Article

Nature 430, 35-44 (1 July 2004) | doi:10.1038/nature02579; Received 3 February 2004; Accepted 19 April 2004

Genome evolution in yeasts

Bernard Dujon1, David Sherman5,6, Gilles Fischer1, Pascal Durrens6,7, Serge Casaregola8, Ingrid Lafontaine1, Jacky de Montigny9, Christian Marck10, Cécile Neuvéglise8, Emmanuel Talla1, Nicolas Goffard6, Lionel Frangeul2, Michel Aigle7, Véronique Anthouard11, Anna Babour8, Valérie Barbe11, Stéphanie Barnay8, Sylvie Blanchin8, Jean-Marie Beckerich8, Emmanuelle Beyne5,6, Claudine Bleykasten9, Anita Boisramé8, Jeanne Boyer1, Laurence Cattolico11, Fabrice Confanioleri12, Antoine de Daruvar6, Laurence Despons9, Emmanuelle Fabre1, Cécile Fairhead1, Hélène Ferry-Dumazet6, Alexis Groppi6, Florence Hantraye3, Christophe Hennequin1, Nicolas Jauniaux9, Philippe Joyet8, Rym Kachouri13, Alix Kerrest1, Romain Koszul1, Marc Lemaire14, Isabelle Lesur5, Laurence Ma2, Héloïse Muller1, Jean-Marc Nicaud8, Macha Nikolski5, Sophie Oztas11, Odile Ozier-Kalogeropoulos1, Stefan Pellenz1, Serge Potier9, Guy-Franck Richard1, Marie-Laure Straub9, Audrey Suleau8, Dominique Swennen8, Fredj Tekaia1, Micheline Wésolowski-Louvel14, Eric Westhof13, Bénédicte Wirth9, Maria Zeniou-Meyer9, Ivan Zivanovic12, Monique Bolotin-Fukuhara12, Agnès Thierry1, Christiane Bouchier2, Bernard Caudron4, Claude Scarpelli11, Claude Gaillardin8, Jean Weissenbach11, Patrick Wincker11 & Jean-Luc Souciet9

  1. Unité de Génétique Moléculaire des Levures (URA 2171 CNRS and UFR 927 Université Pierre et Marie Curie),
  2. Plate-forme génomique, Pasteur Génopole Ile-de-France,
  3. Unité de Génétique des interactions macromoléculaires (URA 2171 CNRS), Institut Pasteur, 25 rue du Docteur Roux, 75724 Paris Cedex 15, France
  4. Groupe Logiciels et Banques de données, Institut Pasteur, 25 rue du Docteur Roux, 75724 Paris Cedex 15, France
  5. Laboratoire Bordelais de Recherche en Informatique (LaBRI, UMR 5800 CNRS), 351 cours de la Libération, 33405 Talence Cedex, France
  6. Centre de Bioinformatique de Bordeaux, Université Victor Ségalen (Bordeaux 2), 146 rue Léo Saignat, 33076 Bordeaux Cedex, France
  7. Institut de Biochimie et Génétique Cellulaires (UMR 5095 CNRS), Université Victor Ségalen (Bordeaux 2), 1 rue Camille Saint-Säens, 33077 Bordeaux Cedex, France
  8. Collection de Levures d'Intérêt Biotechnologique et Laboratoire de Génétique Moléculaire et Cellulaire (UMR 216 INRA and URA 1925 CNRS), INA-PG, PO Box 01, 78850 Thiverval-Grignon, France
  9. Laboratoire de Dynamique, Evolution et Expression des Génomes de Microorganismes (FRE 2326 CNRS), Université Louis Pasteur, 28 rue Goethe, 67000 Strasbourg, France
  10. Service de Biochimie et de Génétique Moléculaire, CEA/Saclay, 91191 Gif-sur Yvette, France
  11. Génoscope (UMR 8030 CNRS), 2 rue Gaston Crémieux, 91057 Evry Cedex, France
  12. Institut de Génétique Moléculaire (UMR 8621 CNRS), Université de Paris Sud, Bâtiment 400, 91405 Orsay Cedex, France
  13. Modélisations et Simulations des Acides Nucléiques, IBMC (UPR 9002 CNRS), 15 rue René Descartes, 67000 Strasbourg, France
  14. Laboratoire de Génétique des Levures (UMR 5122 CNRS), Université Claude Bernard, Bâtiment Lwoff, 43 Boulevard du 11 novembre 1918, 69622 Villeurbanne Cedex, France

Correspondence to: Bernard Dujon1Jean-Luc Souciet9 Email: souciet@gem.u-strasbg.fr
Email: bdujon@pasteur.fr
Sequences have been deposited in EMBL under accession numbers CR380947–CR380959 for C. glabrata, CR382121–CR382126 for K. lactis, CR382127–CR382132 for Y. lipolytica and CR382133–CR382139 for D. hansenii.

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Identifying the mechanisms of eukaryotic genome evolution by comparative genomics is often complicated by the multiplicity of events that have taken place throughout the history of individual lineages, leaving only distorted and superimposed traces in the genome of each living organism. The hemiascomycete yeasts, with their compact genomes, similar lifestyle and distinct sexual and physiological properties, provide a unique opportunity to explore such mechanisms. We present here the complete, assembled genome sequences of four yeast species, selected to represent a broad evolutionary range within a single eukaryotic phylum, that after analysis proved to be molecularly as diverse as the entire phylum of chordates. A total of approximately 24,200 novel genes were identified, the translation products of which were classified together with Saccharomyces cerevisiae proteins into about 4,700 families, forming the basis for interspecific comparisons. Analysis of chromosome maps and genome redundancies reveal that the different yeast lineages have evolved through a marked interplay between several distinct molecular mechanisms, including tandem gene repeat formation, segmental duplication, a massive genome duplication and extensive gene loss.