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

Louis, Véronique Leh ; Despons, Laurence ; Friedrich, Anne ; Martin, Tiphaine ; Durrens, Pascal ; Casarégola, Serge ; Neuvéglise, Cécile ; Fairhead, Cécile ; Marck, Christian and Cruz, José A. , et al. (2012) In G3: Genes, Genomes, Genetics 2(2). p.299-311
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) andmay 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... (More)

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) andmay 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 amosaic 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.

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publication status
published
keywords
Allopolyploidy, Genome evolution, Hybridization, Loss of heterozygosity, Osmotolerant Yeast P. sorbitophila
in
G3: Genes, Genomes, Genetics
volume
2
issue
2
pages
13 pages
publisher
Genetics Society of America
external identifiers
  • scopus:84860499250
ISSN
2160-1836
DOI
10.1534/g3.111.000745
language
English
LU publication?
no
id
0271d6f1-7fba-4c10-b118-dff31fa7d641
date added to LUP
2018-10-09 09:55:27
date last changed
2019-11-25 09:23:47
@article{0271d6f1-7fba-4c10-b118-dff31fa7d641,
  abstract     = {<p>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) andmay 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 amosaic 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.</p>},
  author       = {Louis, Véronique Leh and Despons, Laurence and Friedrich, Anne and Martin, Tiphaine and Durrens, Pascal and Casarégola, Serge and Neuvéglise, Cécile and Fairhead, Cécile and Marck, Christian and Cruz, José A. and Straub, Marie Laure and Kugler, Valérie and Sacerdot, Christine and Uzunov, Zlatyo and Thierry, Agnes and Weiss, Stéphanie and Bleykasten, Claudine and Montigny, Jacky De and Jacques, Noemie and Jung, Paul and Lemaire, Marc and Mallet, Sandrine and Morel, Guillaume and Richard, Guy Franck and Sarkar, Anasua and Savel, Guilhem and Schacherer, Joseph and Seret, Marie Line and Talla, Emmanuel and Samson, Gaelle and Jubin, Claire and Poulain, Julie and Vacherie, Benoît and Barbe, Valérie and Pelletier, Eric and Sherman, David J. and Westhof, Eric and Weissenbach, Jean and Baret, Philippe V. and Wincker, Patrick and Gaillardin, Claude and Dujon, Bernard and Souciet, Jean Luc},
  issn         = {2160-1836},
  language     = {eng},
  month        = {02},
  number       = {2},
  pages        = {299--311},
  publisher    = {Genetics Society of America},
  series       = {G3: Genes, Genomes, Genetics},
  title        = {Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization},
  url          = {http://dx.doi.org/10.1534/g3.111.000745},
  doi          = {10.1534/g3.111.000745},
  volume       = {2},
  year         = {2012},
}