Parallel evolution of amphioxus and vertebrate small-scale gene duplications

Abstract 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...

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Main Authors: Marina Brasó-Vives, Ferdinand Marlétaz, Amina Echchiki, Federica Mantica, Rafael D. Acemel, José L. Gómez-Skarmeta, Diego A. Hartasánchez, Lorlane Le Targa, Pierre Pontarotti, Juan J. Tena, Ignacio Maeso, Hector Escriva, Manuel Irimia, Marc Robinson-Rechavi
Format: Article
Language:English
Published: BMC 2022-11-01
Series:Genome Biology
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Online Access:https://doi.org/10.1186/s13059-022-02808-6
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author Marina Brasó-Vives
Ferdinand Marlétaz
Amina Echchiki
Federica Mantica
Rafael D. Acemel
José L. Gómez-Skarmeta
Diego A. Hartasánchez
Lorlane Le Targa
Pierre Pontarotti
Juan J. Tena
Ignacio Maeso
Hector Escriva
Manuel Irimia
Marc Robinson-Rechavi
author_facet Marina Brasó-Vives
Ferdinand Marlétaz
Amina Echchiki
Federica Mantica
Rafael D. Acemel
José L. Gómez-Skarmeta
Diego A. Hartasánchez
Lorlane Le Targa
Pierre Pontarotti
Juan J. Tena
Ignacio Maeso
Hector Escriva
Manuel Irimia
Marc Robinson-Rechavi
author_sort Marina Brasó-Vives
collection DOAJ
description Abstract 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.
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spelling doaj.art-3eafdefd55364d779da2b39cb4429adb2022-12-22T02:52:01ZengBMCGenome Biology1474-760X2022-11-0123112410.1186/s13059-022-02808-6Parallel evolution of amphioxus and vertebrate small-scale gene duplicationsMarina Brasó-Vives0Ferdinand Marlétaz1Amina Echchiki2Federica Mantica3Rafael D. Acemel4José L. Gómez-Skarmeta5Diego A. Hartasánchez6Lorlane Le Targa7Pierre Pontarotti8Juan J. Tena9Ignacio Maeso10Hector Escriva11Manuel Irimia12Marc Robinson-Rechavi13Department of Ecology and Evolution, University of LausanneDepartment of Genetics, Evolution and Environment (GEE), University College LondonDepartment of Ecology and Evolution, University of LausanneCentre for Genomic Regulation (CRG), Barcelona Institute of Science and TechnologyAndalusian Centre for Developmental Biology (CABD), CSIC-Pablo Olavide UniversityAndalusian Centre for Developmental Biology (CABD), CSIC-Pablo Olavide UniversityDepartment of Computational Biology, University of LausanneIRD, APHM, MEPHI, Aix Marseille UniversitéIRD, APHM, MEPHI, Aix Marseille UniversitéAndalusian Centre for Developmental Biology (CABD), CSIC-Pablo Olavide UniversityAndalusian Centre for Developmental Biology (CABD), CSIC-Pablo Olavide UniversityBiologie Intégrative des Organismes Marins, BIOM, CNRS-Sorbonne UniversityCentre for Genomic Regulation (CRG), Barcelona Institute of Science and TechnologyDepartment of Ecology and Evolution, University of LausanneAbstract 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.https://doi.org/10.1186/s13059-022-02808-6AmphioxusBranchiostoma lanceolatumGene duplicationSmall-scale duplicationGenome assemblyVertebrate
spellingShingle Marina Brasó-Vives
Ferdinand Marlétaz
Amina Echchiki
Federica Mantica
Rafael D. Acemel
José L. Gómez-Skarmeta
Diego A. Hartasánchez
Lorlane Le Targa
Pierre Pontarotti
Juan J. Tena
Ignacio Maeso
Hector Escriva
Manuel Irimia
Marc Robinson-Rechavi
Parallel evolution of amphioxus and vertebrate small-scale gene duplications
Genome Biology
Amphioxus
Branchiostoma lanceolatum
Gene duplication
Small-scale duplication
Genome assembly
Vertebrate
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 Amphioxus
Branchiostoma lanceolatum
Gene duplication
Small-scale duplication
Genome assembly
Vertebrate
url https://doi.org/10.1186/s13059-022-02808-6
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