Using fate mapping techniques, we have analyzed development of cells of the dorsal marginal region in wild-type and mutant zebrafish. We define a domain in the early gastrula that is located just at the margin and centered on the dorsal midline, in which most cells generate clones that develop exclusively as notochord. The borders of the notochord domain are sharp at the level of single cells, and coincide almost exactly with the border of the expression domain of the homeobox gene floating head (flh; zebrafish homologue of Xnot), a gene essential for notochord development. In flh mutants, cells in the notochord domain generate clones of muscle cells. In contrast, notochord domain cells form mesenchyme in embryos mutant for no tail (ntl; zebrafish homologue of Brachyury). A minority of cells in the notochord domain in wild-type embryos develop as unrestricted mesoderm, invariably located in the tail, suggesting that early gastrula expression of flh does not restrict cellular potential to the notochord fate. The unrestricted tail mesodermal fate is also expressed by the forerunner cells, a cluster of cells located outside the blastoderm, adjacent to the notochord domain. We show that cells can leave the dorsal blastoderm to join the forerunners, suggesting that relocation between fate map domains might respecify notochord domain cells to the tail mesodermal fate. An intermediate fate of the forerunners is to form the epithelial lining of Kupffer's vesicle, a transient structure of the teleost tailbud. The forerunners appear to generate the entire structure of Kupffer's vesicle, which also develops in most flh mutants. Although forerunner cells are present in ntl mutants, Kupffer's vesicle never appears, which is correlated with the later severe disruption of tail development.

Reference

Davidson
E. H.
(
1990
)
How embryos work: a comparative view of diverse modes of cell fate specification.
Development
108
,
365
389
Davidson
E. H.
(
1993
)
Later embryogenesis: regulatory circuitry in morphogenetic fields.
Development
118
,
665
690
Fan
C. M.
,
Tessier Lavigne
M.
(
1994
)
Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog.
Cell
79
,
1175
1186
Garcia Martinez
V.
,
Alvarez
I. S.
,
Schoenwolf
G. C.
(
1993
)
Locations of the ectodermal and nonectodermal subdivisions of the epiblast at stages 3 and 4 of avian gastrulation and neurulation.
J. Exp. Zool
267
,
431
446
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
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
Hammerschmidt
M.
,
Nusslein-Volhard
C.
(
1993
)
The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation.
Development
119
,
1107
1118
Hashimoto
K.
,
Fujimoto
H.
,
Nakatsuji
N.
(
1987
)
An ECM substratumallows mouse mesodermal cells isolated from the primitive streak to exhibit motility similar to that inside the mouse embryo and reveals a deficiency in the T/T mutant cells.
Development
100
,
587
598
Hatta
K.
,
Kimmel
C. B.
(
1993
)
Midline structures and central nervous system coordinates in zebrafish.
Perspect. Dev. Neurobiol
1
,
257
268
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
Hauptmann
G.
,
Gerster
T.
(
1994
)
Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos.
Trends Genet
10
,
266
–.
Ho
R. K.
,
Kane
D. A.
(
1990
)
Cell-autonomous action of zebrafish spt-1 mutation in specific meosdermal precursors.
Nature
348
,
728
730
Ho
R. K.
,
Kimmel
C. B.
(
1993
)
Commitment of cell fate in the early zebrafish embryo.
Science
261
,
109
111
Joly
J. S.
,
Joly
C.
,
Schulte-Merker
S.
,
Boulekbache
H.
,
Condamine
H.
(
1993
)
The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos.
Development
119
,
1261
1275
Jowett
T.
,
Lettice
L.
(
1994
)
Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin-and fluorescein-labeled probes.
Trends Genet
10
,
73
74
Keller
R. E.
(
1975
)
Vital dye mapping of the gastrula and neurula of Xenopus laevis. I. Prospective areas and morphogenetic movements of the superficial layer.
Dev. Biol
42
,
222
241
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.
,
Ballard
W. W.
,
Kimmel
S. R.
,
Ullmann
B.
,
Schilling
T. F.
(
1995
)
Stages of embryonic development of the zebrafish.
Dev. Dyn
203
,
253
310
Kimmel
C. B.
,
Warga
R. M.
(
1987
)
Cell lineages generating axial muscle in the zebrafish embryo.
Nature
327
,
234
237
Kimmel
C. B.
,
Warga
R. M.
,
Schilling
T. F.
(
1990
)
Origin and organization of the zebrafish fate map.
Development
108
,
581
594
Kispert
A.
,
Hermann
B. G.
(
1993
)
The Brachyury gene encodes a novel DNA binding protein.
EMBOJ
12
,
4898
4899
Koseki
H.
,
Wallin
J.
,
Wilting
J.
,
Mizutani
Y.
,
Kispert
A.
,
Ebensperger
C.
