Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization

Author:

Louis Véronique Leh11,Despons Laurence1,Friedrich Anne1,Martin Tiphaine2,Durrens Pascal2,Casarégola Serge3,Neuvéglise Cécile3,Fairhead Cécile4,Marck Christian5,Cruz José A6,Straub Marie-Laure1,Kugler Valérie1,Sacerdot Christine7,Uzunov Zlatyo8,Thierry Agnes7,Weiss Stéphanie3,Bleykasten Claudine1,De Montigny Jacky1,Jacques Noemie3,Jung Paul1,Lemaire Marc9,Mallet Sandrine3,Morel Guillaume3,Richard Guy-Franck7,Sarkar Anasua10,Savel Guilhem10,Schacherer Joseph1,Seret Marie-Line11,Talla Emmanuel12,Samson Gaelle13,Jubin Claire13,Poulain Julie13,Vacherie Benoît13,Barbe Valérie13,Pelletier Eric13,Sherman David J2,Westhof Eric6,Weissenbach Jean13,Baret Philippe V11,Wincker Patrick13,Gaillardin Claude3,Dujon Bernard7,Souciet Jean-Luc11

Affiliation:

1. Université de Strasbourg, CNRS UMR7156, F-67000 Strasbourg, France

2. Université de Bordeaux 1, LaBRI INRIA Bordeaux Sud-Ouest (MAGNOME), F-33405 Talence, France

3. INRA UMR 1319 Micalis, AgroParisTech, Bat. CBAI, F-78850 Thiverval-Grignon, France

4. Institut de Génétique et Microbiologie, Université Paris-Sud, UMR CNRS 8621, F-91405 Orsay CEDEX, France

5. Institut de Biologie et de Technologies de Saclay (iBiTec-S), CEA, F-91191 Gif-sur-Yvette CEDEX, France

6. Université de Strasbourg, Architecture et Réactivité de l’ARN, Institut de Biologie Moléculaire et Cellulaire du CNRS, F-67084 Strasbourg, France

7. Institut Pasteur, CNRS URA2171, Université Pierre et Maris Curie, Paris 6 UFR927, F-75724, Paris-CEDEX 15, France

8. Sofia University St. Kliment Ohridski, Faculty of Biology, Department of General and Applied Microbiology, 1164, Sofia, Bulgaria

9. Université de Lyon, F-69622, Lyon, France; Université Lyon 1, Villeurbanne; CNRS, UMR5240 Microbiologie, Adaptation et Pathogénie; INSA de Lyon, F-69621, Villeurbanne, France

10. Université de Bordeaux 1, CNRS UMR5800, F-33405 Talence, France

11. Earth and Life Institute, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium

12. Université de la Méditerranée, Laboratoire de Chimie Bactérienne, CNRS-UPR9043, 31 chemin Joseph Aiguier, F-13402 Marseille CEDEX 20, France

13. CEA, DSV, IG, Génoscope; CNRS UMR 8030; Université d’Evry Val d’ Essonne, 2 rue Gaston Crémieux, F-91057 Evry, France

Abstract

Abstract Polyploidization is an important process in the evolution of eukaryotic genomes, but ensuing molecular mechanisms remain to be clarified. Autopolyploidization or whole-genome duplication events frequently are resolved in resulting lineages by the loss of single genes from most duplicated pairs, causing transient gene dosage imbalance and accelerating speciation through meiotic infertility. Allopolyploidization or formation of interspecies hybrids raises the problem of genetic incompatibility (Bateson-Dobzhansky-Muller effect) and may be resolved by the accumulation of mutational changes in resulting lineages. In this article, we show that an osmotolerant yeast species, Pichia sorbitophila, recently isolated in a concentrated sorbitol solution in industry, illustrates this last situation. Its genome is a mosaic of homologous and homeologous chromosomes, or parts thereof, that corresponds to a recently formed hybrid in the process of evolution. The respective parental contributions to this genome were characterized using existing variations in GC content. The genomic changes that occurred during the short period since hybrid formation were identified (e.g., loss of heterozygosity, unilateral loss of rDNA, reciprocal exchange) and distinguished from those undergone by the two parental genomes after separation from their common ancestor (i.e., NUMT (NUclear sequences of MiTochondrial origin) insertions, gene acquisitions, gene location movements, reciprocal translocation). We found that the physiological characteristics of this new yeast species are determined by specific but unequal contributions of its two parents, one of which could be identified as very closely related to an extant Pichia farinosa strain.

Publisher

Oxford University Press (OUP)

Subject

Genetics(clinical),Genetics,Molecular Biology

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