Reiterative pattern ofsonic hedgehogexpression in the catshark dentition reveals a phylogenetic template for jawed vertebrates

Abstract

For a dentition representing the most basal extant gnathostomes, that of the shark can provide us with key insights into the evolution of vertebrate dentitions. To detail the pattern of odontogenesis, we have profiled the expression of sonic hedgehog, a key regulator of tooth induction. We find in the catshark (Scyliorhinus canicula) that intense shh expression first occurs in a bilaterally symmetrical pattern restricted to broad regions in each half of the dentition in the embryo jaw. As in the mouse, there follows a changing temporal pattern of shh spatial restriction corresponding to epithelial bands of left and right dental fields, but also a subfield for symphyseal teeth. Then, intense shh expression is restricted to loci coincident with a temporal series of teeth in iterative jaw positions. The developmental expression of shh reveals previously undetected timing within epithelial stages of tooth formation. Each locus at alternate, even then odd, jaw positions establishes precise sequential timing for successive replacement within each tooth family. Shh appears first in the central cusp, iteratively along the jaw, then reiteratively within each tooth for secondary cusps. This progressive, sequential restriction of shh is shared by toothed gnathostomes and conserved through 500 million years of evolution.

Evolution and development of the mammalian dentition: Insights from the marsupial Monodelphis domestica

“…Shh and Fgf8 are expressed in the dental lamina in mouse (Bitgood and McMahon, 1995;Kettunen and Thesleff, 1998). Shh is also expressed in the dental lamina of snakes (Buchtova et al, 2008), shrews (Yamanaka et al, 2007), and catsharks (Smith et al, 2009), suggesting a strong conservation at this early stage of tooth development and a role in the generation of replacement teeth.…”

Evolution and developmental diversity of tooth regeneration

“…The collaboration of these two genes may infer tooth competence [25][26][27][28]. In sharks, the thickening or proliferation of the cells in the odontogenic band continues posto-dorsally coincident with an in-pushing of the basal layer into the underlying and condensed mesenchyme [29][30][31] (Fig. 1).…”

“…1). This creates a fold of epithelium that is continuous along the jaw, known as the dental lamina [30][31][32]. The oro-lingual extent of the dental lamina is where new tooth replacements are formed (Fig.…”

Tooth shape formation and tooth renewal: evolving with the same signals

“…In cichlids, the replacement teeth bud off directly from oral epithelium (Vandervennet and Huysseune, 2005). In trout and salmon, replacement teeth form from a thickening in the outer enamel epithelium of the unerupted predecessor tooth (Fraser et al, 2006;Huysseune and Witten, 2006;Smith et al, 2009). In the pharyngeal dentition of zebrafish, the replacement tooth forms from a successional dental lamina that buds from the crypt epithelium of the already erupted and functional tooth (Huysseune, 2006).…”