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Parallel evolution of amphioxus and vertebrate small-scale gene duplications

BACKGROUND: Amphioxus are non-vertebrate chordates characterized by a slow morphological and molecular evolution. They share the basic chordate body-plan and genome organization with vertebrates but lack their 2R whole-genome duplications and their developmental complexity. For these reasons, amphio...

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Autores principales: Brasó-Vives, Marina, Marlétaz, Ferdinand, Echchiki, Amina, Mantica, Federica, Acemel, Rafael D., Gómez-Skarmeta, José L., Hartasánchez, Diego A., Le Targa, Lorlane, Pontarotti, Pierre, Tena, Juan J., Maeso, Ignacio, Escriva, Hector, Irimia, Manuel, Robinson-Rechavi, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9673378/
https://www.ncbi.nlm.nih.gov/pubmed/36401278
http://dx.doi.org/10.1186/s13059-022-02808-6
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author Brasó-Vives, Marina
Marlétaz, Ferdinand
Echchiki, Amina
Mantica, Federica
Acemel, Rafael D.
Gómez-Skarmeta, José L.
Hartasánchez, Diego A.
Le Targa, Lorlane
Pontarotti, Pierre
Tena, Juan J.
Maeso, Ignacio
Escriva, Hector
Irimia, Manuel
Robinson-Rechavi, Marc
author_facet Brasó-Vives, Marina
Marlétaz, Ferdinand
Echchiki, Amina
Mantica, Federica
Acemel, Rafael D.
Gómez-Skarmeta, José L.
Hartasánchez, Diego A.
Le Targa, Lorlane
Pontarotti, Pierre
Tena, Juan J.
Maeso, Ignacio
Escriva, Hector
Irimia, Manuel
Robinson-Rechavi, Marc
author_sort Brasó-Vives, Marina
collection PubMed
description BACKGROUND: Amphioxus are non-vertebrate chordates characterized by a slow morphological and molecular evolution. They share the basic chordate body-plan and genome organization with vertebrates but lack their 2R whole-genome duplications and their developmental complexity. For these reasons, amphioxus are frequently used as an outgroup to study vertebrate genome evolution and Evo-Devo. Aside from whole-genome duplications, genes continuously duplicate on a smaller scale. Small-scale duplicated genes can be found in both amphioxus and vertebrate genomes, while only the vertebrate genomes have duplicated genes product of their 2R whole-genome duplications. Here, we explore the history of small-scale gene duplications in the amphioxus lineage and compare it to small- and large-scale gene duplication history in vertebrates. RESULTS: We present a study of the European amphioxus (Branchiostoma lanceolatum) gene duplications thanks to a new, high-quality genome reference. We find that, despite its overall slow molecular evolution, the amphioxus lineage has had a history of small-scale duplications similar to the one observed in vertebrates. We find parallel gene duplication profiles between amphioxus and vertebrates and conserved functional constraints in gene duplication. Moreover, amphioxus gene duplicates show levels of expression and patterns of functional specialization similar to the ones observed in vertebrate duplicated genes. We also find strong conservation of gene synteny between two distant amphioxus species, B. lanceolatum and B. floridae, with two major chromosomal rearrangements. CONCLUSIONS: In contrast to their slower molecular and morphological evolution, amphioxus’ small-scale gene duplication history resembles that of the vertebrate lineage both in quantitative and in functional terms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02808-6.
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spelling pubmed-96733782022-11-19 Parallel evolution of amphioxus and vertebrate small-scale gene duplications Brasó-Vives, Marina Marlétaz, Ferdinand Echchiki, Amina Mantica, Federica Acemel, Rafael D. Gómez-Skarmeta, José L. Hartasánchez, Diego A. Le Targa, Lorlane Pontarotti, Pierre Tena, Juan J. Maeso, Ignacio Escriva, Hector Irimia, Manuel Robinson-Rechavi, Marc Genome Biol Research BACKGROUND: Amphioxus are non-vertebrate chordates characterized by a slow morphological and molecular evolution. They share the basic chordate body-plan and genome organization with vertebrates but lack their 2R whole-genome duplications and their developmental complexity. For these reasons, amphioxus are frequently used as an outgroup to study vertebrate genome evolution and Evo-Devo. Aside from whole-genome duplications, genes continuously duplicate on a smaller scale. Small-scale duplicated genes can be found in both amphioxus and vertebrate genomes, while only the vertebrate genomes have duplicated genes product of their 2R whole-genome duplications. Here, we explore the history of small-scale gene duplications in the amphioxus lineage and compare it to small- and large-scale gene duplication history in vertebrates. RESULTS: We present a study of the European amphioxus (Branchiostoma lanceolatum) gene duplications thanks to a new, high-quality genome reference. We find that, despite its overall slow molecular evolution, the amphioxus lineage has had a history of small-scale duplications similar to the one observed in vertebrates. We find parallel gene duplication profiles between amphioxus and vertebrates and conserved functional constraints in gene duplication. Moreover, amphioxus gene duplicates show levels of expression and patterns of functional specialization similar to the ones observed in vertebrate duplicated genes. We also find strong conservation of gene synteny between two distant amphioxus species, B. lanceolatum and B. floridae, with two major chromosomal rearrangements. CONCLUSIONS: In contrast to their slower molecular and morphological evolution, amphioxus’ small-scale gene duplication history resembles that of the vertebrate lineage both in quantitative and in functional terms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02808-6. BioMed Central 2022-11-18 /pmc/articles/PMC9673378/ /pubmed/36401278 http://dx.doi.org/10.1186/s13059-022-02808-6 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
Brasó-Vives, Marina
Marlétaz, Ferdinand
Echchiki, Amina
Mantica, Federica
Acemel, Rafael D.
Gómez-Skarmeta, José L.
Hartasánchez, Diego A.
Le Targa, Lorlane
Pontarotti, Pierre
Tena, Juan J.
Maeso, Ignacio
Escriva, Hector
Irimia, Manuel
Robinson-Rechavi, Marc
Parallel evolution of amphioxus and vertebrate small-scale gene duplications
title Parallel evolution of amphioxus and vertebrate small-scale gene duplications
title_full Parallel evolution of amphioxus and vertebrate small-scale gene duplications
title_fullStr Parallel evolution of amphioxus and vertebrate small-scale gene duplications
title_full_unstemmed Parallel evolution of amphioxus and vertebrate small-scale gene duplications
title_short Parallel evolution of amphioxus and vertebrate small-scale gene duplications
title_sort parallel evolution of amphioxus and vertebrate small-scale gene duplications
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9673378/
https://www.ncbi.nlm.nih.gov/pubmed/36401278
http://dx.doi.org/10.1186/s13059-022-02808-6
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