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      Organization and evolution of transposable elements along the bread wheat chromosome 3B

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          Abstract

          Background

          The 17 Gb bread wheat genome has massively expanded through the proliferation of transposable elements (TEs) and two recent rounds of polyploidization. The assembly of a 774 Mb reference sequence of wheat chromosome 3B provided us with the opportunity to explore the impact of TEs on the complex wheat genome structure and evolution at a resolution and scale not reached so far.

          Results

          We develop an automated workflow, CLARI-TE, for TE modeling in complex genomes. We delineate precisely 56,488 intact and 196,391 fragmented TEs along the 3B pseudomolecule, accounting for 85% of the sequence, and reconstruct 30,199 nested insertions. TEs have been mostly silent for the last one million years, and the 3B chromosome has been shaped by a succession of bursts that occurred between 1 to 3 million years ago. Accelerated TE elimination in the high-recombination distal regions is a driving force towards chromosome partitioning. CACTAs overrepresented in the high-recombination distal regions are significantly associated with recently duplicated genes. In addition, we identify 140 CACTA-mediated gene capture events with 17 genes potentially created by exon shuffling and show that 19 captured genes are transcribed and under selection pressure, suggesting the important role of CACTAs in the recent wheat adaptation.

          Conclusion

          Accurate TE modeling uncovers the dynamics of TEs in a highly complex and polyploid genome. It provides novel insights into chromosome partitioning and highlights the role of CACTA transposons in the high level of gene duplication in wheat.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13059-014-0546-4) contains supplementary material, which is available to authorized users.

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          Most cited references52

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          The Sorghum bicolor genome and the diversification of grasses.

          Sorghum, an African grass related to sugar cane and maize, is grown for food, feed, fibre and fuel. We present an initial analysis of the approximately 730-megabase Sorghum bicolor (L.) Moench genome, placing approximately 98% of genes in their chromosomal context using whole-genome shotgun sequence validated by genetic, physical and syntenic information. Genetic recombination is largely confined to about one-third of the sorghum genome with gene order and density similar to those of rice. Retrotransposon accumulation in recombinationally recalcitrant heterochromatin explains the approximately 75% larger genome size of sorghum compared with rice. Although gene and repetitive DNA distributions have been preserved since palaeopolyploidization approximately 70 million years ago, most duplicated gene sets lost one member before the sorghum-rice divergence. Concerted evolution makes one duplicated chromosomal segment appear to be only a few million years old. About 24% of genes are grass-specific and 7% are sorghum-specific. Recent gene and microRNA duplications may contribute to sorghum's drought tolerance.
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            The Bioperl toolkit: Perl modules for the life sciences.

            The Bioperl project is an international open-source collaboration of biologists, bioinformaticians, and computer scientists that has evolved over the past 7 yr into the most comprehensive library of Perl modules available for managing and manipulating life-science information. Bioperl provides an easy-to-use, stable, and consistent programming interface for bioinformatics application programmers. The Bioperl modules have been successfully and repeatedly used to reduce otherwise complex tasks to only a few lines of code. The Bioperl object model has been proven to be flexible enough to support enterprise-level applications such as EnsEMBL, while maintaining an easy learning curve for novice Perl programmers. Bioperl is capable of executing analyses and processing results from programs such as BLAST, ClustalW, or the EMBOSS suite. Interoperation with modules written in Python and Java is supported through the evolving BioCORBA bridge. Bioperl provides access to data stores such as GenBank and SwissProt via a flexible series of sequence input/output modules, and to the emerging common sequence data storage format of the Open Bioinformatics Database Access project. This study describes the overall architecture of the toolkit, the problem domains that it addresses, and gives specific examples of how the toolkit can be used to solve common life-sciences problems. We conclude with a discussion of how the open-source nature of the project has contributed to the development effort.
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              The origin of new genes: glimpses from the young and old.

              Genome data have revealed great variation in the numbers of genes in different organisms, which indicates that there is a fundamental process of genome evolution: the origin of new genes. However, there has been little opportunity to explore how genes with new functions originate and evolve. The study of ancient genes has highlighted the antiquity and general importance of some mechanisms of gene origination, and recent observations of young genes at early stages in their evolution have unveiled unexpected molecular and evolutionary processes.
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                Author and article information

                Contributors
                josquin.daron@clermont.inra.fr
                natasha-marie.glover@clermont.inra.fr
                lise.pingault@gmail.com
                sebastien.theil@bordeaux.inra.fr
                veronique.jamilloux@versailles.inra.fr
                etienne.paux@clermont.inra.fr
                vbarbe@genoscope.cns.fr
                smangenot@genoscope.cns.fr
                aalberti@genoscope.cns.fr
                pwincker@genoscope.cns.fr
                hadi.quesneville@versailles.inra.fr
                catherine.feuillet@bayer.com
                frederic.choulet@clermont.inra.fr
                Journal
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1465-6906
                1465-6914
                3 December 2014
                3 December 2014
                2014
                : 15
                : 12
                : 546
                Affiliations
                [ ]INRA UMR1095 Genetics, Diversity and Ecophysiology of Cereals, 5 chemin de Beaulieu, 63039 Clermont-Ferrand, France
                [ ]University Blaise Pascal UMR1095 Genetics, Diversity and Ecophysiology of Cereals, 5 chemin de Beaulieu, 63039 Clermont-Ferrand, France
                [ ]INRA-URGI, Centre de Versailles, Route de Saint Cyr, 78026 Versailles, France
                [ ]CEA/DSV/IG/Genoscope, 2 rue Gaston Cremieux, 91000 Evry, France
                [ ]CNRS UMR 8030, 2 rue Gaston Crémieux, 91000 Evry, France
                [ ]Université d’Evry, P5706 Evry, France
                Article
                546
                10.1186/s13059-014-0546-4
                4290129
                25476263
                265d5c07-e24b-4777-b18c-d2027492d6d6
                © Daron et al.; licensee BioMed Central. 2014

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
                : 25 July 2014
                : 17 November 2014
                Categories
                Research
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                © The Author(s) 2014

                Genetics
                Genetics

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