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      Horizontal transfer of a non-autonomous Helitron among insect and viral genomes

      research-article
      BMC Genomics
      BioMed Central
      Horizontal transposon transfer, Viral vectors

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          Abstract

          Background

          The movement of mobile elements among species by horizontal transposon transfer (HTT) influences the evolution of genomes through the modification of structure and function. Helitrons are a relatively new lineage of DNA-based (class II) transposable elements (TEs) that propagate by rolling-circle replication, and are capable of acquiring host DNA. The rapid spread of Helitrons among animal lineages by HTT is facilitated by shuttling in viral particles or by unknown mechanisms mediated by close organism associations (e.g. between hosts and parasites).

          Results

          A non-autonomous Helitron independently annotated as BmHel-2 from Bombyx mori and the MITE01 element from Ostrinia nubilalis was predicted in the genomes of 24 species in the insect Order Lepidoptera. Integrated Helitrons retained ≥ 65% sequence identity over a 250 bp consensus, and were predicted to retain secondary structures inclusive of a 3′-hairpin and a 5′-subterminal inverted repeat. Highly similar Hel-2 copies were predicted in the genomes of insects and associated viruses, which along with a previous documented case of real-time virus-insect cell line transposition suggests that this Helitron has likely propagated by HTT.

          Conclusions

          These findings provide evidence that insect virus may mediate the HTT of Helitron-like TEs. This movement may facilitate the shuttling of DNA elements among insect genomes. Further sampling is required to determine the putative role of HTT in insect genome evolution.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12864-015-1318-6) contains supplementary material, which is available to authorized users.

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          Most cited references51

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          The evolutionary dynamics of repetitive DNA in eukaryotes.

          Repetitive DNA sequences form a large portion of the genomes of eukaryotes. The 'selfish DNA' hypothesis proposes that they are maintained by their ability to replicate within the genome. The behaviour of repetitive sequences can result in mutations that cause genetic diseases, and confer significant fitness losses on the organism. Features of the organization of repetitive sequences in eukaryotic genomes, and their distribution in natural populations, reflect the evolutionary forces acting on selfish DNA.
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            Inferring phylogeny despite incomplete lineage sorting.

            It is now well known that incomplete lineage sorting can cause serious difficulties for phylogenetic inference, but little attention has been paid to methods that attempt to overcome these difficulties by explicitly considering the processes that produce them. Here we explore approaches to phylogenetic inference designed to consider retention and sorting of ancestral polymorphism. We examine how the reconstructability of a species (or population) phylogeny is affected by (a) the number of loci used to estimate the phylogeny and (b) the number of individuals sampled per species. Even in difficult cases with considerable incomplete lineage sorting (times between divergences less than 1 N(e) generations), we found the reconstructed species trees matched the "true" species trees in at least three out of five partitions, as long as a reasonable number of individuals per species were sampled. We also studied the tradeoff between sampling more loci versus more individuals. Although increasing the number of loci gives more accurate trees for a given sampling effort with deeper species trees (e.g., total depth of 10 N(e) generations), sampling more individuals often gives better results than sampling more loci with shallower species trees (e.g., depth = 1 N(e)). Taken together, these results demonstrate that gene sequences retain enough signal to achieve an accurate estimate of phylogeny despite widespread incomplete lineage sorting. Continued improvement in our methods to reconstruct phylogeny near the species level will require a shift to a compound model that considers not only nucleotide or character state substitutions, but also the population genetics processes of lineage sorting. [Coalescence; divergence; population; speciation.].
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              Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize.

              We report a whole-genome comparison of gene content in allelic BAC contigs from two maize inbred lines. Genic content polymorphisms involve as many as 10,000 sequences and are mainly generated by DNA insertions. The termini of eight of the nine genic insertions that we analyzed shared the structural hallmarks of helitron rolling-circle transposons. DNA segments defined by helitron termini contained multiple gene-derived fragments and had a structure typical of nonautonomous helitron-like transposons. Closely related insertions were found in multiple genomic locations. Some of these produced transcripts containing segments of different genes, supporting the idea that these transposition events have a role in exon shuffling and the evolution of new proteins. We identified putative autonomous helitron elements and found evidence for their transcription. Helitrons in maize seem to continually produce new nonautonomous elements responsible for the duplicative insertion of gene segments into new locations and for the unprecedented genic diversity. The maize genome is in constant flux, as transposable elements continue to change both the genic and nongenic fractions of the genome, profoundly affecting genetic diversity.
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                Author and article information

                Contributors
                brad.coates@ars.usda.gov
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                27 February 2015
                27 February 2015
                2015
                : 16
                : 1
                : 137
                Affiliations
                [ ]United States Department of Agriculture, Agricultural Research Service, Corn Insects & Crop Genetics Research Unit, Iowa State University, Ames, IA 50011 USA
                [ ]Department of Entomology, Iowa State University, Ames, IA 50011 USA
                Article
                1318
                10.1186/s12864-015-1318-6
                4344730
                780749a6-b4b3-46f2-b84b-186d1a3aaea1
                © Coates; licensee BioMed Central. 2015

                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
                : 26 June 2014
                : 3 February 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Genetics
                horizontal transposon transfer,viral vectors
                Genetics
                horizontal transposon transfer, viral vectors

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