Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system

Abstract

BackgroundThe gene regulatory network involved in tooth morphogenesis has been extremely well described in mammals and its modeling has allowed predictions of variations in regulatory pathway that may have led to evolution of tooth shapes. However, very little is known outside of mammals to understand how this regulatory framework may also account for tooth shape evolution at the level of gnathostomes. In this work, we describe expression patterns and proliferation/apoptosis assays to uncover homologous regulatory pathways in the catshark Scyliorhinus canicula.ResultsBecause of their similar structural and developmental features, gene expression patterns were described over the four developmental stages of both tooth and scale buds in the catshark. These gene expression patterns differ from mouse tooth development, and discrepancies are also observed between tooth and scale development within the catshark. However, a similar nested expression of Shh and Fgf suggests similar signaling involved in morphogenesis of all structures, although apoptosis assays do not support a strictly equivalent enamel knot system in sharks. Similarities in the topology of gene expression pattern, including Bmp signaling pathway, suggest that mouse molar development is more similar to scale bud development in the catshark.ConclusionsThese results support the fact that no enamel knot, as described in mammalian teeth, can be described in the morphogenesis of shark teeth or scales. However, homologous signaling pathways are involved in growth and morphogenesis with variations in their respective expression patterns. We speculate that variations in this topology of expression are also a substrate for tooth shape evolution, notably in regulating the growth axis and symmetry of the developing structure.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0557-0) contains supplementary material, which is available to authorized users.

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

“…Developing body denticles are highly proliferative units similar to teeth and dental lamina [40, 42] (Fig. 8j–l).…”

Dental ontogeny of a white shark embryo

“…Bemis et al (2015) suggested that the pair of small cusps that develop on both sides of the crown in juvenile white sharks is not homologous to the lateral cusplets of other lamniform sharks, because the cusps of juvenile white sharks seem to develop by a process that is different from the lateral cusplet development of other lamniform sharks, and thus, should be renamed "serrational cusplets." We feel that their hypothesis should be supported by further evidence such as gene expression patterns related to the formation of lateral cusplets in tooth development (e.g., Debiais-Thibaud et al, 2015). We do not discuss the homology of this structure here, and follow the great majority of previous studies in using the term "lateral cusplets.…”

Developmental mechanisms driving complex tooth shape in reptiles

“…It is still unclear whether signaling centers are apomorphies of mammals and drive the bud‐cap transition or participate in tooth shape formation in nonmammalian species. In the shark Scyliorhinus canicula , a chondrychthian, cytologically distinct structures reminiscent of mammalian EKs have been observed . The folded tip of the epithelial bud is formed by slowly proliferating cells, but apoptosis has not been detected.…”

“…The folded tip of the epithelial bud is formed by slowly proliferating cells, but apoptosis has not been detected. However, co‐expression of Shh and Fgf8 orthologs is present in this area . In reptiles, structures resembling primary EKs have been indicated in the alligator, which has single cuspid teeth, and also in several squamate species with both single and multicuspid teeth .…”