Cell fate decisions in early embryonic cells are controlled by interactions among developmental regulatory genes. Zebrafish floating head mutants lack a notochord; instead, muscle forms under the neural tube. As shown previously, axial mesoderm in floating head mutant gastrulae fails to maintain expression of notochord genes and instead expresses muscle genes. Zebrafish spadetail mutant gastrulae have a nearly opposite phenotype; notochord markers are expressed in a wider domain than in wild-type embryos and muscle marker expression is absent. We examined whether these two phenotypes revealed an antagonistic genetic interaction by constructing the double mutant. Muscle does not form in the spadetail;floating head double mutant midline, indicating that spadetail function is required for floating head mutant axial mesoderm to transfate to muscle. Instead, the midline of spadetail;floating head double mutants is greatly restored compared to that of floating head mutants; the floor plate is almost complete and an anterior notochord develops. In addition, we find that floating head mutant cells can make both anterior and posterior notochord when transplanted into a wild-type host, showing that enviromental signals can override the predisposition of floating head mutant midline cells to make muscle. Taken together, these results suggest that repression of spadetail function by floating head is critical to promote notochord fate and prevent midline muscle development, and that cells can be recruited to the notochord by environmental signals.

REFERENCES

Ang
S.-L.
,
Rossant
J.
(
1994
)
HNF-3β is essential for node and notochord formation in mouse development.
Cell
78
,
561
574
Beattie
C. E.
,
Hatta
K.
,
Halpern
M. E.
,
Liu
H.
,
Eisen
J. S.
,
Kimmel
C. B.
(
1997
)
Temporal separation in the specification of primary and secondary motoneurons in zebrafish.
Dev. Biol
187
,
171
182
Catala
M.
,
Teillet
M.-A.
,
De Robertis
E. M.
,
Le Douarin
N. M.
(
1996
)
A spinal cord fate map in the avian embryo: while regressing, Hensen's node lays down the notochord and floor plate thus joining the spinal cord lateral walls.
Development
122
,
2599
2610
Chesley
P.
(
1935
)
Development of the short-tailed mutant in the house mouse.
J. Exp. Zool
70
,
429
459
Christian
J. L.
,
Moon
R. T.
(
1993
)
Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus.
Genes Dev
7
,
13
28
Cossu
G.
,
Tajbakhsh
S.
,
Buckingham
M.
(
1996
)
How is myogenesis initiated in the embryo?.
Trends Genet
12
,
218
223
Cunliffe
V.
,
Smith
J. C.
(
1992
)
Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue.
Nature
358
,
427
430
Cunliffe
V.
,
Smith
J. C.
(
1994
)
Specification of mesodermal pattern in Xenopus laevis by interactions between Brachyury, noggin, and Xwnt-8.
EMBO J
13
,
349
359
Currie
P. D.
,
Ingham
P. W.
(
1996
)
Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish.
Nature
382
,
452
455
Devoto
S. H.
,
Melançon
E.
,
Eisen
J. S.
,
Westerfield
M.
(
1996
)
Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation.
Development
122
,
3371
3380
Domingo
C.
,
Keller
R.
(
1995
)
Induction of notochord cell intercalation behavior and differentiation by progressive signals in the gastrula of Xenopus laevis.
Development
121
,
3311
3321
Gont
L. K.
,
Steinbeisser
H.
,
Blumberg
B.
,
De Robertis
E. M.
(
1993
)
Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip.
Development
119
,
991
1004
Gont
L. K.
,
Fainsod
A.
,
Kim
S.-H.
,
De Robertis
E. M.
(
1996
)
Overexpression of the homeobox gene Xnot-2 leads to notochord formation in Xenopus.
Dev. Biol
174
,
174
178
Gurdon
J. B.
(
1988
)
A community effect in animal development.
Nature
336
,
772
774
Halpern
M. E.
,
Ho
R. K.
,
Walker
C.
,
Kimmel
C. B.
(
1993
)
Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation.
Cell
75
,
99
111
Halpern
M. E.
,
Thisse
C.
,
Ho
R. K.
,
Thisse
B.
,
Riggleman
B.
,
Trevarrow
B.
,
Weinberg
E. S.
,
Postlethwait
J. H.
,
Kimmel
C. B.
(
1995
)
Cell-autonomous shift from axial to paraxial mesodermal development in zebrafish floating head mutants.
Development
121
,
4257
4264
Halpern
M. E.
,
Hatta
K.
,
Amacher
S. L.
,
Talbot
W. S.
,
Yan
Y.-L.
,
Thisse
B.
,
Thisse
C.
,
Postlethwait
J. H.
,
Kimmel
C. B.
(
1997
)
Genetic interactions in zebrafish midline development.
Dev. Biol
187
,
154
170
Hammerschmidt
M.
