1887

Abstract

Ancient events of polyploidy have been linked to huge evolutionary leaps in the tree of life, while increasing evidence shows that newly established polyploids have adaptive advantages in certain stress conditions compared to their relatives with a lower ploidy. The genus is a good model for studying such events, as it contains an ancient whole-genome duplication event and many sequenced are, evolutionary speaking, newly formed polyploids. Many polyploids have unstable genomes and go through large genome erosions; however, it is still unknown what mechanisms govern this reduction. Here, we sequenced and studied the natural × hybrid strain, VIN7, which was selected for its commercial use in the wine industry. The most singular observation is that its nuclear genome is highly unstable and drastic genomic alterations were observed in only a few generations, leading to a widening of its phenotypic landscape. To better understand what leads to the loss of certain chromosomes in the VIN7 cell population, we looked for genetic features of the genes, such as physical interactions, complex formation, epistatic interactions and stress responding genes, which could have beneficial or detrimental effects on the cell if their dosage is altered by a chromosomal copy number variation. The three chromosomes lost in our VIN7 population showed different patterns, indicating that multiple factors could explain the mechanisms behind the chromosomal loss. However, one common feature for two out of the three chromosomes is that they are among the smallest ones. We hypothesize that small chromosomes alter their copy numbers more frequently as a low number of genes is affected, meaning that it is a by-product of genome instability, which might be the chief driving force of the adaptability and genome architecture of this hybrid.

Funding
This study was supported by the:
  • Christina Toft , Dirección General de Universidades e Investigación , (Award JCI-2012–14056)
  • Christina Toft , European Molecular Biology Organization , (Award ALTF 730-2011)
  • Miguel Morard , Conselleria d'Educació, Investigació, Cultura i Esport , (Award ACIF/2015/194)
  • Eladio Barrio , Ministerio de Ciencia, Innovación y Universidades , (Award RTI2018-093744-B-C32)
  • Amparo Querol , Ministerio de Ciencia, Innovación y Universidades , (Award RTI2018-093744-B-C31)
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000448
2020-10-06
2020-10-20
Loading full text...

Full text loading...

/deliver/fulltext/mgen/10.1099/mgen.0.000448/mgen000448.html?itemId=/content/journal/mgen/10.1099/mgen.0.000448&mimeType=html&fmt=ahah

References

  1. Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000; 408:796–815 [CrossRef][PubMed]
    [Google Scholar]
  2. Bowers JE, Chapman BA, Rong J, Paterson AH. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003; 422:433–438 [CrossRef][PubMed]
    [Google Scholar]
  3. Paterson AH, Bowers JE, Chapman BA. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 2004; 101:9903–9908 [CrossRef][PubMed]
    [Google Scholar]
  4. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007; 449:463–467 [CrossRef][PubMed]
    [Google Scholar]
  5. Wei F, Coe E, Nelson W, Bharti AK, Engler F et al. Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 2007; 3:e123 [CrossRef][PubMed]
    [Google Scholar]
  6. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N et al. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 2004; 431:946–957 [CrossRef][PubMed]
    [Google Scholar]
