Impact of combined wine-related stressors on Saccharomyces cerevisiae and mapping of the associated QTLs

Jiao Jiang , Hongfei Yu , Xingmeng Lei , Hanyu Yang , Dongqing Ye , Jin Zhang , Yuyang Song , Yi Qin , & Yanlin Liu

Food Innovation and Advances ›› 2025, Vol. 4 ›› Issue (3) : 342 -351.

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Food Innovation and Advances ›› 2025, Vol. 4 ›› Issue (3) : 342 -351. DOI: 10.48130/fia-0025-0032
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Impact of combined wine-related stressors on Saccharomyces cerevisiae and mapping of the associated QTLs

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Abstract

Ethanol, hyperosmotic stress, and certain levels of SO2 are the main abiotic factors inhibiting the survival of Saccharomyces cerevisiae during winemaking, but how combinations of these stressors impact yeast growth and the underlying genetic basis are not well studied. To illustrate these questions, ten randomly selected Chinese indigenous haploid S. cerevisiae were first evaluated for multi-stressor tolerance using a three-factor, three-level orthogonal test. Great variation in growth was observed in a medium containing 6% v/v ethanol, 300 mg/L SO2, and hyperosmotic stress equivalent to 200 g/L fructose. One hundred and eighteen haploids were further tested under the mentioned stress levels. Their growth shared common features of quantitative traits, which indicates the underlying mechanism can be investigated by quantitative trait locus (QTL) mapping. The parental haploids with opposite tolerance to the combined stressors were selected to generate the F1 hybrid and F2 segregants. Further characterization of the F2 population allowed the assembly of two pools, each composed of 15 individuals showing divergent tolerance to the multi-stressor. The associated major QTLs were mapped by genome-wide comparison of single-nucleotide polymorphism profiles between the two pools. Two regions located on Chromosomes III and XIV were identified to be associated with the multi-stressor tolerance. Based on GO and KEGG enrichment analysis, seven genes involved in nucleotide binding, methylation, and sterol synthesis were finally selected as potential quantitative trait genes that play a role in supporting yeast growth under the multi-stressor. The findings of this study expand current knowledge on the genetic determinants of variation in yeast tolerance to combined ethanol-hyperosmotic-SO2 stressors.

Keywords

Saccharomyces cerevisiae / Ethanol-hyperosmotic-SO2 stressors / Stress tolerance / Bulk segregant analysis / Quantitative trait loci

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Jiao Jiang, Hongfei Yu, Xingmeng Lei, Hanyu Yang, Dongqing Ye, Jin Zhang, Yuyang Song, Yi Qin, & Yanlin Liu. Impact of combined wine-related stressors on Saccharomyces cerevisiae and mapping of the associated QTLs. Food Innovation and Advances, 2025, 4(3): 342-351 DOI:10.48130/fia-0025-0032

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Author contributions

The authors confirm their contributions to the paper as follows: study conception and design: Jiang J, Yu H, Lei X; data collection: Jiang J, Yu H, Lei X, Yang H; analysis and interpretation of results: Jiang J, Yu H, Lei X, Yang H; writing - draft manuscript preparation: Jiang J, Yu H, Ye D; supervision: Liu Y, Qin Y, Jiang J; writing - review and editing: Jiang J, Yu H, Liu Y, Zhang J, Qin Y, Song Y. All authors reviewed the results and approved the final version of the manuscript.

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Acknowledgments

We extend our thanks to the College of Enology at Northwest A&F University. This work was financially supported by Ningxia Hui Autonomous Region Key R&D Project (Grant No. 2023BCF01027), the National Natural Science Foundation of China (Grant Nos U21A20269, 32372312, 32402163), the National Foreign Expert Program of China(Grant No. G2022172022L), Northwest A&F University (Grant No.Z2220221027), and the earmarked fund for CARS (CARS-29-jg-3)

Conflict of interest

The authors declare that they have no conflict of interest.

