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      Multiple Lineages of Ancient CR1 Retroposons Shaped the Early Genome Evolution of Amniotes

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          Abstract

          Chicken repeat 1 (CR1) retroposons are long interspersed elements (LINEs) that are ubiquitous within amniote genomes and constitute the most abundant family of transposed elements in birds, crocodilians, turtles, and snakes. They are also present in mammalian genomes, where they reside as numerous relics of ancient retroposition events. Yet, despite their relevance for understanding amniote genome evolution, the diversity and evolution of CR1 elements has never been studied on an amniote-wide level. We reconstruct the temporal and quantitative activity of CR1 subfamilies via presence/absence analyses across crocodilian phylogeny and comparative analyses of 12 crocodilian genomes, revealing relative genomic stasis of retroposition during genome evolution of extant Crocodylia. Our large-scale phylogenetic analysis of amniote CR1 subfamilies suggests the presence of at least seven ancient CR1 lineages in the amniote ancestor; and amniote-wide analyses of CR1 successions and quantities reveal differential retention (presence of ancient relics or recent activity) of these CR1 lineages across amniote genome evolution. Interestingly, birds and lepidosaurs retained the fewest ancient CR1 lineages among amniotes and also exhibit smaller genome sizes. Our study is the first to analyze CR1 evolution in a genome-wide and amniote-wide context and the data strongly suggest that the ancestral amniote genome contained myriad CR1 elements from multiple ancient lineages, and remnants of these are still detectable in the relatively stable genomes of crocodilians and turtles. Early mammalian genome evolution was thus characterized by a drastic shift from CR1 prevalence to dominance and hyperactivity of L2 LINEs in monotremes and L1 LINEs in therians.

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          Most cited references51

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          Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition.

          R2 is a non-LTR retrotransposable element that inserts at a specific site in the 28S rRNA genes of most insects. We have expressed the open reading frame of the R2 element from Bombyx mori, R2Bm, in E. coli and shown that it encodes both sequence-specific endonuclease and reverse transcriptase activities. The R2 protein makes a specific nick in one of the DNA strands at the insertion site and uses the 3' hydroxyl group exposed by this nick to prime reverse transcription of its RNA transcript. After reverse transcription, cleavage of the second DNA strand occurs. A similar mechanism of insertion may be used by other non-LTR retrotransposable elements as well as short interspersed nucleotide elements.
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            Genome analysis of the platypus reveals unique signatures of evolution.

            We present a draft genome sequence of the platypus, Ornithorhynchus anatinus. This monotreme exhibits a fascinating combination of reptilian and mammalian characters. For example, platypuses have a coat of fur adapted to an aquatic lifestyle; platypus females lactate, yet lay eggs; and males are equipped with venom similar to that of reptiles. Analysis of the first monotreme genome aligned these features with genetic innovations. We find that reptile and platypus venom proteins have been co-opted independently from the same gene families; milk protein genes are conserved despite platypuses laying eggs; and immune gene family expansions are directly related to platypus biology. Expansions of protein, non-protein-coding RNA and microRNA families, as well as repeat elements, are identified. Sequencing of this genome now provides a valuable resource for deep mammalian comparative analyses, as well as for monotreme biology and conservation.
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              The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage

              Background We describe the genome of the western painted turtle, Chrysemys picta bellii, one of the most widespread, abundant, and well-studied turtles. We place the genome into a comparative evolutionary context, and focus on genomic features associated with tooth loss, immune function, longevity, sex differentiation and determination, and the species' physiological capacities to withstand extreme anoxia and tissue freezing. Results Our phylogenetic analyses confirm that turtles are the sister group to living archosaurs, and demonstrate an extraordinarily slow rate of sequence evolution in the painted turtle. The ability of the painted turtle to withstand complete anoxia and partial freezing appears to be associated with common vertebrate gene networks, and we identify candidate genes for future functional analyses. Tooth loss shares a common pattern of pseudogenization and degradation of tooth-specific genes with birds, although the rate of accumulation of mutations is much slower in the painted turtle. Genes associated with sex differentiation generally reflect phylogeny rather than convergence in sex determination functionality. Among gene families that demonstrate exceptional expansions or show signatures of strong natural selection, immune function and musculoskeletal patterning genes are consistently over-represented. Conclusions Our comparative genomic analyses indicate that common vertebrate regulatory networks, some of which have analogs in human diseases, are often involved in the western painted turtle's extraordinary physiological capacities. As these regulatory pathways are analyzed at the functional level, the painted turtle may offer important insights into the management of a number of human health disorders.
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                Author and article information

                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                January 2015
                11 December 2014
                11 December 2014
                : 7
                : 1
                : 205-217
                Affiliations
                1Institute of Experimental Pathology (ZMBE), University of Münster, Germany
                2Department of Evolutionary Biology (EBC), Uppsala University, Sweden
                3Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University
                4Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University
                5Department of Biological Sciences, Texas Tech University
                6Genetic Information Research Institute, Mountain View, California
                7Institute for Systems Biology, Seattle, Washington
                8Department of Biology, University of Florida
                9Department of Biomolecular Engineering, University of California
                10Department of Biology and Genetics Institute, University of Florida
                11Present address: Cancer Prevention and Control Program, Fox Chase Cancer Center, Philadelphia, PA
                12Present address: Department of Biology, Temple University, Philadelphia, PA
                Author notes
                *Corresponding author: E-mail: alexander.suh@ 123456ebc.uu.se .

                Associate editor: Ellen Pritham

                Deceased.

                These authors contributed equally to this work.

                Data deposition: Raw survey sequence data have been deposited at Sequence Read Archive (SRA; accession number SRP048845). Sanger sequence data have been deposited at GenBank (accession numbers KP159624-KP159743).

                Article
                evu256
                10.1093/gbe/evu256
                4316615
                25503085
                de6c302e-9928-4a3b-9217-051d193dd0e4
                © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 November 2014
                Page count
                Pages: 13
                Categories
                Research Article

                Genetics
                transposable elements,chicken repeat 1,phylogenomics,comparative genomics,crocodilian genomes,amniotes

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