  7. Aury JM, Jaillon O, Duret L, Noel B, Jubin C et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 2006; 444:171–178 [CrossRef][PubMed]
    [Google Scholar]
  8. McLysaght A, Hokamp K, Wolfe KH. Extensive genomic duplication during early chordate evolution. Nat Genet 2002; 31:200–204 [CrossRef][PubMed]
    [Google Scholar]
  9. Kellis M, Birren BW, Lander ES. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 2004; 428:617–624 [CrossRef][PubMed]
    [Google Scholar]
  10. Marcet-Houben M, Gabaldón T. Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker's yeast lineage. PLoS Biol 2015; 13:e1002220 [CrossRef][PubMed]
    [Google Scholar]
  11. Wolfe KH, Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997; 387:708–713 [CrossRef][PubMed]
    [Google Scholar]
  12. Arroyo-López FN, Pérez-Través L, Querol A, Barrio E. Exclusion of Saccharomyces kudriavzevii from a wine model system mediated by Saccharomyces cerevisiae. Yeast 2011; 28:423–435 [CrossRef][PubMed]
    [Google Scholar]
  13. Vasseur F, Fouqueau L, de Vienne D, Nidelet T, Violle C et al. Nonlinear phenotypic variation uncovers the emergence of heterosis in Arabidopsis thaliana. PLoS Biol 2019; 17:e3000214 [CrossRef][PubMed]
    [Google Scholar]
  14. Lairón-Peris M, Pérez-Través L, Muñiz-Calvo S, Guillamón JM, Heras JM et al. Differential contribution of the parental genomes to a S. cerevisiae × S. uvarum hybrid, inferred by phenomic, genomic, and transcriptomic analyses, at different industrial stress conditions. Front Bioeng Biotechnol 2020; 8:129 [CrossRef][PubMed]
    [Google Scholar]
  15. Paun O, Forest F, Fay MF, Chase MW. Hybrid speciation in angiosperms: parental divergence drives ploidy. New Phytol 2009; 182:507–518 [CrossRef][PubMed]
    [Google Scholar]
  16. Tang H, Bowers JE, Wang X, Paterson AH. Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci USA 2010; 107:472–477 [CrossRef][PubMed]
    [Google Scholar]
  17. Lamichhaney S, Han F, Webster MT, Andersson L, Grant BR et al. Rapid hybrid speciation in Darwin's finches. Science 2018; 359:224–228 [CrossRef][PubMed]
    [Google Scholar]
  18. Van de Peer Y, Mizrachi E, Marchal K. The evolutionary significance of polyploidy. Nat Rev Genet 2017; 18:411–424 [CrossRef][PubMed]
    [Google Scholar]
  19. Chaudhary B. Plant domestication and resistance to herbivory. Int J Plant Genomics 2013; 2013:572784 [CrossRef][PubMed]
    [Google Scholar]
  20. Burger JC, Chapman MA, Burke JM. Molecular insights into the evolution of crop plants. Am J Bot 2008; 95:113–122 [CrossRef][PubMed]
    [Google Scholar]
  21. Iorizzo M, Ellison S, Senalik D, Zeng P, Satapoomin P et al. A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat Genet 2016; 48:657–666 [CrossRef][PubMed]
    [Google Scholar]
  22. Gallone B, Steensels J, Mertens S, Dzialo MC, Gordon JL et al. Interspecific hybridization facilitates niche adaptation in beer yeast. Nat Ecol Evol 2019; 3:1562–1575 [CrossRef][PubMed]
    [Google Scholar]
  23. Langdon QK, Peris D, Baker EP, Opulente DA, Nguyen H-V et al. Fermentation innovation through complex hybridization of wild and domesticated yeasts. Nat Ecol Evol 2019; 3:1576–1586 [CrossRef][PubMed]
    [Google Scholar]
  24. Morard M, Benavent-Gil Y, Ortiz-Tovar G, Pérez-Través L, Querol A et al. Genome structure reveals the diversity of mating mechanisms in Saccharomyces cerevisiae x Saccharomyces kudriavzevii hybrids, and the genomic instability that promotes phenotypic diversity. Microb Genom 2020; 6:e000333 [CrossRef][PubMed]
    [Google Scholar]
