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      Characterization and Phylogenetic Analysis of the Mitochondrial Genome of Shiraia bambusicola Reveals Special Features in the Order of Pleosporales

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          Abstract

          Shiraia bambusicola P. Henn. is a pathogenic fungus of bamboo, and its fruiting bodies are regarded as folk medicine. We determined and analyzed its complete mitochondrial DNA sequence (circular DNA molecule of 39,030 bp, G + C content of 25.19%). It contains the typical genes encoding proteins involved in electron transport and coupled oxidative phosphorylation ( nad1-6 and nad4L, cob and cox1-3), one ATP synthase subunit ( atp6), 4 hypothetical proteins, and two genes for large and small rRNAs ( rnl and rns). There is a set of 32 tRNA genes comprising all 20 amino acids, and these genes are evenly distributed on the two strands. Phylogenetic analyses based on concatenated mitochondrial proteins indicated that S. bambusicola clustered with members of the order Pleosporales, which is in agreement with previous results. The gene arrangements of Dothideomycetes species contained three regions of gene orders partitioned in their mitochondrial genomes, including block 1 ( nad6-atp6), block 2 ( nad1-cox3) and block 3 (genes around rns). S. bambusicola displayed unique special features that differed from the other Pleosporales species, especially in the coding regions around rns ( trnR-trnY). Moreover, a comparison of gene orders in mitochondrial genomes from Pezizomycotina revealed that although all encoded regions are located on the same strand in most Pezizomycotina mtDNAs, genes from Dothideomycetes species had different orientations, as well as diverse positions and colocalization of genes (such as cox3, cox1-cox2 and nad2–nad3); these distinctions were regarded as class-specific features. Interestingly, two incomplete copies of the atp6 gene were found on different strands of the mitogenomic DNA, a finding that has not been observed in the other analyzed fungal species. In our study, mitochondrial genomes from Dothideomycetes species were comprehensively analyzed for the first time, including many species that have not appeared in previous reports.

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Mitochondrial evolution.

            The serial endosymbiosis theory is a favored model for explaining the origin of mitochondria, a defining event in the evolution of eukaryotic cells. As usually described, this theory posits that mitochondria are the direct descendants of a bacterial endosymbiont that became established at an early stage in a nucleus-containing (but amitochondriate) host cell. Gene sequence data strongly support a monophyletic origin of the mitochondrion from a eubacterial ancestor shared with a subgroup of the alpha-Proteobacteria. However, recent studies of unicellular eukaryotes (protists), some of them little known, have provided insights that challenge the traditional serial endosymbiosis-based view of how the eukaryotic cell and its mitochondrion came to be. These data indicate that the mitochondrion arose in a common ancestor of all extant eukaryotes and raise the possibility that this organelle originated at essentially the same time as the nuclear component of the eukaryotic cell rather than in a separate, subsequent event.
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              The genome sequence of Rickettsia prowazekii and the origin of mitochondria.

              We describe here the complete genome sequence (1,111,523 base pairs) of the obligate intracellular parasite Rickettsia prowazekii, the causative agent of epidemic typhus. This genome contains 834 protein-coding genes. The functional profiles of these genes show similarities to those of mitochondrial genes: no genes required for anaerobic glycolysis are found in either R. prowazekii or mitochondrial genomes, but a complete set of genes encoding components of the tricarboxylic acid cycle and the respiratory-chain complex is found in R. prowazekii. In effect, ATP production in Rickettsia is the same as that in mitochondria. Many genes involved in the biosynthesis and regulation of biosynthesis of amino acids and nucleosides in free-living bacteria are absent from R. prowazekii and mitochondria. Such genes seem to have been replaced by homologues in the nuclear (host) genome. The R. prowazekii genome contains the highest proportion of non-coding DNA (24%) detected so far in a microbial genome. Such non-coding sequences may be degraded remnants of 'neutralized' genes that await elimination from the genome. Phylogenetic analyses indicate that R. prowazekii is more closely related to mitochondria than is any other microbe studied so far.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 March 2015
                2015
                : 10
                : 3
                : e0116466
                Affiliations
                [1 ]College of Life Science, Capital Normal University, Beijing, People’s Republic of China
                [2 ]Key Laboratory of Bamboo and Rattan Science and Technology of the SFA, International Centre for Bamboo and Rattan, Beijing, People’s Republic of China
                University Paris South, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: XYS LF. Performed the experiments: XYS TL SC. Analyzed the data: XYS LF JG CLH. Contributed reagents/materials/analysis tools: XYS LF JG CLH. Wrote the paper: XYS LF JG CLH.

                Article
                PONE-D-14-43764
                10.1371/journal.pone.0116466
                4366305
                25790308
                81621012-5122-4cc0-9e57-31ec17c96dee
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 11 October 2014
                : 8 December 2014
                Page count
                Figures: 3, Tables: 4, Pages: 20
                Funding
                CLH was supported by Key Program of Science and Technology Development Project of Beijing Municipal Education Commission (KZ201110028036), the National Natural Science Foundation of China (No. 31170019), and the Beijing Natural Science Foundation (and No. 5132009). LF was supported by the National Natural Science Foundation of China (No. 31270058) and the Beijing Natural Science Foundation (No. 5122003). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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