Abstract
In order to characterize the molecular bases of mineralizing cell evolution, we targeted type X collagen, a nonfibrillar network forming collagen encoded by the Col10a1 gene. It is involved in the process of endochondral ossification in ray-finned fishes and tetrapods (Osteichthyes), but until now unknown in cartilaginous fishes (Chondrichthyes). We show that holocephalans and elasmobranchs have respectively five and six tandemly duplicated Col10a1 gene copies that display conserved genomic synteny with osteichthyan Col10a1 genes. All Col10a1 genes in the catshark Scyliorhinus canicula are expressed in ameloblasts and/or odontoblasts of teeth and scales, during the stages of extracellular matrix protein secretion and mineralization. Only one duplicate is expressed in the endoskeletal (vertebral) mineralizing tissues. We also show that the expression of type X collagen is present in teeth of two osteichthyans, the zebrafish Danio rerio and the western clawed frog Xenopus tropicalis, indicating an ancestral jawed vertebrate involvement of type X collagen in odontode formation. Our findings push the origin of Col10a1 gene prior to the divergence of osteichthyans and chondrichthyans, and demonstrate its ancestral association with mineralization of both the odontode skeleton and the endoskeleton.
Highlights
Several factors make type X collagen an excellent candidate to study the evolution of the genetic mechanisms involved in skeletogenesis
Duplication of Collagen 10a1 (Col10a1) Gene in Holocephalan and Elasmobranchs We searched the whole elephant shark genome assembly and identified five Col10a1 genes on scaffold 71, one Collagen 8a1 (Col8a1) gene on scaffold 42, and one Collagen 8a2 (Col8a2) gene on scaffold 121. Using these predicted coding sequences (CDS) to screen transcriptomic data of other chondrichthyan species led to the identification of six similar coding sequences in the catshark S. canicula and thornback ray Ra. clavata, as well as a single Col8a1 and Col8a2 sequence
Our analysis of genome and transcriptome data from a variety of chondrichthyan species led to the identification of five Col10a1 gene duplicates in holocephalans, and six Col10a1 gene duplicates in elasmobranchs
Summary
Several factors make type X collagen an excellent candidate to study the evolution of the genetic mechanisms involved in skeletogenesis. Studies in nonamniote osteichthyans have revealed that Col10a1 is not limited to cartilage mineralization as it is expressed by osteoblasts in the amphibian Xenopus tropicalis (Aldea et al 2013) and the actinopterygians: the medaka Oryzias latipes (Renn and Winkler 2010), the spotted gar Lepisosteus oculatus, and the zebrafish Danio rerio (Laue et al 2008; Albertson et al 2010; Eames et al 2012) This suggests that in osteichthyans, type X collagen was originally involved in the mineralization of both the cartilage and bone matrix of the endoskeleton. This suggests that Col10a1 should have been ancestrally present in chondrichthyans, and raises the question of when it was recruited to the skeletal mineralization processes
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