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      Drosophila Muller F Elements Maintain a Distinct Set of Genomic Properties Over 40 Million Years of Evolution

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      G3: Genes|Genomes|Genetics

      Genetics Society of America

      codon bias, evolution of heterochromatin, gene size, melting characteristics, transposons

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          Abstract

          The Muller F element (4.2 Mb, ~80 protein-coding genes) is an unusual autosome of Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To investigate how these properties impact the evolution of repeats and genes, we manually improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. grimshawi F elements and euchromatic domains from the Muller D element. We find that F elements have greater transposon density (25–50%) than euchromatic reference regions (3–11%). Among the F elements, D. grimshawi has the lowest transposon density (particularly DINE-1: 2% vs. 11–27%). F element genes have larger coding spans, more coding exons, larger introns, and lower codon bias. Comparison of the Effective Number of Codons with the Codon Adaptation Index shows that, in contrast to the other species, codon bias in D. grimshawi F element genes can be attributed primarily to selection instead of mutational biases, suggesting that density and types of transposons affect the degree of local heterochromatin formation. F element genes have lower estimated DNA melting temperatures than D element genes, potentially facilitating transcription through heterochromatin. Most F element genes (~90%) have remained on that element, but the F element has smaller syntenic blocks than genome averages (3.4–3.6 vs. 8.4–8.8 genes per block), indicating greater rates of inversion despite lower rates of recombination. Overall, the F element has maintained characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.

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          Most cited references 67

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          Consed: a graphical tool for sequence finishing.

          Sequencing of large clones or small genomes is generally done by the shotgun approach (Anderson et al. 1982). This has two phases: (1) a shotgun phase in which a number of reads are generated from random subclones and assembled into contigs, followed by (2) a directed, or finishing phase in which the assembly is inspected for correctness and for various kinds of data anomalies (such as contaminant reads, unremoved vector sequence, and chimeric or deleted reads), additional data are collected to close gaps and resolve low quality regions, and editing is performed to correct assembly or base-calling errors. Finishing is currently a bottleneck in large-scale sequencing efforts, and throughput gains will depend both on reducing the need for human intervention and making it as efficient as possible. We have developed a finishing tool, consed, which attempts to implement these principles. A distinguishing feature relative to other programs is the use of error probabilities from our programs phred and phrap as an objective criterion to guide the entire finishing process. More information is available at http:// www.genome.washington.edu/consed/consed. html.
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            Evolution of genes and genomes on the Drosophila phylogeny.

            Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.
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              The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.

