The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions

Sabeeha S. Merchant,^1* Simon E. Prochnik,^2* Olivier Vallon,³ Elizabeth H. Harris,⁴ Steven J. Karpowicz,¹ George B. Witman,⁵ Astrid Terry,² Asaf Salamov,² Lillian K. Fritz-Laylin,⁶ Laurence Maréchal-Drouard,⁷ Wallace F. Marshall,⁸ Liang-Hu Qu,⁹ David R. Nelson,¹⁰ Anton A. Sanderfoot,¹¹ Martin H. Spalding,¹² Vladimir V. Kapitonov,¹³ Qinghu Ren,¹⁴ Patrick Ferris,¹⁵ Erika Lindquist,² Harris Shapiro,² Susan M. Lucas,² Jane Grimwood,¹⁶ Jeremy Schmutz,¹⁶ Pierre Cardol,^3,17 Heriberto Cerutti,¹⁸ Guillaume Chanfreau,¹ Chun-Long Chen,⁹ Valérie Cognat,⁷ Martin T. Croft,¹⁹ Rachel Dent,²⁰ Susan Dutcher,²¹ Emilio Fernández,²² Hideya Fukuzawa,²³ David González-Ballester,²⁴ Diego González-Halphen,²⁵ Armin Hallmann,²⁶ Marc Hanikenne,¹⁷ Michael Hippler,²⁷ William Inwood,²⁰ Kamel Jabbari,²⁸ Ming Kalanon,²⁹ Richard Kuras,³ Paul A. Lefebvre,¹¹ Stéphane D. Lemaire,³⁰ Alexey V. Lobanov,³¹ Martin Lohr,³² Andrea Manuell,³³ Iris Meier,³⁴ Laurens Mets,³⁵ Maria Mittag,³⁶ Telsa Mittelmeier,³⁷ James V. Moroney,³⁸ Jeffrey Moseley,²⁴ Carolyn Napoli,³⁹ Aurora M. Nedelcu,⁴⁰ Krishna Niyogi,²⁰ Sergey V. Novoselov,³¹ Ian T. Paulsen,¹⁴ Greg Pazour,⁴¹ Saul Purton,⁴² Jean-Philippe Ral,⁴³ Diego Mauricio Riaño-Pachón,⁴⁴ Wayne Riekhof,⁴⁵ Linda Rymarquis,⁴⁶ Michael Schroda,⁴⁷ David Stern,⁴⁸ James Umen,¹⁵ Robert Willows,⁴⁹ Nedra Wilson,⁵⁰ Sara Lana Zimmer,⁴⁸ Jens Allmer,⁵¹ Janneke Balk,¹⁹ Katerina Bisova,⁵² Chong-Jian Chen,⁹ Marek Elias,⁵³ Karla Gendler,³⁹ Charles Hauser,⁵⁴ Mary Rose Lamb,⁵⁵ Heidi Ledford,²⁰ Joanne C. Long,¹ Jun Minagawa,⁵⁶ M. Dudley Page,¹ Junmin Pan,⁵⁷ Wirulda Pootakham,²⁴ Sanja Roje,⁵⁸ Annkatrin Rose,⁵⁹ Eric Stahlberg,³⁴ Aimee M. Terauchi,¹ Pinfen Yang,⁶⁰ Steven Ball,⁶¹ Chris Bowler,^28,62 Carol L. Dieckmann,³⁷ Vadim N. Gladyshev,³¹ Pamela Green,⁴⁶ Richard Jorgensen,³⁹ Stephen Mayfield,³³ Bernd Mueller-Roeber,⁴⁴ Sathish Rajamani,⁶³ Richard T. Sayre,³⁴ Peter Brokstein,² Inna Dubchak,² David Goodstein,² Leila Hornick,² Y. Wayne Huang,² Jinal Jhaveri,² Yigong Luo,² Diego Martínez,² Wing Chi Abby Ngau,² Bobby Otillar,² Alexander Poliakov,² Aaron Porter,² Lukasz Szajkowski,² Gregory Werner,² Kemin Zhou,² Igor V. Grigoriev,² Daniel S. Rokhsar,^2,6 Arthur R. Grossman²⁴

Chlamydomonas reinhardtii is a unicellular green alga whose lineage diverged from land plants over 1 billion years ago. It is a model system for studying chloroplast-based photosynthesis, as well as the structure, assembly, and function of eukaryotic flagella (cilia), which were inherited from the common ancestor of plants and animals, but lost in land plants. We sequenced the 120-megabase nuclear genome of Chlamydomonas and performed comparative phylogenomic analyses, identifying genes encoding uncharacterized proteins that are likely associated with the function and biogenesis of chloroplasts or eukaryotic flagella. Analyses of the Chlamydomonas genome advance our understanding of the ancestral eukaryotic cell, reveal previously unknown genes associated with photosynthetic and flagellar functions, and establish links between ciliopathy and the composition and function of flagella.

