Differential Gene Expression and Allele Frequency Changes Favour Adaptation of a Heterogeneous Yeast Population to Nitrogen-Limited Fermentations

Kessi-Pérez, Eduardo I.; Ponce, Belén; Li, Jing; Molinet, Jennifer; Baeza, Camila; Figueroa, David J.; Bastías, Camila; Gaete, Marco; Liti, Gianni; Díaz‐Barrera, Alvaro; Salinas, F.; Martı́nez, Claudio

doi:10.3389/fmicb.2020.01204

Cited by 4 publications

(5 citation statements)

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“…Using the parameters obtained from the microculture growth curves as phenotypic information, we mapped 109 genetic variants by GWAS (Additional file 1: Table S2 and Additional file 2: Figures S14 – S16 ). Interestingly, several genetic variants are found in the coding and/or regulatory regions of genes mapped for adaptation to nitrogen limitation in a previous work of our group [ 30 ]: USE1 and ECM38 , which were previously identified by QTL mapping; MHO1 , which showed de novo mutations; RRT5 , OPT2 , ECM38 , ADY3 and CDA1 , whose transcription was upregulated in SM60 compared to SM300; and ATR1 and RPL42A , whose transcription was downregulated in SM60 compared to SM300. In the present work, we found several genetic variants that fall within autonomously replicating sequences (ARSs) (sv9386, sv43187, sv57282, sv65176, sv73285, sv73286, sv78694), or close to an ARS (sv50798) or a tRNA (sv56522, sv56526).…”

Section: Discussionmentioning

confidence: 95%

“…In principle, it can be expected that domesticated yeast strains are better adapted than wild ones to nitrogen limitation due to their use in that condition. However, recent evidence points in the opposite direction, given the scarcity of nitrogen sources that wild yeast strains have to face in natural environments, and therefore the need for these strains to adapt to this limitation [ 30 , 38 ]. The results show that domesticated yeast strains have higher values of efficiency, rate and AUC, but, interestingly, wild yeast strains show a lower value of lag (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…In the last decades, QTL (Quantitative Trait Loci) mapping has been the main experimental approximation to fill the gap between genotype and phenotype in yeast, being widely used to map the causatives genes that affect phenotypes such as thermotolerance, chemical resistance, translation termination, and production/consumption of metabolites during alcoholic fermentation, among many others [ 17 – 30 ]. However, other strategies like GWAS (Genome-Wide Association Studies), which has been successfully applied in human populations for the detection of disease-associated risk genetic variants, have rarely been used in yeast.…”

Section: Introductionmentioning

confidence: 99%

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Single nucleotide polymorphisms associated with wine fermentation and adaptation to nitrogen limitation in wild and domesticated yeast strains

et al. 2023

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For more than 20 years, Saccharomyces cerevisiae has served as a model organism for genetic studies and molecular biology, as well as a platform for biotechnology (e.g., wine production). One of the important ecological niches of this yeast that has been extensively studied is wine fermentation, a complex microbiological process in which S. cerevisiae faces various stresses such as limited availability of nitrogen. Nitrogen deficiencies in grape juice impair fermentation rate and yeast biomass production, leading to sluggish or stuck fermentations, resulting in considerable economic losses for the wine industry. In the present work, we took advantage of the “1002 Yeast Genomes Project” population, the most complete catalogue of the genetic variation in the species and a powerful resource for genotype-phenotype correlations, to study the adaptation to nitrogen limitation in wild and domesticated yeast strains in the context of wine fermentation. We found that wild and domesticated yeast strains have different adaptations to nitrogen limitation, corroborating their different evolutionary trajectories. Using a combination of state-of-the-art bioinformatic (GWAS) and molecular biology (CRISPR-Cas9) methodologies, we validated that PNP1, RRT5 and PDR12 are implicated in wine fermentation, where RRT5 and PDR12 are also involved in yeast adaptation to nitrogen limitation. In addition, we validated SNPs in these genes leading to differences in fermentative capacities and adaptation to nitrogen limitation. Altogether, the mapped genetic variants have potential applications for the genetic improvement of industrial yeast strains.

