Homologues of the murine Brachyury (T) gene have been cloned from several vertebrates, and are implicated in mesoderm formation and in differentiation of the notochord. In contrast, the roles of the ascidian Brachyury gene may be restricted to presumptive notochord. To understand the evolution of Brachyury genes and their developmental roles, we have searched for homologues in amphioxus, representing the third chordate subphylum and the probable closest relative of the vertebrates. We report the isolation of two amphioxus cDNA clones with clear homology to Brachyury genes, and demonstrate that these derive from separate loci resultant from a recent gene duplication. This finding represents an exception to the emerging consensus of an archetypal prevertebrate genome in amphioxus. The spatial and temporal distribution of Brachyury transcripts during amphioxus development is remarkably similar to vertebrate Brachyury, in presumptive mesoderm, posterior mesoderm and the notochord. Gene expression extends throughout the anteroposterior axis of the notochord, despite the most rostral regions being a more recent specialization; it also persists into larval stages, despite differentiation into contractile tissue. We propose that roles of Brachyury in notochord differentiation are more ancient than roles in mesoderm formation, and that the latter are shared by cephalochordates and all vertebrates.

Reference

Agulnik
S. I.
,
Bollag
R. J.
,
Silver
L. M.
(
1995
)
Conservation of the T-box gene family from Mus musculus to Caenorhabditis elegans.
Genomics
25
,
214
219
Beddington
R. S. P.
,
Smith
J. C.
(
1993
)
Control of vertebrate gastrulation: inducing signals and responding genes.
Curr. Opin. Genet. Dev
3
,
655
661
Bollag
R. J.
,
Siegfried
Z.
,
Cebra-Thomas
J. A.
,
Garvey
N.
,
Davison
E. M.
,
Silver
L. M.
(
1994
)
An ancient family of embryonically expressed mouse genes sharing a conserved protein motif with the T locus.
Nature Genetics
7
,
383
389
Chan
S. J.
,
Cao
Q.-P.
,
Steiner
D. F.
(
1990
)
Evolution of the insulin superfamily: cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus.
Proc. Natl. Acad. Sci. USA
87
,
9319
9323
Chesley
P.
(
1935
)
Development of the short-tailed mutation in the house mouse.
J. exp. Zool
70
,
429
459
Conway Morris
S.
(
1993
)
The fossil record and the early evolution of the Metazoa.
Nature
361
,
219
225
Dickinson
W. J.
(
1995
)
Molecules and morphology: where's the homology?.
Trends Genet
11
,
119
121
Dobrovolskaia-Zavadskaia
N.
(
1927
)
Sur la mortification sponta-nee de la queue chez la souris nouveau-nee et sur l'existence d'un caractere hereditaire ‘non viable’.
C. R. Soc. Biol
97
,
114
116
Flood
P. R.
,
Guthrie
D. M.
,
Banks
J. R.
(
1969
)
Paramyosin muscle in the notochord of amphioxus.
Nature
222
,
87
88
Garcia-Fernàndez
J.
,
Holland
P. W. H.
(
1994
)
Archetypal organization of the amphioxus Hox gene cluster.
Nature
370
,
563
566
Garcia-Fernàndez
J.
,
Baguñà
J.
,
Salo
E.
(
1993
)
Genomic organization and expression of the planarian homeobox genes Dth-1 and Dth-2.
Development
118
,
241
253
Glucksohn-Schönheimer
S.
(
1944
)
The development of normal and homozygous Brachyury (T/T) mouse embryos in the extraembryonic coelom of the chick.
Proc. natl. Acad. Sci. USA
30
,
134
140
Gruneberg
H.
(
1958
)
Genetical studies on the skeleton of the mouse XXIII: the development of Brachyury and Anury.
J. embryol. exp. Morph
6
,
424
443
Guthrie
D. M.
,
Banks
J. R.
(
1970
)
Observations on the function and physiological properties of a fast paramyosin muscle- the notochord of amphioxus (Branchiostoma lanceolatum).
J. exp. Biol
52
,
125
138
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
Herrmann
B. G.
(
1991
)
Expression pattern of the Brachyury gene in whole-mount Twis/Twis mutant embryos.
Development
113
,
913
917
Herrmann
B. G.
,
Kispert
A.
(
1994
)
The T genes in embryogenesis.
Trends Genet
8
,
280
286
Herrmann
B. G.
,
Barlow
D. P.
,
Lehrach
H.
(
1987
)
A large inverted duplication allows homologous recombination between chromosomes heterozygous for the proximal t complex inversion.
Cell
48
,
813
825
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
Holland
P. W. H.
,
Holland
L. Z.
,
Williams
N. A.
,
Holland
N. D.
(
1992
)
An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution.
Development
116
,
653
661
Kispert
A.
,
Herrmann
B. G.
(
1993
)
The Brachyury gene encodes a novel DNA binding protein.
EMBO J
12
,
3211
3220
Kispert
A.
,
Herrmann
B. G.
(
1994
)
Immunohistochemical analysis of the Brachyury protein in wild-type and mutant mouse embryos.
Dev. Biol
161
,
179
193
Kispert
A.
,
Herrmann
B. G.
,
Leptin
M.
,
Reuter
R.
(
1994
)
Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium and Locusta.
Genes Dev
8
,
2137
2150
Kozak
M.
(
1986
)
Point mutations define a sequence flanking AUG initiator codons that modulates translation by eukaryotic chromosomes.
Cell
44
,
283
292
Lacalli
T. C.
,
Holland
N. D.
,
West
J. E.
(
1994
)
Landmarks in the anterior central nervous system of amphioxus larvae.
Phil. Trans. Roy. Soc. B
344
,
165
185
Lundin
L.
(
1993
)
Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse.
Genomics
16
,
1
19
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.
,
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
Sitnikova
T.
,
Rzhetsky
A.
,
Nei
M.
(
1995
)
Interior-branch and bootstrap tests of phylogenetic trees.
Molec. Biol. Evol
12
,
319
333
Smith
J. C.
,
Price
B. M. J.
,
Green
J. B. A.
,
Weigel
D.
,
Herrmann
B. G.
(
1991
)
Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction.
Cell
67
,
79
87
Wada
H.
,
Satoh
N.
(
1993
)
Details of the evolutionary history from invertebrates, as deduced from the sequences of 18S rDNA.
Proc. Natn. Acad. Sci. USA
91
,
1801
1804
Wilkinson
D. G.
,
Bhatt
S.
,
Herrmann
B. G.
(
1990
)
Expression pattern of the mouse T gene and its role in mesoderm formation.
Nature
343
,
657
659
Yasuo
H.
,
Satoh
N.
(
1993
)
Function of the vertebrate T gene.
Nature
364
,
582
583
Yasuo
H.
,
Satoh
N.
(
1994
)
An ascidian homolog of the mouse Brachyury (T) gene is expressed exclusively in notochord cells at the fate restricted stage.
Dev. Growth Differ
36
,
9
18
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