Abstract
BackgroundVertebrate teeth exhibit a wide range of regenerative systems. Many species, including most mammals, reptiles, and amphibians, form replacement teeth at a histologically distinct location called the successional dental lamina, while other species do not employ such a system. Notably, a ‘lamina-less’ tooth replacement condition is found in a paraphyletic array of ray-finned fishes, such as stickleback, trout, cod, medaka, and bichir. Furthermore, the position, renewal potential, and latency times appear to vary drastically across different vertebrate tooth regeneration systems. The progenitor cells underlying tooth regeneration thus present highly divergent arrangements and potentials. Given the spectrum of regeneration systems present in vertebrates, it is unclear if morphologically divergent tooth regeneration systems deploy an overlapping battery of genes in their naïve dental tissues.ResultsIn the present work, we aimed to determine whether or not tooth progenitor epithelia could be composed of a conserved cell type between vertebrate dentitions with divergent regeneration systems. To address this question, we compared the pharyngeal tooth regeneration processes in two ray-finned fishes: zebrafish (Danio rerio) and threespine stickleback (Gasterosteus aculeatus). These two teleost species diverged approximately 250 million years ago and demonstrate some stark differences in dental morphology and regeneration. Here, we find that the naïve successional dental lamina in zebrafish expresses a battery of nine genes (bmpr1aa, bmp6, cd34, gli1, igfbp5a, lgr4, lgr6, nfatc1, and pitx2), while active Wnt signaling and Lef1 expression occur during early morphogenesis stages of tooth development. We also find that, despite the absence of a histologically distinct successional dental lamina in stickleback tooth fields, the same battery of nine genes (Bmpr1a, Bmp6, CD34, Gli1, Igfbp5a, Lgr4, Lgr6, Nfatc1, and Pitx2) are expressed in the basalmost endodermal cell layer, which is the region most closely associated with replacement tooth germs. Like zebrafish, stickleback replacement tooth germs additionally express Lef1 and exhibit active Wnt signaling. Thus, two fish systems that either have an organized successional dental lamina (zebrafish) or lack a morphologically distinct successional dental lamina (sticklebacks) deploy similar genetic programs during tooth regeneration.ConclusionsWe propose that the expression domains described here delineate a highly conserved “successional dental epithelium” (SDE). Furthermore, a set of orthologous genes is known to mark hair follicle epithelial stem cells in mice, suggesting that regenerative systems in other epithelial appendages may utilize a related epithelial progenitor cell type, despite the highly derived nature of the resulting functional organs.
Highlights
Vertebrate teeth exhibit a wide range of regenerative systems
Stickleback teeth appear to occasionally diverge from the common 1-for-1 mode of tooth replacement: some tooth germs appear to prompt osteoclast activity and shedding of more than one erupted tooth in concert. Despite these differences in modes of tooth regeneration, we find a suite of genes expressed in common between naïve dental epithelial cells in both fish species, suggesting that a conserved epithelial progenitor cell type underlies tooth regeneration, here referred to as the “successional dental epithelium” (SDE)
We propose the use of this term to encompass not just the progenitor cells found in the histologically distinct successional dental lamina (SDL) of animals such as zebrafish, sharks, and tetrapods, and in less-pronounced epithelial regions in fishes like sticklebacks, which still undergo constant tooth regeneration across their tooth fields
Summary
Vertebrate teeth exhibit a wide range of regenerative systems. Many species, including most mammals, reptiles, and amphibians, form replacement teeth at a histologically distinct location called the successional dental lamina, while other species do not employ such a system. Support for the homology of odontodes comes from developmental studies that document similar histogenesis, morphological development, and shared gene expression patterns between teeth and other odontodes across large phylogenetic distances within jawed vertebrates [9,10,11,12]. Despite these deeply conserved, fundamental aspects of tooth and odontode development, teeth have radiated vastly in their arrangement [13], shape [14], size [15], placement within the body plan [16], and the regeneration system they employ [17,18,19,20,21]. This variation in the conservation of different aspects of tooth development presents an interesting case study in the evolution of development: what genetic signatures, if any, are common to disparate dental morphologies? Here, we assess two divergent tooth regeneration strategies found in two different ray-finned fishes: zebrafish (Danio rerio) and threespine stickleback (Gasterosteus aculeatus)
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