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The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications

SIMPLE SUMMARY: Mitochondria are semiautonomous organelles in eukaryotic cells, which play a critical role in cellular energy production. The plant mitochondrial genomes harbor large degrees of variation and complexity in structures. Crassulaceae is the largest family in the order Saxifragales. Howe...

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Autores principales: Ding, Hengwu, Bi, De, Zhang, Sijia, Han, Shiyun, Ye, Yuanxin, Yi, Ran, Yang, Jianke, Liu, Birong, Wu, Longhua, Zhuo, Renying, Kan, Xianzhao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9687357/
https://www.ncbi.nlm.nih.gov/pubmed/36421375
http://dx.doi.org/10.3390/biology11111661
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author Ding, Hengwu
Bi, De
Zhang, Sijia
Han, Shiyun
Ye, Yuanxin
Yi, Ran
Yang, Jianke
Liu, Birong
Wu, Longhua
Zhuo, Renying
Kan, Xianzhao
author_facet Ding, Hengwu
Bi, De
Zhang, Sijia
Han, Shiyun
Ye, Yuanxin
Yi, Ran
Yang, Jianke
Liu, Birong
Wu, Longhua
Zhuo, Renying
Kan, Xianzhao
author_sort Ding, Hengwu
collection PubMed
description SIMPLE SUMMARY: Mitochondria are semiautonomous organelles in eukaryotic cells, which play a critical role in cellular energy production. The plant mitochondrial genomes harbor large degrees of variation and complexity in structures. Crassulaceae is the largest family in the order Saxifragales. However, no entire mitogenome data have been available for species of Crassulaceae up to now. In the present study, we sequenced the first mitogenome of Crassulaceae (presented by Sedum plumbizincicola). Through comprehensive analyses, we found Saxifragales mitogenomes have undergone rapid structural evolution, with low synonymous substitution rates. Moreover, RNA editing, gene transfer, secondary structures of mitochondrial RNAs, and phylogenetic implications were also analyzed by using mitochondrial data. The present work may provide new insights into the mitogenome evolution of Saxifragales. ABSTRACT: As the largest family within the order Saxifragales, Crassulaceae contains about 34 genera with 1400 species. Mitochondria play a critical role in cellular energy production. Since the first land plant mitogenome was reported in Arabidopsis, more than 400 mitogenomic sequences have been deposited in a public database. However, no entire mitogenome data have been available for species of Crassulaceae to date. To better understand the evolutionary history of the organelles of Crassulaceae, we sequenced and performed comprehensive analyses on the mitogenome of Sedum plumbizincicola. The master mitogenomic circle is 212,159 bp in length, including 31 protein-coding genes (PCGs), 14 tRNA genes, and 3 rRNA genes. We further identified totally 508 RNA editing sites in PCGs, and demonstrated that the second codon positions of mitochondrial genes are most prone to RNA editing events. Notably, by neutrality plot analyses, we observed that the mitochondrial RNA editing events have large effects on the driving forces of plant evolution. Additionally, 4 MTPTs and 686 NUMTs were detected in the mitochondrial and nuclear genomes of S. plumbizincicola, respectively. Additionally, we conducted further analyses on gene transfer, secondary structures of mitochondrial RNAs, and phylogenetic implications. Therefore, the findings presented here will be helpful for future investigations on plant mitogenomes.
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spelling pubmed-96873572022-11-25 The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications Ding, Hengwu Bi, De Zhang, Sijia Han, Shiyun Ye, Yuanxin Yi, Ran Yang, Jianke Liu, Birong Wu, Longhua Zhuo, Renying Kan, Xianzhao Biology (Basel) Article SIMPLE SUMMARY: Mitochondria are semiautonomous organelles in eukaryotic cells, which play a critical role in cellular energy production. The plant mitochondrial genomes harbor large degrees of variation and complexity in structures. Crassulaceae is the largest family in the order Saxifragales. However, no entire mitogenome data have been available for species of Crassulaceae up to now. In the present study, we sequenced the first mitogenome of Crassulaceae (presented by Sedum plumbizincicola). Through comprehensive analyses, we found Saxifragales mitogenomes have undergone rapid structural evolution, with low synonymous substitution rates. Moreover, RNA editing, gene transfer, secondary structures of mitochondrial RNAs, and phylogenetic implications were also analyzed by using mitochondrial data. The present work may provide new insights into the mitogenome evolution of Saxifragales. ABSTRACT: As the largest family within the order Saxifragales, Crassulaceae contains about 34 genera with 1400 species. Mitochondria play a critical role in cellular energy production. Since the first land plant mitogenome was reported in Arabidopsis, more than 400 mitogenomic sequences have been deposited in a public database. However, no entire mitogenome data have been available for species of Crassulaceae to date. To better understand the evolutionary history of the organelles of Crassulaceae, we sequenced and performed comprehensive analyses on the mitogenome of Sedum plumbizincicola. The master mitogenomic circle is 212,159 bp in length, including 31 protein-coding genes (PCGs), 14 tRNA genes, and 3 rRNA genes. We further identified totally 508 RNA editing sites in PCGs, and demonstrated that the second codon positions of mitochondrial genes are most prone to RNA editing events. Notably, by neutrality plot analyses, we observed that the mitochondrial RNA editing events have large effects on the driving forces of plant evolution. Additionally, 4 MTPTs and 686 NUMTs were detected in the mitochondrial and nuclear genomes of S. plumbizincicola, respectively. Additionally, we conducted further analyses on gene transfer, secondary structures of mitochondrial RNAs, and phylogenetic implications. Therefore, the findings presented here will be helpful for future investigations on plant mitogenomes. MDPI 2022-11-13 /pmc/articles/PMC9687357/ /pubmed/36421375 http://dx.doi.org/10.3390/biology11111661 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Ding, Hengwu
Bi, De
Zhang, Sijia
Han, Shiyun
Ye, Yuanxin
Yi, Ran
Yang, Jianke
Liu, Birong
Wu, Longhua
Zhuo, Renying
Kan, Xianzhao
The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications
title The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications
title_full The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications
title_fullStr The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications
title_full_unstemmed The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications
title_short The Mitogenome of Sedum plumbizincicola (Crassulaceae): Insights into RNA Editing, Lateral Gene Transfer, and Phylogenetic Implications
title_sort mitogenome of sedum plumbizincicola (crassulaceae): insights into rna editing, lateral gene transfer, and phylogenetic implications
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9687357/
https://www.ncbi.nlm.nih.gov/pubmed/36421375
http://dx.doi.org/10.3390/biology11111661
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