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References

[1]

Monnin L, Nidelet T, Noble J, Galeote V. 2024. Insights into intraspecific diversity of central carbon metabolites in Saccharomyces cerevisiae during wine fermentation. Food Microbiology 121:104513

[2]

Qiu F, Du B, Zhang C, Zhu L, Yan Y, et al. 2024. Effects of Saccharomyces cerevisiae on microbial community and flavor metabolites in solid-state fermentation of strong-flavor Baijiu. Food Bioscience 59:103925

[3]

Vion C, Muro M, Bernard M, Richard B, Valentine F, et al. 2023. New malic acid producer strains of Saccharomyces cerevisiae for preserving wine acidity during alcoholic fermentation. Food Microbiology 112:104209

[4]

Du Q, Ye D, Zang X, Nan H, Liu Y. 2022. Effect of low temperature on the shaping of yeast-derived metabolite compositions during wine fermentation. Food Research International 162:112016

[5]

van Leeuwen C, Sgubin G, Bois B, Ollat N, Swingedouw D, et al. 2024. Climate change impacts and adaptations of wine production. Nature Reviews Earth & Environment 5:258-75

[6]

Rogiers SY, Greer DH, Liu Y, Baby T, Xiao Z. 2022. Impact of climate change on grape berry ripening: an assessment of adaptation strategies for the Australian vineyard. Frontiers in Plant Science 13:1094633

[7]

Samakkarn W, Ratanakhanokchai K, Soontorngun N. 2021. Reprogramming of the ethanol stress response in Saccharomyces cerevisiae by the transcription factor Znf1 and its effect on the biosynthesis of glycerol and ethanol. Applied and Environmental Microbiology 87:e0058821

[8]

Rodrigues JA, Nunes C, Coimbra MA, Goodfellow BJ, Gil AM. 2022. Chitosan film as a replacement for conventional sulphur dioxide treatment of white wines: a 1H NMR metabolomic study. Foods 11:3428

[9]

Koyama H, Kamiya K, Sasaki Y, Yamakawa R, Kuniyoshi H, et al. 2023. Cloning of glutamine synthetase gene from abdominal muscle of kuruma shrimp Marsupenaeus japonicus and its expression profile. Fisheries Science 89:215-22

[10]

Yu J, Gai Z, Cheng J, Tian F, Du K, et al. 2023. Construction of beta-cyclodextrin modified holographic sensor for the determination of ibuprofen in plasma and urine. Sensors and Actuators B: Chemical 385:133650

[11]

de Nadal E, Posas F. 2022. The HOG pathway and the regulation of osmoadaptive responses in yeast. FEMS Yeast Research 22:foac013

[12]

Ding J, Huang X, Zhang L, Zhao N, Yang D, et al. 2009. Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Applied Microbiology and Biotechnology 85:253-63

[13]

Yoshida M, Kato S, Fukuda S, Izawa S. 2021. Acquired resistance to severe ethanol stress in Saccharomyces cerevisiae protein quality control. Applied and Environmental Microbiology 87:e02353-20

[14]

Li R, Miao Y, Yuan S, Li Y, Wu Z, et al. 2019. Integrated transcriptomic and proteomic analysis of the ethanol stress response in Saccharomyces cerevisiae Sc131. Journal of Proteomics 203:103377

[15]

Xiao C, Pan Y, Huang M. 2023. Advances in the dynamic control of metabolic pathways in Saccharomyces cerevisiae. Engineering Microbiology 3:100103

[16]

Li R, Xiong G, Yuan S, Wu Z, Miao Y, Weng P. 2017. Investigating the underlying mechanism of Saccharomyces cerevisiae in response to ethanol stress employing RNA-seq analysis. World Journal of Microbiology and Biotechnology 33:206

[17]

Soufi B, Kelstrup CD, Stoehr G, Fröhlich F, Walther TC, et al. 2009. Global analysis of the yeast osmotic stress response by quantitative proteomics. Molecular BioSystems 5:1337-46

[18]

Lage P, Sampaio-Marques B, Ludovico P, Mira NP, Mendes-Ferreira A. 2019. Transcriptomic and chemogenomic analyses unveil the essential role of Com2-regulon in response and tolerance of Saccharomyces cerevisiae to stress induced by sulfur dioxide. Microbial Cell 6:509-23

[19]

Bartle L, Peltier E, Sundstrom JF, Sumby K, Mitchell JG, et al. 2021. QTL mapping: an innovative method for investigating the genetic determinism of yeast-bacteria interactions in wine. Applied Microbiology and Biotechnology 105:5053-66

[20]