,
Nusslein-Volhard
C.
(
1993
)
The expression of a zebrafish gene homologous to Drosophilasnail suggests a conserved function in invertebrate and vertebrate gastrulation.
Development
119
,
1107
1118
Hammerschmidt
M.
,
Pelegri
F.
,
Mullins
M.
,
Kane
D. A.
,
Brand
M.
,
van Eeden
F. J. M.
,
Furutani-Seiki
M.
,
Granato
M.
,
Haffter
P.
,
Heisenberg
C.-P.
,
Jiang
Y.-J.
,
Kelsh
R. N.
,
Odenthal
J.
,
Warga
R.
,
Nusslein-Volhard
C.
(
1996
)
Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio.
Development
123
,
143
151
Hammerschmidt
M.
,
Pelegri
F.
,
Mullins
M.
,
Kane
D. A.
,
van Eeden
F. J. M.
,
Granato
M.
,
Brand
M.
,
Furutani-Seiki
M.
,
Haffter
P.
,
Heisenberg
C.-P.
,
Jiang
Y.-J.
,
Kelsh
R. N.
,
Odenthal
J.
,
Warga
R.
,
Nusslein-Volhard
C.
(
1996
)
dino and mercedes, two genes regulating dorsal development in the zebrafish embryo.
Development
123
,
95
102
Harland
R. M.
(
1994
)
The transforming growth factor β family and induction of the vertebrate mesoderm: Bone morphogenetic proteins are ventral inducers.
Proc. Natl. Acad. Sci. USA
91
,
10243
10246
Hatta
K.
,
Kimmel
C. B.
,
Ho
R. K.
,
Walker
C.
(
1991
)
The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system.
Nature
350
,
339
341
Herrmann
B. G.
,
Labeit
S.
,
Poustka
A.
,
King
T. R.
,
Lehrach
H.
(
1990
)
Cloning of the T gene required in mesoderm formation in the mouse.
Nature
343
,
617
622
Ho
R. K.
,
Kane
D. A.
(
1990
)
Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors.
Nature
348
,
728
730
Hoppler
S.
,
Brown
J. D.
,
Moon
R. T.
(
1996
)
Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos.
Genes Dev
10
,
2805
2817
Isaacs
H. V.
,
Pownall
M. E.
,
Slack
J. M. W.
(
1994
)
eFGF regulates Xbra expression during Xenopus gastrulation.
EMBO J
13
,
4469
4481
Keller
R. E.
(
1976
)
Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep layer.
Dev. Biol
51
,
118
137
Kimmel
C. B.
,
Kane
D. A.
,
Walker
C.
,
Warga
R. M.
,
Rothman
M. B.
(
1989
)
A mutation that changes cell movement and cell fate in the zebrafish embryo.
Nature
337
,
358
362
Kimmel
C. B.
,
Warga
R. M.
,
Schilling
T. F.
(
1990
)
Origin and organization of the zebrafish fate map.
Development
108
,
581
594
Kimmel
C. B.
,
Ballard
W. W.
,
Kimmel
S. R.
,
Ullmann
B.
,
Schilling
T.
(
1995
)
Stages of embryonic development of the zebrafish.
Dev. Dyn
203
,
253
310
Knezevic
V.
,
Ranson
M.
,
Mackem
S.
(
1995
)
The organizer-associated chick homeobox gene, Gnot1, is expressed before gastrulation and regulated synergistically by activin and retinoic acid.
Dev. Biol
171
,
458
470
Krauss
S.
,
Concordet
J.-P.
,
Ingham
P. W.
(
1993
)
A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos.
Cell
75
,
1431
1444
Lawson
K. A.
,
Meneses
J. J.
,
Pedersen
R. A.
(
1991
)
Clonal analysis of epiblast fate during germ layer formation in the mouse embryo.
Development
113
,
891
911
Leyns
L.
,
Bouwmeester
T.
,
Kim
S.-H.
,
Piccolo
S.
,
De Robertis
E. M.
(
1997
)
Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer.
Cell
88
,
747
756
Melby
A. E.
,
Warga
R. M.
,
Kimmel
C. B.
(
1996
)
Specification of cell fates at the dorsal margin of the zebrafish gastrula.
Development
122
,
2225
2237
Melby
A. E.
,
Kimelman
D.
,
Kimmel
C. B.
(
1997
)
Spatial regulation of floating head expression in the developing notochord.
Dev. Dyn
209
,
156
165
O'Reilly
M.-A. J.
,
Smith
J. C.
,
Cunliffe
V.
(
1995
)
Patterning of the mesoderm in Xenopus: dose-dependent and synergistic effects of Brachyury and Pintallavis.
Development
121
,
1351
1359
Odenthal
J.
,
Haffter
P.
,
Vogelsang
E.
