The avian equivalent of Spemann's organizer, Hensen's node, begins to lose its ability to induce a nervous system from area opaca epiblast cells at stage 4+, immediately after the full primitive streak stage. From this stage, the node is no longer able to induce regions of the nervous system anterior to the hindbrain. Stage 4+ is marked by the emergence from the node of a group of cells, the prechordal mesendoderm. Here we have investigated whether the prechordal region possesses the lost functions of the organizer, using quail-chick chimaeras to distinguish graft- and host-derived cells, together with several region-specific molecular markers. We find that the prechordal region does not have neural inducing ability, as it is unable to divert extraembryonic epiblast cells to a neural fate. However, it can confer more anterior character to prospective hindbrain cells of the host, making them acquire expression of the forebrain markers tailless and Otx-2. It can also rescue the expression of Krox-20 and Otx-2 from nervous system induced by an older (stage 5) node in extraembryonic epiblast. We show that these properties reflect a true change of fate of cells rather than recruitment from other regions. The competence of neuroectoderm to respond to anteriorizing signals declines by stages 7–9, but both posteriorizing signals and the ability of neuroectoderm to respond to them persist after this stage.

REFERENCES

Adelman
H. B.
(
1922
)
The significance of the prechordal plate: an interpretative study.
Am. J. Anat
31
,
55
101
Ang
S. L.
,
Conlon
R. A.
,
Jin
O.
,
Rossant
J.
(
1994
)
Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants.
Development
120
,
2979
2989
Ang
S. L.
,
Rossant
J.
(
1993
)
Anterior mesendoderm induces mouse engrailed genes in explant cultures.
Development
118
,
139
149
Ang
S. L.
,
Rossant
J.
(
1994
)
HNF-3is essential for node and notochord formation in mouse development.
Cell
78
,
561
574
Bally-Cuif
L.
,
Alvarado-Mallart
R. M.
,
Darnell
D. K.
,
Wassef
M.
(
1992
)
Relationship between Wnt-1 and En-2 expression domains during early development of normal and ectopic met-mesencephalon.
Development
115
,
999
1009
Bally-Cuif
L.
,
Gulisano
M.
,
Broccoli
V.
,
Boncinelli
E.
(
1995
)
c-otx2 is expressed in two different phases of gastrulation and is sensitive to retinoic acid treatment in chick embryo.
Mech. Dev
49
,
49
63
Chavrier
P.
,
Zerial
M.
,
Lemaire
P.
,
Almendral
J.
,
Bravo
R.
,
Charnay
P.
(
1988
)
A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells.
EMBO J
7
,
29
35
Clavert
A.
(
1978
)
Étude de la formation et de l'evolution normale et pathologique de l'ebauche neurectodermique de l'oeil.
Arch. Anat. Histol. Embryol
61
,
89
142
Couly
G. F.
,
Coltey
P. M.
,
Le Douarin
N. M.
(
1992
)
The developmental fate of the cephalic mesoderm in quail-chick chimeras.
Development
114
,
1
15
Cox
W. G.
,
Hemmati-Brivanlou
A.
(
1995
)
Caudalization of neural fate by tissue recombination and bFGF.
Development
121
,
4349
4358
Darnell
D. K.
,
Schoenwolf
G. C.
,
Ordahl
C. P.
(
1992
)
Changes in dorsoventral but not rostrocaudal regionalization of the chick neural tube in the absence of cranial notochord, as revealed by expression of engrailed-2.
Dev. Dynam
193
,
389
396
Dias
M. S.
,
Schoenwolf
G. C.
(
1990
)
Formation of ectopic neuroepithelium in chick blastoderms: age related capacities for induction and self-differentiation following transplantation of quail Hensen's nodes.
Anat. Rec
229
,
437
448
Doniach
T.
(
1993
)
Planar and vertical induction of anteroposterior pattern during the development of the amphibian central nervous system.
J. Neurobiol
24
,
1256
1275
Doniach
T.
,
Philips
C. R.
,
Gerhart
J. C.
(
1992
)
Planar induction of anteroposterior pattern in the developing central nervous system of Xenopus laevis.
Science
257
,
542
545
Fukushima
M.
,
Nakamura
M.
,
Ohta
K.
,
Okamura
R.
,
Negi
A.
(
1996
)
Regional specification of motoneurons along the anterior-posterior axis is independent of the notochord.
Development
122
,
905
914
Gallera
J.
(
1948
)
Recherches comparees sur le developpement du neuroblaste prechordal transplante sur l'embryon ou enrobe dans l'ectoblaste ‘in vitro’ (‘Triton alpestris’).
Rev. Suisse Zool
55
,
295
303
Gallera
J.
(
1970
)
Difference de la reactivite à l'inducteur neurogene entre l'ectoblaste de l'aire opaque et celui de l'aire pellucide chez le poulet.
