4.5 Article

Domestication reprogrammed the budding yeast life cycle

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NATURE ECOLOGY & EVOLUTION
卷 6, 期 4, 页码 448-+

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NATURE PORTFOLIO
DOI: 10.1038/s41559-022-01671-9

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资金

  1. Agence Nationale de la Recherche [ANR-15-IDEX-01, ANR-18-CE12-0004, ANR-20-CE13-0010, ANR-20-CE12-0020]
  2. Fondation pour la Recherche Medicale [EQU202003010413]
  3. CEFIPRA
  4. Fondation ARC [ARCPJA32020070002320]
  5. Swedish Research Council [2014-6547, 2014-4605, 2018-03638, 2018-03453]
  6. Slovenian Research Agency [P1-0207]
  7. COFUND BoostUrCAreer programme - EU [847581]
  8. COFUND BoostUrCAreer programme (Region SUD PACA)
  9. COFUND BoostUrCAreer programme (IDEX UCAjedi)
  10. Swedish Research Council [2018-03453, 2018-03638] Funding Source: Swedish Research Council
  11. Agence Nationale de la Recherche (ANR) [ANR-20-CE12-0020, ANR-20-CE13-0010] Funding Source: Agence Nationale de la Recherche (ANR)

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This study assesses the impact of domestication on the evolution of budding yeast and reveals significant differences between domesticated and wild strains in terms of reproductive capacity, tolerance, and life span. Domestication systematically enhances fermentative growth and reduces respiratory growth, alters tolerance to various stresses, and abolishes or impairs the sexual life cycle. The genetic origins of the yeast domestication syndrome were traced using genome-wide association analysis and genetic engineering, involving aneuploidy, gene presence/absence variations, copy number variations, and single-nucleotide polymorphisms.
This study assesses the capacity for sexual and asexual reproduction and the chronological life span across 1,011 genome-sequenced budding yeast isolates and shows the remarkable impact of domestication on budding yeast evolution. Domestication of plants and animals is the foundation for feeding the world human population but can profoundly alter the biology of the domesticated species. Here we investigated the effect of domestication on one of our prime model organisms, the yeast Saccharomyces cerevisiae, at a species-wide level. We tracked the capacity for sexual and asexual reproduction and the chronological life span across a global collection of 1,011 genome-sequenced yeast isolates and found a remarkable dichotomy between domesticated and wild strains. Domestication had systematically enhanced fermentative and reduced respiratory asexual growth, altered the tolerance to many stresses and abolished or impaired the sexual life cycle. The chronological life span remained largely unaffected by domestication and was instead dictated by clade-specific evolution. We traced the genetic origins of the yeast domestication syndrome using genome-wide association analysis and genetic engineering and disclosed causative effects of aneuploidy, gene presence/absence variations, copy number variations and single-nucleotide polymorphisms. Overall, we propose domestication to be the most dramatic event in budding yeast evolution, raising questions about how much domestication has distorted our understanding of the natural biology of this key model species.

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