  25. Ortiz-Tovar G, Pérez-Torrado R, Adam AC, Barrio E, Querol A. A comparison of the performance of natural hybrids Saccharomyces cerevisiae × Saccharomyces kudriavzevii at low temperatures reveals the crucial role of their S. kudriavzevii genomic contribution. Int J Food Microbiol 2018; 274:12–19 [CrossRef][PubMed]
    [Google Scholar]
  26. García-Ríos E, Guillén A, de la Cerda R, Pérez-Través L, Querol A et al. Improving the cryotolerance of wine yeast by interspecific hybridization in the genus Saccharomyces. Front Microbiol 2019; 9:3232 [CrossRef][PubMed]
    [Google Scholar]
  27. De Storme N, Mason A. Plant speciation through chromosome instability and ploidy change: cellular mechanisms, molecular factors and evolutionary relevance. Curr Plant Biol 2014; 1:10–33 [CrossRef]
    [Google Scholar]
  28. Hegarty MJ, Barker GL, Brennan AC, Edwards KJ, Abbott RJ et al. Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Philos Trans R Soc Lond B Biol Sci 2008; 363:3055–3069 [CrossRef][PubMed]
    [Google Scholar]
  29. Levasseur A, Pontarotti P. The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics. Biol Direct 2011; 6:11 [CrossRef][PubMed]
    [Google Scholar]
  30. Sipiczki M. Interspecies hybridisation and genome chimerisation in Saccharomyces: combining of gene pools of species and its biotechnological perspectives. Front Microbiol 2018; 9:3071 [CrossRef][PubMed]
    [Google Scholar]
  31. Sémon M, Wolfe KH. Consequences of genome duplication. Curr Opin Genet Dev 2007; 17:505–512 [CrossRef][PubMed]
    [Google Scholar]
  32. Xu G, Guo C, Shan H, Kong H. Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci USA 2012; 109:1187–1192 [CrossRef][PubMed]
    [Google Scholar]
  33. Runemark A, Vallejo-Marin M, Meier JI. Eukaryote hybrid genomes. PLoS Genet 2019; 15:e1008404 [CrossRef][PubMed]
    [Google Scholar]
  34. Gordon JL, Byrne KP, Wolfe KH. Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 2009; 5:e1000485 [CrossRef][PubMed]
    [Google Scholar]
  35. Seoighe C, Wolfe KH. Extent of genomic rearrangement after genome duplication in yeast. Proc Natl Acad Sci USA 1998; 95:4447–4452 [CrossRef][PubMed]
    [Google Scholar]
  36. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 2003; 423:241–254 [CrossRef][PubMed]
    [Google Scholar]
  37. Peris D, Alexander WG, Fisher KJ, Moriarty RV, Basuino MG et al. Synthetic hybrids of six yeast species. Nat Commun 2020; 11:2085 [CrossRef][PubMed]
    [Google Scholar]
  38. Krogerus K, Magalhães F, Vidgren V, Gibson B. Novel brewing yeast hybrids: creation and application. Appl Microbiol Biotechnol 2017; 101:65–78 [CrossRef][PubMed]
    [Google Scholar]
  39. van den Broek M, Bolat I, Nijkamp JF, Ramos E, Luttik MAH et al. Chromosomal copy number variation in Saccharomyces pastorianus is evidence for extensive genome dynamics in industrial lager brewing strains. Appl Environ Microbiol 2015; 81:6253–6267 [CrossRef][PubMed]
    [Google Scholar]
  40. Antunovics Z, Nguyen H-V, Gaillardin C, Sipiczki M. Gradual genome stabilisation by progressive reduction of the Saccharomyces uvarum genome in an interspecific hybrid with Saccharomyces cerevisiae. FEMS Yeast Res 2005; 5:1141–1150 [CrossRef]
    [Google Scholar]
  41. Pfliegler WP, Antunovics Z, Sipiczki M. Double sterility barrier between Saccharomyces species and its breakdown in allopolyploid hybrids by chromosome loss. FEMS Yeast Res 2012; 12:703–718 [CrossRef][PubMed]
    [Google Scholar]
  42. Pfliegler WP, Atanasova L, Karanyicz E, Sipiczki M, Bond U et al. Generation of new genotypic and phenotypic features in artificial and natural yeast hybrids. Food Technol Biotechnol 2014; 52:46–57
    [Google Scholar]
