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WIREs Dev Biol
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Development of the vertebrate tailbud

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The anatomical tailbud is a defining feature of all embryonic chordates, including vertebrates that do not end up with a morphological tail. Due to its seamless continuity with trunk tissues, the tailbud is often overlooked as a mere extension of the body axis; however, the formation of the tail from the tailbud undoubtedly involves unique and distinct mechanisms for forming axial tissues, such as the secondary neurulation process that generates the tailbud‐derived spinal cord. Tailbud formation in the frog Xenopus laevis has been demonstrated to involve interaction of three posterior regions of the embryo that first come into alignment at the end of gastrulation, and molecular models for tailbud outgrowth and patterning have been proposed. While classical studies of other vertebrate models, such as the chicken, initially appeared to draw incompatible conclusions, molecular studies have subsequently shown the involvement of at least some similar genetic pathways. Finally, there is an emerging consensus that at least some vertebrate tailbud cells are multipotent progenitors with the ability to form tissues normally derived from different germ layers‐ a trait normally associated with regeneration of complex appendages, or stem‐like cells. WIREs Dev Biol 2015, 4:33–44. doi: 10.1002/wdev.163 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan
Primary vs. secondary neurogenesis. The neural tube of the primary body axis is formed from the rolling up of the lateral edges of ectodermal neural plate toward the midline [marked by the dorsal mesoderm, or notochord, (red circle) that runs directly underneath]. Cells of the neural plate first become columnar and polarized, before becoming wedge shaped, forcing the plate to bend. The neural folds eventually meet in the midline and cell adhesion changes cause budding off from the epidermal epithelium to form the neural tube. The tailbud derived neural tube is derived directly from condensing mesenchymal cells that undergo a mesenchymal to epithelial conversion. Although the source of the cells and the mechanism of tube formation are totally different, the trunk and tail neural tubes form a continuous structure. Diagram based on information in Catala et al.
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A proposed developmental pathway for outgrowth of the tailbud. (a) Drawings of cross sections through a Stage 31 Xenopus tailbud showing the location of the cnh, pw, and expression of five genes. Lfng (lime green) in the dorsal half of the tailbud and dll1/notch (blue) in the posterior wall suggests that notch signaling (hatched blue/green) could be active in the tail tip. Wnt3a (red) is present in a posterior to anterior gradient in the dorsal neural tube and evx1 (purple) in the tailbud tip. (b) Activating notch signaling in a graft in the neural plate of the trunk or anterior TFR results in an ectopic tail containing neural tube from the graft and fin from the host, and with tailbud markers expressed at the tip. If placed too far anterior, the graft fails to make a tail and is incorporated into the host neural tube. If wnt3a is added, anterior grafts also form tails, suggesting Wnt inhibition in anterior neural plate regions prevents notch from inducing tail outgrowth. Data from Beck and Slack.
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The NMC model for tailbud induction and tail inducing assays. (a) dorsal view of Stage 12.5 Xenopus embryo to show approximate location of the tailbud (TB) and tail forming region (TFR), cross‐sectional drawing of same stage through the midline, anterior to left, showing the germ layers and location of the chordoneural hinge (cnh) at the dorsal blastopore lip (boxed). The location of C, N and M regions in the cnh are indicated. B) side view of Stage 24 embryo with dotted line outlining approximate limits of the TFR, cross section through midline to show germ layers (endoderm = yellow, mesoderm = red, and ectoderm = blue), tailbud (boxed), cnh and posterior wall (pw) and the location of the neurenteric canal (nec). Close up of box shows the location of N, M, and C in the tailbud following neurulation, as determined in Tucker and Slack. (c) Grafts of the hinge region of exogastrulae, which contain unfolded NMC regions, or tailbuds, can induce formation of secondary tails if placed inside the blastopore cavity of a blastula stage embryo (einsteck graft). NE, neuroectoderm and ME, mesendoderm. (d) 180° rotations of the neural plate at Stage 13 result in the formation of two new N/M boundaries. The posterior one lies over C and is induced to form a secondary tail in the normal location, the original N/M boundary has been exposed to C and so develops into a tail with reversed dorsal (d) ventral (v) polarity and the most anterior one does not form a tail, as it has not received a C signal. (e) Tailbud inducing activity assay, animal caps expressing test genes are removed at Stages 9–10 and trimmed into 100 × 600 μM rectangles before inserting into the neural plate of a host Stage 13 embryo. Ectopic tails may be formed from the graft if they contain tailbud‐like activity. In this case, the dorsal ventral polarity seems to come from the host. Germ layers in A and B are coloured as standard: Blue for ectoderm, red for mesoderm and yellow for endoderm. The M region is mesodermal in fate but ectodermal in origin and is therefore coloured purple. Data from Tucker and Slack, and Beck and Slack.
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The Xenopus tailbud does not regenerate. (a) Stage 28 tadpole key showing regions extirpated and corresponding bar graph of the number of somites formed by Stage 40. Colour of dotted line indicates extirpated region in bar graph. Uncut tadpoles generate 42 somites. Removal of the tail forming region (TFR, which includes trunk derived post anal tail tissues), leaves only 13 somites. Removal of the anatomical tailbud (TB) leaves 19 somites, and removal of smaller parts of the tailbud results in a corresponding decrease in the number of somites absent at stage 40. (b) Drawings indicating the effect of removing either the tail forming region or the tailbud at Stage 28 and culturing the two pieces separately. The extirpated TFR and TB develop autonomously, but the number of somites combined between explant and remaining tadpole is always 42. The ‘tail’ seen following removal of the tailbud is formed from displaced trunk tissues, and not by regeneration. Data from Tucker and Slack.
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