,
Brand
M.
,
van Eeden
F. J. M.
,
Furutani-Seiki
M.
,
Granato
M.
,
Hammerschmidt
M.
,
Heisenberg
C.-P.
,
Jiang
Y.-J.
,
Kane
D. A.
,
Kelsh
R. N.
,
Mullins
M. C.
,
Warga
R. M.
,
Allende
M. L.
,
Weinberg
E. S.
,
Nusslein-Volhard
C.
(
1996
)
Mutations affecting the formation of the notochord in the zebrafish, Danio rerio.
Development
123
,
103
115
Oxtoby
E.
,
Jowett
T.
(
1993
)
Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development.
Nucl. Acids Res
21
,
1087
1095
Piccolo
S.
,
Sasai
Y.
,
Lu
B.
,
De Robertis
E. M.
(
1996
)
Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of Chordin to BMP-4.
Cell
86
,
589
598
Placzek
M.
(
1995
)
The role of the notochord and floor plate in inductive interactions.
Curr. Opin. Genet. Dev
5
,
499
506
Postlethwait
J. H.
,
Johnson
S. L.
,
Midson
C. N.
,
Talbot
W. S.
,
Gates
M.
,
Ballinger
E. W.
,
Africa
D.
,
Andrews
R.
,
Carl
T.
,
Eisen
J. S.
,
Horne
S.
,
Kimmel
C. B.
,
Hutchinson
M.
,
Johnson
M.
,
Rodriquez
A.
(
1994
)
A genetic linkage map for the zebrafish.
Science
264
,
699
703
Schulte-Merker
S.
,
Ho
R. K.
,
Herrmann
B. G.
,
Nusslein-Volhard
C.
(
1992
)
The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo.
Development
116
,
1021
1032
Schulte-Merker
S.
,
van Eeden
F. J. M.
,
Halpern
M. E.
,
Kimmel
C. B.
,
Nusslein-Volhard
C.
(
1994
)
no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene.
Development
120
,
1009
1015
Schulte-Merker
S.
,
Lee
K. J.
,
McMahon
A. P.
,
Hammerschmidt
M.
(
1997
)
The zebrafish organizer requires chordino.
Nature
387
,
862
863
Selleck
M. A. J.
,
Stern
C. D.
(
1991
)
Fate mapping and cell lineage analysis of Hensen's node in the chick embryo.
Development
112
,
615
626
Shih
J.
,
Fraser
S. E.
(
1995
)
Distribution of tissue progenitors within the shield region of the zebrafish gastrula.
Development
121
,
2755
2765
Stein
S.
,
Niβ
K.
,
Kessel
M.
(
1996
)
Differential activation of the clustered homeobox genes CNOT2 and CNOT1 during notogenesis in the chick.
Dev. Biol
180
,
519
533
Talbot
W. S.
,
Trevarrow
B.
,
Halpern
M. E.
,
Melby
A. E.
,
Farr
G.
,
Postlethwait
J. H.
,
Jowett
T.
,
Kimmel
C. B.
,
Kimelman
D.
(
1995
)
A homeobox gene essential for zebrafish notochord development.
Nature
378
,
150
157
Thisse
C.
,
Thisse
B.
,
Schilling
T. F.
,
Postlethwait
J. H.
(
1993
)
Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail, and no tail mutant embryos.
Development
119
,
1203
1215
Thisse
C.
,
Thisse
B.
,
Postlethwait
J. H.
(
1995
)
Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos.
Dev. Biol
172
,
86
99
von Dassow
G.
,
Schmidt
J. E.
,
Kimelman
D.
(
1993
)
Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeobox gene.
Genes Dev
7
,
355
366
Wang
S.
,
Krinks
M.
,
Lin
K.
,
Luyten
F. P.
,
Moos
M.
Jr
(
1997
)
Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8.
Cell
88
,
757
766
Weinberg
E. S.
,
Allende
M. L.
,
Kelly
C. S.
,
Abdelhamid
A.
,
Murakami
T.
,
Andermann
P.
,
Doerre
O. G.
,
Grunwald
D. J.
,
Riggleman
B.
(
1996
)
Developmental regulation of zebrafish MyoD in wild-type, no tail, and spadetail embryos.
Development
122
,
271
280
Weinstein
D. C.
,
Ruiz i Altaba
A.
,
Chen
W. S.
,
Hoodless
P.
,
Prezioso
V. R.
,
Jessell
T. M.
,
Darnell
J. E.
Jr
(
1994
)
The winged-helix transcription factor HNF-3β is required for notochord development in the mouse embryo.
Cell
78
,
575
588
Zimmerman
L. B.
,
De Jesús-Escobar
J. M.
,
Harland
R. M.
(
1996
)
The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4.
Cell
86
,
599
606
This content is only available via PDF.