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The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination
BACKGROUND: Mitochondrial genomes of flowering plants (angiosperms) are highly dynamic in genome structure. The mitogenome of the earliest angiosperm Amborella is remarkable in carrying rampant foreign DNAs, in contrast to Liriodendron, the other only known early angiosperm mitogenome that is descri...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092842/ https://www.ncbi.nlm.nih.gov/pubmed/30107780 http://dx.doi.org/10.1186/s12864-018-4991-4 |
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author | Dong, Shanshan Zhao, Chaoxian Chen, Fei Liu, Yanhui Zhang, Shouzhou Wu, Hong Zhang, Liangsheng Liu, Yang |
author_facet | Dong, Shanshan Zhao, Chaoxian Chen, Fei Liu, Yanhui Zhang, Shouzhou Wu, Hong Zhang, Liangsheng Liu, Yang |
author_sort | Dong, Shanshan |
collection | PubMed |
description | BACKGROUND: Mitochondrial genomes of flowering plants (angiosperms) are highly dynamic in genome structure. The mitogenome of the earliest angiosperm Amborella is remarkable in carrying rampant foreign DNAs, in contrast to Liriodendron, the other only known early angiosperm mitogenome that is described as ‘fossilized’. The distinctive features observed in the two early flowering plant mitogenomes add to the current confusions of what early flowering plants look like. Expanded sampling would provide more details in understanding the mitogenomic evolution of early angiosperms. Here we report the complete mitochondrial genome of water lily Nymphaea colorata from Nymphaeales, one of the three orders of the earliest angiosperms. RESULTS: Assembly of data from Pac-Bio long-read sequencing yielded a circular mitochondria chromosome of 617,195 bp with an average depth of 601×. The genome encoded 41 protein coding genes, 20 tRNA and three rRNA genes with 25 group II introns disrupting 10 protein coding genes. Nearly half of the genome is composed of repeated sequences, which contributed substantially to the intron size expansion, making the gross intron length of the Nymphaea mitochondrial genome one of the longest among angiosperms, including an 11.4-Kb intron in cox2, which is the longest organellar intron reported to date in plants. Nevertheless, repeat mediated homologous recombination is unexpectedly low in Nymphaea evidenced by 74 recombined reads detected from ten recombinationally active repeat pairs among 886,982 repeat pairs examined. Extensive gene order changes were detected in the three early angiosperm mitogenomes, i.e. 38 or 44 events of inversions and translocations are needed to reconcile the mitogenome of Nymphaea with Amborella or Liriodendron, respectively. In contrast to Amborella with six genome equivalents of foreign mitochondrial DNA, not a single horizontal gene transfer event was observed in the Nymphaea mitogenome. CONCLUSIONS: The Nymphaea mitogenome resembles the other available early angiosperm mitogenomes by a similarly rich 64-coding gene set, and many conserved gene clusters, whereas stands out by its highly repetitive nature and resultant remarkable intron expansions. The low recombination level in Nymphaea provides evidence for the predominant master conformation in vivo with a highly substoichiometric set of rearranged molecules. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4991-4) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6092842 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-60928422018-08-20 The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination Dong, Shanshan Zhao, Chaoxian Chen, Fei Liu, Yanhui Zhang, Shouzhou Wu, Hong Zhang, Liangsheng Liu, Yang BMC Genomics Research Article BACKGROUND: Mitochondrial genomes of flowering plants (angiosperms) are highly dynamic in genome structure. The mitogenome of the earliest angiosperm Amborella is remarkable in carrying rampant foreign DNAs, in contrast to Liriodendron, the other only known early angiosperm mitogenome that is described as ‘fossilized’. The distinctive features observed in the two early flowering plant mitogenomes add to the current confusions of what early flowering plants look like. Expanded sampling would provide more details in understanding the mitogenomic evolution of early angiosperms. Here we report the complete mitochondrial genome of water lily Nymphaea colorata from Nymphaeales, one of the three orders of the earliest angiosperms. RESULTS: Assembly of data from Pac-Bio long-read sequencing yielded a circular mitochondria chromosome of 617,195 bp with an average depth of 601×. The genome encoded 41 protein coding genes, 20 tRNA and three rRNA genes with 25 group II introns disrupting 10 protein coding genes. Nearly half of the genome is composed of repeated sequences, which contributed substantially to the intron size expansion, making the gross intron length of the Nymphaea mitochondrial genome one of the longest among angiosperms, including an 11.4-Kb intron in cox2, which is the longest organellar intron reported to date in plants. Nevertheless, repeat mediated homologous recombination is unexpectedly low in Nymphaea evidenced by 74 recombined reads detected from ten recombinationally active repeat pairs among 886,982 repeat pairs examined. Extensive gene order changes were detected in the three early angiosperm mitogenomes, i.e. 38 or 44 events of inversions and translocations are needed to reconcile the mitogenome of Nymphaea with Amborella or Liriodendron, respectively. In contrast to Amborella with six genome equivalents of foreign mitochondrial DNA, not a single horizontal gene transfer event was observed in the Nymphaea mitogenome. CONCLUSIONS: The Nymphaea mitogenome resembles the other available early angiosperm mitogenomes by a similarly rich 64-coding gene set, and many conserved gene clusters, whereas stands out by its highly repetitive nature and resultant remarkable intron expansions. The low recombination level in Nymphaea provides evidence for the predominant master conformation in vivo with a highly substoichiometric set of rearranged molecules. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4991-4) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-14 /pmc/articles/PMC6092842/ /pubmed/30107780 http://dx.doi.org/10.1186/s12864-018-4991-4 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Dong, Shanshan Zhao, Chaoxian Chen, Fei Liu, Yanhui Zhang, Shouzhou Wu, Hong Zhang, Liangsheng Liu, Yang The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination |
title | The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination |
title_full | The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination |
title_fullStr | The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination |
title_full_unstemmed | The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination |
title_short | The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination |
title_sort | complete mitochondrial genome of the early flowering plant nymphaea colorata is highly repetitive with low recombination |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092842/ https://www.ncbi.nlm.nih.gov/pubmed/30107780 http://dx.doi.org/10.1186/s12864-018-4991-4 |
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