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Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates
In bony vertebrates, skeletal mineralization relies on the secretory calcium-binding phosphoproteins (Scpp) family whose members are acidic extracellular proteins posttranslationally regulated by the Fam20°C kinase. As scpp genes are absent from the elephant shark genome, they are currently thought...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9122587/ https://www.ncbi.nlm.nih.gov/pubmed/35535508 http://dx.doi.org/10.1093/molbev/msac099 |
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author | Leurs, Nicolas Martinand-Mari, Camille Marcellini, Sylvain Debiais-Thibaud, Mélanie |
author_facet | Leurs, Nicolas Martinand-Mari, Camille Marcellini, Sylvain Debiais-Thibaud, Mélanie |
author_sort | Leurs, Nicolas |
collection | PubMed |
description | In bony vertebrates, skeletal mineralization relies on the secretory calcium-binding phosphoproteins (Scpp) family whose members are acidic extracellular proteins posttranslationally regulated by the Fam20°C kinase. As scpp genes are absent from the elephant shark genome, they are currently thought to be specific to bony fishes (osteichthyans). Here, we report a scpp gene present in elasmobranchs (sharks and rays) that evolved from local tandem duplication of sparc-L 5′ exons and show that both genes experienced recent gene conversion in sharks. The elasmobranch scpp is remarkably similar to the osteichthyan scpp members as they share syntenic and gene structure features, code for a conserved signal peptide, tyrosine-rich and aspartate/glutamate-rich regions, and harbor putative Fam20°C phosphorylation sites. In addition, the catshark scpp is coexpressed with sparc-L and fam20°C in tooth and scale ameloblasts, similarly to some osteichthyan scpp genes. Despite these strong similarities, molecular clock and phylogenetic data demonstrate that the elasmobranch scpp gene originated independently from the osteichthyan scpp gene family. Our study reveals convergent events at the sparc-L locus in the two sister clades of jawed vertebrates, leading to parallel diversification of the skeletal biomineralization toolkit. The molecular evolution of sparc-L and its coexpression with fam20°C in catshark ameloblasts provides a unifying genetic basis that suggests that all convergent scpp duplicates inherited similar features from their sparc-L precursor. This conclusion supports a single origin for the hypermineralized outer odontode layer as produced by an ancestral developmental process performed by Sparc-L, implying the homology of the enamel and enameloid tissues in all vertebrates. |
format | Online Article Text |
id | pubmed-9122587 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-91225872022-05-23 Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates Leurs, Nicolas Martinand-Mari, Camille Marcellini, Sylvain Debiais-Thibaud, Mélanie Mol Biol Evol Discoveries In bony vertebrates, skeletal mineralization relies on the secretory calcium-binding phosphoproteins (Scpp) family whose members are acidic extracellular proteins posttranslationally regulated by the Fam20°C kinase. As scpp genes are absent from the elephant shark genome, they are currently thought to be specific to bony fishes (osteichthyans). Here, we report a scpp gene present in elasmobranchs (sharks and rays) that evolved from local tandem duplication of sparc-L 5′ exons and show that both genes experienced recent gene conversion in sharks. The elasmobranch scpp is remarkably similar to the osteichthyan scpp members as they share syntenic and gene structure features, code for a conserved signal peptide, tyrosine-rich and aspartate/glutamate-rich regions, and harbor putative Fam20°C phosphorylation sites. In addition, the catshark scpp is coexpressed with sparc-L and fam20°C in tooth and scale ameloblasts, similarly to some osteichthyan scpp genes. Despite these strong similarities, molecular clock and phylogenetic data demonstrate that the elasmobranch scpp gene originated independently from the osteichthyan scpp gene family. Our study reveals convergent events at the sparc-L locus in the two sister clades of jawed vertebrates, leading to parallel diversification of the skeletal biomineralization toolkit. The molecular evolution of sparc-L and its coexpression with fam20°C in catshark ameloblasts provides a unifying genetic basis that suggests that all convergent scpp duplicates inherited similar features from their sparc-L precursor. This conclusion supports a single origin for the hypermineralized outer odontode layer as produced by an ancestral developmental process performed by Sparc-L, implying the homology of the enamel and enameloid tissues in all vertebrates. Oxford University Press 2022-05-10 /pmc/articles/PMC9122587/ /pubmed/35535508 http://dx.doi.org/10.1093/molbev/msac099 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Discoveries Leurs, Nicolas Martinand-Mari, Camille Marcellini, Sylvain Debiais-Thibaud, Mélanie Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates |
title | Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates |
title_full | Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates |
title_fullStr | Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates |
title_full_unstemmed | Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates |
title_short | Parallel Evolution of Ameloblastic scpp Genes in Bony and Cartilaginous Vertebrates |
title_sort | parallel evolution of ameloblastic scpp genes in bony and cartilaginous vertebrates |
topic | Discoveries |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9122587/ https://www.ncbi.nlm.nih.gov/pubmed/35535508 http://dx.doi.org/10.1093/molbev/msac099 |
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