1. Academic Validation
  2. Spatially restricted dental regeneration drives pufferfish beak development

Spatially restricted dental regeneration drives pufferfish beak development

  • Proc Natl Acad Sci U S A. 2017 May 30;114(22):E4425-E4434. doi: 10.1073/pnas.1702909114.
Alexandre P Thiery 1 2 Takanori Shono 1 2 Daisuke Kurokawa 3 Ralf Britz 4 Zerina Johanson 5 Gareth J Fraser 6 2
Affiliations

Affiliations

  • 1 Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom.
  • 2 Bateson Centre, University of Sheffield, Sheffield S10 2TN, United Kingdom.
  • 3 Misaki Marine Biological Station, University of Tokyo, Tokyo 113-8654, Japan.
  • 4 Department of Life Sciences, Natural History Museum, London, London SW7 5BD, United Kingom.
  • 5 Department of Earth Sciences, Natural History Museum, London, London SW7 5BD, United Kingom.
  • 6 Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom; G.Fraser@sheffield.ac.uk.
Abstract

Vertebrate dentitions are extraordinarily diverse in both morphology and regenerative capacity. The teleost order Tetraodontiformes exhibits an exceptional array of novel dental morphologies, epitomized by constrained beak-like dentitions in several families, i.e., porcupinefishes, three-toothed pufferfishes, ocean sunfishes, and pufferfishes. Modification of tooth replacement within these groups leads to the progressive accumulation of tooth generations, underlying the structure of their beaks. We focus on the dentition of the pufferfish (Tetraodontidae) because of its distinct dental morphology. This complex dentition develops as a result of (i) a reduction in the number of tooth positions from seven to one per quadrant during the transition from first to second tooth generations and (ii) a dramatic shift in tooth morphogenesis following the development of the first-generation teeth, leading to the elongation of dental units along the jaw. Gene expression and 1,1'-Dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) lineage tracing reveal a putative dental epithelial progenitor niche, suggesting a highly conserved mechanism for tooth regeneration despite the development of a unique dentition. MicroCT analysis reveals restricted labial openings in the beak, through which the dental epithelium (lamina) invades the cavity of the highly mineralized beak. Reduction in the number of replacement tooth positions coincides with the development of only four labial openings in the pufferfish beak, restricting connection of the oral epithelium to the dental cavity. Our data suggest the spatial restriction of dental regeneration, coupled with the unique extension of the replacement dental units throughout the jaw, are primary contributors to the evolution and development of this unique beak-like dentition.

Keywords

dental regeneration; diversity; novelty; stem cells; tooth development.

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