Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Leurs, Nicolas, Martinand-Mari, Camille, Marcellini, Sylvain, Debiais-Thibaud, Mélanie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
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
_version_ 1784711377374412800
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
work_keys_str_mv AT leursnicolas parallelevolutionofameloblasticscppgenesinbonyandcartilaginousvertebrates
AT martinandmaricamille parallelevolutionofameloblasticscppgenesinbonyandcartilaginousvertebrates
AT marcellinisylvain parallelevolutionofameloblasticscppgenesinbonyandcartilaginousvertebrates
AT debiaisthibaudmelanie parallelevolutionofameloblasticscppgenesinbonyandcartilaginousvertebrates