Late‐emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron

Abstract

Background: The turtle plastron is composed of a keratinized epidermis overlying nine dermal bones. Its developmental origin has been controversial; recent evidence suggests that the plastral bones derive from trunk neural crest cells (NCCs). Results: This study extends the observations that there is a turtlespecific, second wave of trunk NCC delamination and migration, after the original NCCs have reached their destination and differentiated. This second wave was confirmed by immunohistochemistry in wholemounts and serial sections, by injecting DiI (1,1 0 , di-octadecyl-3,3,3 0 ,3 0 ,-tetramethylindo-carbocyanine perchlorate) into the lumen of the neural tube and tracing labeled cells into the plastron, and by isolating neural tubes from older turtle embryos and observing delaminating NCCs. This later migration gives rise to a plastral ectomesenchyme that expresses NCC markers and can be induced to initiate bone formation. Conclusions: The NCCs of this second migration have properties similar to those of the earlier NCCs, but also express markers characteristic of cranial NCCs. The majority of the cells of the plastron mesenchyme express neural crest markers, and have osteogenic differentiation capabilities that are similar or identical to craniofacial ectomesenchyme. Our evidence supports the contention that turtle plastron bones are derived from a late emigrating population of cells derived from the trunk neural crest. Developmental Dynamics 242:1223-1235, 2013. V C 2013 Wiley Periodicals, Inc.Key words: turtle; neural crest; osteogenesis; plastron; respecification Key findings:There is a turtle-specific population of late-emigrating trunk neural crest cells. These late-emigrating turtle trunk neural crest cells have markers characteristic of cranial neural crest cells. These late-emigrating neural crest cells form an osteogenic ectomesenchyme in the region that generates plastron bones.

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

“…3). This osteogenic potential is maintained in the ventral mesenchyme later in development: mesenchymal cells isolated at G19 differentiated readily into osteoblasts in cell culture (53). At this stage bone spicules begin to form (Fig.…”

“…Several recent studies have shown turtles to be the sister group to the archosaurs (47-51), and a possible ancestral lineage has been proposed (45). The turtle plastron, its possible origin (52,53) and homologies (6,45) to skeletal elements found in other tetrapods have been studied and discussed for decades, yet this is the first study to our knowledge that has established a developmental timeline and location for plastron bone development from their early uncommitted mesenchymal condensations to the development and growth of bone extensions. This study also investigates the patterning information used in plastron bone growth.…”

Molecular Control of the Neural Crest and Peripheral Nervous System Development

“…Unlike cranial NCCs, trunk NCCs are generally restricted from generating ectomesenchymal tissues such as bone and cartilage in vivo (Coelho-Aguiar et al, 2013). However, exceptions have been observed in turtle carapace and plastron development (Cebra-Thomas et al, 2013). NCCs from the vagal and sacral regions generate the enteric nervous system (ENS), while the cranial and sacral NCCs make important contributions to the parasympathetic nervous system.…”

Comparative study of the shell development of hard‐ and soft‐shelled turtles

“…; reviewed by Gross & Hanken, ), it is hypothesized that the turtle crest cells acquire the competence by losing the Hox expression of the trunk – a co‐option of skeletogenic competence from the cephalic neural crest to the trunk neural crest (Cebra‐Thomas et al. , ; Gilbert et al. ).…”