Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
Abstract
BACKGROUND: Although as humans we lose our tails in the second month of embryonic development, a persistent tail is a prominent structural feature of most adult vertebrates. Indeed, the post-anal tail is part of the definition of a chordate. The internal organization of the developing tail--with neural tube, notochord and paired somites--is the same as that of the main body axis, so it can be expected that the mechanism of tail formation has a close relationship to that of the vertebrate body plan as a whole. Despite this, almost nothing is known about how tails arise.
RESULTS: We present evidence to show that the tail bud of Xenopus laevis arises as the result of interactions between distinct zones of tissue at the posterior of the embryo at the neurula stage. These tissue interactions were demonstrated by manipulations of exogastrulae, which normally form no tail, and by transplantation experiments performed on the neural plate of stage 13 neurulae, whereby embryos with supernumary tails were produced.
CONCLUSIONS: We propose a new model of tail bud determination, termed the NMC model, to explain the results we have obtained. In this model, the tail bud is initiated by an interaction between two territories in the neural plate and a posterior mesodermal territory.
Fig. 1. Tail formation in exogastrulae. (a) Exogastrula, corresponding to control stage 30 (pigmented specimen). (b) In situ hybridization
showing expression of Xpo in an exogastrula and a control embryo at stage 30. The arrow indicates the expression round the circumference
of the waist. (c) Expression of Xnot2 in an exogastrula, control stage 28. The arrow indicates the expression on the dorsal side of
the waist region and in the notochord. (d) Expression of Xbra in an exogastrula, control stage 28. The arrow indicates the expression
round the circumference of the waist. (e) Tail produced by the Einsteck procedure: the top embryo was implanted with the ventral side
of the exogastrula waist region; the bottom embryo was implanted with the dorsal side. (f) Section of tail formed by implantation of an
FDA-labelled exogastrula dorsal waist region. All of the axial tissues (notochord, somites, neural tube) are graft-derived. (g) Tail formation
from exogastrula dorsal waist regions that were folded and allowed to develop to control stage 40. (h) Failure of tail formation
from unfolded dorsal waist regions. Scale bars: (f) 100 pm; (g,h) 500 pm.
Fig. 2. Tail formation from neural plate transplantations. (a) Posterior neural plate explant grafted to an anterior site. (b) Higher-power
view of tail showing fluorescence of the FDA-labelled graft tissue. (c-g) Anterior neural plate explant grafted into a slit within 100 pm
of the blastopore at stage 13. (c) Formation of two tails. (d) Higher-power view showing that FDA-labelled graft tissue is present only in
the neural tube of the posteriortail. (e) Section of a similar specimen; arrows show axial structures. (f) In situ hybridization showing
Xpo expression in both tail buds. (g) Triple-tailed specimen (extra tails indicated by arrow heads). (h-k) Posterior 600 pm of neural plate
rotated through 180° . (h) Formation of two tails. (i) Expression of Xpo in both tail buds. (j) Higher-power view of tails showing FDAlabelled
graft tissue. The neural tube and somites of the anteriortail, and the neural tube of the posteriortail, are labelled. (k) Section of
a similar specimen. Arrows show axial structures. (I) Rotations of 300 pm pieces of the neural plate. Top embryo, rotation 600-900 pm
from blastopore; middle embryo, rotation 300-600 pm from blastopore; and bottom embryo, rotation 0-300 pm from blastopore. A
second tail only arises in the last case. Scale bars: (e) 100 pm, (k) 100 pm. Nt, neural tube; Not, notochord, S, somites.
Fig. 3. Manipulations of stage 13 neurulae.
Fig. 4. NMC model for tail formation. (a,b)
Fate of regions at the caudal end of the
embryo. (a) Dil dot marking the midline
neural plate, less than 100 pm from the
blastopore of a stage 13 embryo, showing
labelling of muscle at stage 35. (b) Dil dot
marking the midline neural plate, more
than 100 pm from the blastopore of a stage
13 embryo, showing labelling of neural
tube floorplate at stage 35. (c) Diagram
depicting the tail bud-forming zone at
stage 13, and the approximate arrangement
of the tail bud tissue types at the late
tail bud stage. The three regions important
for tail development, N, M and C, are
shown. In this model, C is restricted to
about 200 pm from the blastopore, and M
runs from the blastopore to a point about
100 pm along the neural plate. (d) Folding
of the dorsal waist region of an exogastrula
causes the N/M junction to come into contact
with C so that a tail can form (see
Fig. g). (e) Insertion of a piece of anterior
neural plate into a slit in the posterior
neural plate, dividing the M region (surface
red colour indicates fluorescent
labelling). The insertion causes the original
tail N/M junction to be pushed anteriorly
away from its original position. This N/M
boundary was previously over C, and so
has already received a signal from this
region. A tail can thus form, which has no
labelling from the graft. The insertion of
the new N tissue creates two new N/M
boundaries. The more posterior one is
located over C, so a tail would be
expected to form here, the neural tube of
which should be labelled. If the middle
N/M boundary is formed over C, a third
tail would be predicted (see Fig. 2c), but
the inserted piece of N would have to be
extremely small for this to occur. With a
larger piece of inserted N, the middle N/M
junction would not come into contact with
C and so a two-tailed embryo forms (see
Fig. 2c-f). (f) Rotation of a piece of posterior
neural plate by 180 ° . The rotation
shifts the original N/M boundary anteriorly,
but it can form a tail as it has previously
been in contact with C. This tail
would be expected to be labelled. The
rotation forms two new N/M boundaries.
The most posterior is found over C, so a
tail forms, the neural tube of which is
labelled. The new anterior boundary,
however, has no contact with C so does
not form a tail (see Fig. 2h-k).
