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Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales

BACKGROUND: Although knowledge of the sizes, contents, and forms of plant mitochondrial genomes (mitogenomes) is increasing, little is known about the mechanisms underlying their structural diversity. Evolutionary information on the mitogenomes of Primula, an important ornamental taxon, is more limi...

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Autores principales: Wei, Lei, Liu, Tong-Jian, Hao, Gang, Ge, Xue-Jun, Yan, Hai-Fei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686101/
https://www.ncbi.nlm.nih.gov/pubmed/36424546
http://dx.doi.org/10.1186/s12864-022-08983-x
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author Wei, Lei
Liu, Tong-Jian
Hao, Gang
Ge, Xue-Jun
Yan, Hai-Fei
author_facet Wei, Lei
Liu, Tong-Jian
Hao, Gang
Ge, Xue-Jun
Yan, Hai-Fei
author_sort Wei, Lei
collection PubMed
description BACKGROUND: Although knowledge of the sizes, contents, and forms of plant mitochondrial genomes (mitogenomes) is increasing, little is known about the mechanisms underlying their structural diversity. Evolutionary information on the mitogenomes of Primula, an important ornamental taxon, is more limited than the information on their nuclear and plastid counterparts, which has hindered the comprehensive understanding of Primula mitogenomic diversity and evolution. The present study reported and compared three Primula mitogenomes and discussed the size expansion of mitogenomes in Ericales. RESULTS: Mitogenome master circles were sequenced and successfully assembled for three Primula taxa and were compared with publicly available Ericales mitogenomes. The three mitogenomes contained similar gene contents and varied primarily in their structures. The Primula mitogenomes possessed relatively high nucleotide diversity among all examined plant lineages. In addition, high nucleotide diversity was found among Primula species between the Mediterranean and Himalaya-Hengduan Mountains. Most predicted RNA editing sites appeared in the second amino acid codon, increasing the hydrophobic character of the protein. An early stop in atp6 caused by RNA editing was conserved across all examined Ericales species. The interfamilial relationships within Ericales and interspecific relationships within Primula could be well resolved based on mitochondrial data. Transfer of the two longest mitochondrial plastid sequences (MTPTs) occurred before the divergence of Primula and its close relatives, and multiple independent transfers could also occur in a single MTPT sequence. Foreign sequence [MTPTs and mitochondrial nuclear DNA sequences (NUMTs)] uptake and repeats were to some extent associated with changes in Ericales mitogenome size, although none of these relationships were significant overall. CONCLUSIONS: The present study revealed relatively conserved gene contents, gene clusters, RNA editing, and MTPTs but considerable structural variation in Primula mitogenomes. Relatively high nucleotide diversity was found in the Primula mitogenomes. In addition, mitogenomic genes, collinear gene clusters, and locally collinear blocks (LCBs) all showed phylogenetic signals. The evolutionary history of MTPTs in Primula was complicated, even in a single MTPT sequence. Various reasons for the size variation observed in Ericales mitogenomes were found. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08983-x.
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spelling pubmed-96861012022-11-25 Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales Wei, Lei Liu, Tong-Jian Hao, Gang Ge, Xue-Jun Yan, Hai-Fei BMC Genomics Research BACKGROUND: Although knowledge of the sizes, contents, and forms of plant mitochondrial genomes (mitogenomes) is increasing, little is known about the mechanisms underlying their structural diversity. Evolutionary information on the mitogenomes of Primula, an important ornamental taxon, is more limited than the information on their nuclear and plastid counterparts, which has hindered the comprehensive understanding of Primula mitogenomic diversity and evolution. The present study reported and compared three Primula mitogenomes and discussed the size expansion of mitogenomes in Ericales. RESULTS: Mitogenome master circles were sequenced and successfully assembled for three Primula taxa and were compared with publicly available Ericales mitogenomes. The three mitogenomes contained similar gene contents and varied primarily in their structures. The Primula mitogenomes possessed relatively high nucleotide diversity among all examined plant lineages. In addition, high nucleotide diversity was found among Primula species between the Mediterranean and Himalaya-Hengduan Mountains. Most predicted RNA editing sites appeared in the second amino acid codon, increasing the hydrophobic character of the protein. An early stop in atp6 caused by RNA editing was conserved across all examined Ericales species. The interfamilial relationships within Ericales and interspecific relationships within Primula could be well resolved based on mitochondrial data. Transfer of the two longest mitochondrial plastid sequences (MTPTs) occurred before the divergence of Primula and its close relatives, and multiple independent transfers could also occur in a single MTPT sequence. Foreign sequence [MTPTs and mitochondrial nuclear DNA sequences (NUMTs)] uptake and repeats were to some extent associated with changes in Ericales mitogenome size, although none of these relationships were significant overall. CONCLUSIONS: The present study revealed relatively conserved gene contents, gene clusters, RNA editing, and MTPTs but considerable structural variation in Primula mitogenomes. Relatively high nucleotide diversity was found in the Primula mitogenomes. In addition, mitogenomic genes, collinear gene clusters, and locally collinear blocks (LCBs) all showed phylogenetic signals. The evolutionary history of MTPTs in Primula was complicated, even in a single MTPT sequence. Various reasons for the size variation observed in Ericales mitogenomes were found. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08983-x. BioMed Central 2022-11-24 /pmc/articles/PMC9686101/ /pubmed/36424546 http://dx.doi.org/10.1186/s12864-022-08983-x 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
Wei, Lei
Liu, Tong-Jian
Hao, Gang
Ge, Xue-Jun
Yan, Hai-Fei
Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales
title Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales
title_full Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales
title_fullStr Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales
title_full_unstemmed Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales
title_short Comparative analyses of three complete Primula mitogenomes with insights into mitogenome size variation in Ericales
title_sort comparative analyses of three complete primula mitogenomes with insights into mitogenome size variation in ericales
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686101/
https://www.ncbi.nlm.nih.gov/pubmed/36424546
http://dx.doi.org/10.1186/s12864-022-08983-x
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