Genome Evolution in Yeasts

Abstract

Used empirically over millennia for a variety of fermentation processes, the microscopic yeasts representing unicellular forms of modern fungi adapted to a large diversity of habitats have become powerful model organisms to understand eukaryotic genome evolution. Their broad evolutionary range offers unique views on both short‐ and long‐term genomic changes, with the possibility to confront observations with experimental results. Processes of duplications, gene loss and gene creation form the bases of genome evolution, along with horizontal acquisitions and an unexpectedly high frequency of interspecies hybridisations. This short review summarises our present knowledge about genome evolution focussing on the subphylum of budding yeasts or , by far the most extensively studied lineage, without ignoring the multiphyletic origin of yeasts.

Key Concepts

  • Yeasts represent long‐evolved unicellular forms of modern fungi, adapted to rapid clonal expansions under favourable conditions, not primitive eukaryotes.
  • Over 1600 yeast species are presently described in the different subphyla of Ascomycota and Basidiomycota, within which the budding yeasts (Saccharomycotina) represent the largest deep‐branching lineage useful for genome evolution studies.
  • The different genome architectures of well‐circumscribed subgroups of Saccharomycotina indicate major evolutionary divides within which ancient events can be inferred.
  • Important modifications of the role of RNA occurred at the origin of Saccharomycotina (massive loss of spliceosomal introns and loss of RNAi control) and continued during their evolution (fixation of 5S RNA gene, change of deciphering mode and significance for synonymous codons).
  • All yeast genomes exhibit significant levels of redundancy, reflecting small‐scale duplications and, in one lineage, a whole‐genome duplication followed by extensive gene loss.
  • The balance between gene gains and losses accelerated yeast genome evolution beyond sequence divergence and chromosomal dynamics.
  • Novel genes regularly appeared during yeast genome evolution, resulting from duplication followed by sequence divergence, horizontal acquisition and de novo gene creation.
  • Interspecies hybridisation is a common phenomenon.
  • Resolution of hybrid genomes suggests an important role for interspecific exchanges in evolution.

Keywords: sequence; orphan gene; synteny; gene loss; duplication; hybrid; introgression; centromere; telomere; polymorphism

Figure 1. Yeast genomics 10 years ago. Sequenced yeast genomes at the end of 2004 with original references: (1) Goffeau et al. (), (2) Wood et al. (), (3) Kellis et al. (), (4) Dietrich et al. (), (5) Jones et al. () and (6) Dujon et al. (). Available data distinguished four major types of genome architectures (coloured backgrounds), suggesting deep evolutionary divides between them. Species designation and tree topology (arbitrary branch lengths) are according to Kurtzman et al. (). Blue, red and purple arrows point to major evolutionary events reconstituted from parsimony: WGD, whole‐genome duplication; CTG, alteration of genetic code; LCM, loss of genes for complex I of the respiratory chain in mitochondrial DNA.
Figure 2. Taxon sampling of sequenced yeast species. Pie charts represent the distribution of yeast species in different subphyla of (blue) and (green). (a) Total of 1576 species described in Kurtzman et al. (). (b) Total of 66 sequenced yeast species (59 yeasts compiled from Tables and , plus 7 yeasts, not shown). Hybrids were ignored.
Figure 3. Major genome architectures in and global reconstruction of major evolutionary events Tree topology is adapted from Kurtzman et al. (2011) . Left column: major subgroups defined from genome architectures and proteome comparisons (Figure). symbolises outgroup. Central column: most representative species (Tables and ). Right column: major genomic characteristics. Circled numbers indicate major evolutionary changes deduced from genomic data using maximal parsimony. 0, extensive loss of spliceosomal introns and partial loss of RNAi control machinery at the very origin of ; 1, reduction of rDNA locus number and fixation of 5S rRNA gene in them, switch to bacterial decoding mode for Arg CGN codons and selection for increased genome compactness; 2, additional loss of spliceosomal introns, acquisition of point centromeres, switch to bacterial decoding mode for Leu CUN codons, triplication of mating cassettes and loss of complex I genes in mtDNA; 3, additional loss of spliceosomal introns and acquisition of novel Ser tRNA reading CUG codons; 4, whole genome duplication.
Figure 4. Clustering the members of subdivisions from pairwise comparisons between predicted proteomes. The figure illustrates the two first factorial planes, representing together 40% of the total information of a pair‐wise comparison matrix between sequence‐predicted proteomes of 40 selected fungal genomes, after correspondence analysis. Each point corresponds to one fungal genome sequence (symbols in insert). Note the distribution of members in four separate clusters (blue, purple, green and orange backgrounds, respectively) corresponding to major subdivisions defined from global genomic anatomies (see text), and their clear‐cut separation from other subphyla and from Adapted with permission from Morales et al. (2013), © Oxford University Press.
Figure 5. Interplay between major mechanisms of genome evolution in yeasts. The yellow circle symbolises yeast genomes with their elements (protein‐coding genes, protogenes, pseudogenes, genes for non‐coding RNAs and retrotransposons). Internal grey circles symbolise the two major evolutionary clocks, governing sequence divergence (outer circle with red arrows) and loss of gene synteny (inner circle with blue arrows). See text for details. Shown by blue arrows are the major evolutionary mechanisms acting on genomes and their genetic elements: (1) small‐scale duplications (SSD), (2) horizontal gene acquisition (red donor), (3) gene loss, (4) gene formation, (5) autopolyploidisation (WGD) and (6) allopolyploidisation (hybrid formation between green and yellow genomes). Small cartoons represent the traces left in genomes by each mechanism. Small rectangles illustrate genes along chromosomes (lines), purple rectangles ancestral genome and blue rectangles evolved genome. Traces of SSD are transferred in the two inserts at the bottom of the figure for clarity. The figure stresses the fact that RNA intermediates ignore chromosomal rearrangements, whereas protogenes and pseudogenes do not and are only separated from actual genes by sequence changes. Processed pseudogenes were not found in yeast genomes.
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Further Reading

Costanzo M, Baryshnikova A, Bellay J, et al. (2010) The genetic landscape of a cell. Science 327: 425–431.

Dujon B (2011) Ten years of genomic exploration in eukaryotes: strategy and progress of Génolevures. (Thematic issue). Comptes Rendus Biologies 334: 577–693.

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Hittinger CT (2013) Saccharomyces diversity and evolution: a budding model genus. Trends in Genetics 29 (5): 309–311.

Neme R and Tautz D (2011) Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution. BMC Genomics 14: 117.

Proux‐Wera E, Byrne KP and Wolfe KH (2013) Evolutionary mobility of the ribosomal DNA array in yeasts. Genome Biology and Evolution 5 (3): 525–531.

Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L, et al. (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458: 342–345.

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Dujon, Bernard(Apr 2015) Genome Evolution in Yeasts. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023986]