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Molecular evolution of hatching enzymes and their paralogous genes in vertebrates

BACKGROUND: Hatching is identified as one of the most important events in the reproduction of oviparous vertebrates. The genes for hatching enzymes, which are vital in the hatching process, are conserved among vertebrates. However, especially in teleost, it is difficult to trace their molecular evol...

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Autores principales: Nagasawa, Tatsuki, Kawaguchi, Mari, Nishi, Kohki, Yasumasu, Shigeki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812170/
https://www.ncbi.nlm.nih.gov/pubmed/35109790
http://dx.doi.org/10.1186/s12862-022-01966-2
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author Nagasawa, Tatsuki
Kawaguchi, Mari
Nishi, Kohki
Yasumasu, Shigeki
author_facet Nagasawa, Tatsuki
Kawaguchi, Mari
Nishi, Kohki
Yasumasu, Shigeki
author_sort Nagasawa, Tatsuki
collection PubMed
description BACKGROUND: Hatching is identified as one of the most important events in the reproduction of oviparous vertebrates. The genes for hatching enzymes, which are vital in the hatching process, are conserved among vertebrates. However, especially in teleost, it is difficult to trace their molecular evolution in detail due to the presence of other C6astacins, which are the subfamily to which the genes for hatching enzymes belong and are highly diverged. In particular, the hatching enzyme genes are diversified with frequent genome translocations due to retrocopy. RESULTS: In this study, we took advantage of the rapid expansion of whole-genome data in recent years to examine the molecular evolutionary process of these genes in vertebrates. The phylogenetic analysis and the genomic synteny analysis revealed C6astacin genes other than the hatching enzyme genes, which was previously considered to be retained only in teleosts, was also retained in the genomes of basal ray-finned fishes, coelacanths, and cartilaginous fishes. These results suggest that the common ancestor of these genes can be traced back to at least the common ancestor of the Gnathostomata. Moreover, we also found that many of the C6astacin genes underwent multiple gene duplications during vertebrate evolution, and the results of gene expression analysis in frogs implied that genes derived from hatching enzyme genes underwent neo-functionalization. CONCLUSIONS: In this study, we describe in detail the molecular evolution of the C6astacin gene in vertebrates, which has not been summarized previously. The results revealed the presence of the previously unknown C6astacin gene in the basal-lineage of jawed vertebrates and large-scale gene duplication of hatching enzyme genes in amphibians. The comprehensive investigation reported in this study will be an important basis for studying the molecular evolution of the vertebrate C6astacin genes, hatching enzyme, and its paralogous genes and for identifying these genes without the need for gene expression and functional analysis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01966-2.
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spelling pubmed-88121702022-02-03 Molecular evolution of hatching enzymes and their paralogous genes in vertebrates Nagasawa, Tatsuki Kawaguchi, Mari Nishi, Kohki Yasumasu, Shigeki BMC Ecol Evol Research BACKGROUND: Hatching is identified as one of the most important events in the reproduction of oviparous vertebrates. The genes for hatching enzymes, which are vital in the hatching process, are conserved among vertebrates. However, especially in teleost, it is difficult to trace their molecular evolution in detail due to the presence of other C6astacins, which are the subfamily to which the genes for hatching enzymes belong and are highly diverged. In particular, the hatching enzyme genes are diversified with frequent genome translocations due to retrocopy. RESULTS: In this study, we took advantage of the rapid expansion of whole-genome data in recent years to examine the molecular evolutionary process of these genes in vertebrates. The phylogenetic analysis and the genomic synteny analysis revealed C6astacin genes other than the hatching enzyme genes, which was previously considered to be retained only in teleosts, was also retained in the genomes of basal ray-finned fishes, coelacanths, and cartilaginous fishes. These results suggest that the common ancestor of these genes can be traced back to at least the common ancestor of the Gnathostomata. Moreover, we also found that many of the C6astacin genes underwent multiple gene duplications during vertebrate evolution, and the results of gene expression analysis in frogs implied that genes derived from hatching enzyme genes underwent neo-functionalization. CONCLUSIONS: In this study, we describe in detail the molecular evolution of the C6astacin gene in vertebrates, which has not been summarized previously. The results revealed the presence of the previously unknown C6astacin gene in the basal-lineage of jawed vertebrates and large-scale gene duplication of hatching enzyme genes in amphibians. The comprehensive investigation reported in this study will be an important basis for studying the molecular evolution of the vertebrate C6astacin genes, hatching enzyme, and its paralogous genes and for identifying these genes without the need for gene expression and functional analysis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01966-2. BioMed Central 2022-02-02 /pmc/articles/PMC8812170/ /pubmed/35109790 http://dx.doi.org/10.1186/s12862-022-01966-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Nagasawa, Tatsuki
Kawaguchi, Mari
Nishi, Kohki
Yasumasu, Shigeki
Molecular evolution of hatching enzymes and their paralogous genes in vertebrates
title Molecular evolution of hatching enzymes and their paralogous genes in vertebrates
title_full Molecular evolution of hatching enzymes and their paralogous genes in vertebrates
title_fullStr Molecular evolution of hatching enzymes and their paralogous genes in vertebrates
title_full_unstemmed Molecular evolution of hatching enzymes and their paralogous genes in vertebrates
title_short Molecular evolution of hatching enzymes and their paralogous genes in vertebrates
title_sort molecular evolution of hatching enzymes and their paralogous genes in vertebrates
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812170/
https://www.ncbi.nlm.nih.gov/pubmed/35109790
http://dx.doi.org/10.1186/s12862-022-01966-2
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