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Evolutionary biology through the lens of budding yeast comparative genomics

Key Points

  • The budding yeast Saccharomyces cerevisiae has become an important model for evolutionary genomics owing to the development of high-throughput sequencing technologies.

  • Comparative genomics analysis of S. cerevisiae and closely related species has contributed to our understanding of how new species emerge and has shed light on the various mechanisms that contribute to reproductive isolation.

  • Population genomics and comparative genomics of Saccharomyces yeasts have revealed that hybridization occurred frequently throughout, and has had substantial effects on, yeast evolution. Hybridization could itself be a mechanism of adaptation and speciation.

  • Genomic analysis of Saccharomyces yeasts has provided a better understanding of the mechanisms underlying large-scale genomic changes, such as polyploidy, and their consequences for genome evolution and cell physiology.

  • Genomic analysis of yeast strains associated with humans has revealed the history of yeast domestication and the mechanisms that have contributed to its adaptation to anthropogenic environments.

  • Genomic approaches are increasingly contributing to our understanding of how budding yeasts adapt to natural environments by identifying the genes that are involved in adaptation within natural substrates.

Abstract

The budding yeast Saccharomyces cerevisiae is a highly advanced model system for studying genetics, cell biology and systems biology. Over the past decade, the application of high-throughput sequencing technologies to this species has contributed to this yeast also becoming an important model for evolutionary genomics. Indeed, comparative genomic analyses of laboratory, wild and domesticated yeast populations are providing unprecedented detail about many of the processes that govern evolution, including long-term processes, such as reproductive isolation and speciation, and short-term processes, such as adaptation to natural and domestication-related environments.

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Figure 1: Mechanisms of postzygotic reproductive isolation in Saccharomyces.
Figure 2: Genomic mechanisms of introgression and loss of heterozygosity (LOH) in Saccharomyces.
Figure 3: Diversification of the galactose utilization network after the budding yeast whole-genome duplication (WGD).
Figure 4: The history of yeast domestication for beer, wine, sake, cocoa and coffee fermentation.
Figure 5: Hallmarks of adaptation in domesticated yeasts.
Figure 6: Functional genomics tools for identifying fitness determinants in natural environments.

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Acknowledgements

The authors thank the members of the Landry laboratory, N. Aubin-Horth and the three anonymous reviewers for useful comments on the manuscript. This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Canadian Institutes of Health Research (CIHR). C.R.L. holds the Canada Research Chair in Evolutionary Cell and Systems Biology.

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Glossary

Anthropogenic

Conditions related to human activities.

Whole-genome duplication

(WGD). Process by which the number of chromosomes is doubled.

Outgroups

A group of species that diverged from the group of interest before its most recent common ancestor.

Reproductive isolation

A mechanism that prevents the production of viable or fertile offspring between species.

Hybridization

Crosses between species or divergent populations.

Ploidy

The number of sets of homologous chromosomes in a cell for a given species, in which haploid cells have one set, diploid cells have two sets and polyploid cells have multiple (more than two) sets.

Postzygotic isolation

A mechanism that limits the reproductive success or survival of offspring.

Prezygotic isolation

A mechanism that prevents the fertilization of eggs or, in the case of yeast, the formation of zygotes.

Aneuploidy

The presence in a cell of an abnormal number of chromosomes that deviates from a multiple of the normal number.

Bateson–Dobzhansky–Muller incompatibilities

(BDMIs). Interactions between genetic elements that reduce the viability or the fertility of hybrids between populations or species. Mito-nuclear BDMIs involve components encoded by the mitochondrial genome and the nuclear genome.

Introgression

The integration of genomic regions of one species or population into the genome of another species or population.

Loss of heterozygosity

(LOH). The loss of one allele at a heterozygous locus. This loss can occur by mutation, deletion or gene conversion, using the other allele as a template. LOH in yeast genomes often corresponds to large-scale chromosomal regions encompassing multiple neighbouring genes.

Epistasis

Interaction between alleles of genes leading to a lower (negative epitasis) or increased (positive epistasis) phenotypic value than expected from their single contributions.

Autopolyploidization

Polyploidization event in which the chromosome sets derive from a single species.

Allopolyploidization

Polyploidization event as a result of hybridization between distinct species.

Syntenic

The physical colocalization of orthologous genes on the same chromosomes between individuals or species.

Ohnologues

Duplicated genes originating from a whole-genome duplication event.

Paralogues

Genes related by duplication within a species.

Single-nucleotide variation

(SNV). A single-nucleotide change observed by comparing genomes within or between populations.

Horizontal gene transfer

(HGT). A process by which an organism incorporates genetic material from another organism that does not belong to its line of ancestry.

Balanced rearrangements

Changes in chromosomal gene order that do not remove or duplicate any of the DNA of the chromosomes. For example, inversions, reciprocal translocations and transpositions.

Chromosomal cores

Internal parts of chromosomes that exclude subtelomeres and terminal chromosome ends.

Convergent evolution

Evolution that leads populations to the same phenotypic or genotypic outcomes from distinct initial genotypes or phenotypes.

Heterosis

Fitness advantage of hybrids over parental species or individuals.

Hitchhiking

A mechanism by which certain mutations increase in frequency because they are linked to advantageous mutations.

Clonal interference

Competition among cells of a population that acquire advantageous mutations. This competition may prevent the fixation of one allele or the other.

Standing genetic variation

Genetic variation that exists at a given point in time in a population.

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Marsit, S., Leducq, JB., Durand, É. et al. Evolutionary biology through the lens of budding yeast comparative genomics. Nat Rev Genet 18, 581–598 (2017). https://doi.org/10.1038/nrg.2017.49

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