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  • Review Article
  • Published:

Yeast evolutionary genomics

Nature Reviews Genetics volume 11, pages 512–524 (2010)Cite this article

Subjects

Key Points

  • This Review summarizes our present knowledge about the diversity of yeast genome architectures. Specific attention is paid to yeast genome evolution and the multiphyletic origin of yeasts among fungi.

  • The structure of yeast populations (as determined from recent genomic analyses) and their specific mode of propagation (in which clonal expansions, drift and irregular genetic transfer dominate normal sexual exchanges) are discussed in terms of their evolutionary impact.

  • The different mechanisms of gene duplication, determined from genome comparisons as well as from direct experimental analyses, are discussed along with their evolutionary consequences. Gene duplication mechanisms in yeast are compared with those in other eukaryotes.

  • Phenomena of asymmetrical mitotic division, preferential inbreeding, horizontal gene acquisition, introgression, interspecific hybridization, delayed karyogamy, loss of heterozygosity and de novo gene formation are discussed in relation to their evolutionary consequences.

  • An attempt is made to integrate experimentally determined mutational rates with observed intra- and interspecific sequence divergences. Comparisons are made between the extensive and abrupt sequence divergence separating the distinct lineages and conservation or loss of synteny.

  • Together with some indications of future directions for investigation, the Review concludes with the apparent contradiction between the extensive mutational spectrum experienced by yeast genomes and their long evolutionary conservation, and proposes hypotheses to reconcile these facts.

Abstract

Over the past few years, genome sequences have become available from an increasing range of yeast species, which has led to notable advances in our understanding of evolutionary mechanisms in eukaryotes. Yeasts offer us a unique opportunity to examine how molecular and reproductive mechanisms combine to affect genome architectures and drive evolutionary changes over a broad range of species. This Review summarizes recent progress in understanding the molecular mechanisms — such as gene duplication, mutation and acquisition of novel genetic material — that underlie yeast evolutionary genomics. I also discuss how results from yeasts can be extended to other eukaryotes.

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Figure 1: Overview of the sequenced yeast genomes.
Figure 2: Asymmetrical cell divisions and consequences for population structures.
Figure 3: Types of spontaneous segmental duplications in Saccharomyces cerevisiae as observed in experimental evolution assays.
Figure 4: Main evolutionary mechanisms in yeasts and their functional and architectural consequences.

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Acknowledgements

I thank the members of the Génolevures Consortium (GDR2354 Centre National de la Recherche Scientifique) for sharing unpublished data and for numerous stimulating discussions. B.D. is a member of Institut Universitaire de France.

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  1. Institut Pasteur, Unité de Génétique Moléculaire des Levures, Centre National de la Recherche Scientifique/University Pierre and Marie Curie-Paris, 25 rue du Docteur Roux, F75724, Paris-CEDEX 15, France

    Bernard Dujon

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Génolevures — Genomic Exploration of the Hemiascomycete Yeasts

Glossary

Clade

A group of taxa that forms a monophyletic unit. It is applicable to any level of the taxonomical hierarchy.

Loss of heterozygosity

Formally, the loss of one active allele in a heterozygous pair. This loss can occur by any mechanism (mutation, deletion or gene conversion using the other allele as template). Loss of heterozygosity in yeast genomes corresponds to large-scale chromosomal regions encompassing multiple neighbouring genes.

Horizontal gene transfer

A process by which an organism incorporates genetic material from another organism that does not belong to its line of ancestry. This process is also called lateral gene transfer.

Allopatric

Refers to organisms, populations or species that inhabit distinct geographical regions.

Bateson–Dobzhansky–Muller effect

A negative effect of allelic reassortment by genetic recombination in hybrids between members of distinct populations. By extension, it is a lethal effect of reassortment by genetic recombination in crosses between parents that exhibit differential gene loss after genome duplication.

Differential gene loss

The loss of opposite copies in a pair of ohnologues between two cells that inherited the ohnologues from a common genome duplication.

Sympatric

Refers to organisms, populations or species inhabiting the same geographic area.

Ascospores

The four cellular products of a meiosis. The four ascospores are embedded in a sac called an ascus (observed in Ascomycota).

Protoploid

A general term created to designate all Saccharomycetaceae yeasts that do not originate from whole-genome duplication.

CTG group

This term is used here to designate a monophyletic group of yeast species that share a common genomic architecture and a common deviation from the universal genetic code (the CUG codon specifies serine) but are taxonomically classified in diverse families, some of which contain yeasts that do not share these genomic properties.

Autopolyploidization

The formation of cells or organisms with more than two pairs of homologous chromosomes as a result of self-fertilization or non-disjunctive segregation of chromosomes during mitosis or meiosis.

Allopolyploidization

The formation of cells or organisms with more than two pairs of homologous chromosomes as a result of hybridization between distinct species.

Synteny

The physical colocalization of genes, or genetic loci, along the same chromosome. It is more often used to designate subgroups of genes along a chromosomal segment.

Ohnologue

One of a pair of paralogues originating from a whole-genome duplication.

Neofunctionalization

The acquisition of a novel function by a gene after mutational changes. This usually applies to one of the two paralogues that are produced from a gene duplication.

Subfunctionalization

Functional specialization after mutational changes of the paralogues that are produced from a gene duplication.

Indels

Mutations due to the insertion or deletion of DNA sequences. In practice the term is often used to designate insertions or deletions that affect only one or a few nucleotides.

Pseudogenes

Genomic DNA sequences that are similar to normal genes but are rendered non-functional after mutations.

Commensal

Refers to an organism living at the expense of another one without causing substantial damage (a case of non-deleterious parasitism).

Introgression

The incorporation of genes of one species into the genetic pool of another. It is classically viewed as the result of hybridization followed by backcrossing, but could result from other mechanisms in yeasts.

Karyogamy

The fusion of distinct nuclei present in the same cell.

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Dujon, B. Yeast evolutionary genomics. Nat Rev Genet 11, 512–524 (2010). https://doi.org/10.1038/nrg2811

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