Home LiteratureArticle Details
PMID: 22384408 Published · ppublish English Journal Article

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

G3 (Bethesda, Md.) ·Vol. 2 ·No. 2 ·2012-02-00 ·Pages 299-311

Louis VL, Despons L, Friedrich A, Martin T, Durrens P, Casarégola S, Neuvéglise C, Fairhead C, Marck C, Cruz JA, Straub ML, Kugler V, Sacerdot C, Uzunov Z, Thierry A, Weiss S, Bleykasten C, De Montigny J, Jacques N, Jung P, Lemaire M, Mallet S, Morel G, Richard GF, Sarkar A, Savel G, Schacherer J, Seret ML, Talla E, Samson G, Jubin C, Poulain J, Vacherie B, Barbe V, Pelletier E, Sherman DJ, Westhof E, Weissenbach J, Baret PV, Wincker P, Gaillardin C, Dujon B, Souciet JL

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.

Keywords
allopolyploidy genome evolution hybridization loss of heterozygosity osmotolerant yeast P. sorbitophila
Authors & Affiliations
43 authors, click to expand affiliations / ORCID
Louis Véronique Leh
Despons Laurence
Friedrich Anne
Martin Tiphaine
Durrens Pascal
Casarégola Serge
Neuvéglise Cécile
Fairhead Cécile
Marck Christian
Cruz José A
Straub Marie-Laure
Kugler Valérie
Sacerdot Christine
Uzunov Zlatyo
Thierry Agnes
Weiss Stéphanie
Bleykasten Claudine
De Montigny Jacky
Jacques Noemie
Jung Paul
Lemaire Marc
Mallet Sandrine
Morel Guillaume
Richard Guy-Franck
Sarkar Anasua
Savel Guilhem
Schacherer Joseph
Seret Marie-Line
Talla Emmanuel
Samson Gaelle
Jubin Claire
Poulain Julie
Vacherie Benoît
Barbe Valérie
Pelletier Eric
Sherman David J
Westhof Eric
Weissenbach Jean
Baret Philippe V
Wincker Patrick
Gaillardin Claude
Dujon Bernard
Souciet Jean-Luc
References (70)
70 references, click to expand
  1. Fungal sex and pathogenesis.
    Clin Microbiol Rev. 2010 Jan;23(1):140-59 PMID: 20065328
  2. Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex.
    Int J Food Microbiol. 2008 Feb 29;122(1-2):188-95 PMID: 18222562
  3. Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids.
    Plant Mol Biol. 2000 Jun;43(2-3):163-77 PMID: 10999402
  4. Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii.
    FEMS Yeast Res. 2006 Jun;6(4):599-607 PMID: 16696655
  5. Genome evolution in yeasts.
    Nature. 2004 Jul 1;430(6995):35-44 PMID: 15229592
  6. Comparative genomics of protoploid Saccharomycetaceae.
    Genome Res. 2009 Oct;19(10):1696-709 PMID: 19525356
  7. ARACHNE: a whole-genome shotgun assembler.
    Genome Res. 2002 Jan;12(1):177-89 PMID: 11779843
  8. The sporulation-specific enzymes encoded by the DIT1 and DIT2 genes catalyze a two-step reaction leading to a soluble LL-dityrosine-containing precursor of the yeast spore wall.
    Proc Natl Acad Sci U S A. 1994 May 10;91(10):4524-8 PMID: 8183942
  9. Characterization of a DL-dityrosine-containing macromolecule from yeast ascospore walls.
    J Biol Chem. 1990 Sep 5;265(25):15118-23 PMID: 2203769
  10. Identification, cloning and characterization of a derepressible Na+-coupled phosphate transporter in Saccharomyces cerevisiae.
    Mol Gen Genet. 1998 Jun;258(6):628-38 PMID: 9671031
  11. A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem.
    Nature. 1995 Aug 24;376(6542):690-5 PMID: 7651518
  12. Multiple alignment of DNA sequences with MAFFT.
    Methods Mol Biol. 2009;537:39-64 PMID: 19378139
  13. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.
    Syst Biol. 2007 Aug;56(4):564-77 PMID: 17654362
  14. Hybridization as an invasion of the genome.
    Trends Ecol Evol. 2005 May;20(5):229-37 PMID: 16701374
  15. Pichia sorbitophila sp nov.
    Antonie Van Leeuwenhoek. 1980;46(2):157-9 PMID: 7436402
  16. Genomic exploration of the hemiascomycetous yeasts: 15. Pichia sorbitophila.
    FEBS Lett. 2000 Dec 22;487(1):87-90 PMID: 11152890
  17. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation.
    Mol Microbiol. 1999 Feb;31(4):1087-104 PMID: 10096077
  18. Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis.
    Genome Res. 2001 Jul;11(7):1175-86 PMID: 11435399
