Phased polyploid genomes provide deeper insight into the multiple origins of domesticated Saccharomyces cerevisiae beer yeasts

Saada, Omar Abou; Tsouris, Andreas; Large, Christopher R. L.; Friedrich, Anne; Dunham, Maitreya J.; Schacherer, Joseph

doi:10.1016/j.cub.2022.01.068

Cited by 22 publications

(22 citation statements)

References 38 publications

(77 reference statements)

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“…Finally, it should also be noted that in Kluyveromyces lactis, no real variability in terms of ploidy was observed, and aneuploidies and CNVs are not predominant. This observation contrasts with other yeast species that have undergone domestication processes, in particular with Kluyveromyces marxianus, for which ploidy variation separates the dairy and non-dairy strains (Ortiz-Merino et al, 2018), but also S. cerevisiae for which some domesticated populations, such as the beer isolates, have been described as having a higher ploidy level Saada et al, 2022).…”

Section: Discussioncontrasting

confidence: 72%

“…Indeed, the exploration of thousands of complete genomes over the past decade provide evidence for various independent and lineage-specific domestication events within this species, leading to different evolutionary trajectories (Duan et al, 2018; Gallone et al, 2016; Peter et al, 2018; Strope et al, 2015). The beer and bakery populations have been shown to be polyphyletic and diverse at the nucleotide and ploidy level, for example (Bigey et al, 2021; Gallone et al, 2016; Peter, De Chiara, et al, 2018; Saada et al, 2022). In contrast, the wine and sake populations are monophyletic and much less genetically diverse.…”

Section: Introductionmentioning

confidence: 99%

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Contrasting genomic evolution between domesticated and wild Kluyveromyces lactis yeast populations

Friedrich

Gounot

Tsouris

et al. 2022

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The process of domestication has variable consequences on genome evolution leading to different phenotypic signatures. Access to the complete genome sequences of a large number of individuals makes it possible to explore the different facets of this domestication process. Here, we sought to explore the genome evolution of the Kluyveromyces lactis yeast species, a well-known species for its involvement in dairy processes but also present in natural environments. Using a combination of short and long-read sequencing strategies, we investigated the genomic variability of 41 Kluyveromyces lactis isolates and found that the overall genetic diversity of this species is very high (π = 2.9 x 10-2) compared to other species such as Saccharomyces cerevisiae (π = 3 x 10-3). However, the domesticated dairy population shows a reduced level of diversity (π = 7 x 10-4), probably due to a domestication bottleneck. In addition, this entire population is characterized by the introgression of the LAC4 and LAC12 genes, responsible for lactose fermentation and coming from the closely related species, Kluyveromyces marxianus, as previously described. Our results also highlighted that the LAC4/LAC12 gene cluster was acquired through multiple and independent introgression events. Finally, we also identified several genes that could play a role in adaptation to dairy environments through copy number variation. These genes are involved in sugar consumption, flocculation and drug resistance, and may play a role in dairy processes. Overall, our study illustrates contrasting genomic evolution and sheds new light on the impact of domestication processes on it.

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Section: Discussioncontrasting

confidence: 72%

Section: Introductionmentioning

confidence: 99%

Contrasting genomic evolution between domesticated and wild Kluyveromyces lactis yeast populations

Friedrich

Gounot

Tsouris

et al. 2022

Preprint

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“…1g, Additional file 2: Table S2 and S3) [24]. These eight different organisms are Arabidopsis thaliana [25,26], Caenorhabditis elegans [27], Gallus gallus (chicken), Drosophila melanogaster [28], Mus musculus (mouse) [29,30], Saccharomyces cerevisiae [31], Schizosaccharomyces pombe, and Danio rerio (zebrafish) [32,33] which are all widely studied and have high-quality reference genomes. At the telomeres, these organisms are known to have (TTA GGG ) n telomeric repeats as humans do (chicken, zebrafish, mouse) [34][35][36], (TTT AGG G) n repeats (A. thaliana) [37], (TG 1-3 ) n repeats (S. cerevisiae) [38], TTAC(A)(C)G 2-8 (S. pombe) [39], (TTA GGC ) n repeats (C. elegans) [40], or retrotransposons (D. melanogaster) [41] (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…A full list of the datasets used in this study is as indicated in Additional file 2: Table S2. Specifically, runs for each of the following organisms were analyzed: A. thaliana (SRR14474199, SRR16149191) [25,26], C. elegans (SRR15993157, SRR16936857) [27], Chicken (SRR15420785, SRR15420786, SRR15420787, SRR15421342 to SRR15421346), D. melanogaster (SRR15107931 to SRR15107934, SRR15107937) [28], Mouse (SRR11606870, SRR14685232, SRR14685224 to SRR14685243) [29,30], S. cerevisiae (ERR6318522, ERR6318523) [31], S. pombe (SRR17382753, SRR18210325), and Zebrafish (SRR17257555, SRR15037325) [32,33].…”

