Beyond the Whole-Genome Duplication: Phylogenetic Evidence for an Ancient Interspecies Hybridization in the Baker's Yeast Lineage

Marcet‐Houben, Marina; Gabaldón, Toni

doi:10.1371/journal.pbio.1002220

Cited by 302 publications

(326 citation statements)

References 64 publications

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“…The two reticulations were deeper in the species phylogeny as compared to those inferred by Yu and Nakhleh. Our findings are consistent with the deeper hybridization events hypothesized by another recent phylogenomic study [53]. We note that neither our study nor the study of Yu and Nakhleh reconstructed recent hybridizations which have been described in the literature.…”

Section: Empirical Studysupporting

confidence: 91%

Fast and accurate statistical inference of phylogenetic networks using large-scale genomic sequence data

Hejase

Vandepol

Bonito

et al. 2017

Preprint

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An emerging discovery in phylogenomics is that interspecific gene flow has played a major role in the evolution of many different organisms. To what extent is the Tree of Life not truly a tree reflecting strict “vertical” divergence, but rather a more general graph structure known as a phylogenetic network which also captures “horizontal”gene flow? The answer to this fundamental question not only depends upon densely sampled and divergent genomic sequence data, but also compu-tational methods which are capable of accurately and efficiently inferring phylogenetic networks from large-scale genomic sequence datasets. Re-cent methodological advances have attempted to address this gap. How-ever, in the 2016 performance study of Hejase and Liu, state-of-the-art methods fell well short of the scalability requirements of existing phy-logenomic studies.The methodological gap remains: how can phylogenetic networks be ac-curately and efficiently inferred using genomic sequence data involving many dozens or hundreds of taxa? In this study, we address this gap by proposing a new phylogenetic divide-and-conquer method which we call FastNet. We conduct a performance study involving a range of evolu-tionary scenarios, and we demonstrate that FastNet outperforms state-of-the-art methods in terms of computational efficiency and topological accuracy.

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Section: Empirical Studysupporting

confidence: 91%

Fast and accurate statistical inference of phylogenetic networks using large-scale genomic sequence data

Hejase

Vandepol

Bonito

et al. 2017

Preprint

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“…45 Such interspecies hybrids occur readily in nature, and indeed recent evidence supports the idea that the ancient "whole genome duplication" (WGD) event that created numerous paralogs in the Saccharomyces lineage may have been the result of an interspecies hybridization event. 46 Following the WGD, many genes were lost, presumably leading to imbalances in the stoichiometry of subunits within complexes. Many opportunities for KADO likely arose as 2 paralogous "alleles" had to compete for a limiting supply of partners with whom they had not yet evolved optimal interactions.…”

Section: Discussionmentioning

confidence: 99%

Kinetic partitioning during de novo septin filament assembly creates a critical G1 “window of opportunity” for mutant septin function

et al. 2016

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Septin proteins form highly conserved cytoskeletal filaments composed of hetero-oligomers with strict subunit stoichiometry. Mutations within one hetero-oligomerization interface (the "G" interface) bias the mutant septin toward conformations that are incompatible with filament assembly, causing disease in humans and, in budding yeast cells, temperature-sensitive defects in cytokinesis. We previously found that, when the amount of other hetero-oligomerization partners is limiting, wild-type and G interfacemutant alleles of a given yeast septin "compete" along parallel but distinct folding pathways for occupancy of a limited number of positions within septin hetero-octamers. Here, we synthesize a mathematical model that outlines the requirements for this phenomenon: if a wild-type septin traverses a folding pathway that includes a single rate-limiting folding step, the acquisition by a mutant septin of additional slow folding steps creates an initially large disparity between wild-type and mutant in the cellular concentrations of oligomerization-competent monomers. When the 2 alleles are co-expressed, this kinetic disparity results in mutant exclusion from hetero-oligomers, even when the folded mutant monomer is oligomerization-competent. To test this model experimentally, we first visualize the kinetic delay in mutant oligomerization in living cells, and then narrow or widen the "window of opportunity" for mutant septin oligomerization by altering the length of the G1 phase of the yeast cell cycle, and observe the predicted exacerbation or suppression, respectively, of mutant cellular phenotypes. These findings reveal a fundamental kinetic principle governing in vivo assembly of multiprotein complexes, independent of the ability of the subunits to associate with each other.

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“…Unbalanced chromosomal rearrangements include deletions and duplications of the chromosome segments, which promote reduction and expansion of the gene repertoire, respectively (Llorente et al 2000;Dujon et al 2004;Wapinski et al 2007;Butler et al 2009;Souciet et al 2009;Scannell et al 2011;Gabaldon et al 2013). Whole-genome duplication (WGD) and hybridization events also affect gene repertoire, as well-documented in yeasts (Semon and Wolfe 2007;Louis et al 2012; Morales and Dujon 2012;Marcet-Houben and Gabaldon 2015). The impact of horizontal gene transfers (HGTs), although seemingly important in Pezizomycotina, is limited in Saccharomycotina, with only a few dozen reported events so far (Rolland et al 2009;Galeote et al 2010;Marcet-Houben and Gabaldon 2010;Wisecaver et al 2014;Marsit et al 2015).…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

et al. 2016

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Reconstructing genome history is complex but necessary to reveal quantitative principles governing genome evolution. Such reconstruction requires recapitulating into a single evolutionary framework the evolution of genome architecture and gene repertoire. Here, we reconstructed the genome history of the genus Lachancea that appeared to cover a continuous evolutionary range from closely related to more diverged yeast species. Our approach integrated the generation of a high-quality genome data set; the development of AnChro, a new algorithm for reconstructing ancestral genome architecture; and a comprehensive analysis of gene repertoire evolution. We found that the ancestral genome of the genus Lachancea contained eight chromosomes and about 5173 protein-coding genes. Moreover, we characterized 24 horizontal gene transfers and 159 putative gene creation events that punctuated species diversification. We retraced all chromosomal rearrangements, including gene losses, gene duplications, chromosomal inversions and translocations at single gene resolution. Gene duplications outnumbered losses and balanced rearrangements with 1503, 929, and 423 events, respectively. Gene content variations between extant species are mainly driven by differential gene losses, while gene duplications remained globally constant in all lineages. Remarkably, we discovered that balanced chromosomal rearrangements could be responsible for up to 14% of all gene losses by disrupting genes at their breakpoints. Finally, we found that nonsynonymous substitutions reached fixation at a coordinated pace with chromosomal inversions, translocations, and duplications, but not deletions. Overall, we provide a granular view of genome evolution within an entire eukaryotic genus, linking gene content, chromosome rearrangements, and protein divergence into a single evolutionary framework.

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Beyond the Whole-Genome Duplication: Phylogenetic Evidence for an Ancient Interspecies Hybridization in the Baker's Yeast Lineage

Cited by 302 publications

References 64 publications

Fast and accurate statistical inference of phylogenetic networks using large-scale genomic sequence data

Fast and accurate statistical inference of phylogenetic networks using large-scale genomic sequence data

Kinetic partitioning during de novo septin filament assembly creates a critical G1 “window of opportunity” for mutant septin function

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

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