Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution

Abstract Background Pleuronectiformes, also known as flatfish, are important model and economic animals. However, a comprehensive genome survey of their important organelles, mitochondria, has been limited. Therefore, we aim to analyze the genomic structure, codon preference, nucleotide diversity, s...

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Main Authors: Suxu Tan, Wenwen Wang, Jinjiang Li, Zhenxia Sha
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11204-w
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author Suxu Tan
Wenwen Wang
Jinjiang Li
Zhenxia Sha
author_facet Suxu Tan
Wenwen Wang
Jinjiang Li
Zhenxia Sha
author_sort Suxu Tan
collection DOAJ
description Abstract Background Pleuronectiformes, also known as flatfish, are important model and economic animals. However, a comprehensive genome survey of their important organelles, mitochondria, has been limited. Therefore, we aim to analyze the genomic structure, codon preference, nucleotide diversity, selective pressure and repeat sequences, as well as reconstruct the phylogenetic relationship using the mitochondrial genomes of 111 flatfish species. Results Our analysis revealed a conserved gene content of protein-coding genes and rRNA genes, but varying numbers of tRNA genes and control regions across species. Various gene rearrangements were found in flatfish species, especially for the rearrangement of nad5-nad6-cytb block in Samaridae family, the swapping rearrangement of nad6 and cytb gene in Bothidae family, as well as the control region translocation and tRNA-Gln gene inversion in the subfamily Cynoglossinae, suggesting their unique evolutionary history and/or functional benefit. Codon usage showed obvious biases, with adenine being the most frequent nucleotide at the third codon position. Nucleotide diversity and selective pressure analysis suggested that different protein-coding genes underwent varying degrees of evolutionary pressure, with cytb and cox genes being the most conserved ones. Phylogenetic analysis using both whole mitogenome information and concatenated independently aligned protein-coding genes largely mirrored the taxonomic classification of the species, but showed different phylogeny. The identification of simple sequence repeats and various long repetitive sequences provided additional complexity of genome organization and offered markers for evolutionary studies and breeding practices. Conclusions This study represents a significant step forward in our comprehension of the flatfish mitochondrial genomes, providing valuable insights into the structure, conservation and variation within flatfish mitogenomes, with implications for understanding their evolutionary history, functional genomics and fisheries management. Future research can delve deeper into conservation biology, evolutionary biology and functional usages of variations.
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spelling doaj-art-8083d23a544d441695c261785684c2722025-01-26T12:16:46ZengBMCBMC Genomics1471-21642025-01-0126112110.1186/s12864-025-11204-wComprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolutionSuxu Tan0Wenwen Wang1Jinjiang Li2Zhenxia Sha3Institute of Aquatic Biotechnology, College of Life Sciences, Qingdao UniversityInstitute of Aquatic Biotechnology, College of Life Sciences, Qingdao UniversityInstitute of Aquatic Biotechnology, College of Life Sciences, Qingdao UniversityInstitute of Aquatic Biotechnology, College of Life Sciences, Qingdao UniversityAbstract Background Pleuronectiformes, also known as flatfish, are important model and economic animals. However, a comprehensive genome survey of their important organelles, mitochondria, has been limited. Therefore, we aim to analyze the genomic structure, codon preference, nucleotide diversity, selective pressure and repeat sequences, as well as reconstruct the phylogenetic relationship using the mitochondrial genomes of 111 flatfish species. Results Our analysis revealed a conserved gene content of protein-coding genes and rRNA genes, but varying numbers of tRNA genes and control regions across species. Various gene rearrangements were found in flatfish species, especially for the rearrangement of nad5-nad6-cytb block in Samaridae family, the swapping rearrangement of nad6 and cytb gene in Bothidae family, as well as the control region translocation and tRNA-Gln gene inversion in the subfamily Cynoglossinae, suggesting their unique evolutionary history and/or functional benefit. Codon usage showed obvious biases, with adenine being the most frequent nucleotide at the third codon position. Nucleotide diversity and selective pressure analysis suggested that different protein-coding genes underwent varying degrees of evolutionary pressure, with cytb and cox genes being the most conserved ones. Phylogenetic analysis using both whole mitogenome information and concatenated independently aligned protein-coding genes largely mirrored the taxonomic classification of the species, but showed different phylogeny. The identification of simple sequence repeats and various long repetitive sequences provided additional complexity of genome organization and offered markers for evolutionary studies and breeding practices. Conclusions This study represents a significant step forward in our comprehension of the flatfish mitochondrial genomes, providing valuable insights into the structure, conservation and variation within flatfish mitogenomes, with implications for understanding their evolutionary history, functional genomics and fisheries management. Future research can delve deeper into conservation biology, evolutionary biology and functional usages of variations.https://doi.org/10.1186/s12864-025-11204-wFlatfishMitochondrial genomeDiversitySSRRepeatPhylogeny
spellingShingle Suxu Tan
Wenwen Wang
Jinjiang Li
Zhenxia Sha
Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution
BMC Genomics
Flatfish
Mitochondrial genome
Diversity
SSR
Repeat
Phylogeny
title Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution
title_full Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution
title_fullStr Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution
title_full_unstemmed Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution
title_short Comprehensive analysis of 111 Pleuronectiformes mitochondrial genomes: insights into structure, conservation, variation and evolution
title_sort comprehensive analysis of 111 pleuronectiformes mitochondrial genomes insights into structure conservation variation and evolution
topic Flatfish
Mitochondrial genome
Diversity
SSR
Repeat
Phylogeny
url https://doi.org/10.1186/s12864-025-11204-w
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AT jinjiangli comprehensiveanalysisof111pleuronectiformesmitochondrialgenomesinsightsintostructureconservationvariationandevolution
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