Experimental evolution of the model eukaryote Saccharomyces cerevisiae yields insight into the molecular mechanisms underlying adaptation

Voordeckers, Karin; Verstrepen, Kevin J.

doi:10.1016/j.mib.2015.06.018

Cited by 33 publications

(27 citation statements)

References 74 publications

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“…We hypothesized that changes in the regulation of FLO1 cause the flocculation phenotype in nearly all of the evolved clones, and that deleting FLO1 would be a promising route for slowing the evolution of flocculation. Deleting a combination of FLO genes has been previously employed as a method to try to make laboratory strains easier to work with over long-term experimental evolution (Voordeckers and Verstrepen 2015), and modification of the FLO1 promoter has been effectively employed in biological circuits controlling flocculation (Ellis et al 2009); however, it is unknown if specifically deleting FLO1 would be effective on its own. We constructed a flo1 strain, and evolved 32 chemostat vessels of wild type, concurrently with 32 chemostat vessels of the flo1 knockout strain, in glucose limited medium, for >250 generations.…”

Section: Resultsmentioning

confidence: 99%

Experimental Evolution Reveals Favored Adaptive Routes to Cell Aggregation in Yeast

Hope¹,

Amorosi²,

Miller

et al. 2017

Genetics

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Yeast flocculation is a community-building cell aggregation trait that is an important mechanism of stress resistance and a useful phenotype for brewers; however, it is also a nuisance in many industrial processes, in clinical settings, and in the laboratory. Chemostat-based evolution experiments are impaired by inadvertent selection for aggregation, which we observe in 35% of populations. These populations provide a testing ground for understanding the breadth of genetic mechanisms Saccharomyces cerevisiae uses to flocculate, and which of those mechanisms provide the biggest adaptive advantages. In this study, we employed experimental evolution as a tool to ask whether one or many routes to flocculation are favored, and to engineer a strain with reduced flocculation potential. Using a combination of whole genome sequencing and bulk segregant analysis, we identified causal mutations in 23 independent clones that had evolved cell aggregation during hundreds of generations of chemostat growth. In 12 of those clones, we identified a transposable element insertion in the promoter region of known flocculation gene FLO1, and, in an additional five clones, we recovered loss-of-function mutations in transcriptional repressor TUP1, which regulates FLO1 and other related genes. Other causal mutations were found in genes that have not been previously connected to flocculation. Evolving a flo1 deletion strain revealed that this single deletion reduces flocculation occurrences to 3%, and demonstrated the efficacy of using experimental evolution as a tool to identify and eliminate the primary adaptive routes for undesirable traits.

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Section: Resultsmentioning

confidence: 99%

Experimental Evolution Reveals Favored Adaptive Routes to Cell Aggregation in Yeast

Hope¹,

Amorosi²,

Miller

et al. 2017

Genetics

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“…Indeed, CCNV offers a fast way to modify gene copy number during natural evolution of eukaryotes and to increase evolvability by allowing neofunctionalization of amplified essential genes (51, 94–96). Under selective conditions, mutants with CCNV will outgrow the parental population whenever positive effects of CCNV on fitness outweigh any negative impacts of AASR, while further mutations that enhance positive effects or decrease AASR can further increase the initial fitness benefit.…”

Section: Ccnv In Evolutionary Engineeringmentioning

confidence: 99%

Industrial Relevance of Chromosomal Copy Number Variation in Saccharomyces Yeasts

Vries

Pronk

Daran

2017

Appl Environ Microbiol

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Chromosomal copy number variation (CCNV) plays a key role in evolution and health of eukaryotes. The unicellular yeast Saccharomyces cerevisiae is an important model for studying the generation, physiological impact, and evolutionary significance of CCNV. Fundamental studies of this yeast have contributed to an extensive set of methods for analyzing and introducing CCNV. Moreover, these studies provided insight into the balance between negative and positive impacts of CCNV in evolutionary contexts. A growing body of evidence indicates that CCNV not only frequently occurs in industrial strains of Saccharomyces yeasts but also is a key contributor to the diversity of industrially relevant traits. This notion is further supported by the frequent involvement of CCNV in industrially relevant traits acquired during evolutionary engineering. This review describes recent developments in genome sequencing and genome editing techniques and discusses how these offer opportunities to unravel contributions of CCNV in industrial Saccharomyces strains as well as to rationally engineer yeast chromosomal copy numbers and karyotypes.

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“…However, these approaches are limited to identifying only a subset of high frequency and easy to sequence mutations. Moreover, separating the adaptive mutations from those that are merely hitchhiking remains a challenge (Voordeckers and Verstrepen, 2015). For example, in many studies the sequenced clones were isolated after hundreds or thousands of generations to ensure the presence of adaptive mutations, resulting in multiple mutations per clone (Barrick et al, 2009; Kryazhimskiy et al, 2014; Tenaillon et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Development of a Comprehensive Genotype-to-Fitness Map of Adaptation-Driving Mutations in Yeast

Venkataram

Dunn

et al. 2016

Cell

228

449

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Summary Adaptive evolution plays a large role in generating the phenotypic diversity observed in nature, yet current methods are impractical for characterizing the molecular basis and fitness effects of large numbers of individual adaptive mutations. Here we used a DNA barcoding approach to generate the genotype-to-fitness map for adaptation-driving mutations from a Saccharomyces cerevisiae population experimentally evolved by serial transfer under limiting glucose. We isolated and measured the fitness of thousands of independent adaptive clones, and sequenced the genomes of hundreds of clones. We found only two major classes of adaptive mutations: self-diploidization, and mutations in the nutrient-responsive Ras/PKA and TOR/Sch9 pathways. Our large sample size and precision of measurement allowed us to determine that there are significant differences in fitness between mutations in different genes, between different paralogs, and even between different classes of mutations within the same gene.

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Experimental evolution of the model eukaryote Saccharomyces cerevisiae yields insight into the molecular mechanisms underlying adaptation

Cited by 33 publications

References 74 publications

Experimental Evolution Reveals Favored Adaptive Routes to Cell Aggregation in Yeast

Experimental Evolution Reveals Favored Adaptive Routes to Cell Aggregation in Yeast

Industrial Relevance of Chromosomal Copy Number Variation in Saccharomyces Yeasts

Development of a Comprehensive Genotype-to-Fitness Map of Adaptation-Driving Mutations in Yeast

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