April 26, 2016

Significance

The plastron, the order-defining skeletal structure for turtles, provides a bony exoskeleton for the ventral side of the turtle. We provide here the first molecular analysis of plastron bone formation. We show that plastron bone morphogenesis in the ventral mesenchyme employs a program of bone formation that usually characterizes the vertebrate face and skull. The plastron bones, however, have a preliminary step that is not included in head formation: They must suppress the usual chondrogenic programs that would create the sternum cartilage. We suggest that the early osteogenic fate adopted by the ventral mesenchyme prevents the chondrogenic sternal development in turtles and that this was a critical step in forming the ossification centers for this new type of vertebrate structure.

Abstract

The dorsal and ventral aspects of the turtle shell, the carapace and the plastron, are developmentally different entities. The carapace contains axial endochondral skeletal elements and exoskeletal dermal bones. The exoskeletal plastron is found in all extant and extinct species of crown turtles found to date and is synaptomorphic of the order Testudines. However, paleontological reconstructed transition forms lack a fully developed carapace and show a progression of bony elements ancestral to the plastron. To understand the evolutionary development of the plastron, it is essential to know how it has formed. Here we studied the molecular development and patterning of plastron bones in a cryptodire turtle Trachemys scripta. We show that plastron development begins at developmental stage 15 when osteochondrogenic mesenchyme forms condensates for each plastron bone at the lateral edges of the ventral mesenchyme. These condensations commit to an osteogenic identity and suppress chondrogenesis. Their development overlaps with that of sternal cartilage development in chicks and mice. Thus, we suggest that in turtles, the sternal morphogenesis is prevented in the ventral mesenchyme by the concomitant induction of osteogenesis and the suppression of chondrogenesis. The osteogenic subroutines later direct the growth and patterning of plastron bones in an autonomous manner. The initiation of plastron bone development coincides with that of carapacial ridge formation, suggesting that the development of dorsal and ventral shells are coordinated from the start and that adopting an osteogenesis-inducing and chondrogenesis-suppressing cell fate in the ventral mesenchyme has permitted turtles to develop their order-specific ventral morphology.

Development of the turtle plastron, the order-defining skeletal structure.

Proceedings of the National Academy of Sciences (advance online publication)

doi: 10.1073/pnas.1600958113