Evolution of dental tissue mineralization: an analysis of the jawed vertebrate SPARC and SPARC-L families

Abstract

BackgroundThe molecular bases explaining the diversity of dental tissue mineralization across gnathostomes are still poorly understood. Odontodes, such as teeth and body denticles, are serial structures that develop through deployment of a gene regulatory network shared between all gnathostomes. Dentin, the inner odontode mineralized tissue, is produced by odontoblasts and appears well-conserved through evolution. In contrast, the odontode hypermineralized external layer (enamel or enameloid) produced by ameloblasts of epithelial origin, shows extensive structural variations. As EMP (Enamel Matrix Protein) genes are as yet only found in osteichthyans where they play a major role in the mineralization of teeth and others skeletal organs, our understanding of the molecular mechanisms leading to the mineralized odontode matrices in chondrichthyans remains virtually unknown.ResultsWe undertook a phylogenetic analysis of the SPARC/SPARC-L gene family, from which the EMPs are supposed to have arisen, and examined the expression patterns of its members and of major fibrillar collagens in the spotted catshark Scyliorhinus canicula, the thornback ray Raja clavata, and the clawed frog Xenopus tropicalis. Our phylogenetic analyses reveal that the single chondrichthyan SPARC-L gene is co-orthologous to the osteichthyan SPARC-L1 and SPARC-L2 paralogues. In all three species, odontoblasts co-express SPARC and collagens. In contrast, ameloblasts do not strongly express collagen genes but exhibit strikingly similar SPARC-L and EMP expression patterns at their maturation stage, in the examined chondrichthyan and osteichthyan species, respectively.ConclusionsA well-conserved odontoblastic collagen/SPARC module across gnathostomes further confirms dentin homology. Members of the SPARC-L clade evolved faster than their SPARC paralogues, both in terms of protein sequence and gene duplication. We uncover an osteichthyan-specific duplication that produced SPARC-L1 (subsequently lost in pipidae frogs) and SPARC-L2 (independently lost in teleosts and tetrapods).Our results suggest the ameloblastic expression of the single chondrichthyan SPARC-L gene at the maturation stage reflects the ancestral gnathostome situation, and provide new evidence in favor of the homology of enamel and enameloids in all gnathostomes.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1241-y) contains supplementary material, which is available to authorized users.

Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans

“…All four genes belong to the SCPP gene family that arose by gene duplication ( Kawasaki and Weiss, 2003 ; Kawasaki et al., 2017 ). It is notable that no SCPP genes have been identified in chondrichthyans ( Figure 1 A) ( Venkatesh et al., 2014 ; Enault et al., 2018 ).…”

Skeletal Mineralization in Association with Type X Collagen Expression Is an Ancestral Feature for Jawed Vertebrates

“…Strikingly, SCPPs could not be identified in chondrichthyan genomes (Venkatesh et al. 2014; Enault et al. 2018).…”

Somite Compartments in Amphioxus and Its Implications on the Evolution of the Vertebrate Skeletal Tissues

“…(d) 2R of whole genome duplication ( Simakov et al, 2020 ). (e) SPARCL1L1 ( SPARCL2 in Enault et al, 2018 ) in chondrichtyhans is likely originated from an asymmetric duplication of Sparcb ( Kawasaki et al, 2017 ; Kawasaki, 2018 ). (f) SPARCL1L1 tandem duplicates, subsequent copies diverged into the SCPP gene family ( Kawasaki et al, 2017 ; Kawasaki, 2018 ).…”