs
J.
,
Groenen
J. T.
,
Plasterk
R. H.
(
1993
)
Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank.
Proc. Natl. Acad. Sci. USA
90
,
7431
7435
This content is only available via PDF.