The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues

Abstract

The vertebrate tooth is covered with enamel in most sarcopterygians or enameloid in chondrichthyans and actinopterygians. The evolutionary relationship among these two tissues, the hardest tissue in the body, and other mineralized tissues has long been controversial. We have recently reported that specific combinations of secretory calcium-binding phosphoprotein (SCPP) genes are involved in the mineralization of bone, dentin, enameloid, and enamel. Thus, the early repertoire of SCPP genes would elucidate the evolutionary relationship across these tissues. However, the diversity of SCPP genes in teleosts and tetrapods and the roles of these genes in distinct tissues have remained unclear, mainly because many SCPP genes are lineage-specific. In this study, I show that the repertoire of SCPP genes in the zebrafish, frog, and humans includes many lineage-specific genes and some widely conserved genes that originated in stem osteichthyans or earlier. Expression analysis demonstrates that some frog and zebrafish SCPP genes are used primarily in bone, but also in dentin, while the reverse is true of other genes, similar to some mammalian SCPP genes. Dentin and enameloid initially use shared genes in the matrix, but enameloid is subsequently hypermineralized. Notably, enameloid and enamel use an orthologous SCPP gene in the hypermineralization process. Thus, the hypermineralization machinery ancestral to both enameloid and enamel arose before the actinopterygian-sarcopterygian divergence. However, enamel employs specialized SCPPs as structuring proteins, not used in enameloid, reflecting the divergence of enamel from enameloid. These results show graded differences in mineralized dental tissues and reinforce the hypothesis that bone-dentin-enameloid-enamel constitutes an evolutionary continuum.