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      Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida)

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          Abstract

          Doubly uniparental inheritance (DUI) describes a mode of mtDNA transmission widespread in gonochoric freshwater mussels (Bivalvia: Palaeoheterodonta: Unionida). In this system, both female- and male-transmitted mtDNAs, named F and M respectively, coexist in the same species. In unionids, DUI is strictly correlated to gonochorism and to the presence of the atypical open reading frames (ORFans) F- orf and M- orf, respectively inside F and M mtDNAs, which are hypothesized to participate in sex determination. However, DUI is not found in all three Unionida superfamilies (confirmed in Hyrioidea and Unionoidea but not in Etherioidea), raising the question of its origin in these bivalves. To reconstruct the co-evolution of DUI and of ORFans, we sequenced the mtDNAs of four unionids (two gonochoric with DUI, one gonochoric and one hermaphroditic without DUI) and of the related gonochoric species Neotrigonia margaritacea (Palaeoheterodonta: Trigoniida). Our analyses suggest that rearranged mtDNAs appeared early during unionid radiation, and that a duplicated and diverged atp8 gene evolved into the M- orf associated with the paternal transmission route in Hyrioidea and Unionoidea, but not in Etherioidea. We propose that novel mtDNA-encoded genes can deeply influence bivalve sex determining systems and the evolution of the mitogenomes in which they occur.

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          tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence

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            T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension

            This article introduces a new interface for T-Coffee, a consistency-based multiple sequence alignment program. This interface provides an easy and intuitive access to the most popular functionality of the package. These include the default T-Coffee mode for protein and nucleic acid sequences, the M-Coffee mode that allows combining the output of any other aligners, and template-based modes of T-Coffee that deliver high accuracy alignments while using structural or homology derived templates. These three available template modes are Expresso for the alignment of protein with a known 3D-Structure, R-Coffee to align RNA sequences with conserved secondary structures and PSI-Coffee to accurately align distantly related sequences using homology extension. The new server benefits from recent improvements of the T-Coffee algorithm and can align up to 150 sequences as long as 10 000 residues and is available from both http://www.tcoffee.org and its main mirror http://tcoffee.crg.cat.
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              Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species.

              The mitochondrial genome (mtDNA) of Metazoa is a good model system for evolutionary genomic studies and the availability of more than 1000 sequences provides an almost unique opportunity to decode the mechanisms of genome evolution over a large phylogenetic range. In this paper, we review several structural features of the metazoan mtDNA, such as gene content, genome size, genome architecture and the new parameter of gene strand asymmetry in a phylogenetic framework. The data reviewed here show that: (1) the plasticity of Metazoa mtDNA is higher than previously thought and mainly due to variation in number and location of tRNA genes; (2) an exceptional trend towards stabilization of genomic features occurred in deuterostomes and was exacerbated in vertebrates, where gene content, genome architecture and gene strand asymmetry are almost invariant. Only tunicates exhibit a very high degree of genome variability comparable to that found outside deuterostomes. In order to analyse the genomic evolutionary process at short evolutionary distances, we have also compared mtDNAs of species belonging to the same genus: the variability observed in congeneric species significantly recapitulates the evolutionary dynamics observed at higher taxonomic ranks, especially for taxa showing high levels of genome plasticity and/or fast nucleotide substitution rates. Thus, the analysis of congeneric species promises to be a valuable approach for the assessment of the mtDNA evolutionary trend in poorly or not yet sampled metazoan groups.
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                Author and article information

                Contributors
                davide.guerra@umontreal.ca
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                8 May 2017
                8 May 2017
                2017
                : 7
                : 1551
                Affiliations
                [1 ]ISNI 0000 0001 2292 3357, GRID grid.14848.31, , Université de Montréal, Département de Sciences Biologiques, ; Montréal, H2V 2S9 Quebéc Canada
                [2 ]ISNI 0000 0004 1757 1758, GRID grid.6292.f, , Università di Bologna, Dipartimento di Scienze Biologiche, Geologiche ed Ambientali (BiGeA), ; Bologna, 40126 Italy
                [3 ]ISNI 0000 0004 1936 9633, GRID grid.411959.1, , Acadia University, Department of Biology, ; Wolfville, B4P 2R6 Nova Scotia Canada
                [4 ]ISNI 0000 0001 2226 059X, GRID grid.421582.8, , North Carolina Museum of Natural Sciences, ; Raleigh, 27607 NC USA
                [5 ]ISNI 0000 0001 0656 9343, GRID grid.258518.3, , Kent State University, Department of Biological Sciences, ; Kent, 44242 OH USA
                Author information
                http://orcid.org/0000-0002-8242-7731
                http://orcid.org/0000-0001-5920-7557
                Article
                1708
                10.1038/s41598-017-01708-1
                5431520
                28484275
                b9d49f3a-bea3-4d49-9ba9-15438bf7fe6b
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 January 2017
                : 31 March 2017
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