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Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Single nucleotide polymorphisms associated with wine fermentation and adaptation to nitrogen limitation in wild and domesticated yeast strains

et al. 2023

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“…For example, low levels of yeast assimilable nitrogen (below 140 mg/L) in grape must are the primary source of sluggish or stuck fermentations ( Gobert et al, 2019 ; Kessi-Pérez et al, 2020a ). In this context, recent studies have demonstrated that alleles from a wild S. cerevisiae strain might play a decisive role in the adaptation to low nitrogen concentrations ( Molinet et al, 2019 ; Kessi-Pérez et al, 2020a , b ). SAP185 , TOR2 , SCH9 , and NPR1 alleles derived from an oak strain increased amino acid consumption (aspartic acid, histidine, glutamine, and threonine) compared to wine alleles under wine fermentation conditions ( Molinet et al, 2019 ).…”

Section: Wild S Cerevisiae Strains: Genetic Stockmentioning

confidence: 99%

Wild Yeast for the Future: Exploring the Use of Wild Strains for Wine and Beer Fermentation

Molinet

Cubillos

2020

Front. Genet.

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The continuous usage of single Saccharomyces cerevisiae strains as starter cultures in fermentation led to the domestication and propagation of highly specialized strains in fermentation, resulting in the standardization of wines and beers. In this way, hundreds of commercial strains have been developed to satisfy producers' and consumers' demands, including beverages with high/low ethanol content, nutrient deprivation tolerance, diverse aromatic profiles, and fast fermentations. However, studies in the last 20 years have demonstrated that the genetic and phenotypic diversity in commercial S. cerevisiae strains is low. This lack of diversity limits alternative wines and beers, stressing the need to explore new genetic resources to differentiate each fermentation product. In this sense, wild strains harbor a higher than thought genetic and phenotypic diversity, representing a feasible option to generate new fermentative beverages. Numerous recent studies have identified alleles in wild strains that could favor phenotypes of interest, such as nitrogen consumption, tolerance to cold or high temperatures, and the production of metabolites, such as glycerol and aroma compounds. Here, we review the recent literature on the use of commercial and wild S. cerevisiae strains in wine and beer fermentation, providing molecular evidence of the advantages of using wild strains for the generation of improved genetic stocks for the industry according to the product style.

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“…Biotechnology and genetic engineering, once again, come to the rescue in this matter. In selection experiments in which SGRP-4X population was employed (four strains of yeast lineages—North American, Sake, West African and Wine European—were outcrossed for 12 generations giving rise to the SGRP-4X population, ~10–100 million random segregants) the ECM38 allele from the North American strain was detected as the effector of the best growth rate when nitrogen-limited conditions were used [ 120 ]. The TORC1 pathway has been seen to act as the main mechanism in nitrogen-limiting adaptation (amongst other genetic elements), which situates the genes involved as interesting targets for modifications to this end [ 118 , 121 , 122 , 123 , 124 , 125 ].…”

Section: Other Oenological Traitsmentioning

confidence: 99%

Next Generation Winemakers: Genetic Engineering in Saccharomyces cerevisiae for Trendy Challenges

Molina‐Espeja

2020

Bioengineering

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The most famous yeast of all times, Saccharomyces cerevisiae, has been used by humankind for at least 8000 years, to produce bread, beer and wine, even without knowing about its existence. Only in the last century we have been fully aware of the amazing power of this yeast not only for ancient uses but also for biotechnology purposes. In the last decades, wine culture is becoming more and more demanding all over the world. By applying a powerful biotechnological tool as genetic engineering in S. cerevisiae, new horizons appear to develop fresh, improved or modified wine characteristics, properties, flavors, fragrances or production processes, to fulfill an increasingly sophisticated market that moves around 31.4 billion € per year.

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Differential Gene Expression and Allele Frequency Changes Favour Adaptation of a Heterogeneous Yeast Population to Nitrogen-Limited Fermentations

Cited by 4 publications

References 83 publications

Single nucleotide polymorphisms associated with wine fermentation and adaptation to nitrogen limitation in wild and domesticated yeast strains

Single nucleotide polymorphisms associated with wine fermentation and adaptation to nitrogen limitation in wild and domesticated yeast strains

Wild Yeast for the Future: Exploring the Use of Wild Strains for Wine and Beer Fermentation

Next Generation Winemakers: Genetic Engineering in Saccharomyces cerevisiae for Trendy Challenges

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