Lessons from the Genome Sequence of Neurospora Crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism Katherine A
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MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS, Mar. 2004, p. 1–108 Vol. 68, No. 1 1092-2172/04/$08.00ϩ0 DOI: 10.1128/MMBR.68.1.1–108.2004 Copyright © 2004, American Society for Microbiology. All Rights Reserved. Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism Katherine A. Borkovich,1* Lisa A. Alex,2 Oded Yarden,3 Michael Freitag,4 Gloria E. Turner,5 Nick D. Read,6 Stephan Seiler,7 Deborah Bell-Pedersen,8 John Paietta,9 Nora Plesofsky,10 Michael Plamann,11 Marta Goodrich-Tanrikulu,12 Ulrich Schulte,13 Gertrud Mannhaupt,14 Frank E. Nargang,15 Alan Radford,16 Claude Selitrennikoff,17 James E. Galagan,18 Jay C. Dunlap,19 Jennifer J. Loros,20 David Catcheside,21 Hirokazu Inoue,22 Rodolfo Aramayo,8 Michael Polymenis,23 4 24 25 26 27 Eric U. Selker, Matthew S. Sachs, George A. Marzluf, Ian Paulsen, Rowland Davis, Downloaded from Daniel J. Ebbole,28 Alex Zelter,6 Eric R. Kalkman,6 Rebecca O’Rourke,29 Frederick Bowring,21 Jane Yeadon,21 Chizu Ishii,22 Keiichiro Suzuki,22 Wataru Sakai,22 and Robert Pratt8 Department of Plant Pathology, University of California, Riverside, California 925211; Department of Chemistry, California State Polytechnic University, Pomona, California 917682; Department of Plant Pathology and Microbiology, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, Rehovot 76100, Israel3; Institute of Molecular Biology, University of Oregon, Eugene, Oregon 974034; Department of Chemistry and Biochemistry, University of California, Los Angeles, California 900955; Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JH,6 and School of Biology, Leeds University, Leeds LS2 9JT,16 United Kingdom; Department of Molecular Microbiology & Genetics, Institute of Microbiology 7 13 & Genetics, Georg-August-University, D-37077 Goettingen, Institute of Biochemistry, Heinrich Heine University, 40225 Dusseldorf, http://mmbr.asm.org/ and Department of Genome Oriented Bioinformatics, Technical University of Munich, 85350 Freising-Weihenstephan,14 Germany; Department of Biology,8 Department of Biochemistry and Biophysics,23 and Department of Plant Pathology and Microbiology,28 Texas A&M University, College Station, Texas 77843; Department of Biochemistry and Molecular Biology, Wright State University, Dayton, Ohio 454359; Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 5510810; School of Biological Sciences, University of Missouri—Kansas City, Kansas City, Missouri 6411011; Bio-Rad Laboratories, Inc., Hercules, California 9454712; Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada15; Department of Cell and Developmental Biology17 and Department of Cellular and Structural Biology,29 University of Colorado Health Sciences Center, Denver, Colorado 80262; Whitehead Institute Center for Genome Research, Cambridge, Massachusetts 0214118; Department of Genetics19 and Department of Biochemistry,20 Dartmouth Medical School, Hanover, New Hampshire 03755; School of Biological Sciences, Flinders University, Adelaide 5001, Australia21; Laboratory of Genetics, Department of Regulation Biology, Saitama 22 University, Saitama City, Saitama 338-8570, Japan ; Department of Environmental and Biomolecular Systems, School of Science on September 12, 2018 by guest and Engineering, Oregon Health and Science University, Beaverton, Oregon 9700624; Department of Biochemistry, Ohio State University, Columbus, Ohio 4321025; The Institute for Genomic Research, Rockville, Maryland 2087826; and Department of Molecular Biology and Biochemistry, University of California, Irvine, California 9269727 INTRODUCTION ...........................................................................................................................................................3 Neurospora crassa: a Model Filamentous Fungus...................................................................................................3 Basic Features of the Neurospora Genome ..............................................................................................................6 Sequencing and assembly ......................................................................................................................................6 Integration of the sequence with the genetic map .............................................................................................7 Nuclear and mitochondrial genes.........................................................................................................................7 Codon bias ...............................................................................................................................................................8 Comparative multigene family and domain analysis.........................................................................................8 CHROMATIN ASSEMBLY AND GENE REGULATION.........................................................................................8 Centromere Organization and Kinetochore Complexes........................................................................................8 Organization of centromeres.................................................................................................................................9 Kinetochore complexes and motors that move chromosomes........................................................................10 Chromosomes move through checkpoints .........................................................................................................10 Chromatin Structure and Gene Regulation..........................................................................................................11 Nucleosome assembly and histone modification (i) Nucleosome assembly and nucleosome spacing......................................................................................11 (ii) Histone modifications................................................................................................................................12 Chromatin assembly and remodeling ................................................................................................................14 (i) CAFs..............................................................................................................................................................14 (ii) CRFs ............................................................................................................................................................15 Transcription Factors...............................................................................................................................................16 Zn(II)2Cys6 fungal binuclear cluster family .....................................................................................................17 * Corresponding author. Mailing address: Department of Plant Pa- thology, 2338 Webber Hall, 900 University Ave., University of Cali- fornia, Riverside, CA 92521. Phone: (909) 787-2753. Fax: (909) 787- 4294. E-mail: [email protected]. 1 2 BORKOVICH ET AL. MICROBIOL.MOL.BIOL.REV. C2H2 zinc fingers..................................................................................................................................................17 GATA factors.........................................................................................................................................................19 bHLH transcription factors.................................................................................................................................21 B-ZIP transcription factors.................................................................................................................................21 Miscellaneous factors...........................................................................................................................................22 Translation Factors ..................................................................................................................................................22 GENOME DEFENSE, DNA REPAIR, AND RECOMBINATION.........................................................................23 Genome Defense Mechanisms.................................................................................................................................23 Heterochromatin silencing and DNA methylation...........................................................................................23 RIP..........................................................................................................................................................................26 RNA-dependent silencing.....................................................................................................................................26 DNA Repair ...............................................................................................................................................................27 Photoreactivation ..................................................................................................................................................27 Downloaded from Excision ..................................................................................................................................................................27 (i) NER...............................................................................................................................................................27