  19. Hybrid fitness across time and habitats.
    Trends Ecol Evol. 2010 Sep;25(9):530-6 PMID: 20598770
  20. Interspecies hybridization and recombination in Saccharomyces wine yeasts.
    FEMS Yeast Res. 2008 Nov;8(7):996-1007 PMID: 18355270
  21. Characterization of a glycerol/H+ symport in the halotolerant yeast Pichia sorbitophila.
    Yeast. 1995 Feb;11(2):111-9 PMID: 7732721
  22. Mechanisms of salt tolerance conferred by overexpression of the HAL1 gene in Saccharomyces cerevisiae.
    Yeast. 1997 May;13(6):515-28 PMID: 9178503
  23. Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii.
    Appl Environ Microbiol. 2009 Apr;75(8):2534-44 PMID: 19251887
  24. Evidence for domesticated and wild populations of Saccharomyces cerevisiae.
    PLoS Genet. 2005 Jul;1(1):66-71 PMID: 16103919
  25. Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species.
    Microbiology (Reading). 1999 Sep;145 ( Pt 9):2577-2585 PMID: 10517611
  26. Cation/H+ antiporters mediate potassium and sodium fluxes in Pichia sorbitophila. Cloning of the PsNHA1 and PsNHA2 genes and expression in Saccharomyces cerevisiae.
    Yeast. 2002 Nov;19(15):1365-72 PMID: 12402245
  27. The complex and dynamic genomes of industrial yeasts.
    FEMS Microbiol Lett. 2009 Apr;293(1):1-10 PMID: 19175410
  28. Promiscuous DNA in the nuclear genomes of hemiascomycetous yeasts.
    FEMS Yeast Res. 2008 Sep;8(6):846-57 PMID: 18673395
  29. Yeast orthologues associated with glycerol transport and metabolism.
    FEMS Yeast Res. 2004 Oct;5(1):51-62 PMID: 15381122
  30. Mechanisms underlying the halotolerant way of Debaryomyces hansenii.
    FEMS Yeast Res. 2005 May;5(8):693-701 PMID: 15943004
  31. Genome sequence of the lager brewing yeast, an interspecies hybrid.
    DNA Res. 2009 Apr;16(2):115-29 PMID: 19261625
  32. Recent allopolyploid origin of Zygosaccharomyces rouxii strain ATCC 42981.
    Yeast. 2008 Jun;25(6):449-56 PMID: 18509846
  33. Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres.
    Mol Biol Evol. 2005 Apr;22(4):856-73 PMID: 15616141
  34. Yeasty clocks: dating genomic changes in yeasts.
    C R Biol. 2011 Aug-Sep;334(8-9):620-8 PMID: 21819943
  35. The evolution of sex: a perspective from the fungal kingdom.
    Microbiol Mol Biol Rev. 2010 Jun;74(2):298-340 PMID: 20508251
  36. Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans.
    Genome Res. 2009 Dec;19(12):2231-44 PMID: 19745113
  37. Codon--anticodon pairing: the wobble hypothesis.
    J Mol Biol. 1966 Aug;19(2):548-55 PMID: 5969078
  38. Demonstration of loss of heterozygosity by single-nucleotide polymorphism microarray analysis and alterations in strain morphology in Candida albicans strains during infection.
    Eukaryot Cell. 2005 Jan;4(1):156-65 PMID: 15643071
  39. Hybrid speciation in experimental populations of yeast.
    Science. 2002 Nov 29;298(5599):1773-5 PMID: 12459586
  40. A genome-wide analysis reveals no nuclear dobzhansky-muller pairs of determinants of speciation between S. cerevisiae and S. paradoxus, but suggests more complex incompatibilities.
    PLoS Genet. 2010 Jul 29;6(7):e1001038 PMID: 20686707
  41. Sequence diversity, reproductive isolation and species concepts in Saccharomyces.
    Genetics. 2006 Oct;174(2):839-50 PMID: 16951060
  42. Pure and mixed genetic lines of Saccharomyces bayanus and Saccharomyces pastorianus and their contribution to the lager brewing strain genome.
    Appl Environ Microbiol. 2006 Jun;72(6):3968-74 PMID: 16751504
  43. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
    Syst Biol. 2003 Oct;52(5):696-704 PMID: 14530136
  44. Uniparental loss of ribosomal DNA in the allotetraploid grass Zingeria trichopoda (2n = 8).
    Genome. 2003 Feb;46(1):156-63 PMID: 12669808
  45. Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis.
    Nat Biotechnol. 2007 Mar;25(3):319-26 PMID: 17334359