,
Herrmann
B. G.
,
Christ
B.
,
Balling
R.
(
1993
)
A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae.
Development
119
,
649
660
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
Myers
P. Z.
,
Bastiani
M. J.
(
1991
)
NeuroVideo: a program for capturing and processing time-lapse video.
Comput. Methods Programs Biomed
34
,
27
33
O'Reilly
M. A.
,
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
Oppenheimer
J. M.
(
1936
)
Processes of localization in developing Fundulus.
J. Exp. Biol
73
,
405
444
Pasteels
J.
(
1943
)
Proliferations et croissance dans la gastrulation et la formation de la queue des Vertebres.
Arch. Biol
54
,
2
51
Raible
D. W.
,
Wood
A.
,
Hodsdon
W.
,
Henion
P. D.
,
Weston
J. A.
,
Eisen
J. S.
(
1992
)
Segregation and early dispersal of neural crest cells in the embryonic zebrafish.
Dev. Dyn
195
,
29
42
Sasai
Y.
,
Lu
B.
,
Steinbeisser
H.
,
Geissert
D.
,
Gont
L. K.
,
De Robertis
E. M.
(
1994
)
Xenopuschordin: a novel dorsalizing factor activated by organizer-specific homeobox genes.
Cell
79
,
779
790
Schilling
T. F.
,
Kimmel
C. B.
(
1994
)
Segment and cell type lineagerestrictions during pharyngeal arch development in the zebrafish embryo.
Development
120
,
483
494
Schoenwolf
G. C.
,
Garcia Martinez
V.
,
Dias
M. S.
(
1992
)
Mesoderm movement and fate during avian gastrulation and neurulation.
Dev. Dyn
193
,
235
248
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.
,
Hammerschmidt
M.
,
Beuchle
D.
,
Cho
K. W.
,
De Robertis
E. M.
,
Nusslein-Volhard
C.
(
1994
)
Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos.
Development
120
,
843
852
Schulte-Merker
S.
,
van Eeden
F. J.
,
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
Selleck
M. A.
,
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
Smith
J. L.
,
Gesteland
K. M.
,
Schoenwolf
G. C.
(
1994
).
Prospective fate map of the mouse primitive streak at 7.5 days of gestation.
Dev. Dyn
201
,
279
89
Stachel
S. E.
,
Grunwald
D. J.
,
Myers
P. Z.
(
1993
)
Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish.
Development
117
,
1261
1274
Strähle
U.
,
Blader
P.
,
Henrique
D.
,
Ingham
P. W.
(
1993
)
axial, a zebrafish gene expressed along the developing body axis, shows altered expression in cyclops mutant embryos.
Genes Dev
7
,
1436
1446
Streisinger
G.
,
Singer
F.
,
Walker
C.
,
Knauber
D.
,
Dower
N.
(
1986
)
Segregation analysis and gene-centromere distances in zebrafish.
Genetics
112
,
311
319
Talbot
W.
,
Trevarrow
W.
,
Halpern
M. E.
,
Melby
A. E.
,
Farr
H.
,
Postlethwait
J. H.
,
Jowett
T.
,
Kimmel
C. B.
,
Kimelman
D.
(
1995
)
Requirement for the homeobox gene floating head in zebrafish notochord development.
Nature
378
,
150
157
Thisse
C.
,
Thisse
B.
,
Halpern
M. E.
,
Postlethwait
J. H.
(
1994
)
goosecoid expression in neurectoderm and mesendoderm is disrupted in zebrafish cyclops gastrulas.
Dev. Biol
164
,
420
429
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
Tucker
A. S.
,
Slack
J. M. W.
(
1995
)
The Xenopus laevis tail-forming region.
Development
121
,
249
262
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 homeo box gene.
Genes Dev
7
,
355
66
Warga
R. M.
,
Kimmel
C. B.
(
1990
)
Cell movements during epiboly and gastrulation in zebrafish.
Development
108
,
569
580
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
Weintraub
H.
(
1993
)
The MyoD family and myogenesis: redundancy, networks, and thresholds.
Cell
75
,
1241
4
Wilson
V.
,
Manson
L.
,
Skarnes
W. C.
,
Beddington
R. S.
(
1995
)
The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation.
Development
121
,
877
886
Wilson
V.
,
Rashbass
P.
,
Beddington
R. S.
(
1993
)
Chimeric analysis of T (Brachyury) gene function.
Development
117
,
1321
1331
Wood
A.
,
Thorogood
P.
(
1984
)
An analysis of in vivo cell migration during teleost fin morphogenesis.
J. Cell Sci
66
,
205
222
Yamada
T.
,
Placzek
M.
,
Tanaka
H.
,
Dodd
J.
,
Jessell
T. M.
(
1991
)
Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord.
Cell
64
,
635
647
This content is only available via PDF.