Article

Nature 444, 171-178 (9 November 2006) | doi:10.1038/nature05230; Received 4 May 2006; Accepted 31 August 2006; Published online 1 November 2006

Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia

Jean-Marc Aury1,9, Olivier Jaillon1,9, Laurent Duret2, Benjamin Noel1, Claire Jubin1, Betina M. Porcel1, Béatrice Ségurens1, Vincent Daubin2, Véronique Anthouard1, Nathalie Aiach1, Olivier Arnaiz3, Alain Billaut1, Janine Beisson3, Isabelle Blanc3, Khaled Bouhouche4, Francisco Câmara5, Sandra Duharcourt4, Roderic Guigo5, Delphine Gogendeau3, Michael Katinka1, Anne-Marie Keller3, Roland Kissmehl6, Catherine Klotz3, France Koll3, Anne Le Mouël4, Gersende Lepère4, Sophie Malinsky4, Mariusz Nowacki4, Jacek K. Nowak7, Helmut Plattner6, Julie Poulain1, Françoise Ruiz3, Vincent Serrano4, Marek Zagulski7, Philippe Dessen8, Mireille Bétermier3,4, Jean Weissenbach1, Claude Scarpelli1, Vincent Schächter1, Linda Sperling3, Eric Meyer4, Jean Cohen3 & Patrick Wincker1

  1. Genoscope and CNRS UMR 8030, 2 rue Gaston Crémieux CP5706, 91057 Evry, France
  2. Laboratoire de Biométrie et Biologie Évolutive CNRS UMR 5558, Université Lyon 1, Villeurbanne, France
  3. Centre de Génétique Moléculaire, CNRS, 91198 Gif-sur-Yvette Cedex, France
  4. Laboratoire de Génétique Moléculaire, CNRS UMR 8541, École Normale Supérieure, 46 rue d'Ulm, 75005 Paris, France
  5. Center for Genomic Regulation, Institut Municipal d'Investigacio Mèdica, Universitat Pompeu Fabra, Pg. Maritim de la Barceloneta 37-49, Barcelone, Catalonia, Spain
  6. Department of Biology, University of Konstanz, PO Box 5560, 78457 Konstanz, Germany
  7. Institute of Biochemistry and Biophysics, DNA Sequencing Laboratory, Polish Academy of Sciences, Pawinskiego 5a, 02-106 Warsaw, Poland
  8. Laboratoire Génomes et Cancers, FRE 2939 CNRS, Institut Gustave Roussy, 94805 Villejuif Cedex, France
  9. These authors contributed equally to this work.

Correspondence to: Patrick Wincker1 Correspondence and requests for materials should be addressed to P.W. (Email: pwincker@genoscope.cns.fr).

The final assembly and annotation are deposited in the EMBL/Genbank/DDBJ databases under accession numbers CT867985–CT868681. An annotation browser and further information on the project are available from http://www.genoscope.cns.fr/paramecium and http://paramecium.cgm.cnrs-gif.fr.

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The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints.

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