Morphogenesis transforms the C. elegans embryo from a ball of cells into a vermiform larva. During this transformation, the embryo increases fourfold in length; present data indicates this elongation results from contraction of the epidermal actin cytoskeleton. In sma-1 mutants, the extent of embryonic elongation is decreased and the resulting sma-1 larvae, although viable, are shorter than normal. We find that sma-1 mutants elongate for the same length of time as wild-type embryos, but at a decreased rate. The sma-1 mutants we have isolated vary in phenotypic severity, with the most severe alleles showing the greatest decrease in elongation rate. The sma-1 gene encodes a homolog of betaH-spectrin, a novel beta-spectrin isoform first identified in Drosophila. sma-1 RNA is expressed in epithelial tissues in the C. elegans embryo: in the embryonic epidermis at the start of morphogenesis and subsequently in the developing pharynx, intestine and excretory cell. In Drosophila, betaH-spectrin associates with the apical plasma membrane of epithelial cells; beta-spectrin is found at the lateral membrane. We propose that SMA-1 is a component of an apical membrane skeleton in the C. elegans embryonic epidermis that determines the rate of elongation during morphogenesis.
REFERENCES
Albertson
D. G.
, Thomson
J. N.
(1976
) The pharynx of Caenorhabditis elegans.
Phil. Trans. Roy. Soc. London
275
, 299
–325
Bennett
V.
, Gilligan
D. M.
(1993
) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane.
Ann. Rev. Cell Biol
9
, 27
–66
Brenner
S.
(1974
) The genetics of Caenorhabditis elegans.
Genetics
77
, 71
–94
Byers
T. J.
, Husain-Chishti
A.
, Dubreuil
R. R.
, Branton
D.
, Goldstein
L. S. B.
(1989
) Sequence similarity of the amino-terminal domain of Drosophila beta spectrin to alpha actinin and dystrophin.
J. Cell Biol
109
, 1633
–1641
Byers
T. J.
, Brandin
E.
, Lue
R. A.
, Winograd
E.
, Branton
D.
(1992
) The complete sequence of Drosophila -spectrin reveals supra-motifs comprising eight 106-residue segments.
Proc. Nat. Acad. Sci. USA
89
, 6187
–6191
Costa
M.
, Draper
B. W.
, Priess
J. R.
(1997
) The role of actin filaments in patterning the Caenorhabditis elegans cuticle.
Dev. Biol
184
, 373
–384
de Cuevas
M.
, Lee
J. K.
, Spradling
A. C.
(1996
) -spectrin is required for germline cell division and differentiation in the Drosophila ovary.
Development
122
, 3959
–3968
Dubreuil
R. R.
, Byers
T. J.
, Sillman
A. L.
, Bar-Zivi
D.
, Goldstein
L. S. B.
, Branton
D.
(1989
) The complete sequence of Drosophila-spectrin: conservation of structural domains between -spectrin and-actinin.
J. Cell Biol
109
, 2197
–2205
Dubreuil
R. R.
, Byers
T. J.
, Stewart
C. T.
, Kiehart
D. P.
(1990
) A-spectrin isoform from Drosophila () is similar in size to vertebrate dystrophin.
J. Cell. Biol
111
, 1849
–1858
Dubreuil
R. R.
, Maddux
P. B.
, Grushko
T. A.
, MacVicar
G. R.
(1997
) Segregation of two spectrin isoforms: polarized membrane-binding sites direct polarized membrane skeleton assembly.
Mol. Biol. Cell
8
, 1933
–1942
Fire
A.
, Albertson
D.
, Harrison
S. W.
, Moerman
D. G.
(1991
) Production of antisense RNA leads to effective and specific inhibition of gene expression in C. elegans muscle.
Development
113
, 503
–514
Francis
R.
, Waterston
R. H.
(1991
) Muscle cell attachment in Caenorhabditis elegans.
J. Cell Biol
114
, 465
–479
Glenney
J. R.
, Glenney
P.
, Osborn
M.
, Weber
K.
(1982
) An F-actin and calmodulin-binding protein from isolated intestinal brush borders has a morphology related to spectrin.
Cell
28
, 843
–854
Guo
S.
