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Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea

BACKGROUND: Few exceptions have been described from strict maternal inheritance of mitochondrial DNA in animals, including sea mussels (Mytilidae), clams (Donacidae, Veneridae and Solenidae) and freshwater mussels (Unionoidae) order. In these bivalves mitochondria and their DNA are transferred throu...

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Autores principales: Sańko, Tomasz J, Burzyński, Artur
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3941564/
https://www.ncbi.nlm.nih.gov/pubmed/24575766
http://dx.doi.org/10.1186/1471-2156-15-28
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author Sańko, Tomasz J
Burzyński, Artur
author_facet Sańko, Tomasz J
Burzyński, Artur
author_sort Sańko, Tomasz J
collection PubMed
description BACKGROUND: Few exceptions have been described from strict maternal inheritance of mitochondrial DNA in animals, including sea mussels (Mytilidae), clams (Donacidae, Veneridae and Solenidae) and freshwater mussels (Unionoidae) order. In these bivalves mitochondria and their DNA are transferred through two separate routes. The females inherit only the maternal mitochondrial DNA whereas the males inherit maternal as well as paternal mitochondrial DNA, which is usually present only in gonads and sperm. The mechanism controlling this phenomenon is unclear but leads to the existence of two separate mitochondrial DNA lineages in a single species. The lineages are usually well differentiated: up to 20-50% divergence in nucleotide sequence. Occasionally, a maternal mitochondrial DNA can invade the paternal transmission route, eventually replacing the diverged M-type and lowering the divergence. Such role reversal (masculinization) event has happened recently in the Mytilus population of the Baltic Sea which consists of M. edulis × M. trossulus hybrids, but the functional status of the resulting mitochondrial genome was unknown. RESULTS: In this paper we sequenced transcripts from one specimen that was identified as male carrying both the female mitochondrial genome and a recently masculinized mitochondrial genome. Additionally, the analysis of the control region has showed that the recently masculinized, recombinant genome, not only has an M-type control region and all coding regions derived from the F-type, but also is transcriptionally active along side the maternally inherited F-type genome. In the comparative analysis, the two genomes exhibit different substitution patterns, typical for the M vs. F genome comparisons. The genetic distances and ratios of non-synonymous substitutions also suggest that one of the genomes is transitioning from the maternal to the paternal inheritance mode, consistent with its recent masculinization. CONCLUSION: We have shown, for the first time, that the recently masculinized mitochondrial genome is active and that it accumulates excess of non-synonymous substitutions across its coding sequence. This suggests, that, under certain cytonuclear incompatibility conditions, masculinization may serve to restore the endangered functionality of the paternally inherited genome. This is also another example of a mitochondrial genome in which the recombination in the control region predated its transition from paternal to maternal transmission route.
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spelling pubmed-39415642014-03-05 Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea Sańko, Tomasz J Burzyński, Artur BMC Genet Research Article BACKGROUND: Few exceptions have been described from strict maternal inheritance of mitochondrial DNA in animals, including sea mussels (Mytilidae), clams (Donacidae, Veneridae and Solenidae) and freshwater mussels (Unionoidae) order. In these bivalves mitochondria and their DNA are transferred through two separate routes. The females inherit only the maternal mitochondrial DNA whereas the males inherit maternal as well as paternal mitochondrial DNA, which is usually present only in gonads and sperm. The mechanism controlling this phenomenon is unclear but leads to the existence of two separate mitochondrial DNA lineages in a single species. The lineages are usually well differentiated: up to 20-50% divergence in nucleotide sequence. Occasionally, a maternal mitochondrial DNA can invade the paternal transmission route, eventually replacing the diverged M-type and lowering the divergence. Such role reversal (masculinization) event has happened recently in the Mytilus population of the Baltic Sea which consists of M. edulis × M. trossulus hybrids, but the functional status of the resulting mitochondrial genome was unknown. RESULTS: In this paper we sequenced transcripts from one specimen that was identified as male carrying both the female mitochondrial genome and a recently masculinized mitochondrial genome. Additionally, the analysis of the control region has showed that the recently masculinized, recombinant genome, not only has an M-type control region and all coding regions derived from the F-type, but also is transcriptionally active along side the maternally inherited F-type genome. In the comparative analysis, the two genomes exhibit different substitution patterns, typical for the M vs. F genome comparisons. The genetic distances and ratios of non-synonymous substitutions also suggest that one of the genomes is transitioning from the maternal to the paternal inheritance mode, consistent with its recent masculinization. CONCLUSION: We have shown, for the first time, that the recently masculinized mitochondrial genome is active and that it accumulates excess of non-synonymous substitutions across its coding sequence. This suggests, that, under certain cytonuclear incompatibility conditions, masculinization may serve to restore the endangered functionality of the paternally inherited genome. This is also another example of a mitochondrial genome in which the recombination in the control region predated its transition from paternal to maternal transmission route. BioMed Central 2014-02-28 /pmc/articles/PMC3941564/ /pubmed/24575766 http://dx.doi.org/10.1186/1471-2156-15-28 Text en Copyright © 2014 Sańko and Burzyński; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.
spellingShingle Research Article
Sańko, Tomasz J
Burzyński, Artur
Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea
title Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea
title_full Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea
title_fullStr Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea
title_full_unstemmed Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea
title_short Co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtDNA genome in a male Mytilus trossulus mussel from the Baltic Sea
title_sort co-expressed mitochondrial genomes: recently masculinized, recombinant mitochondrial genome is co-expressed with the female – transmitted mtdna genome in a male mytilus trossulus mussel from the baltic sea
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3941564/
https://www.ncbi.nlm.nih.gov/pubmed/24575766
http://dx.doi.org/10.1186/1471-2156-15-28
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