Section: Evaluation Of Repeat Calling Errors In Model Organismsmentioning

confidence: 99%

Identifying and correcting repeat-calling errors in nanopore sequencing of telomeres

et al. 2022

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Nanopore long-read sequencing is an emerging approach for studying genomes, including long repetitive elements like telomeres. Here, we report extensive basecalling induced errors at telomere repeats across nanopore datasets, sequencing platforms, basecallers, and basecalling models. We find that telomeres in many organisms are frequently miscalled. We demonstrate that tuning of nanopore basecalling models leads to improved recovery and analysis of telomeric regions, with minimal negative impact on other genomic regions. We highlight the importance of verifying nanopore basecalls in long, repetitive, and poorly defined regions, and showcase how artefacts can be resolved by improvements in nanopore basecalling models.

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“…No survey has focused on LOH accumulation and its potential variability in natural isolates showing different ploidy levels. Natural S. cerevisiae isolates are mainly diploid, but polyploid isolates (3-5n) are frequent and enriched in specific subpopulations such as the beer clade (Gallone et al, 2016; Saada et al, 2022). In addition, other yeast species (such as C. neoformans and C. albicans ) are predominantly polyploids and LOH events are widespread (up to 20% of the genome) (Abbey et al, 2014; Feldmesser et al, 2000; Mba et al, 2022; Selmecki et al, 2010; Smith and Hickman, 2020).…”

Section: Introductionmentioning

confidence: 99%

Loss of heterozygosity spectrum varies with ploidy levels in natural yeast populations

Dutta

Dutreux

Schacherer

2022

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The appearance of genomic variations such as loss of heterozygosity (LOH) has a significant impact on phenotypic diversity observed in a population. Recent large-scale yeast population genomic surveys have shown a high frequency of these events in natural isolates and more particularly in polyploids. However, the frequency, extent, and spectrum of LOH in polyploid organisms have never been explored and is poorly characterized to date. Here, we accumulated 5,163 LOH events over 1,875 generations in 76 mutation accumulation (MA) lines comprising nine natural heterozygous diploid, triploid, and tetraploid natural S. cerevisiae isolates from different ecological and geographical origins. We found that the rate and spectrum of LOH are variable across ploidy levels. Of the total accumulated LOH events, 8.5%, 21%, and 70.5% of them were found in diploid, triploid, and tetraploid MA lines, respectively. Our results clearly shows that the frequency of generated LOH events increases with ploidy level. In fact, the cumulative LOH rates were estimated to be 9.3 x 10-3, 2.2 x 10-2, and 8.4 x 10-2 events per division for diploids, triploids, and tetraploids, respectively. In addition, a clear bias towards the accumulation of interstitial and short LOH tracts is observed in triploids and tetraploids compared to diploids. The variation of the frequency and spectrum of LOH events across ploidy level could be related to the genomic instability, characterizing higher ploidy isolates.

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Phased polyploid genomes provide deeper insight into the multiple origins of domesticated Saccharomyces cerevisiae beer yeasts

Cited by 22 publications

References 38 publications

Contrasting genomic evolution between domesticated and wild Kluyveromyces lactis yeast populations

Contrasting genomic evolution between domesticated and wild Kluyveromyces lactis yeast populations

Identifying and correcting repeat-calling errors in nanopore sequencing of telomeres

Loss of heterozygosity spectrum varies with ploidy levels in natural yeast populations

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