The two serotonergic HSN motor neurons of the nematode Caenorhabditis elegans innervate the vulval muscles and stimulate egg laying by hermaphrodites. By analyzing mutant and laser-operated animals, we find that both epithelial cells of the developing vulva and axons of the ventral nerve cord are required for HSN axonal guidance. Vulval precursor cells help guide the growth cone of the emerging HSN axon to the ventral nerve cord. Vulval cells also cause the two HSN axons to join the ventral nerve cord in two separate fascicles and to defasciculate from the ventral nerve cord and branch at the vulva. The axons of either the PVP or PVQ neurons are also necessary for the HSN axons to run in two separate fascicles within the ventral nerve cord. Our observations indicate that the outgrowth of the HSN axon is controlled in multiple ways by both neuronal and nonneuronal cells.
REFERENCES
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
Bentley
D.
, Caudy
M.
(1983
) Pioneer axons lose directed growth after selective killing of guidepost cells.
Nature
304
, 62
–65
Bentley
D.
, Keshishian
H.
(1982
) Pathfinding by peripheral pioneer neurons in grasshoppers.
Science
218
, 1082
–1088
Brenner
S.
(1974
) The genetics of Caenorhabditis elegans.
Genetics
77
, 71
–94
Desai
C.
, Garriga
G.
, McIntire
S. L.
, Horvitz
H. R.
(1988
) A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons.
Nature
336
, 638
–646
Desai
C.
, Horvitz
H. R.
(1989
) Caenorhabditis elegans mutants defective in the functioning of the motor neurons responsible for egg laying.
Genetics
121
, 703
–721
Ferguson
E. L.
, Horvitz
H. R.
(1985
) Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans.
Genetics
110
, 17
–72
Ferguson
E. L.
, Sternberg
P. W.
, Horvitz
H. R.
(1987
) A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans.
Nature
326
, 259
–267
Fixsen
W.
, Sternberg
P.
, Ellis
H.
, Horvitz
R.
(1985
) Genes that affect cell fates during the development of Caenorhabditis elegans. Cold Spring Harbor Symp.
Quant. Biol
50
, 99
–104
Fujisawa
H.
(1987
) Mode of growth of retinal axons within the tectum of Xenopus tadpoles, and implications in the ordered neuronal connection between retina and tectum.
J. Comp. Neurol
260
, 127
–139
Greenwald
I. S.
, Sternberg
P. W.
, Horvitz
H. R.
(1983
) The lin-12 locus specifies cell fates in Caenorhabditis elegans.
Cell
34
, 435
–444
Harris
W. A.
, Holt
C. E.
, Bonhoeffer
F.
(1987
) Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibers in vivo.
Development
101
, 123
–133
Hedgecock
E. M.
, Culotti
J. G.
, Thomson
J. N.
, Perkins
L. A.
(1985
) Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes.
Dev. Biol
111
, 158
–170
Hedgecock
E. M.
, Culotti
J. G.
, Hall
D. H.
, Stern
B. D.
(1987
) Genetics of cell and axon migrations in Caenorhabditis elegans.
Development
100
, 365
–382
Hedgecock
E. M.
, Culotti
J. G.
, Hall
D. H.
(1990
) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans.
Neuron
4
, 61
–85
Heffner
C. D.
, Lumsden
A. G. S.
, O'Leary
D. D. M.
(1990
) Targetcontrol of collateral extension and directional axon growth in the mammalian brain.
Science
247
, 217
–220
Horvitz
H. R.
, Brenner
S.
, Hodgkin
J.
, Herman
R. K.
(1979
) A uniform genetic nomenclature for the nematode Caenorhabditis elegans.
Mol. Gen. Genet
175
, 129
–133
Horvitz
H. R.
, Sternberg
P. W.
(1991
) Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva.
Nature
351
, 535
–541
Kimble
J.
, Hirsh
D.
(1979
) The post-embryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans.
Dev. Biol
70
, 396
–417
Li
C.
, Chalfie
M.
(1990
) Organogenesis in C. elegans: positioning of neurons and muscles in the egg-laying system.
Neuron
4
, 681
–695
Lumsden
A. G. S.
, Davies
A. M.
(1983
) Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor.