¹ Department of Chemistry and Biochemistry, University of California at Los Angeles, Los Angeles, CA 90095, USA.
² U.S. Department of Energy (DOE) Joint Genome Institute (JGI), Walnut Creek, CA 94598, USA.
³ CNRS, Université Paris 6, Institut de Biologie Physico-Chimique, 75005 Paris, France.
⁴ Department of Biology, Duke University, Durham, NC 27708, USA.
⁵ Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA 01655, USA.
⁶ Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, CA 94720, USA.
⁷ Institut de Biologie Moléculaire des Plantes, CNRS, 67084 Strasbourg Cedex, France.
⁸ Department of Biochemistry and Biophysics, University of California at San Francisco, San Francisco, CA 94143, USA.
⁹ Biotechnology Research Center, Zhongshan University, Guangzhou 510275, China.
¹⁰ Department of Molecular Sciences and Center of Excellence in Genomics and Bioinformatics, University of Tennessee, Memphis, TN 38163, USA.
¹¹ Department of Plant Biology, University of Minnesota, St. Paul, MN 55108, USA.
¹² Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IA 50011, USA.
¹³ Genetic Information Research Institute, Mountain View, CA 94043, USA.
¹⁴ The Institute for Genomic Research, Rockville, MD 20850, USA.
¹⁵ Plant Biology Laboratory, Salk Institute, La Jolla, CA 92037, USA.
¹⁶ Stanford Human Genome Center, Stanford University School of Medicine, Palo Alto, CA 94304, USA.
¹⁷ Plant Biology Institute, Department of Life Sciences, University of Liège, B-4000 Liège, Belgium.
¹⁸ University of Nebraska-Lincoln, School of Biological Sciences–Plant Science Initiative, Lincoln, NE 68588, USA.
¹⁹ Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK.
²⁰ Department of Plant and Microbial Biology, University of California at Berkeley, Berkeley, CA 94720, USA.
²¹ Department of Genetics, Washington University School of Medicine, St. Louis, MO 63110, USA.
²² Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Córdoba, Campus de Rabanales, 14071 Córdoba, Spain.
²³ Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan.
²⁴ Department of Plant Biology, Carnegie Institution, Stanford, CA 94306, USA.
²⁵ Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México 04510 DF, Mexico.
²⁶ Department of Cellular and Developmental Biology of Plants, University of Bielefeld, D-33615 Bielefeld, Germany.
²⁷ Department of Biology, Institute of Plant Biochemistry and Biotechnology, University of Münster, 48143 Münster, Germany.
²⁸ CNRS UMR 8186, Département de Biologie, Ecole Normale Supérieure, 75230 Paris, France.
²⁹ Plant Cell Biology Research Centre, The School of Botany, The University of Melbourne, Parkville, Melbourne, VIC 3010, Australia.
³⁰ Institut de Biotechnologie des Plantes, UMR 8618, CNRS/Université Paris-Sud, Orsay, France.
³¹ Department of Biochemistry, N151 Beadle Center, University of Nebraska, Lincoln, NE 68588–0664, USA.
³² Institut für Allgemeine Botanik, Johannes Gutenberg-Universität, 55099 Mainz, Germany.
³³ Department of Cell Biology and Skaggs Institute for Chemical Biology, Scripps Research Institute, La Jolla, CA 92037, USA.
³⁴ PCMB and Plant Biotechnology Center, Ohio State University, Columbus, OH 43210, USA.
³⁵ Molecular Genetics and Cell Biology, University of Chicago, Chicago, IL 60637, USA.
³⁶ Institut für Allgemeine Botanik und Pflanzenphysiologie, Friedrich-Schiller-Universität Jena, 07743 Jena, Germany.
³⁷ Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA.
³⁸ Department of Biological Science, Louisiana State University, Baton Rouge, LA 70803, USA.
³⁹ Department of Plant Sciences, University of Arizona, Tucson, AZ 85721, USA.
⁴⁰ Department of Biology, University of New Brunswick, Fredericton, NB, Canada E3B 6E1.
⁴¹ Department of Physiology, University of Massachusetts Medical School, Worcester, MA 01605, USA.
⁴² Department of Biology, University College London, London WC1E 6BT, UK.
⁴³ Unité de Glycobiologie Structurale et Fonctionnelle, UMR8576 CNRS/USTL, IFR 118, Université des Sciences et Technologies de Lille, Cedex, France.
⁴⁴ Universität Potsdam, Institut für Biochemie und Biologie, D-14476 Golm, Germany.
⁴⁵ Department of Medicine, National Jewish Medical and Research Center, Denver, CO 80206, USA.
⁴⁶ Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711, USA.
⁴⁷ Institute of Biology II/Plant Biochemistry, 79104 Freiburg, Germany.
⁴⁸ Boyce Thompson Institute for Plant Research at Cornell University, Ithaca, NY 14853, USA.
⁴⁹ Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney 2109, Australia.
⁵⁰ Department of Anatomy and Cell Biology, Oklahoma State University, Center for Health Sciences, Tulsa, OK 74107, USA.
⁵¹ Izmir Ekonomi Universitesi, 35330 Balcova-Izmir Turkey.
⁵² Institute of Microbiology, Czech Academy of Sciences, Czech Republic.
⁵³ Department of Plant Physiology, Faculty of Sciences, Charles University, 128 44 Prague 2, Czech Republic.
⁵⁴ Bioinformatics Program, St. Edward's University, Austin, TX 78704, USA.
⁵⁵ Department of Biology, University of Puget Sound, Tacoma, WA 98407, USA.
⁵⁶ Institute of Low-Temperature Science, Hokkaido University, 060-0819, Japan.
⁵⁷ Department of Biology, Tsinghua University, Beijing, China 100084.
⁵⁸ Institute of Biological Chemistry, Washington State University, Pullman, WA99164, USA.
⁵⁹ Appalachian State University, Boone, NC 28608, USA.
⁶⁰ Department of Biology, Marquette University, Milwaukee, WI 53233, USA.
⁶¹ UMR8576 CNRS, Laboratory of Biological Chemistry, 59655 Villeneuve d'Ascq, France.
⁶² Cell Signaling Laboratory, Stazione Zoologica, I 80121 Naples, Italy.
⁶³ Graduate Program in Biophysics, Ohio State University, Columbus, OH 43210, USA.

^* These authors contributed equally to this work.

To whom correspondence should be addressed. E-mail: dsrokhsar{at}lbl.gov (D.S.R.); arthurg{at}stanford.edu (A.R.G.)

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