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      The Genome of Nectria haematococca: Contribution of Supernumerary Chromosomes to Gene Expansion

      research-article
      1 , 2 , 3 , 1 , 4 , 5 , 1 , 6 , 7 , 6 , 7 , 8 , 1 , 9 , 9 , 10 , 11 , 12 , 13 , 12 , 12 , 14 , 15 , 1 , 1 , 16 , 17 , 1 , 18 , 19 , 20 , 1 , 21 , 22 , 5 , 5 , 5 , 5 , 9 , 5 , 23 , 24 , 1 , 25 , 1 , *
      PLoS Genetics
      Public Library of Science

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          Abstract

          The ascomycetous fungus Nectria haematococca, (asexual name Fusarium solani), is a member of a group of >50 species known as the “ Fusarium solani species complex”. Members of this complex have diverse biological properties including the ability to cause disease on >100 genera of plants and opportunistic infections in humans. The current research analyzed the most extensively studied member of this complex, N. haematococca mating population VI (MPVI). Several genes controlling the ability of individual isolates of this species to colonize specific habitats are located on supernumerary chromosomes. Optical mapping revealed that the sequenced isolate has 17 chromosomes ranging from 530 kb to 6.52 Mb and that the physical size of the genome, 54.43 Mb, and the number of predicted genes, 15,707, are among the largest reported for ascomycetes. Two classes of genes have contributed to gene expansion: specific genes that are not found in other fungi including its closest sequenced relative, Fusarium graminearum; and genes that commonly occur as single copies in other fungi but are present as multiple copies in N. haematococca MPVI. Some of these additional genes appear to have resulted from gene duplication events, while others may have been acquired through horizontal gene transfer. The supernumerary nature of three chromosomes, 14, 15, and 17, was confirmed by their absence in pulsed field gel electrophoresis experiments of some isolates and by demonstrating that these isolates lacked chromosome-specific sequences found on the ends of these chromosomes. These supernumerary chromosomes contain more repeat sequences, are enriched in unique and duplicated genes, and have a lower G+C content in comparison to the other chromosomes. Although the origin(s) of the extra genes and the supernumerary chromosomes is not known, the gene expansion and its large genome size are consistent with this species' diverse range of habitats. Furthermore, the presence of unique genes on supernumerary chromosomes might account for individual isolates having different environmental niches.

          Author Summary

          Nectria haematococca MPVI occurs as a saprophyte in diverse habitats and as a plant and animal pathogen. It also was the first fungus shown to contain supernumerary chromosomes with unique habitat-defining genes. The current study reveals that it has one of the largest fungal genomes (15,707 genes), which may be related to its habitat diversity, and describes two additional supernumerary chromosomes. Two classes of genes were identified that have contributed to gene expansion: 1) specific genes that are not found in other fungi, and 2) genes that are present as multiple copies in N. haematococca but commonly occur as a single copy in other fungi. Some of these genes have properties suggesting their acquisition by horizontal gene transfer. We show that the three supernumerary chromosomes are different from the normal chromosomes; they contain more repeat sequences, are particularly enriched in unique and duplicated genes, and have a lower G+C content. Additionally, the biochemical functions of genes on these chromosomes suggest they may be involved in niche adaptation. The dispensable nature and possession of habitat-determining genes by these chromosomes make them the biological equivalent of bacterial plasmids. We believe they contribute to microbial diversity and have been overlooked in models of fungal evolution.

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          Gene Ontology: tool for the unification of biology

          Genomic sequencing has made it clear that a large fraction of the genes specifying the core biological functions are shared by all eukaryotes. Knowledge of the biological role of such shared proteins in one organism can often be transferred to other organisms. The goal of the Gene Ontology Consortium is to produce a dynamic, controlled vocabulary that can be applied to all eukaryotes even as knowledge of gene and protein roles in cells is accumulating and changing. To this end, three independent ontologies accessible on the World-Wide Web (http://www.geneontology.org) are being constructed: biological process, molecular function and cellular component.
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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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              Orthologs, paralogs, and evolutionary genomics.

