title: Differential gene retention as an evolutionary mechanism to generate biodiversity and adaptation in yeasts.
abstract: The evolutionary history of the characters underlying the adaptation of microorganisms to food and biotechnological uses is poorly understood. We undertook comparative genomics to investigate evolutionary relationships of the dairy yeast Geotrichum candidum within Saccharomycotina. Surprisingly, a remarkable proportion of genes showed discordant phylogenies, clustering with the filamentous fungus subphylum (Pezizomycotina), rather than the yeast subphylum (Saccharomycotina), of the Ascomycota. These genes appear not to be the result of Horizontal Gene Transfer (HGT), but to have been specifically retained by G. candidum after the filamentous fungi-yeasts split concomitant with the yeasts' genome contraction. We refer to these genes as SRAGs (Specifically Retained Ancestral Genes), having been lost by all or nearly all other yeasts, and thus contributing to the phenotypic specificity of lineages. SRAG functions include lipases consistent with a role in cheese making and novel endoglucanases associated with degradation of plant material. Similar gene retention was observed in three other distantly related yeasts representative of this ecologically diverse subphylum. The phenomenon thus appears to be widespread in the Saccharomycotina and argues that, alongside neo-functionalization following gene duplication and HGT, specific gene retention must be recognized as an important mechanism for generation of biodiversity and adaptation in yeasts.
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Guillaume
authors.initials: G
authors.lastname: Morel
authors.affiliation: 1] Department of Plant Systems Biology VIB, Technologiepark 927, 9052 Gent, Belgium [2] Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, 9052 Gent, Belgium.
authors.forename: Lieven
authors.initials: L
authors.lastname: Sterck
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Dominique
authors.initials: D
authors.lastname: Swennen
authors.affiliation: 1] Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Dr. Aiguader 88, Barcelona 08003, Spain [2] Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain.
authors.forename: Marina
authors.initials: M
authors.lastname: Marcet-Houben
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Djamila
authors.initials: D
authors.lastname: Onesime
authors.affiliation: INRA UMR1163, Biotechnologie des Champignons Filamenteux, Aix-Marseille Université, Polytech Marseille, 163 avenue de Luminy, CP 925, 13288 Marseille Cedex 09, France.
authors.forename: Anthony
authors.initials: A
authors.lastname: Levasseur
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Noémie
authors.initials: N
authors.lastname: Jacques
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Sandrine
authors.initials: S
authors.lastname: Mallet
authors.affiliation: CEA, Institut de Génomique, Genoscope, 2 Rue Gaston Crémieux, Évry F-91000, France.
authors.forename: Arnaux
authors.initials: A
authors.lastname: Couloux
authors.affiliation: CEA, Institut de Génomique, Genoscope, 2 Rue Gaston Crémieux, Évry F-91000, France.
authors.forename: Karine
authors.initials: K
authors.lastname: Labadie
authors.affiliation: INRA UR1164, Unité de Recherche Génomique - Info, 78000 Versailles, France.
authors.forename: Joëlle
authors.initials: J
authors.lastname: Amselem
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Jean-Marie
authors.initials: JM
authors.lastname: Beckerich
authors.affiliation: CNRS, UMR 7257, Aix-Marseille Université, 13288 Marseille, France.
authors.forename: Bernard
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: 1] Department of Plant Systems Biology VIB, Technologiepark 927, 9052 Gent, Belgium [2] Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, 9052 Gent, Belgium [3] Genomics Research Institute, University of Pretoria, Hatfield Campus, Pretoria 0028, South Africa.
authors.forename: Yves
authors.initials: Y
authors.lastname: Van de Peer
authors.affiliation: 1] CEA, Institut de Génomique, Genoscope, 2 Rue Gaston Crémieux, Évry F-91000, France [2] CNRS UMR 8030, 2 Rue Gaston Crémieux, Évry, 91000, France [3] Université d'Evry, Bd François Mitterand, Evry,91025, France.
authors.forename: Patrick
authors.initials: P
authors.lastname: Wincker
authors.affiliation: Université de Strasbourg, CNRS UMR7156, Strasbourg, 67000, France.
authors.forename: Jean-Luc
authors.initials: JL
authors.lastname: Souciet
authors.affiliation: 1] Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Dr. Aiguader 88, Barcelona 08003, Spain [2] Universitat Pompeu Fabra (UPF), Barcelona 08003, Spain.
authors.forename: Toni
authors.initials: T
authors.lastname: Gabaldón
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Colin R
authors.initials: CR
authors.lastname: Tinsley
authors.affiliation: 1] INRA UMR1319, Micalis Institute, CIRM-Levures, 78850 F-Thiverval-Grignon, France [2] AgroParisTech UMR1319, Micalis Institute, 78850 F-Thiverval-Grignon, France.
authors.forename: Serge
authors.initials: S
authors.lastname: Casaregola
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D044822:Biodiversity; D004271:DNA, Fungal / Q000737:chemistry / Q000235:genetics; D019143:Evolution, Molecular; D005656:Fungal Proteins / Q000235:genetics; D022761:Gene Transfer, Horizontal; D005800:Genes, Fungal / Q000235:genetics*; D014644:Genetic Variation; D016681:Genome, Fungal / Q000235:genetics; D054629:Genome, Mitochondrial / Q000235:genetics; D005848:Geotrichum / Q000235:genetics* / Q000254:growth & development; D008969:Molecular Sequence Data; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D013045:Species Specificity; D015003:Yeasts / Q000145:classification / Q000235:genetics* / Q000254:growth & development
chemical_list: D004271:DNA, Fungal; D005656:Fungal Proteins