An ancient dental gene set governs development and continuous regeneration of teeth in sharks

Abstract

The evolution of oral teeth is considered a major contributor to the overall success of jawed vertebrates. This is especially apparent in cartilaginous fishes including sharks and rays, which develop elaborate arrays of highly specialized teeth, organized in rows and retain the capacity for life-long regeneration. Perpetual regeneration of oral teeth has been either lost or highly reduced in many other lineages including important developmental model species, so cartilaginous fishes are uniquely suited for deep comparative analyses of tooth development and regeneration. Additionally, sharks and rays can offer crucial insights into the characters of the dentition in the ancestor of all jawed vertebrates. Despite this, tooth development and regeneration in chondrichthyans is poorly understood and remains virtually uncharacterized from a developmental genetic standpoint. Using the emerging chondrichthyan model, the catshark (Scyliorhinus spp.), we characterized the expression of genes homologous to those known to be expressed during stages of early dental competence, tooth initiation, morphogenesis, and regeneration in bony vertebrates. We have found that expression patterns of several genes from Hh, Wnt/β-catenin, Bmp and Fgf signalling pathways indicate deep conservation over ~450 million years of tooth development and regeneration. We describe how these genes participate in the initial emergence of the shark dentition and how they are redeployed during regeneration of successive tooth generations. We suggest that at the dawn of the vertebrate lineage, teeth (i) were most likely continuously regenerative structures, and (ii) utilised a core set of genes from members of key developmental signalling pathways that were instrumental in creating a dental legacy redeployed throughout vertebrate evolution. These data lay the foundation for further experimental investigations utilizing the unique regenerative capacity of chondrichthyan models to answer evolutionary, developmental, and regenerative biological questions that are impossible to explore in classical models.

Morphology and distribution of taste papillae and oral denticles in the developing oropharyngeal cavity of the bamboo shark,Chiloscyllium punctatum

“…Our findings reveal that taste papillae appear early in development, closely linked with the timing of tooth development (Rasch et al, 2016) and we show that these taste buds are functional during later stages of embryo development before hatching. Densities of taste papillae were greatest in oral regions associated with the dentition and we suggest that there is a relationship between prey contact (jaws and teeth) and taste papillae density.…”

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

“…Fixed samples were stained with Alcian blue (cartilage) and/or Alizarin red S as previously described (14).…”

“…Probes for β-catenin, bmp4, fgf3, fgf10, lef1, shh, sox2, and pitx2 were cloned as described previously (14). A 1-kb probe for sparc was cloned using the primer sequences (Forward-GCCTGGTGCTCTCTCACTG, Reverse-TAGCGATGGGCAGCAATAG).…”

“…1 and Movie S1). The shark dentition, emerging from tightly constrained developmental fields on the anterior jaw margins (6,14), includes adjoining tooth families embedded within a permanent epithelial dental lamina (DL) (Fig. 1 C-G).…”

Animal models of craniofacial anomalies

“…Chicken embryos are also easily manipulated and have been used to model both genetic and environmental factors contributing to craniofacial anomalies (Kiecker, 2016;Schock et al, 2015). Several comparative systems are also highlighted, such as avian models, and the new and emerging cichlid fishes and catsharks (Fish, 2015;Powder and Albertson, 2015;Rasch et al, 2016). Finally, a very intriguing paper proposes the use of wasp genetics to understand complex genetic interactions in the craniofacial complex (Werren et al, 2015).…”