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      The complete mitochondrial genome of Taxus cuspidata (Taxaceae): eight protein-coding genes have transferred to the nuclear genome

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          Abstract

          Background

          Gymnosperms represent five of the six lineages of seed plants. However, most sequenced plant mitochondrial genomes (mitogenomes) have been generated for angiosperms, whereas mitogenomic sequences have been generated for only six gymnosperms. In particular, complete mitogenomes are available for all major seed plant lineages except Conifer II (non-Pinaceae conifers or Cupressophyta), an important lineage including six families, which impedes a comprehensive understanding of the mitogenomic diversity and evolution in gymnosperms.

          Results

          Here, we report the complete mitogenome of Taxus cuspidata in Conifer II. In comparison with previously released gymnosperm mitogenomes, we found that the mitogenomes of Taxus and Welwitschia have lost many genes individually, whereas all genes were identified in the mitogenomes of Cycas, Ginkgo and Pinaceae. Multiple tRNA genes and introns also have been lost in some lineages of gymnosperms, similar to the pattern observed in angiosperms. In general, gene clusters could be less conserved in gymnosperms than in angiosperms. Moreover, fewer RNA editing sites were identified in the Taxus and Welwitschia mitogenomes than in other mitogenomes, which could be correlated with fewer introns and frequent gene losses in these two species.

          Conclusions

          We have sequenced the Taxus cuspidata mitogenome, and compared it with mitogenomes from the other four gymnosperm lineages. The results revealed the diversity in size, structure, gene and intron contents, foreign sequences, and mutation rates of gymnosperm mitogenomes, which are different from angiosperm mitogenomes.

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          Most cited references74

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          OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets

          Mitochondria and plastids (chloroplasts) are cell organelles of endosymbiotic origin that possess their own genetic information. Most organellar DNAs map as circular double-stranded genomes. Across the eukaryotic kingdom, organellar genomes display great size variation, ranging from ∼15 to 20 kb (the size of the mitochondrial genome in most animals) to >10 Mb (the size of the mitochondrial genome in some lineages of flowering plants). We have developed OrganellarGenomeDraw (OGDRAW), a suite of software tools that enable users to create high-quality visual representations of both circular and linear annotated genome sequences provided as GenBank files or accession numbers. Although all types of DNA sequences are accepted as input, the software has been specifically optimized to properly depict features of organellar genomes. A recent extension facilitates the plotting of quantitative gene expression data, such as transcript or protein abundance data, directly onto the genome map. OGDRAW has already become widely used and is available as a free web tool (http://ogdraw.mpimp-golm.mpg.de/). The core processing components can be downloaded as a Perl module, thus also allowing for convenient integration into custom processing pipelines.
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            Evolution of mitochondrial gene content: gene loss and transfer to the nucleus.

            Mitochondrial gene content is highly variable across extant eukaryotes. The number of mitochondrial protein genes varies from 3 to 67, while tRNA gene content varies from 0 to 27. Moreover, these numbers exclude the many diverse lineages of non-respiring eukaryotes that lack a mitochondrial genome yet still contain a mitochondrion, albeit one often highly derived in ultrastructure and metabolic function, such as the hydrogenosome. Diversity in tRNA gene content primarily reflects differential usage of imported tRNAs of nuclear origin. In the case of protein genes, most of this diversity reflects differential degrees of functional gene transfer to the nucleus, with more minor contributions resulting from gene loss from the cell as a consequence of either substitution via a functional nuclear homolog or the cell's dispensation of the function of the gene product. The tempo and pattern of mitochondrial gene loss is highly episodic, both across the broad sweep of eukaryotes and within such well-studied groups as angiosperms. All animals, some plants, and certain other groups of eukaryotes are mired in profound stases in mitochondrial gene content, whereas other lineages have experienced relatively frequent gene loss. Loss and transfer to the nucleus of ribosomal protein and succinate dehydrogenase genes has been especially frequent, sporadic, and episodic during angiosperm evolution. Potential mechanisms for activation of transferred genes have been inferred, and intermediate stages in the process have been identified by comparative studies. Several hypotheses have been proposed for why mitochondrial genes are transferred to the nucleus, why mitochondria retain genomes, and why functional gene transfer is almost exclusively unidirectional.
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              Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae).

              The mitochondrial genomes of seed plants are unusually large and vary in size by at least an order of magnitude. Much of this variation occurs within a single family, the Cucurbitaceae, whose genomes range from an estimated 390 to 2,900 kb in size. We sequenced the mitochondrial genomes of Citrullus lanatus (watermelon: 379,236 nt) and Cucurbita pepo (zucchini: 982,833 nt)--the two smallest characterized cucurbit mitochondrial genomes--and determined their RNA editing content. The relatively compact Citrullus mitochondrial genome actually contains more and longer genes and introns, longer segmental duplications, and more discernibly nuclear-derived DNA. The large size of the Cucurbita mitochondrial genome reflects the accumulation of unprecedented amounts of both chloroplast sequences (>113 kb) and short repeated sequences (>370 kb). A low mutation rate has been hypothesized to underlie increases in both genome size and RNA editing frequency in plant mitochondria. However, despite its much larger genome, Cucurbita has a significantly higher synonymous substitution rate (and presumably mutation rate) than Citrullus but comparable levels of RNA editing. The evolution of mutation rate, genome size, and RNA editing are apparently decoupled in Cucurbitaceae, reflecting either simple stochastic variation or governance by different factors.
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                Author and article information

                Contributors
                jinhua_ran@ibcas.ac.cn
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                20 January 2020
                20 January 2020
                2020
                : 20
                : 10
                Affiliations
                [1 ]ISNI 0000 0004 0596 3367, GRID grid.435133.3, State Key Laboratory of Systematic and Evolutionary Botany, , Institute of Botany, Chinese Academy of Sciences, ; Beijing, 100093 China
                [2 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, University of Chinese Academy of Sciences, ; Beijing, 100049 China
                Author information
                http://orcid.org/0000-0002-1140-4559
                Article
                1582
                10.1186/s12862-020-1582-1
                6971862
                31959109
                24eab323-794b-4773-9db6-35058c63b30d
                © The Author(s). 2020

                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.

                History
                : 23 October 2019
                : 13 January 2020
                Funding
                Funded by: the National Key R&D Program of China
                Award ID: 2017YFA0605100
                Award Recipient :
                Funded by: the Key Research Program of Frontier Sciences, CAS
                Award ID: QYZDJ-SSW-SMC027
                Award Recipient :
                Funded by: the National Natural Science Foundation of China
                Award ID: 31330008
                Award ID: 31370250
                Award ID: 31770238
                Award Recipient :
                Funded by: the Youth Innovation Promotion Association, Chinese Academy of Sciences
                Award ID: 2012070
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Evolutionary Biology
                taxus cuspidata,mitogenome,endosymbiotic gene transfer,rna editing,gymnosperms

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