, Kemphues
K.
(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
Howe
C. L.
, Sacramone
L. M.
, Mooseker
M. S.
, Morrow
J. S.
(1985
) Mechanisms of cytoskeletal regulation: modulation of membrane affinity in avian brush border and erythrocyte spectrins.
J. Cell Biol
101
, 1379
–1385
Kennedy
S. P.
, Warren
S. L.
, Forget
B. G.
, Morrow
J. S.
(1991
) Ankyrin binds to the 15th repetitive unit of erythroid and nonerythroid-spectrin.
J. Cell Biol
115
, 267
–277
Miller
D. M.
, Stockdale
F. E.
, Karn
J.
(1986
) Immunological identification of the genes encoding the four myosin heavy chain isoforms of Caenorhabditis elegans.
Proc. Nat. Acad. Sci. USA
83
, 2305
–2309
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
Pulak
R.
, Anderson
P.
(1993
) mRNA surveillance by the Caenorhabditis elegans smg genes.
Genes Dev
7
, 1885
–1897
Rhind
N. R.
, Miller
L. M.
, Kopczynski
J. B.
, Meyer
B. J.
(1995
) xol-1 acts as an early switch in the C. elegans male/hermaphrodite decision.
Cell
8
, 71
–82
Rocheleau
C. E.
, Downs
W. D.
, Lin
R.
, Wittman
C.
, Bei
Y.
, Cha
Y. H.
, Ali
M.
, Priess
J. R.
(1997
) Wnt signalling and an APC-related gene specify endoderm in early C. elegans embryos.
Cell
90
, 707
–716
Seydoux
G.
, Fire
A.
(1994
) Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans.
Development
120
, 2823
–2834
Speicher
D. W.
, Desilva
T. M.
, Speicher
K. D.
, Ursitti
J. A.
, Hembrach
P.
, Weglarz
L.
(1993
) Location of the human red cell spectrin tetramer binding site and detection of a related ‘closed’ hairpin loop dimer using proteolytic footprinting.
J. Biol. Chem
268
, 4227
–4235
Starich
T. A.
, Herman
R. K.
, Kari
C. K.
, Yeh
W.-H.
, Schackwitz
W. S.
, Schuyler
M. W.
, Collet
J.
, Thomas
J. H.
, Riddle
D. L.
(1995
) Mutations affecting the chemosensory neurons of Caenorhabditis elegans.
Genetics
139
, 171
–188
Sulston
J. E.
, Horvitz
H. R.
(1977
) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans.
Dev. Biol
56
, 110
–156
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
Thomas
G. H.
, Kiehart
D. P.
(1994
) Heavy-spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis.
Development
120
, 2039
–2050
Thomas
G. H.
, Newbern
E. C.
, Korte
C. C.
, Bales
M. A.
, Muse
S. V.
, Clark
A. G.
, Kiehart
D. P.
(1997
) Intragenic duplication and divergence in the spectrin superfamily of proteins.
Mol. Biol. Evol
14
, 1285
–1295
Thomas
G. H.
, Zarnescu
D. C.
, Juedes
A. E.
, Bales
M. A.
, Londergan
A.
, Korte
C. C.
, Kiehart
D. P.
(1998
) DrosophilaHeavy-spectrin is essential for development and contributes to specific cell fates in the eye.
Development
125
, 2125
–2134
Waterston
R.
, Sulston
J.
(1995
) The genome of Caenorhabditis elegans.
Proc. Nat. Acad. Sci.USA
92
, 10836
–10840
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
Williams-Masson
E. M.
, Malik
A. N.
, Hardin
J.
(1997
) An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis.
Development
124
, 2889
–2901
Winkelmann
J. C.
, Forget
B. G.
(1993
) Erythroid and nonerythroid spectrins.
Blood
81
, 3173
–3185
Wissman
A.
, Ingles
J.
, McGhee
J. D.
, Mains
P.
(1997
) Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape.
Genes Dev
11
, 409
–422
Yandell
M. D.
, Edgar
L.
, Wood
W. B.
(1994
) Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans.
Proc. Nat. Acad. Sci.USA
91
, 1381
–1385
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