Evidence for the neural crest origin of turtle plastron bones

Clark, Karen; Bender, Günes; Murray, Brian Patrick; Panfilio, Kristen A.; Cook, Steven J.; Davis, Raquel; Murnen, Katherine; Tuan, Rocky S.; Gilbert, Scott F.

doi:10.1002/gene.10012

Cited by 51 publications

(52 citation statements)

References 25 publications

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“…Immunohistochemistry with antibodies to PS1 (a gift of Dr. Carl-Henrik Heldin, Ludwig Institute for Cancer Research, Sweden) and Hall's stain for cartilage and bone were performed on paraffin sections of hatchling turtle carapace as previously described (Clark et al, 2001). For RNA isolation, the carapace of a 14-day old T. scripta hatchling was dissected away from internal tissues and incubated in 2% (w/v) trypsin (Type II, Sigma) in PBS at room temperature for 50 min (modified from Jiang et al,'99).…”

Section: Analysis Of Bone Formation and Bmp2 Expression In The Carapacementioning

confidence: 99%

How the turtle forms its shell: a paracrine hypothesis of carapace formation

et al. 2005

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We propose a two-step model for the evolutionary origin of the turtle shell. We show here that the carapacial ridge (CR) is critical for the entry of the ribs into the dorsal dermis. Moreover, we demonstrate that the maintenance of the CR and its ability to attract the migrating rib precursor cells depend upon fibroblast growth factor (FGF) signaling. Inhibitors of FGF allow the CR to degenerate, with the consequent migration of ribs along the ventral body wall. Beads containing FGF10 can rearrange rib migration in the chick, suggesting that the CR FGF10 plays an important role in attracting the rib rudiments. The co-ordinated growth of the carapacial plate and the ribs may be a positive feedback loop (similar to that of the limbs) caused by the induction of Fgf8 in the distal tips of the ribs by the FGF10-secreting mesenchyme of the CR. Once in the dermis, the ribs undergo endochrondral ossification. We provide evidence that the ribs act as signaling centers for the dermal ossification and that this ossification is due to bone morphogenetic proteins secreted by the rib. Thus, once the ribs are within the dermis, the ossification of the dermis is not difficult to achieve. This relatively rapid means of carapace formation would allow for the appearance of turtles in the fossil record without obvious intermediates.

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Section: Analysis Of Bone Formation and Bmp2 Expression In The Carapacementioning

confidence: 99%

How the turtle forms its shell: a paracrine hypothesis of carapace formation

et al. 2005

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“…1). Because these postcranial skeletal elements express the HNK-1 epitope, which stains a variety of neural crest derivatives, it has been proposed that the plastron derives from the neural crest (Clark et al 2001).…”

Section: Introductionmentioning

confidence: 99%

Msx genes are expressed in the carapacial ridge of turtle shell: a study of the European pond turtle, Emys orbicularis

et al. 2003

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The turtle shell forms by extensive ossification of dermis ventrally and dorsally. The carapacial ridge (CR) controls early dorsal shell formation and is thought to play a similar role in shell growth as the apical ectodermal ridge during limb development. However, the molecular mechanisms underlying carapace development are still unknown. Msx genes are involved in the development of limb mesenchyme and of various skeletal structures. In particular, precocious Msx expression is recorded in skeletal precursors that develop close to the ectoderm, such as vertebral spinous processes or skull. Here, we have studied the embryonic expression of Msx genes in the European pond turtle, Emys orbicularis. The overall Msx expression in head, limb, and trunk is similar to what is observed in other vertebrates. We have focused on the CR area and pre-skeletal shell condensations. The CR expresses Msx genes transiently, in a pattern similar to that of fgf10. In the future carapace domain, the dermis located dorsal to the spinal cord expresses Msx genes, as in other vertebrates, but we did not see expansion of this expression in the dermis located more laterally, on top of the dermomyotomes. In the ventral plastron, although the dermal osseous condensations form in the embryonic Msx-positive somatopleura, we did not observe enhanced Msx expression around these elements. These observations may indicate that common mechanisms participate in limb bud and CR early development, but that pre-differentiation steps differ between shell and other skeletal structures and involve other gene activities than that of Msx genes.

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“…Dermal bone (bone forming directly in the dermis, by bone-forming cells without a preliminary cartilaginous precursor) starts to form between the ribs only after hatching, and its rate of formation is influenced by environmental conditions. [13] The dermal bones meet in the middle between each pair of ribs, and a fibrous suture separates them at their interface. The presence of the sutures allows further growth of the shell, as well as specialized mechanical properties.…”

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confidence: 99%

“…[12][13][14][15][16][17][18] Recently, some histological features of the shell structure have been described by Scheyer and coworkers from a paleontological-evolutionary perspective. [19][20][21][22] However, little is known about the detailed structural aspects of the shell, and their implications on its mechanical function and performance.…”

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confidence: 99%