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      Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements

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          Abstract

          Transfer RNAs (tRNAs) are present in all types of cells as well as in organelles. tRNAs of animal mitochondria show a low level of primary sequence conservation and exhibit ‘bizarre’ secondary structures, lacking complete domains of the common cloverleaf. Such sequences are hard to detect and hence frequently missed in computational analyses and mitochondrial genome annotation. Here, we introduce an automatic annotation procedure for mitochondrial tRNA genes in Metazoa based on sequence and structural information in manually curated covariance models. The method, applied to re-annotate 1876 available metazoan mitochondrial RefSeq genomes, allows to distinguish between remaining functional genes and degrading ‘pseudogenes’, even at early stages of divergence. The subsequent analysis of a comprehensive set of mitochondrial tRNA genes gives new insights into the evolution of structures of mitochondrial tRNA sequences as well as into the mechanisms of genome rearrangements. We find frequent losses of tRNA genes concentrated in basal Metazoa, frequent independent losses of individual parts of tRNA genes, particularly in Arthropoda, and wide-spread conserved overlaps of tRNAs in opposite reading direction. Direct evidence for several recent Tandem Duplication-Random Loss events is gained, demonstrating that this mechanism has an impact on the appearance of new mitochondrial gene orders.

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          tRNAdb 2009: compilation of tRNA sequences and tRNA genes

          One of the first specialized collections of nucleic acid sequences in life sciences was the ‘compilation of tRNA sequences and sequences of tRNA genes’ (http://www.trna.uni-bayreuth.de). Here, an updated and completely restructured version of this compilation is presented (http://trnadb.bioinf.uni-leipzig.de). The new database, tRNAdb, is hosted and maintained in cooperation between the universities of Leipzig, Marburg, and Strasbourg. Reimplemented as a relational database, tRNAdb will be updated periodically and is searchable in a highly flexible and user-friendly way. Currently, it contains more than 12 000 tRNA genes, classified into families according to amino acid specificity. Furthermore, the implementation of the NCBI taxonomy tree facilitates phylogeny-related queries. The database provides various services including graphical representations of tRNA secondary structures, a customizable output of aligned or un-aligned sequences with a variety of individual and combinable search criteria, as well as the construction of consensus sequences for any selected set of tRNAs.
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            Big trees from little genomes: mitochondrial gene order as a phylogenetic tool.

            Gene arrangement comparisons are a powerful tool for phylogenetic studies, especially those focused on ancient relationships. Recent reports using metazoan mitochondrial genomes address evolutionary relationships as well as rates and mechanisms of rearrangement. Mitochondrial systems serve as a model for larger-scale comparisons of whole organismal genomes and a stimulus for developing methods for reconstructing the patterns of rearrangement.
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              A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus.

              We determined the complete mtDNA sequence of the centipede Lithobius forficatus and found that only one of the 22 inferred tRNA genes encodes a fully paired aminoacyl acceptor stem. The other 21 genes encode tRNAs with up to five mismatches in these stems, and some of these overlap extensively with the downstream genes. Because a well-paired acceptor stem is required for proper tRNA functioning, RNA editing in the products of these genes was suspected. We investigated this hypothesis by studying cDNA sequences from eight tRNAs and found the editing of up to 5 nt at their 3' ends. This editing appears to occur by a novel mechanism with the 5' end of the acceptor stem being used as a template for the de novo synthesis of the 3' end, presumably by an RNA-dependent RNA polymerase. In addition, unusual secondary structures for several tRNAs were found, including those lacking a TPsiC (T) or a dihydrouridine (D) arm, and having an unusual number of base pairs in the acceptor or anticodon stems.
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                Author and article information

                Journal
                Nucleic Acids Res
                Nucleic Acids Res
                nar
                nar
                Nucleic Acids Research
                Oxford University Press
                0305-1048
                1362-4962
                April 2012
                April 2012
                1 December 2011
                1 December 2011
                : 40
                : 7
                : 2833-2845
                Affiliations
                1Bioinformatics Group, Department of Computer Science, Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany, 2Architecture et Réactivité de l'ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, F-67084 Strasbourg, France, 3Parallel Computing and Complex Systems Group, Department of Computer Science, University of Leipzig, Johannisgasse 26, D-04103 Leipzig, Germany, 4Zentrum für Molekulare Biodiversitätsforschung, Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany, 5Max Planck Institute for Mathematics in the Sciences, Inselstraße 22, D-04103 Leipzig, Germany, 6Fraunhofer Institut für Zelltherapie und Immunologie – IZI, Perlickstraße 1, D-04103 Leipzig, Germany, 7Center for non-coding RNA in Technology and Health, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg, Denmark, 8Department of Theoretical Chemistry, University of Vienna, Währingerstraße 17, A-1090 Wien, Austria and 9Santa Fe Institute, 1399 Hyde Park Rd., Santa Fe, NM 87501, USA
                Author notes
                *To whom correspondence should be addressed. Tel: +33 3 88 417059; Fax: +33 3 88 602218; Email: c.florentz@ 123456ibmc-cnrs.unistra.fr
                Correspondence may also be addressed to Peter F. Stadler. Tel: +49 341 9716691; Fax: +49 341 9716679; Email: stadler@ 123456bioinf.uni-leipzig.de

                The authors wish it to be known that, in their opinion, the first two authors should be regarded as joint First Authors.

                Article
                gkr1131
                10.1093/nar/gkr1131
                3326299
                22139921
                8e822ebc-68f4-4112-ae52-5cb12b86ada5
                © The Author(s) 2011. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 8 September 2011
                : 24 October 2011
                : 8 September 2011
                Page count
                Pages: 13
                Categories
                Computational Biology

                Genetics
                Genetics

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