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Uniparental Genome Elimination in Australian Carp Gudgeons

Metazoans usually reproduce sexually, blending the unique identity of parental genomes for the next generation through functional crossing-over and recombination in meiosis. However, some metazoan lineages have evolved reproductive systems where offspring are either full (clonal) or partial (hemiclo...

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Autores principales: Majtánová, Zuzana, Dedukh, Dmitrij, Choleva, Lukáš, Adams, Mark, Ráb, Petr, Unmack, Peter J, Ezaz, Tariq
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245195/
https://www.ncbi.nlm.nih.gov/pubmed/33591327
http://dx.doi.org/10.1093/gbe/evab030
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author Majtánová, Zuzana
Dedukh, Dmitrij
Choleva, Lukáš
Adams, Mark
Ráb, Petr
Unmack, Peter J
Ezaz, Tariq
author_facet Majtánová, Zuzana
Dedukh, Dmitrij
Choleva, Lukáš
Adams, Mark
Ráb, Petr
Unmack, Peter J
Ezaz, Tariq
author_sort Majtánová, Zuzana
collection PubMed
description Metazoans usually reproduce sexually, blending the unique identity of parental genomes for the next generation through functional crossing-over and recombination in meiosis. However, some metazoan lineages have evolved reproductive systems where offspring are either full (clonal) or partial (hemiclonal) genetic replicas. In the latter group, the process of uniparental genome elimination selectively eliminates either the maternal or paternal genome from germ cells, and only one parental genome is selected for transmission. Although fairly common in plants, hybridogenesis (i.e., clonal haploidization via chromosome elimination) remains a poorly understood process in animals. Here, we explore the proximal cytogenomic mechanisms of somatic and germ cell chromosomes in sexual and hybrid genotypes of Australian carp gudgeons (Hypseleotris) by tracing the fate of each set during mitosis (in somatic tissues) and meiosis (in gonads). Our comparative study of diploid hybrid and sexual individuals revealed visually functional gonads in male and female hybrid genotypes and generally high karyotype variability, although the number of chromosome arms remains constant. Our results delivered direct evidence for classic hybridogenesis as a reproductive mode in carp gudgeons. Two parental sets with integral structure in the hybrid soma (the F1 constitution) contrasted with uniparental chromosomal inheritance detected in gonads. The inheritance mode happens through premeiotic genome duplication of the parental genome to be transmitted, whereas the second parental genome is likely gradually eliminated already in juvenile individuals. The role of metacentric chromosomes in hybrid evolution is also discussed.
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spelling pubmed-82451952021-07-01 Uniparental Genome Elimination in Australian Carp Gudgeons Majtánová, Zuzana Dedukh, Dmitrij Choleva, Lukáš Adams, Mark Ráb, Petr Unmack, Peter J Ezaz, Tariq Genome Biol Evol Within-individual genome variation and germline/soma distinction Metazoans usually reproduce sexually, blending the unique identity of parental genomes for the next generation through functional crossing-over and recombination in meiosis. However, some metazoan lineages have evolved reproductive systems where offspring are either full (clonal) or partial (hemiclonal) genetic replicas. In the latter group, the process of uniparental genome elimination selectively eliminates either the maternal or paternal genome from germ cells, and only one parental genome is selected for transmission. Although fairly common in plants, hybridogenesis (i.e., clonal haploidization via chromosome elimination) remains a poorly understood process in animals. Here, we explore the proximal cytogenomic mechanisms of somatic and germ cell chromosomes in sexual and hybrid genotypes of Australian carp gudgeons (Hypseleotris) by tracing the fate of each set during mitosis (in somatic tissues) and meiosis (in gonads). Our comparative study of diploid hybrid and sexual individuals revealed visually functional gonads in male and female hybrid genotypes and generally high karyotype variability, although the number of chromosome arms remains constant. Our results delivered direct evidence for classic hybridogenesis as a reproductive mode in carp gudgeons. Two parental sets with integral structure in the hybrid soma (the F1 constitution) contrasted with uniparental chromosomal inheritance detected in gonads. The inheritance mode happens through premeiotic genome duplication of the parental genome to be transmitted, whereas the second parental genome is likely gradually eliminated already in juvenile individuals. The role of metacentric chromosomes in hybrid evolution is also discussed. Oxford University Press 2021-02-16 /pmc/articles/PMC8245195/ /pubmed/33591327 http://dx.doi.org/10.1093/gbe/evab030 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Within-individual genome variation and germline/soma distinction
Majtánová, Zuzana
Dedukh, Dmitrij
Choleva, Lukáš
Adams, Mark
Ráb, Petr
Unmack, Peter J
Ezaz, Tariq
Uniparental Genome Elimination in Australian Carp Gudgeons
title Uniparental Genome Elimination in Australian Carp Gudgeons
title_full Uniparental Genome Elimination in Australian Carp Gudgeons
title_fullStr Uniparental Genome Elimination in Australian Carp Gudgeons
title_full_unstemmed Uniparental Genome Elimination in Australian Carp Gudgeons
title_short Uniparental Genome Elimination in Australian Carp Gudgeons
title_sort uniparental genome elimination in australian carp gudgeons
topic Within-individual genome variation and germline/soma distinction
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8245195/
https://www.ncbi.nlm.nih.gov/pubmed/33591327
http://dx.doi.org/10.1093/gbe/evab030
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