Spatially restricted dental regeneration drives pufferfish beak development

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 firstgeneration 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.tooth development | diversity | dental regeneration | stem cells | novelty

Tooth development and replacement in the Atlantic Cutlassfish, Trichiurus lepturus, with comparisons to other Scombroidei

“…The source of epithelial cells for new tooth formation can either be from the preceding generation of teeth, a condition known as a successional dental lamina (Huysseune, 2006), or the epithelium can enter directly through replacement pores that extend the dental lamina from its initial site in the oral epithelium (Bemis et al, 2005;Thiery et al, 2017). Huysseune (2006) described a successional dental lamina in the pharyngeal jaw of Danio rerio, which has extraosseous tooth replacement, in which a new tooth germ is derived in part from the epithelium of a predecessor tooth, that is, there is an epithelial strand connecting the new tooth germ with its predecessor.…”

“…We term this a direct dental lamina to distinguish it from the successional lamina described by Huysseune (2006). Such a direct dental lamina occurs in other species with intraosseous tooth replacement in the oral jaws (e.g., Bemis et al, 2005;Bemis & Bemis, 2015;Thiery et al, 2017) although this is our first use of the term direct dental lamina. We think that characters related to the type of tooth replacement (extraosseous vs. intraosseous), the position of the dental lamina (successional vs. direct), the occurrence of replacement pores (present or absent), and the position of replacement pores (lingual side, labial side, or crest of dentigerous bone) have phylogenetic signals.…”

“…If there are multiple rows of teeth, then tooth germs can enter from both sides of the dentigerous bone (e.g., Atlantic Wolffish, Anarhichas lupus, Bemis & Bemis, 2015). This variation may be phylogenetically informative, but the position of new tooth germs and replacement pores has not been widely surveyed or considered in a phylogenetic context (Bemis et al, 2005;Thiery et al, 2017).…”

Evolution and developmental diversity of skin spines in pufferfish

“…To understand the function of these pathways during spine development and also the potential role of Notch, an additional key developmental signaling pathway during spine development, we inhibited each pathway in vivo through the use of small molecules (pharmacological agents; e.g. 56,57 ). After hatching, embryos were exposed to small molecules in water for 72 hours, covering the key stages of early spine development (initiation, determination of patterning and initial primordium formation).…”

Craniofacial skeleton of MEXICAN tetra (Astyanax mexicanus): As a bone disease model

“…Several teleost fish species have already been identified as animal models for craniofacial research. This includes zebrafish (Yelick and Schilling, ; Stock, ; Mork and Crump, ), medaka (Kimura et al, ; Atukorala et al, ; Witten et al, ), cichlids (Fraser et al, ; Powder and Albertson, ), stickleback (Kimmel et al, ; Ellis et al, ), carp (Gidmark et al, , ), Polypterus (Vandenplas et al, ; Noda et al, ) and many others (Meredith and Butler, ; Ferry et al, ; Staab et al, ; Lyon et al, ; Edds‐Walton et al, ; Fritsch et al, ; Thiery et al, ).…”