The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.

Mitochondrial genomes of vascular plants are well known for their liability in architecture evolution. However, the evolutionary features of mitogenomes at intra-generic level are seldom studied in vascular plants, especially among gymnosperms. Here we present the complete mitogenome of Cycas debaoe...

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Main Authors: Sadaf Habib, Shanshan Dong, Yang Liu, Wenbo Liao, Shouzhou Zhang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0255091
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spelling doaj-d9aff08ae2b641c8885bf322e81da3f62021-08-03T04:32:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032021-01-01167e025509110.1371/journal.pone.0255091The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.Sadaf HabibShanshan DongYang LiuWenbo LiaoShouzhou ZhangMitochondrial genomes of vascular plants are well known for their liability in architecture evolution. However, the evolutionary features of mitogenomes at intra-generic level are seldom studied in vascular plants, especially among gymnosperms. Here we present the complete mitogenome of Cycas debaoensis, an endemic cycad species to the Guangxi region in southern China. In addition to assemblage of draft mitochondrial genome, we test the conservation of gene content and mitogenomic stability by comparing it to the previously published mitogenome of Cycas taitungensis. Furthermore, we explored the factors such as structural rearrangements and nuclear surveillance of double-strand break repair (DSBR) proteins in Cycas in comparison to other vascular plant groups. The C. debaoensis mitogenome is 413,715 bp in size and encodes 69 unique genes, including 40 protein coding genes, 26 tRNAs, and 3 rRNA genes, similar to that of C. taitungensis. Cycas mitogenomes maintained the ancestral intron content of seed plants (26 introns), which is reduced in other lineages of gymnosperms, such as Ginkgo biloba, Taxus cuspidata and Welwitschia mirabilis due to selective pressure or retroprocessing events. C. debaoensis mitogenome holds 1,569 repeated sequences (> 50 bp), which partially account for fairly large intron size (1200 bp in average) of Cycas mitogenome. The comparison of RNA-editing sites revealed 267 shared non-silent editing site among predicted vs. empirically observed editing events. Another 33 silent editing sites from empirical data increase the total number of editing sites in Cycas debaoensis mitochondrial protein coding genes to 300. Our study revealed unexpected conserved evolution between the two Cycas species. Furthermore, we found strict collinearity of the gene order along with the identical set of genomic content in Cycas mt genomes. The stability of Cycas mt genomes is surprising despite the existence of large number of repeats. This structural stability may be related to the relative expansion of three DSBR protein families (i.e., RecA, OSB, and RecG) in Cycas nuclear genome, which inhibit the homologous recombinations, by monitoring the accuracy of mitochondrial chromosome repair.https://doi.org/10.1371/journal.pone.0255091
collection DOAJ
language English
format Article
sources DOAJ
author Sadaf Habib
Shanshan Dong
Yang Liu
Wenbo Liao
Shouzhou Zhang
spellingShingle Sadaf Habib
Shanshan Dong
Yang Liu
Wenbo Liao
Shouzhou Zhang
The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.
PLoS ONE
author_facet Sadaf Habib
Shanshan Dong
Yang Liu
Wenbo Liao
Shouzhou Zhang
author_sort Sadaf Habib
title The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.
title_short The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.
title_full The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.
title_fullStr The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.
title_full_unstemmed The complete mitochondrial genome of Cycas debaoensis revealed unexpected static evolution in gymnosperm species.
title_sort complete mitochondrial genome of cycas debaoensis revealed unexpected static evolution in gymnosperm species.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2021-01-01
description Mitochondrial genomes of vascular plants are well known for their liability in architecture evolution. However, the evolutionary features of mitogenomes at intra-generic level are seldom studied in vascular plants, especially among gymnosperms. Here we present the complete mitogenome of Cycas debaoensis, an endemic cycad species to the Guangxi region in southern China. In addition to assemblage of draft mitochondrial genome, we test the conservation of gene content and mitogenomic stability by comparing it to the previously published mitogenome of Cycas taitungensis. Furthermore, we explored the factors such as structural rearrangements and nuclear surveillance of double-strand break repair (DSBR) proteins in Cycas in comparison to other vascular plant groups. The C. debaoensis mitogenome is 413,715 bp in size and encodes 69 unique genes, including 40 protein coding genes, 26 tRNAs, and 3 rRNA genes, similar to that of C. taitungensis. Cycas mitogenomes maintained the ancestral intron content of seed plants (26 introns), which is reduced in other lineages of gymnosperms, such as Ginkgo biloba, Taxus cuspidata and Welwitschia mirabilis due to selective pressure or retroprocessing events. C. debaoensis mitogenome holds 1,569 repeated sequences (> 50 bp), which partially account for fairly large intron size (1200 bp in average) of Cycas mitogenome. The comparison of RNA-editing sites revealed 267 shared non-silent editing site among predicted vs. empirically observed editing events. Another 33 silent editing sites from empirical data increase the total number of editing sites in Cycas debaoensis mitochondrial protein coding genes to 300. Our study revealed unexpected conserved evolution between the two Cycas species. Furthermore, we found strict collinearity of the gene order along with the identical set of genomic content in Cycas mt genomes. The stability of Cycas mt genomes is surprising despite the existence of large number of repeats. This structural stability may be related to the relative expansion of three DSBR protein families (i.e., RecA, OSB, and RecG) in Cycas nuclear genome, which inhibit the homologous recombinations, by monitoring the accuracy of mitochondrial chromosome repair.
url https://doi.org/10.1371/journal.pone.0255091
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