SCPP Genes and Their Relatives in Gar: Rapid Expansion of Mineralization Genes in Osteichthyans

Abstract

Gar is an actinopterygian that has bone, dentin, enameloid, and ganoin (enamel) in teeth and/or scales. Mineralization of these tissues involves genes encoding various secretory calcium-binding phosphoproteins (SCPPs) in osteichthyans, but no SCPP genes have been identified in chondrichthyans to date. In the gar genome, we identified 38 SCPP genes, seven of which encode "acidic-residue-rich" proteins and 31 encode "Pro/Gln (P/Q) rich" proteins. These gar SCPP genes constitute the largest known repertoire, including many newly identified P/Q-rich genes expressed in teeth and/or scales. Among gar SCPP genes, six acidic and three P/Q-rich genes were identified as orthologs of sarcopterygian genes. The sarcopterygian orthologs of most of these acidic genes are involved in bone and/or dentin formation, and sarcopterygian orthologs of all three P/Q-rich genes participate in enamel formation. The finding of these genes in gar suggests that an elaborate SCPP gene-based genetic system for tissue mineralization was already present in stem osteichthyans. While SCPP genes have been thought to originate from ancient SPARCL1, SPARCL1L1 appears to be more closely related to these genes, because it established a structure similar to acidic SCPP genes probably in stem gnathostomes, perhaps at about the same time with the origin of tissue mineralization. Assuming enamel evolved in stem osteichthyans, all P/Q-rich SCPP genes likely arose within the osteichthyan lineage. Furthermore, the absence of acidic SCPP genes in chondrichthyans might be explained by the secondary loss of earliest acidic genes. It appears that many SCPP genes expanded rapidly in stem osteichthyans and in basal actinopterygians.

AMBN mutations causing hypoplastic amelogenesis imperfecta and Ambn knockout‐NLS‐lacZ knockin mice exhibiting failed amelogenesis and Ambn tissue‐specificity

“…This occurs in all vertebrates that make true enamel, and existed 450 MY ago in the most recent common ancestor of humans and gar. Ameloblastin ( Ambn ) and enamelin ( Enam ) are expressed during tooth and scale formation in the gar, whereas amelogenin ( Amel ) is not (Braasch et al, ; Kawasaki et al, ). Amelogenin apparently evolved shortly thereafter, as it is found in sarcopterygian genomes, such as the coelacanth (Kawasaki & Amemiya, ), but not in gar or teleosts (Kawasaki, ).…”

“…The spotted gar ( Lepisosteus oculatus ) is among the most distant extant relatives of tetrapods that make enamel (Sire, , ). In the gar, enamel (also called ganoin) forms on both its teeth and scales, and Ambn expression is specifically associated with the formation of these mineralized organs, and is not expressed in gar bone, embryos, or any of the nine organs included in the PhyloFish database (Braasch et al, ; Kawasaki et al, ). AMBN is a tooth‐specific gene that is required for amelogenesis, although there are some reports that AMBN functions in other tissues, such as bone (Atsawasuwan et al, ; Jacques et al, ).…”

“…All AMBN introns are phase 0 (located between complete codons), so duplication and deletion of exons during evolution, and alternative mRNA splicing, does not shift the downstream reading frame. Virtually all introns in secretory calcium‐binding phosphoprotein genes (SCPPs), including AMBN , are phase 0 (Kawasaki et al, ).…”

The Spotted Gar: Genomic Journeys into a Lost World

“…Kawasaki et al. () expanded their investigations of the evolution of the SCPP protein family involved in the formation of mineralized tissues such as bone, dentine, enamel, and ganoin, finding that the SCPP family is larger in gar than any other vertebrate studied thus far.…”

“…Martin and Holland (2017) used the spotted gar hox gene cluster complement as a pre-TGD reference point to follow the dynamic evolution of hox genes within the genomically underexplored teleost lineage of osteoglossomorphs. Kawasaki et al (2017) expanded their investigations of the evolution of the SCPP protein family involved in the formation of mineralized tissues such as bone, dentine, enamel, and ganoin, finding that the SCPP family is larger in gar than any other vertebrate studied thus far. Wcisel, Ota, Litman, and Yoder (2017) investigated the gar immune gene repertoire and found that although the gar innate immune receptors share more sequence similarities with teleost sequences, their genomic organization often resembles that possessed by tetrapod genomes.…”