Transcriptome profiling reveals novel gene networks regulating tooth regeneration in sharks

The dentition of elasmobranchs (sharks, skates and rays) is uniquely productive, capable of both rapid and continuous, lifelong regeneration. Elasmobranchs represent an important group of vertebrates with a deep evolutionary history, possessing several ancient and basal characters, i.e., the continuously regenerative dentition from a specialized dental lamina. The dental lamina is an expanded component of the oral epithelia that is responsible for initiating and producing new teeth among all toothed-vertebrates. In sharks, this dynamic epithelial unit is permanent and continuous – meaning it extends to cover the entirety of each jaw (jaw-wide) and develops early during embryogenesis and retained to produce teeth for the life of the shark. It is rare for a truly embryonic vertebrate tissue to be retained for its original function for the life of the organism. The dental lamina in sharks is unique and houses teeth in a developmental series from the deepest part, where teeth are initiated, through stages of tooth development in the form of a related, family of teeth to eruption and functionality of the advanced teeth at the jaw margin. How teeth are made and regenerated is an important question in vertebrate biology; here we investigated this question in the small spotted catshark (Scyliorhinus canicula), a new model in the field of developmental biology. Specifically, we divided the shark dental lamina into stage-compartments as follows: (i) the initiation site – the successional lamina (SL); (ii) the early developing teeth (ET); (iii) the late stage developing teeth (LT); (iv) the tooth-taste junction between the superficial oral and dental epithelium at the jaw margin that separates the taste territory and the dental lamina proper (TTJ); and basi-hyal oral epithelium that is strictly non-dental and only contains taste buds (BHTB). These 5 compartments each house both a shared and unique signature of gene transcripts. This study aims to understand the transcriptomic basis of continuous tooth regeneration in the shark. In this study we combine X-ray computed tomography, classic histology, insitu hybridization, immunohistochemistry, and functional assays of novel markers, and de novo and genome guided transcriptome assemblies for each of these 5 dental lamina compartments of the hatchling (stage 34) catshark (S. canicula). We produced both a de novo and genome-guided transcriptome assembly and expression analysis of the 5 dental lamina compartments (SL, ET, LT, TTJ and BHTB) of developing dentition in the hatching-stage (stage 34) small-spotted catshark (Scyliorhinus canicula).