  46. Molecular analysis of maltotriose active transport and fermentation by Saccharomyces cerevisiae reveals a determinant role for the AGT1 permease.
    Appl Environ Microbiol. 2008 Mar;74(5):1494-501 PMID: 18203856
  47. The secreted form of invertase in Saccharomyces cerevisiae is synthesized from mRNA encoding a signal sequence.
    Mol Cell Biol. 1983 Mar;3(3):439-47 PMID: 6341817
  48. Evolution of pathogenicity and sexual reproduction in eight Candida genomes.
    Nature. 2009 Jun 4;459(7247):657-62 PMID: 19465905
  49. Chemical composition of the yeast ascospore wall. The second outer layer consists of chitosan.
    J Biol Chem. 1988 Aug 15;263(23):11569-74 PMID: 3042773
  50. Genome-wide mapping of nuclear mitochondrial DNA sequences links DNA replication origins to chromosomal double-strand break formation in Schizosaccharomyces pombe.
    Genome Res. 2010 Sep;20(9):1250-61 PMID: 20688779
  51. Isolation and characterisation of mutants from the halotolerant yeast Pichia sorbitophila defective in H+/glycerol symport activity.
    FEMS Microbiol Lett. 1996 Sep 1;142(2-3):147-53 PMID: 8810497
  52. Speciation in the large-spored Metschnikowia clade and establishment of a new species, Metschnikowia borealis comb. nov.
    FEMS Yeast Res. 2004 Mar;4(6):587-96 PMID: 15040946
  53. Conservation and release of osmolytes by yeasts during hypo-osmotic stress.
    Arch Microbiol. 2001 Dec;177(1):29-35 PMID: 11797041
  54. The closely related species Candida albicans and Candida dubliniensis can mate.
    Eukaryot Cell. 2004 Aug;3(4):1015-27 PMID: 15302834
  55. Novel p-type ATPases mediate high-affinity potassium or sodium uptake in fungi.
    Eukaryot Cell. 2004 Apr;3(2):359-68 PMID: 15075266
  56. Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus.
    Genome Res. 2008 Oct;18(10):1610-23 PMID: 18787083
  57. Yeast evolutionary genomics.
    Nat Rev Genet. 2010 Jul;11(7):512-24 PMID: 20559329
  58. Loss of heterozygosity in commensal isolates of the asexual diploid yeast Candida albicans.
    Fungal Genet Biol. 2009 Feb;46(2):159-68 PMID: 19059493
  59. Physiological characterization of osmotolerant yeast Pichia sorbitophila and comparison with a putative synonym Pichia farinosa.
    Folia Microbiol (Praha). 2003;48(2):211-7 PMID: 12800505
  60. Mate choice assays and mating propensity differences in natural yeast populations.
    Biol Lett. 2006 Dec 22;2(4):553-6 PMID: 17148286
  61. Nucleotide sequence of the yeast SUC2 gene for invertase.
    Nucleic Acids Res. 1983 Mar 25;11(6):1943-54 PMID: 6300785
  62. Genomic convergence toward diploidy in Saccharomyces cerevisiae.
    PLoS Genet. 2006 Sep 22;2(9):e145 PMID: 17002497
  63. The complete mitochondrial genome of the yeast Pichia sorbitophila.
    FEMS Yeast Res. 2009 Sep;9(6):903-10 PMID: 19594828
  64. Chromosomal G + C content evolution in yeasts: systematic interspecies differences, and GC-poor troughs at centromeres.
    Genome Biol Evol. 2010;2:572-83 PMID: 20693156
  65. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts.
    Nature. 2006 Mar 16;440(7082):341-5 PMID: 16541074
  66. The diploid genome sequence of Candida albicans.
    Proc Natl Acad Sci U S A. 2004 May 11;101(19):7329-34 PMID: 15123810
  67. Multiple molecular mechanisms cause reproductive isolation between three yeast species.
    PLoS Biol. 2010 Jul 20;8(7):e1000432 PMID: 20652018
  68. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species.
    Cell. 2008 Dec 12;135(6):1065-73 PMID: 19070577
  69. Locus-specific ribosomal RNA gene silencing in nucleolar dominance.
    PLoS One. 2007 Aug 29;2(8):e815 PMID: 17726545
  70. Structure of the multigene family of MAL loci in Saccharomyces.
    Mol Gen Genet. 1989 May;217(1):60-9 PMID: 2549370
Article Info
Journal
G3 (Bethesda, Md.)
Abbr.
G3 (Bethesda)
ISSN
2160-1836
Published
2012-02-00
Epub
2012-00-01
Pages
299-311
Language
English
Region
England
NLM ID
101566598
PMCID
PMC3284337
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]