Experientia
26
,
1353
1354
Gallera
J.
(
1971
)
Primary induction in birds.
Adv. Morph
9
,
149
180
García-Martínez
V.
,
Álvarez
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
Gardner
C. A.
,
Barald
K. F.
(
1992
)
Expression patterns of Engrailed-like proteins in the chick embryo.
Dev. Dynam
193
,
370
388
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
Grapin-Botton
A.
,
Bonnin
M. A.
,
McNaughton
L. A.
,
Krumlauf
R.
,
Le Douarin
N.
(
1995
)
Plasticity of transposed rhombomeres: Hox gene induction is correlated with phenotypic modifications.
Development
121
,
2707
2721
Hamburger
V.
,
Hamilton
H. L.
(
1951
)
A series of normal stages in the development of the chick embryo.
J. Morph
88
,
49
92
Hemmati-Brivanlou
A.
,
Kelly
O. G.
,
Melton
D. A.
(
1994
)
Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity.
Cell
77
,
238
295
Hermesz
E.
,
Mackem
S.
,
Mahon
K. A.
(
1996
)
Rpx: a novel anterior-restricted homeobox gene progressively activated in the prechordal plate, anterior neural plate and Rathke's pouch of the mouse embryo.
Development
122
,
41
52
Honig
M. G.
,
Hume
R. I.
(
1989
)
Di and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing.
Trends Neurosci
12
,
333
336
Itasaki
N.
,
Ichijo
H.
,
Hama
L.
,
Matsuno
T.
,
Nakamura
H.
(
1991
)
Establishment of rostrocaudal polarity in tectal primordium: engrailed expression and subsequent rectal polarity.
Development
113
,
1133
1144
Itasaki
N.
,
Sharpe
J.
,
Morrison
A.
,
Krumlauf
R.
(
1996
)
Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition.
Neuron
16
,
487
500
Izpisúa-Belmonte
J. C.
,
De Robertis
E. M.
,
Storey
K. G.
,
Stern
C. D.
(
1993
)
The homeobox gene goosecoid and the origin of the organizer cells in the early chick blastoderm.
Cell
74
,
645
659
Jacob
M.
,
Jacob
H. J.
,
Wachtler
F.
,
Christ
B.
(
1984
)
Ontogeny of avian extrinsic ocular muscles. I. A light-and electron-microscopic study.
Cell Tiss. Res
237
,
549
557
Johnston
M. C.
,
Noden
D. M.
,
Hazelton
R. D.
,
Coulombre
J. L.
,
Coulombre
A. J.
(
1979
)
Origins of avian ocular and periocular tissues.
Exp Eye Res
29
,
27
43
Kintner
C. R.
,
Dodd
J.
(
1991
)
Hensen's node induces neural tissue inXenopus ectoderm. Implications for the action of the organizer in neural induction.
Development
113
,
1495
1505
Lamb
T. M.
,
Harland
R. M.
(
1995
)
Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern.
Development
121
,
3627
3636
Lamb
T. M.
,
Knecht
A. K.
,
Smith
W. C.
,
Stachel
S. E.
,
Economides
A. N.
,
Stahl
N.
,
Yancopoulos
G. D.
,
Harland
R. M.
(
1993
)
Neural induction by the secreted polypeptide noggin.
Science
262
,
713
718
Launay
C.
,
Fromentoux
V.
,
Shi
D. L.
,
Boucaut
J. C.
(
1996
)
A truncated FGF receptor blocks neural induction by endogenous Xenopus inducers.
Development
122
,
869
880
Lemaire
L.
,
Roesser
T.
,
Izpisúa-Belmonte
J. C.
,
Kessel
M.
(
1997
)
Segregating expression domains of two goosecoid genes during the transition from gastrulation to neurulation in chick embryos.
Development
124
,
1443
1452
Liem
K. F.
Jr.
,
Tremml
G.
,
Roelink
H.
,
Jessell
T. M.
(
1995
)
Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm.
Cell
82
,
969
979
McGrew
L. L.
,
Lai
C. J.
,
Moon
R. T.
(
1995
)
Specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin.
Dev. Biol
172
,
337
342
Martínez
S.
,
Wassef
M.
,
Alvarado-Mallart
R. M.
(
1991
)
Induction of a mesencephalic phenotype in the 2-day-old chick prosencephalon is preceded by the early expression of the homeobox gene en.
Neuron
6
,
971
981
Meier
S.
(
1981
)
Development of the chick embryo mesoblast: morphogenesis of the prechordal plate and cranial segments.
Dev. Biol
83
,
49
61
Monaghan
A. P.
,
Grau
E.
,
Bock
D.
,
Schutz
G.
