Whole-Genome Duplication and Yeast’s Fruitful Way of Life

Escalera‐Fanjul, Ximena; Quezada, Héctor; Riego-Ruíz, Lina; González, Alicia

doi:10.1016/j.tig.2018.09.008

Cited by 26 publications

(23 citation statements)

References 82 publications

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“…The diversification at the expression level could open up the possibility to diverge functionally, as the rate of evolution is highly linked to its expression, although recently it has been shown that low-expression transcription factors adapt through cooperation rather than functional divergence ( 34 , 63 ). It has been suggested that the whole-genome duplication even facilitated the Saccharomyces yeast to evolve the ability to ferment sugars under anaerobic conditions, which is not the case for other yeasts (reviewed in references 64 to 66 ). Here, we are forcing the yeast to use ethanol as the sole carbon source, meaning it has to perform respiration instead for fermentation, not requiring the Crabtree effect-implicated genes.…”

Section: Discussionmentioning

confidence: 99%

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Transcriptional Rewiring, Adaptation, and the Role of Gene Duplication in the Metabolism of Ethanol of Saccharomyces cerevisiae

et al. 2020

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Ethanol is the main by-product of yeast sugar fermentation that affects microbial growth parameters, being considered a dual molecule, a nutrient and a stressor. Previous works demonstrated that the budding yeast arose after an ancient hybridization process resulted in a tier of duplicated genes within its genome, many of them with implications in this ethanol “produce-accumulate-consume” strategy. The evolutionary link between ethanol production, consumption, and tolerance versus ploidy and stability of the hybrids is an ongoing debatable issue. The implication of ancestral duplicates in this metabolic rewiring, and how these duplicates differ transcriptionally, remains unsolved. Here, we study the transcriptomic adaptive signatures to ethanol as a nonfermentative carbon source to sustain clonal yeast growth by experimental evolution, emphasizing the role of duplicated genes in the adaptive process. As expected, ethanol was able to sustain growth but at a lower rate than glucose. Our results demonstrate that in asexual populations a complete transcriptomic rewiring was produced, strikingly by downregulation of duplicated genes, mainly whole-genome duplicates, whereas small-scale duplicates exhibited significant transcriptional divergence between copies. Overall, this study contributes to the understanding of evolution after gene duplication, linking transcriptional divergence with duplicates’ fate in a multigene trait as ethanol tolerance. IMPORTANCE Gene duplication events have been related with increasing biological complexity through the tree of life, but also with illnesses, including cancer. Early evolutionary theories indicated that duplicated genes could explore alternative functions due to relaxation of selective constraints in one of the copies, as the other remains as ancestral-function backup. In unicellular eukaryotes like yeasts, it has been demonstrated that the fate and persistence of duplicates depend on duplication mechanism (whole-genome or small-scale events), shaping their actual genomes. Although it has been shown that small-scale duplicates tend to innovate and whole-genome duplicates specialize in ancestral functions, the implication of duplicates’ transcriptional plasticity and transcriptional divergence on environmental and metabolic responses remains largely obscure. Here, by experimental adaptive evolution, we show that Saccharomyces cerevisiae is able to respond to metabolic stress (ethanol as nonfermentative carbon source) due to the persistence of duplicated genes. These duplicates respond by transcriptional rewiring, depending on their transcriptional background. Our results shed light on the mechanisms that determine the role of duplicates, and on their evolvability.

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Section: Discussionmentioning

confidence: 99%

“…In plants, it has been observed that duplicated genes diverge transcriptionally soon after duplication ( 66 – 69 ). Furthermore, a correlation between the divergence from the ancestral expression level and stress response has also been observed in plants ( 70 ).…”

Section: Discussionmentioning

confidence: 99%

Transcriptional Rewiring, Adaptation, and the Role of Gene Duplication in the Metabolism of Ethanol of Saccharomyces cerevisiae

et al. 2020

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“…It is proposed that WGD is the result of autopolyploidization or hybridization. However, a hybridization model was recently proposed to explain this WGD (Marcet-Houben and Gabaldón 2015), since genetic rearrangements, gene losses and mutations following the hybridization WGD event lead to genome evolution and adaptation (Wolfe, 2015; Fisher et al, 2018; Escalera-Fanjul et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Mitogenomics and mitochondrial gene phylogeny decipher the evolution of Saccharomycotina yeasts

Christinaki

Kortsinoglou

et al. 2021

Preprint

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Saccharomycotina yeasts contain diverse clades within the kingdom of Fungi and are important to human everyday life. This work investigates the evolutionary relationships among these yeasts from a mitochondrial (mt) genomic perspective. A comparative study of 141 yeast mt genomes representing all major phylogenetic lineages of Saccharomycotina was performed, including genome size and content variability, intron and intergenic regions' diversity, genetic code alterations and syntenic variation. Findings from this study suggest that mt genome size diversity is the result of a ceaseless random process mainly based on genetic recombination and intron mobility. Gene order analysis revealed conserved syntenic units and many occurring rearrangements, which can be correlated with major evolutionary events as shown by the phylogenetic analysis of the concatenated mt protein matrix. For the first time, molecular dating indicated a slower mt genome divergence rate in the early stages of yeast evolution, in contrast with a faster rate in the late evolutionary stages, compared to their nuclear time divergence. Genetic code reassignments of mt genomes are a perpetual process happening in many different parallel evolutionary steps throughout Saccharomycotina evolution. Overall, this work shows that phylogenetic studies that employ the mt genome of yeasts highlight major evolutionary events.

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“…Overall it appeared that genomes behave as n-plications of a core set of sequences followed by reduction. This has been observed in yeasts (Escalera-Fanjul et al 2018) , plants (Clark and Donoghue 2018a) and animals (Hermansen et al 2016) .…”

Section: Probability That the Crispr-guide Rna Recognizes And Cuts Atmentioning

confidence: 61%

Evaluating the Probability of CRISPR-based Gene Drive Contaminating Another Species

Courtier‐Orgogozo

Danchin

Gouyon

et al. 2019

Preprint

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The probability D that a given CRISPR-based gene drive element contaminates another, non-target species can be estimated by the following Drive Risk Assessment Quantitative Estimate (DRAQUE) Equation: D = ( hyb+transf).express.cut.flank.immune.nonextinct with hyb = probability of hybridization between the target species and a non-target species transf = probability of horizontal transfer of a piece of DNA containing the gene drive cassette from the target species to a non-target species (with no hybridization) express = probability that the Cas9 and guide RNA genes are expressed cut = probability that the CRISPR-guide RNA recognizes and cuts at a DNA site in the new host flank = probability that the gene drive cassette inserts at the cut site immune = probability that the immune system does not reject Cas9 -expressing cells nonextinct = probability of invasion of the drive within the populationWe discuss and estimate each of the seven parameters of the equation, with particular emphasis on possible transfers within insects, and between rodents and humans. We conclude from current data that the probability of a gene drive cassette to contaminate another species is not insignificant. We propose strategies to reduce this risk and call for more work on estimating all the parameters of the formula.

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Whole-Genome Duplication and Yeast’s Fruitful Way of Life

Cited by 26 publications

References 82 publications

Transcriptional Rewiring, Adaptation, and the Role of Gene Duplication in the Metabolism of Ethanol of Saccharomyces cerevisiae

Transcriptional Rewiring, Adaptation, and the Role of Gene Duplication in the Metabolism of Ethanol of Saccharomyces cerevisiae

Mitogenomics and mitochondrial gene phylogeny decipher the evolution of Saccharomycotina yeasts

Evaluating the Probability of CRISPR-based Gene Drive Contaminating Another Species

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