              Orthologs and paralogs are two fundamentally different types of homologous genes that evolved, respectively, by vertical descent from a single ancestral gene and by duplication. Orthology and paralogy are key concepts of evolutionary genomics. A clear distinction between orthologs and paralogs is critical for the construction of a robust evolutionary classification of genes and reliable functional annotation of newly sequenced genomes. Genome comparisons show that orthologous relationships with genes from taxonomically distant species can be established for the majority of the genes from each sequenced genome. This review examines in depth the definitions and subtypes of orthologs and paralogs, outlines the principal methodological approaches employed for identification of orthology and paralogy, and considers evolutionary and functional implications of these concepts.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                August 2009
                August 2009
                28 August 2009
                : 5
                : 8
                : e1000618
                Affiliations
                [1 ]Department of Plant Sciences, University of Arizona, Tucson, Arizona, United States of America
                [2 ]Massachusetts General Hospital, Boston, Massachusetts, United States of America
                [3 ]BIO5 Institute and Department of Plant Sciences, University of Arizona, Tucson, Arizona, United States of America
                [4 ]Department of Biology, Duke University, Durham, North Carolina, United States of America
                [5 ]United States Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America
                [6 ]Joint Genome Institute—Stanford Human Genome Center, Palo Alto, California, United States of America
                [7 ]Hudson Alpha Genome Sequencing Center, Hudson Alpha Institute for Biotechnology, Huntsville, Alabama, United States of America
                [8 ]Department of Biology, Okayama University, Okayama, Japan
                [9 ]Laboratory for Molecule and Computational Genomics, University of Wisconsin, Madison, Wisconsin, United States of America
                [10 ]Department of Biochemistry and Biophysics and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America
                [11 ]The Broad Institute, Cambridge, Massachusetts, United States of America
                [12 ]Architecture et Fonction des Macromolécules Biologiques, CNRS, Universités Aix-Marseille I & II, Marseille, France
                [13 ]Institut National de la Recherche Agronomique, Centre de recherche de Sophia-Antipolis, Sophia-Antipolis, France
                [14 ]Department of Molecular Sciences, University of Tennessee, Memphis, Tennessee, United States of America
                [15 ]Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland, United States of America
                [16 ]Department of Biological Sciences, Purdue University, West Lafayette, Indiana, United States of America
                [17 ]Plant Pathology, University of Amsterdam, Amsterdam, The Netherlands
                [18 ]South West Center for Natural Products Research and Commercialization, Office of Arid Lands Studies, University of Arizona, Tucson, Arizona, United States of America
                [19 ]Department of Soil, Water, and Environmental Science, University of Arizona, Tucson, Arizona, United States of America
                [20 ]Department of Biology, Saint Louis University, St. Louis, Missouri, United States of America
                [21 ]Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, United States of America
                [22 ]Institute of Molecular Biology, University of Oregon, Eugene, Oregon, United States of America
                [23 ]Fusarium Research Center, Department of Plant Pathology, The Pennsylvania State University, University Park, Pennsylvania, United States of America
                [24 ]Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia, United States of America
                [25 ]Vilmorin Inc., Tucson, Arizona, United States of America
                University of California San Francisco, United States of America
                Author notes

                Conceived and designed the experiments: CCW DMG SFC ET HDV. Performed the experiments: JJC SDR MRC JS MT GJW SZ MF LjM EGJD DRN DS BMB MR JZ MLF AS HS JP EL CL. Analyzed the data: JJC SDR MRC AK CCW JG MT GJW SZ DCS MF LjM EGJD BH PMC DRN DS CAN BMB MG MR SK IM CR JCK JZ MLF EUS EL IVG SFC. Contributed reagents/materials/analysis tools: PMC. Wrote the paper: JJC MRC CCW GJW HDV.

                Article
                09-PLGE-RA-0658R2
                10.1371/journal.pgen.1000618
                2725324
                19714214
                776d06bd-10f1-4c46-b65b-6733b1fa7d71
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                History
                : 20 April 2009
                : 27 July 2009
                Page count
                Pages: 14
                Categories
                Research Article
                Genetics and Genomics
                Genetics and Genomics/Genomics
                Genetics and Genomics/Microbial Evolution and Genomics

                Genetics
                Genetics

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