  43. Sipiczki M. Interspecies hybridization and recombination in Saccharomyces wine yeasts. FEMS Yeast Res 2008; 8:996–1007 [CrossRef][PubMed]
    [Google Scholar]
  44. Sipiczki M. Diversity, variability and fast adaptive evolution of the wine yeast (Saccharomyces cerevisiae) genome—a review. Ann Microbiol 2011; 61:85–93 [CrossRef]
    [Google Scholar]
  45. Belloch C, Pérez-Torrado R, González SS, Pérez-Ortín JE, García-Martínez J et al. Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Appl Environ Microbiol 2009; 75:2534–2544 [CrossRef][PubMed]
    [Google Scholar]
  46. Dunn B, Sherlock G. Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res 2008; 18:1610–1623 [CrossRef][PubMed]
    [Google Scholar]
  47. Peris D, Lopes CA, Belloch C, Querol A, Barrio E. Comparative genomics among Saccharomyces cerevisiae × Saccharomyces kudriavzevii natural hybrid strains isolated from wine and beer reveals different origins. BMC Genomics 2012; 13:407 [CrossRef][PubMed]
    [Google Scholar]
  48. Peris D, Belloch C, Lopandić K, Álvarez-Pérez JM, Querol A et al. The molecular characterization of new types of Saccharomyces cerevisiae × S. kudriavzevii hybrid yeasts unveils a high genetic diversity. Yeast 2012; 29:81–91 [CrossRef][PubMed]
    [Google Scholar]
  49. Walther A, Hesselbart A, Wendland J. Genome sequence of Saccharomyces carlsbergensis, the world's first pure culture lager yeast. G3 2014; 4:783–793 [CrossRef][PubMed]
    [Google Scholar]
  50. Lopandic K. Saccharomyces interspecies hybrids as model organisms for studying yeast adaptation to stressful environments. Yeast 2018; 35:21–38 [CrossRef][PubMed]
    [Google Scholar]
  51. Peter J, De Chiara M, Friedrich A, Yue J-X, Pflieger D et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature 2018; 556:339–344 [CrossRef][PubMed]
    [Google Scholar]
  52. Zhu YO, Sherlock G, Petrov DA. Whole genome analysis of 132 clinical Saccharomyces cerevisiae strains reveals extensive ploidy variation. G3 2016; 6:2421–2434 [CrossRef][PubMed]
    [Google Scholar]
  53. Gilchrist C, Stelkens R. Aneuploidy in yeast: segregation error or adaptation mechanism?. Yeast 2019; 36:525–539 [CrossRef]
    [Google Scholar]
  54. Chen G, Rubinstein B, Li R. Whole chromosome aneuploidy: big mutations drive adaptation by phenotypic leap. Bioessays 2012; 34:893–900 [CrossRef][PubMed]
    [Google Scholar]
  55. Gorter de Vries AR, Knibbe E, van Roosmalen R, van den Broek M, de la Torre Cortés P et al. Improving industrially relevant phenotypic traits by engineering chromosome copy number in Saccharomyces pastorianus. Front Genet 2020; 11:518 [CrossRef][PubMed]
    [Google Scholar]
  56. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH et al. The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins. FEMS Yeast Res 2012; 12:88–96 [CrossRef][PubMed]
    [Google Scholar]
  57. Borneman AR, Forgan AH, Kolouchova R, Fraser JA, Schmidt SA. Whole genome comparison reveals high levels of inbreeding and strain redundancy across the spectrum of commercial wine strains of Saccharomyces cerevisiae. G3 2016; 6:957–971 [CrossRef][PubMed]
    [Google Scholar]
  58. Querol A, Barrio E, Ramón D. A comparative study of different methods of yeast strain characterization. Syst Appl Microbiol 1992; 15:439–446 [CrossRef]
    [Google Scholar]
  59. Sprouffske K, Wagner A. Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinformatics 2016; 17:172 [CrossRef][PubMed]
    [Google Scholar]
  60. Joshi NA, Fass JN. Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files; 2011. https://github.com/najoshi/sickle..
