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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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      TopHat: discovering splice junctions with RNA-Seq

      Motivation: A new protocol for sequencing the messenger RNA in a cell, known as RNA-Seq, generates millions of short sequence fragments in a single run. These fragments, or ‘reads’, can be used to measure levels of gene expression and to identify novel splice variants of genes. However, current software for aligning RNA-Seq data to a genome relies on known splice junctions and cannot identify novel ones. TopHat is an efficient read-mapping algorithm designed to align reads from an RNA-Seq experiment to a reference genome without relying on known splice sites. Results: We mapped the RNA-Seq reads from a recent mammalian RNA-Seq experiment and recovered more than 72% of the splice junctions reported by the annotation-based software from that study, along with nearly 20 000 previously unreported junctions. The TopHat pipeline is much faster than previous systems, mapping nearly 2.2 million reads per CPU hour, which is sufficient to process an entire RNA-Seq experiment in less than a day on a standard desktop computer. We describe several challenges unique to ab initio splice site discovery from RNA-Seq reads that will require further algorithm development. Availability: TopHat is free, open-source software available from http://tophat.cbcb.umd.edu Contact: cole@cs.umd.edu Supplementary information: Supplementary data are available at Bioinformatics online.
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        BEDTools: a flexible suite of utilities for comparing genomic features

        Motivation: Testing for correlations between different sets of genomic features is a fundamental task in genomics research. However, searching for overlaps between features with existing web-based methods is complicated by the massive datasets that are routinely produced with current sequencing technologies. Fast and flexible tools are therefore required to ask complex questions of these data in an efficient manner. Results: This article introduces a new software suite for the comparison, manipulation and annotation of genomic features in Browser Extensible Data (BED) and General Feature Format (GFF) format. BEDTools also supports the comparison of sequence alignments in BAM format to both BED and GFF features. The tools are extremely efficient and allow the user to compare large datasets (e.g. next-generation sequencing data) with both public and custom genome annotation tracks. BEDTools can be combined with one another as well as with standard UNIX commands, thus facilitating routine genomics tasks as well as pipelines that can quickly answer intricate questions of large genomic datasets. Availability and implementation: BEDTools was written in C++. Source code and a comprehensive user manual are freely available at http://code.google.com/p/bedtools Contact: aaronquinlan@gmail.com; imh4y@virginia.edu Supplementary information: Supplementary data are available at Bioinformatics online.
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          Transcript assembly and abundance estimation from RNA-Seq reveals thousands of new transcripts and switching among isoforms

          High-throughput mRNA sequencing (RNA-Seq) holds the promise of simultaneous transcript discovery and abundance estimation 1-3 . We introduce an algorithm for transcript assembly coupled with a statistical model for RNA-Seq experiments that produces estimates of abundances. Our algorithms are implemented in an open source software program called Cufflinks. To test Cufflinks, we sequenced and analyzed more than 430 million paired 75bp RNA-Seq reads from a mouse myoblast cell line representing a differentiation time series. We detected 13,692 known transcripts and 3,724 previously unannotated ones, 62% of which are supported by independent expression data or by homologous genes in other species. Analysis of transcript expression over the time series revealed complete switches in the dominant transcription start site (TSS) or splice-isoform in 330 genes, along with more subtle shifts in a further 1,304 genes. These dynamics suggest substantial regulatory flexibility and complexity in this well-studied model of muscle development.
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            Author and article information

            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
            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
            25740935
            4426361
            GGG_015966
            10.1534/g3.114.015966
            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.

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