(
1995
)
The mouse homolog of the orphan nuclear receptor tailless is expressed in the developing forebrain.
Development
121
,
839
853
Nakamura
H.
,
Itasaki
N.
,
Matsuno
T.
(
1994
)
Rostrocaudal polarity formation of chick optic tectum.
Int. J. Dev. Biol
38
,
281
286
New
D. A. T.
(
1955
)
A new technique for the cultivation of the chick embryo in vitro.
J. Embryol. exp. Morph
3
,
326
331
Nicholas
J. S.
,
Oppenheimer
J. M.
(
1942
)
Regulation and reconstitution in Fundulus.
J. exp. Zool
90
,
127
153
Nieuwkoop
P. D.
,
Boterenbrood
E. C.
,
Kremer
A.
,
Bloesma
F. F. S. N.
,
Hoessels
E. L. M. J.
,
Meyer
G.
,
Verheyen
F. J.
(
1952
)
Activation and organization of the central nervous system in amphibians.
J. exp. Zool
120
,
1
108
Nieuwkoop
P. D.
,
Nigtevecht
G. V.
(
1954
)
Neural activation and transformation in explants of competent ectoderm under the influence of fragments of anterior notochord in urodeles.
J. Embryol. exp. Morph
2
,
175
193
Noden
D. M.
(
1988
)
Interactions and fates of avian craniofacial mesenchyme.
Development
103
,
121
140
Oliver
G.
,
Loosli
F.
,
Köster
J.
,
Wittbrodt
J.
,
Gruss
P.
(
1996
)
Ectopic lens induction in fish in response to the murine homeobox gene Six3.
Mech. Dev
60
,
233
239
Pannese
M.
,
Polo
C.
,
Andreazzoli
M.
,
Vignali
R.
,
Kablar
B.
,
Barsacchi
G.
,
Boncinelli
E.
(
1995
)
The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions.
Development
121
,
707
720
Patel
N. H.
,
Martín-Blanco
E.
,
Coleman
K. G.
,
Poole
S. J.
,
Ellis
M. C.
,
Kornberg
T. B.
,
Goodman
C. S.
(
1989
)
Expression of the engrailed proteins in arthropods, annelids and chordates.
Cell
58
,
955
968
Placzek
M.
,
Tessier-Lavigne
M.
,
Yamada
T.
,
Jessell
T.
,
Dodd
J.
(
1990
)
Mesodermal control of neural cell identity: floor plate induction by the notochord.
Science
250
,
985
988
Riddle
R. D.
,
Johnson
R. L.
,
Laufer
E.
,
Tabin
C.
(
1993
)
Sonic hedgehog mediates the polarizing activity of the ZPA.
Cell
75
,
1401
1416
Rosenquist
G. C.
(
1983
)
The chorda center in Hensen's node of the chick embryo.
Anat. Rec
207
,
349
355
Ruiz i Altaba
A.
(
1993
)
Induction and axial patterning of the neural plate: planar and vertical signals.
J. Neurobiol
24
,
1276
304
Sasai
Y.
,
Lu
B.
,
Steinbeisser
H.
,
De Robertis
E. M.
(
1995
)
Regulationof neural induction by the Chd and BMP-4 antagonistic patterning signals in Xenopus.
Nature
376
,
333
336
Schoenwolf
G. C.
(
1992
)
Morphological and mapping studies of the paranodal and postnodal levels of the neural plate during chick neurulation.
Anat. Rec
233
,
281
290
Schoenwolf
G. C.
,
Sheard
P.
(
1990
)
Fate mapping the avian epiblast with focal injections of a fluorescent-histochemical marker: ectodermal derivatives.
J. exp. Zool
255
,
323
339
Seifert
R.
,
Jacob
M.
,
Jacob
H. J.
(
1993
)
The avian prechordal head region: a morphological study.
J. Anat
183
,
75
89
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.
(
1996
)
Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage.
Development
122
,
1313
1322
Simeone
A.
,
Avantaggiato
V.
,
Moroni
M. C.
,
Mavilio
F.
,
Arra
C.
,
Cotelli
F.
,
Nigro
V.
,
Acampora
D.
(
1995
)
Retinoic acid induces stage-specific antero-posterior transformation of rostral central nervous system.
Mech. Dev
51
,
83
98
Smith
J. L.
,
Schoenwolf
G. C.
,
Quan
J.
(
1994
)
Quantitative analyses of neuroepithelial cell shapes during bending of the mouse neural plate.
J. Comp. Neurol
342
,
144
151
Spratt
N. T.
(
1952
)
Localization of the prospective neural plate in the early chick blastoderm.
J. exp. Zool
120
,
109
130
Spratt
N. T.
(
1955
)
Analysis of the organizer center in the chick embryo. I Localization of notochord and somite cells.
