Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates
Matrix Gla protein (Mgp) and bone Gla protein (Bgp) are vitamin-K dependent proteins that bind calcium in their γ-carboxylated versions in mammals. They are recognized as positive (Bgp) or negative (Mgp and Bgp) regulators of biomineralization in a number of tissues, including skeletal tissues of bo...
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doaj-7c47be13e30b46dea9f34ff3b1e81bb62021-03-10T05:18:45ZengFrontiers Media S.A.Frontiers in Genetics1664-80212021-03-011210.3389/fgene.2021.620659620659Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed VertebratesNicolas Leurs0Camille Martinand-Mari1Stéphanie Ventéo2Tatjana Haitina3Mélanie Debiais-Thibaud4ISEM, CNRS, IRD, EPHE, Univ. Montpellier, Montpellier, FranceISEM, CNRS, IRD, EPHE, Univ. Montpellier, Montpellier, FranceInstitute for Neurosciences of Montpellier, Saint Eloi Hospital, Inserm UMR 1051, Univ. Montpellier, Montpellier, FranceDepartment of Organismal Biology, Uppsala University, Uppsala, SwedenISEM, CNRS, IRD, EPHE, Univ. Montpellier, Montpellier, FranceMatrix Gla protein (Mgp) and bone Gla protein (Bgp) are vitamin-K dependent proteins that bind calcium in their γ-carboxylated versions in mammals. They are recognized as positive (Bgp) or negative (Mgp and Bgp) regulators of biomineralization in a number of tissues, including skeletal tissues of bony vertebrates. The Mgp/Bgp gene family is poorly known in cartilaginous fishes, which precludes the understanding of the evolution of the biomineralization toolkit at the emergence of jawed vertebrates. Here we took advantage of recently released genomic and transcriptomic data in cartilaginous fishes and described the genomic loci and gene expression patterns of the Mgp/Bgp gene family. We identified three genes, Mgp1, Mgp2, and Bgp, in cartilaginous fishes instead of the single previously reported Mgp gene. We describe their genomic loci, resulting in a dynamic evolutionary scenario for this gene family including several events of local (tandem) duplications, but also of translocation events, along jawed vertebrate evolution. We describe the expression patterns of Mgp1, Mgp2, and Bgp in embryonic stages covering organogenesis in the small-spotted catshark Scyliorhinus canicula and present a comparative analysis with Mgp/Bgp family members previously described in bony vertebrates, highlighting ancestral features such as early embryonic, soft tissues, and neuronal expressions, but also derived features of cartilaginous fishes such as expression in fin supporting fibers. Our results support an ancestral function of Mgp in skeletal mineralization and a later derived function of Bgp in skeletal development that may be related to the divergence of bony vertebrates.https://www.frontiersin.org/articles/10.3389/fgene.2021.620659/fullGla proteinosteocalcinsharkskeletonevo-devobiomineralization |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Nicolas Leurs Camille Martinand-Mari Stéphanie Ventéo Tatjana Haitina Mélanie Debiais-Thibaud |
spellingShingle |
Nicolas Leurs Camille Martinand-Mari Stéphanie Ventéo Tatjana Haitina Mélanie Debiais-Thibaud Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates Frontiers in Genetics Gla protein osteocalcin shark skeleton evo-devo biomineralization |
author_facet |
Nicolas Leurs Camille Martinand-Mari Stéphanie Ventéo Tatjana Haitina Mélanie Debiais-Thibaud |
author_sort |
Nicolas Leurs |
title |
Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates |
title_short |
Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates |
title_full |
Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates |
title_fullStr |
Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates |
title_full_unstemmed |
Evolution of Matrix Gla and Bone Gla Protein Genes in Jawed Vertebrates |
title_sort |
evolution of matrix gla and bone gla protein genes in jawed vertebrates |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Genetics |
issn |
1664-8021 |
publishDate |
2021-03-01 |
description |
Matrix Gla protein (Mgp) and bone Gla protein (Bgp) are vitamin-K dependent proteins that bind calcium in their γ-carboxylated versions in mammals. They are recognized as positive (Bgp) or negative (Mgp and Bgp) regulators of biomineralization in a number of tissues, including skeletal tissues of bony vertebrates. The Mgp/Bgp gene family is poorly known in cartilaginous fishes, which precludes the understanding of the evolution of the biomineralization toolkit at the emergence of jawed vertebrates. Here we took advantage of recently released genomic and transcriptomic data in cartilaginous fishes and described the genomic loci and gene expression patterns of the Mgp/Bgp gene family. We identified three genes, Mgp1, Mgp2, and Bgp, in cartilaginous fishes instead of the single previously reported Mgp gene. We describe their genomic loci, resulting in a dynamic evolutionary scenario for this gene family including several events of local (tandem) duplications, but also of translocation events, along jawed vertebrate evolution. We describe the expression patterns of Mgp1, Mgp2, and Bgp in embryonic stages covering organogenesis in the small-spotted catshark Scyliorhinus canicula and present a comparative analysis with Mgp/Bgp family members previously described in bony vertebrates, highlighting ancestral features such as early embryonic, soft tissues, and neuronal expressions, but also derived features of cartilaginous fishes such as expression in fin supporting fibers. Our results support an ancestral function of Mgp in skeletal mineralization and a later derived function of Bgp in skeletal development that may be related to the divergence of bony vertebrates. |
topic |
Gla protein osteocalcin shark skeleton evo-devo biomineralization |
url |
https://www.frontiersin.org/articles/10.3389/fgene.2021.620659/full |
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