               Mindy Li,  P. Sharp (1987)
              A simple, effective measure of synonymous codon usage bias, the Codon Adaptation Index, is detailed. The index uses a reference set of highly expressed genes from a species to assess the relative merits of each codon, and a score for a gene is calculated from the frequency of use of all codons in that gene. The index assesses the extent to which selection has been effective in moulding the pattern of codon usage. In that respect it is useful for predicting the level of expression of a gene, for assessing the adaptation of viral genes to their hosts, and for making comparisons of codon usage in different organisms. The index may also give an approximate indication of the likely success of heterologous gene expression.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                4 March 2015
                May 2015
                : 5
                : 5
                : 719-740
                Affiliations
                [a ]Department of Biology, Washington University in St. Louis, St. Louis, MO 63130
                [b ]Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35401
                [c ]Department of Biology, Arcadia University, Glenside, PA 19038
                [d ]Department of Biology, Adams State University, Alamosa, CO 81101
                [e ]Department of Biology, Agnes Scott College, Decatur, GA 30030
                [f ]Department of Biology, Albion College, Albion, MI 49224
                [g ]Department of Biology, Amherst College, Amherst, MA 01002
                [h ]Department of Computer Science and Mathematics, Arcadia University, Glenside, PA 19038
                [i ]Science Department, Cabrini College, Radnor, PA 19087
                [j ]Department of Biology, California Lutheran University, Thousand Oaks, CA 91360
                [k ]Department of Chemistry and Biochemistry, California Polytechnic State University, San Luis Obispo, CA 93407
                [l ]Division of Science and Environmental Policy, California State University, Monterey Bay, Seaside, CA 93950
                [m ]Department of Biology, California State University, Stanislaus, Turlock, CA 95382
                [n ]Department of Biology, Calvin College, Grand Rapids, MI 49546
                [o ]Department of Natural Sciences, Cardinal Stritch University, Milwaukee, WI 53217
                [p ]Department of Biology, College of William & Mary, Williamsburg, VA 23187
                [q ]Department of Biology, Denison University, Granville, OH 43023
                [r ]Department of Biology, Duke University, Durham, NC 27708
                [s ]Department of Biology, Georgetown University, Washington, DC 20057
                [t ]Departments of Biomedical Sciences & Cell and Molecular Biology, Grand Valley State University, Allendale, MI 49401
                [u ]Biology Department, Hampden-Sydney College, Hampden-Sydney, VA 23943
                [v ]Department of Biology, Hofstra University, Hempstead, NY 11549
                [w ]Department of Computer Science and Engineering, Johnson C. Smith University, Charlotte, NC 28216
                [x ]Department of Natural Sciences, LaGuardia Community College, Long Island City, NY 11101
                [y ]Chemistry Department, Lindenwood University, St. Charles, MO 63301
                [z ]Department of Biological and Environmental Sciences, Longwood University, Farmville, VA 23909
                [aa ]Department of Biology, Loyola Marymount University, Los Angeles, CA 90045
                [bb ]Biology Department, Luther College, Decorah, IA 52101
                [cc ]Department of Biology, Macalester College, St. Paul, MN 55105
                [dd ]Department of Mathematics, Statistics, and Computer Science, Macalester College, St. Paul, MN 55105
                [ee ]Biology Department, McDaniel College, Westminster, MD 21157
                [ff ]Department of Biology, Missouri Western State University, St. Joseph, MO 64507
                [gg ]Department of Computer Science, Math and Physics, Missouri Western State University, St. Joseph, MO 64507
                [hh ]Department of Biology & Molecular Biology, Montclair State University, Montclair, NJ 07043
                [ii ]Department of Biological Sciences, Moravian College, Bethlehem, PA 18018
                [jj ]Biology Department, Muhlenberg College, Allentown, PA 18104
                [kk ]Department of Biology, New Mexico Highlands University, Las Vegas, NM 87701
                [ll ]Department of Biology, North Carolina A&T State University, Greensboro, NC 27411
                [mm ]Biology Department, North Carolina Central University, Durham, NC 27707
                [nn ]Biology Department, Oberlin College, Oberlin, OH 44074
                [oo ]Department of Biology, Pomona College, Claremont, CA 91711
                [pp ]Department of Biology, Prairie View A&M University, Prairie View, TX 77446
                [qq ]Department of Biology, Saint Joseph’s University, Philadelphia, PA 19131
                [rr ]Department of Biology, Saint Mary’s College, Notre Dame, IN 46556
                [ss ]Department of Biology, Saint Mary’s College of California, Moraga, CA 94556
                [tt ]Department of Biology, San Francisco State University, San Francisco CA 94132
                [uu ]Biology Department, Simmons College, Boston, MA 02115
                [vv ]Department of Chemistry, Simmons College, Boston, MA 02115
                [ww ]Bioinformatics Program, St. Edward’s University, Austin, TX 78704
                [xx ]Grove School of Engineering, City College / CUNY, New York, NY10031
                [yy ]Biology Department, The City College of New York, New York, NY 10031
                [zz ]Department of Biological Sciences, The George Washington University, Washington, DC 20052
                [aaa ]Division of Biological Sciences, University of California, San Diego, La Jolla, CA 92093
                [bbb ]Department of Biology, University of Evansville, Evansville, IN 47722
                [ccc ]Department of Biochemistry, University of Nebraska–Lincoln, Lincoln, NE 68588
                [ddd ]Department of Health Information Management, University of Pittsburgh, Pittsburgh, PA 15213
                [eee ]Department of Biology, University of Puerto Rico at Cayey, Cayey, PR 00736
                [fff ]Department of Biology, University of Puerto Rico at Mayagüez, Mayagüez, PR 00680
                [ggg ]Biology Department, University of the Incarnate Word, San Antonio, TX 78209
                [hhh ]Department of Biology, University of West Florida, Pensacola, FL 32514
                [iii ]Department of Biology, Utah Valley University, Orem, UT 84058
                [jjj ]Department of Biological Sciences, Webster University, Webster Groves, MO 63119
                [kkk ]Department of Biology, Widener University, Chester, PA 19013
                [lll ]Departments of Chemistry and Biochemistry, Widener University, Chester, PA 19013
                [mmm ]Department of Biology, Wilkes University, Wilkes-Barre, PA 18766
                [nnn ]Department of Biology, William Woods University, Fulton, MO 65251
                [ooo ]Biology Department, Worcester State University, Worcester, MA 01602
                [ppp ]Department of Biology, York College / CUNY, Jamaica, NY 11451
                [qqq ]Department of Computer Science and Engineering, Washington University in St. Louis, St. Louis, MO 63130
                [rrr ]Genome Institute, Department of Genetics, Washington University School of Medicine, St. Louis, MO 63108
                Author notes
                [1]

                Department of Biology, University of the Fraser Valley, Abbotsford, BC V2S 7M8, Canada

                [2]

                Biology Department, Massasoit Community College, Brockton, MA 02302

                [3]

                Department of Biology, Washington University in St. Louis, St. Louis, MO 63130

                [4]

                College of Engineering & Science, University of Detroit Mercy, Detroit, MI 48221

                [5]

                Department of Biology, University of San Diego, San Diego, CA 92110

                [6]

                Department of Biology, University of the Cumberlands, Williamsburg, KY 40769

                [7]

                1 Cranberry Hill, Suite 403, Lexington, MA 02421

                [8]

                School of Natural and Health Sciences, Mount Mary University, Milwaukee, WI 53222

                [9]

                Department of Biology, The University of Alabama at Birmingham, Birmingham, AL 35294

                Corresponding author: Sarah C. R. Elgin, Washington University in St. Louis, Campus Box 1137, One Brookings Drive, St. Louis, MO 63130-4899. E-mail: selgin@ 123456wustl.edu
                Article
                GGG_015966
                10.1534/g3.114.015966
                4426361
                25740935
                Copyright © 2015 Leung et al.

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

                Page count
                Pages: 22
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                Categories
                Investigations

                Genetics

                transposons, codon bias, evolution of heterochromatin, gene size, melting characteristics

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