Abstract
Deep understanding of tooth regeneration is hampered by the lack of lifelong replacing oral dentition in most conventional models. Here, we show that the bearded dragon, one of the rare vertebrate species with both polyphyodont and monophyodont teeth, constitutes a key model for filling this gap, allowing direct comparison of extreme dentition types. Our developmental and high-throughput transcriptomic data of microdissected dental cells unveils the critical importance of successional dental lamina patterning, in addition to maintenance, for vertebrate tooth renewal. This patterning process happens at various levels, including directional growth but also gene expression levels, dynamics, and regionalization, and involves a large number of yet uncharacterized dental genes. Furthermore, the alternative renewal mechanism of bearded dragon dentition, with dual location of slow-cycling cells, demonstrates the importance of cell migration and functional specialization of putative epithelial stem/progenitor niches in tissue regeneration, while expanding the diversity of dental replacement strategies in vertebrates.
Highlights
Exposed to the oral cavity of most jawed vertebrates, teeth are continually worn down through food acquisition, a process that must be compensated to maintain the oral apparatus functional (Berkovitz and Shellis, 2016)
The central-most tooth projecting forwards in the midline of the premaxilla consists of the large egg-tooth, which is later replaced by a regular pleurodont successor (Figure 1A)
To visualize oral soft tissue, including the dental lamina (DL) structure, we stained the jaws of juvenile bearded dragons with the contrast agent phosphotungstic acid (PTA) before CT-scanning
Summary
Exposed to the oral cavity of most jawed vertebrates, teeth are continually worn down through food acquisition, a process that must be compensated to maintain the oral apparatus functional (Berkovitz and Shellis, 2016). Recent studies in polyphyodont and diphyodont species from all major vertebrate groups have shown that, with the exception of some teleost fish such as salmonids (Fraser et al, 2006; Jernvall and Thesleff, 2012; Vandenplas et al, 2016), tooth replacement is generally dependent on a specialized epithelial structure, the dental lamina (DL). Our bearded dragon findings reveal a novel mechanism of continuous tooth replacement in vertebrates, which shares with the leopard gecko a source of putative odontogenic progenitor/stem cells in the DL but closely parallels the shark by the presence of a separate second source of cells originating from the OE This novel dental replacement strategy definitely demonstrates that the bearded dragon provides a rare opportunity to expand our understanding of tooth developmental dynamics and diversity, while providing a unique model system to study the function and specialization of epithelial structures and dental progenitor/stem cell niches present in distinct groups of vertebrates. And given the well-established history in captivity and key advantages of the bearded dragon lizard for research (Ollonen et al, 2018) this emerging model organism offers a powerful system to elucidate the developmental and genetic basis of both evolutionary novelty and tooth regeneration, allowing to answer both developmental and evolutionary questions critical for the design of more appropriate therapies targeted at congenital dental disorders and tooth loss in humans
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