  61. Gordon D, Green P. Consed: a graphical editor for next-generation sequencing. Bioinformatics 2013; 29:2936–2937 [CrossRef][PubMed]
    [Google Scholar]
  62. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [CrossRef][PubMed]
    [Google Scholar]
  63. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [CrossRef][PubMed]
    [Google Scholar]
  64. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [CrossRef][PubMed]
    [Google Scholar]
  65. Otto TD, Dillon GP, Degrave WS, Berriman M. RATT: rapid annotation transfer tool. Nucleic Acids Res 2011; 39:e57 [CrossRef][PubMed]
    [Google Scholar]
  66. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 2005; 33:W465–W467 [CrossRef][PubMed]
    [Google Scholar]
  67. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P et al. Artemis: sequence visualization and annotation. Bioinformatics 2000; 16:944–945 [CrossRef][PubMed]
    [Google Scholar]
  68. Costanzo M, VanderSluis B, Koch EN, Baryshnikova A, Pons C et al. A global genetic interaction network maps a wiring diagram of cellular function. Science 2016; 353:aaf1420 [CrossRef][PubMed]
    [Google Scholar]
  69. Pu S, Wong J, Turner B, Cho E, Wodak SJ. Up-to-date catalogues of yeast protein complexes. Nucleic Acids Res 2009; 37:825–831 [CrossRef][PubMed]
    [Google Scholar]
  70. Mattenberger F, Sabater-Muñoz B, Toft C, Sablok G, Fares MA. Expression properties exhibit correlated patterns with the fate of duplicated genes, their divergence, and transcriptional plasticity in Saccharomycotina. DNA Res 2017; 24:559–570 [CrossRef][PubMed]
    [Google Scholar]
  71. Gorter de Vries AR, Pronk JT, Daran J-MG. Industrial relevance of chromosomal copy number variation in Saccharomyces yeasts. Appl Environ Microbiol 2017; 83:e03206-16 [CrossRef][PubMed]
    [Google Scholar]
  72. Hose J, Yong CM, Sardi M, Wang Z, Newton MA et al. Dosage compensation can buffer copy-number variation in wild yeast. eLife 2015; 4:e05462 [CrossRef][PubMed]
    [Google Scholar]
  73. Leducq J-B, Charron G, Diss G, Gagnon-Arsenault I, Dubé AK et al. Evidence for the robustness of protein complexes to inter-species hybridization. PLoS Genet 2012; 8:e1003161 [CrossRef][PubMed]
    [Google Scholar]
  74. Dandage R, Berger CM, Gagnon-Arsenault I, Moon K-M, Stacey RG et al. Frequent assembly of chimeric complexes in the protein interaction network of an interspecies hybrid. bioRxiv 2020 [CrossRef]
    [Google Scholar]
  75. Peris D, Pérez-Torrado R, Hittinger CT, Barrio E, Querol A. On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids. Yeast 2018; 35:51–69 [CrossRef][PubMed]
    [Google Scholar]
  76. Krogerus K, Arvas M, De Chiara M, Magalhães F, Mattinen L et al. Ploidy influences the functional attributes of de novo lager yeast hybrids. Appl Microbiol Biotechnol 2016; 100:7203–7222 [CrossRef][PubMed]
    [Google Scholar]
  77. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 2007; 317:916–924 [CrossRef][PubMed]
    [Google Scholar]
  78. Morard M, Macías LG, Adam AC, Lairón-Peris M, Pérez-Torrado R et al. Aneuploidy and ethanol tolerance in Saccharomyces cerevisiae. Front Genet 2019; 10:82 [CrossRef][PubMed]
    [Google Scholar]
  79. Yona AH, Manor YS, Herbst RH, Romano GH, Mitchell A et al. Chromosomal duplication is a transient evolutionary solution to stress. Proc Natl Acad Sci USA 2012; 109:21010–21015 [CrossRef][PubMed]
    [Google Scholar]
  80. Ravichandran MC, Fink S, Clarke MN, Hofer FC, Campbell CS. Genetic interactions between specific chromosome copy number alterations dictate complex aneuploidy patterns. Genes Dev 2018; 32:1485–1498 [CrossRef][PubMed]
    [Google Scholar]
  81. Zhu J, Pavelka N, Bradford WD, Rancati G, Li R. Karyotypic determinants of chromosome instability in aneuploid budding yeast. PLoS Genet 2012; 8:e1002719 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000448
Loading
/content/journal/mgen/10.1099/mgen.0.000448
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error