Nature
306
, 786
–788
Lumsden
A. G. S.
, Davies
A. M.
(1986
) Chemotrophic effect of specific target epithelium in the developing mammalian nervous system.
Nature
323
, 538
–539
Manser
J.
, Wood
W. B.
(1990
) Mutations affected embryonic cell migrations in Caenorhabditis elegans.
Dev. Genet
11
, 49
–64
McIntire
S. L.
, Garriga
G.
, White
J.
, Jacobson
D.
, Horvitz
H. R.
(1992
) Genes necessary for directed axonal elongation and fasciculation in Caenorhabditis elegans.
Neuron
8
, 307
–322
O'Leary
D. D. M.
, Terashima
T.
(1988
). Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and ‘waiting periods.'.
Neuron
1
, 901
–910
Raper
J. A.
, Bastiani
M.
, Goodman
C. S.
(1983
) Pathfinding by neuronal growth cones in grasshopper embryos. I. Divergent choices made by the growth cones of sibling neurons.
J. Neurosci
3
, 20
–30
Raper
J. A.
, Bastiani
M.
, Goodman
C. S.
(1983
) Guidance of neuronal growth cones: selective fasciculation in the grasshopper embryo. Cold Spring Harbor Symp.
Quant. Biol
48
, 587
–598
Raper
J. A.
, Bastiani
M. J.
, Goodman
C. S.
(1984
) Pathfinding by neuronal growth cones in grasshopper embryos. IV. The effects of ablating the A and P axons upon the behavior of the G growth cones.
J. Neurosci
4
, 2329
–2345
Schinkmann
K.
, Li
C.
(1992
) Localization of FMRFamide-like peptides in Caenorhabditis elegans.
J. Comp. Neurol
316
, 251
–260
Schwab
M. E.
(1990
) Myelin-associated inhibitors of neurite growth and regeneration in the CNS.
Trends Neurosci
13
, 452
–456
Siddiqui
S. S.
, Culotti
J. G.
(1991
) Examination of neurons in wild type and mutants of Caenorhabditis elegans using antibodies to horseradish peroxidase.
J. Neurogenetics
7
, 193
–211
Stern
M. J.
, Horvitz
H. R.
(1991
) A normally attractive cell interaction is repulsive in two C. elegans mesodermal cell migration mutants.
Development
113
, 797
–803
Sulston
J. E.
, Horvitz
H. R.
(1977
) Post-embryonic cell lineages of the nematode Caenorhabditis elegans.
Dev. Biol
56
, 110
–156
Sulston
J. E.
, Horvitz
H. R.
(1981
) Abnormal cell lineages in mutants of the nematode Caenorhabditis elegans.
Dev. Biol
82
, 41
–55
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
Taghert
P. H.
, Bastiani
M. J.
, Ho
R. K.
, Goodman
C. S.
(1982
) Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to lucifer yellow.
Dev. Biol
94
, 391
–399
Tessier-Lavigne
M.
, Plactzek
M.
, Lumsden
A. G. S.
, Dodd
J.
, Jessell
T. M.
(1988
) Chemotropic guidance of developing axons in the mammalian central nervous system.
Nature
336
, 775
–778
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
Trent
C.
, Tsung
N.
, Horvitz
H. R.
(1983
) Egg-laying defective mutants of the nematode Caenorhabditis elegans.
Genetics
104
, 619
–647
Walter
J.
, Allsopp
T. E.
, Bonhoeffer
F.
(1990
) A common denominator of growth cone guidance and collapse.
Trends Neurosci
13
, 447
–452
Walthall
W. W.
, Chalfie
M.
(1988
) Cell-cell interactions in the guidance of late-developing neurons in Caenorhabditis elegans.
Science
239
, 643
–645
White
J. G.
(1985
) Neuronal connectivity in Caenorhabditis elegans.
Trends Neurosci
8
, 277
–283
White
J. G.
, Southgate
E.
, Thomson
J. N.
, Brenner
S.
(1976
) The structure of the ventral nerve cord of Caenorhabditis elegans.
Philos. 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 Caenorhabditis elegans.
Philos. Trans. R. Soc. Lond. B Biol. Sci
314
, 1
–340
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