J. Exp. Zool
128
,
121
163
Stern
C. D.
(
1990
)
The marginal zone and its contribution to the hypoblast and primitive streak of the chick embryo.
Development
109
,
667
682
Stern
C. D.
,
Ireland
G. W.
(
1981
)
An integrated experimental study of endoderm formation in avian embryos.
Anat. Embryol
163
,
245
263
Storey
K. G.
,
Crossley
J. M.
,
De Robertis
E. M.
,
Norris
W. E.
,
Stern
C. D.
(
1992
)
Neural induction and regionalisation in the chick embryo.
Development
114
,
729
741
Storey
K. G.
,
Selleck
M. A. J.
,
Stern
C. D.
(
1995
)
Induction by different subpopulations of cells in Hensen's node.
Development
121
,
417
428
Streit
A.
,
Stern
C. D.
,
Thery
C.
,
Ireland
G. W.
,
Aparicio
S.
,
Sharpe
M. J.
,
Gherardi
E.
(
1995
)
A role for HGF/SF in neural induction and its expression in Hensen's node during gastrulation.
Development
121
,
813
824
Streit
A.
,
Sockanathan
S.
,
Rex
M.
,
Scotting
P. J.
,
Sharpe
P. T.
,
Lovell-Badge
R.
,
Stern
C. D.
(
1997
)
Preventing the loss of competence for neural induction: HGF/SF, L5 and Sox-2.
Development
124
,
1191
1202
Sulik
K.
,
Dehart
D. B.
,
Inagaki
T.
,
Carson
J. L.
,
Vrablic
T.
,
Gesteland
K.
,
Schoenwolf
G. C.
(
1994
)
Morphogenesis of the murine node and notochordal plate.
Dev. Dynamics
201
,
260
278
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
Thery
C.
,
Sharpe
M. J.
,
Batley
S. J.
,
Stern
C. D.
,
Gherardi
E.
(
1995
)
Expression of HGF/SF, HGFl/MSP, and c-met suggests new functions during early chick development.
Dev. Genet
17
,
90
101
Thomas
P.
,
Beddington
R.
(
1996
)
Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo.
Curr. Biol
6
,
1487
1496
Ulshafer
R. J.
,
Clavert
A.
(
1979
)
The use of avian double monsters in studies on induction of the nervous system.
J. Embryol. exp. Morph
53
,
237
243
Uwanogho
D.
,
Rex
M.
,
Cartwright
E. J.
,
Pearl
G.
,
Healy
C.
,
Scotting
P. J.
,
Sharpe
P. T.
(
1995
)
Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development.
Mech. Dev
49
,
23
36
Varlet
I.
,
Collignon
J.
,
Robertson
E. J.
(
1997
)
Nodal expression in the primitive endoderm is required for the specification of the anterior axis during mouse gastrulation.
Development
124
,
1033
1044
Viebahn
C.
,
Mayer
B.
,
Hrabe-de-Angelis
M.
(
1995
)
Signs of the principal body axes prior to primitive streak formation in the rabbit embryo.
Anat. Embryol
192
,
159
169
Wachtler
F.
,
Jacob
H. J.
,
Jacob
M.
,
Christ
B.
(
1984
)
The extrinsic ocular muscles in birds are derived from the prechordal plate.
Naturwiss
71
,
379
380
Waddington
C. H.
(
1932
)
Experiments on the development of chick and duck embryos, cultivated in vitro.
Phil. Trans. R. Soc. Lond. B
221
,
179
230
Waddington
C. H.
(
1933
)
Induction by the primitive streak and its derivatives in the chick.
J. exp. Biol
10
,
38
46
Waddington
C. H.
(
1934
)
Experiments on embryonic induction.
J. exp. Biol
11
,
211
227
Waddington
C. H.
(
1936
)
Organisers in mammalian development.
Nature
138
,
125
–.
Weinstein
D. C.
,
Ruiz i Altaba
A.
,
Chen
W. S.
,
Hoodless
P.
,
Prezioso
V. R.
,
Jessell
T. M.
,
Darnell
J. E.
(
1994
)
The winged-helix transcription factor HNF-3is required for notochord development in the mouse embryo.
Cell
78
,
575
588
Wilkinson
D. G.
,
Bhatt
S.
,
Chavrier
P.
,
Bravo
R.
,
Charnay
P.
(
1989
)
Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse.
Nature
337
,
461
464
Yamada
T.
(
1994
)
Caudalization by the amphibian organizer: brachyury, convergent extension and retinoic acid.
Development
120
,
3051
3062
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
Yu
R. T.
,
McKeown
M.
,
Evans
R. M.
,
Umesono
K.
(
1994
)
Relationship between Drosophila gap gene tailless and a vertebrate nuclear receptor Tlx.
Nature
370
,
375
379
This content is only available via PDF.