Vion C, Peltier E, Bernard M, Muro M, Marullo P. 2021. Marker assisted selection of malic-consuming Saccharomyces cerevisiae strains for winemaking. Efficiency and limits of a QTL's driven breeding program. Journal of fungi 7:304

[21]

Feng L, Jia H, Qin Y, Song Y, Tao S, et al. 2018. Rapid identification of major QTL(S) associated with near-freezing temperature tolerance in Saccharomyces cerevisiae. Frontiers in Microbiology 9:2110

[22]

Valero E, Tronchoni J, Morales P, Gonzalez R. 2020. Autophagy is required for sulfur dioxide tolerance in Saccharomyces cerevisiae. Microbial Biotechnology 13:599-604

[23]

Mavrommati M, Papanikolaou S, Aggelis G. 2023. Improving ethanol tolerance of Saccharomyces cerevisiae through adaptive laboratory evolution using high ethanol concentrations as a selective pressure. Process Biochemistry 124:280-89

[24]

Choi B, Tafur Rangel A, Kerkhoven EJ, Nygård Y. 2024. Engineering of Saccharomyces cerevisiae for enhanced metabolic robustness and L-lactic acid production from lignocellulosic biomass. Metabolic engineering 84:23-33

[25]

Zwietering MH, Jongenburger I, Rombouts FM, van't Riet K. 1990. Modeling of the bacterial growth curve. Applied and Environmental Microbiology 56:1875-81

[26]

Kodama T, Hisatomi T, Uchida K, Yamaki T, Tsuboi M. 2003. Isolation and characterization of the HO gene from the yeast Saccharomyces paradoxus. FEMS Yeast Research 4:51-57

[27]

Feng L, Wang J, Ye D, Song Y, Qin Y, et al. 2020. Yeast population dynamics during spontaneous fermentation of icewine and selection of indigenous Saccharomyces cerevisiae strains for the winemaking in Qilian, China. Journal of the Science of Food and Agriculture 100:5385-94

[28]

Huxley MN. 1990. Exponential sums and lattice points. Proceedings of the London Mathematical Society s3-60:471-502

[29]

Parts L, Stegle O, Winn J, Durbin R. 2011. Joint genetic analysis of gene expression data with inferred cellular phenotypes. PLoS Genetics 7:e1001276

[30]

Mohammed YMM, Mabrouk MEM. 2020. Optimization of methylene blue degradation by Aspergillus terreus YESM 3 using response surface methodology. Water Science and Technology 82:2007-18

[31]

Wang M, Yin Z, Yan L, Yang Y, Zhu F, et al. 2024. RabbitTrim: highly optimized trimming of illumina sequencing data on multi-core platforms. In Bioinformatics Research and Applications. Lecture Notes in Computer Science, eds, Peng W, Cai Z, Skums P. Singapore: Springer. pp. 26-37. doi: 10.1007/978-981-97-5131-0_3

[32]

Shashikant T, Ettensohn CA. 2019. Genome-wide analysis of chromatin accessibility using ATAC-seq. Methods in Cell Biology 151:219-35

[33]

Tristão LE, de Sousa LIS, de Oliveira Vargas B, José J, Carazzolle MF, et al. 2024. Unveiling genetic anchors in Saccharomyces cerevisiae: QTL mapping identifies IRA 2 as a key player in ethanol tolerance and beyond. Molecular Genetics and Genomics 299:103

[34]

Guo X, Chen F, Gao F, Li L, Liu K, et al. 2020. CNSA: a data repository for archiving omics data. Database 2020:baaa055

[35]

Chen FZ, You LJ, Yang F, Wang LN, Guo XQ, et al. 2020. CNGBdb: China National GeneBank DataBase. Hereditas 42:799-809

[36]

Kessi-Pérez EI, Acuña E, Bastías C, Fundora L, Villalobos-Cid M, et al. 2023. Single nucleotide polymorphisms associated with wine fermentation and adaptation to nitrogen limitation in wild and domesticated yeast strains. Biological Research 56:43

[37]

Riles L, Fay JC. 2019. Genetic Basis of Variation in Heat and Ethanol Tolerance in Saccharomyces cerevisiae. G3 Genes|Genomes|Genetics 9:179-88

[38]

McCorkle CM, Nolan MF, Jamtgaard K, Gilles JL. 1989. Social research in international agricultural R&D: Lessons from the small ruminant CRSP. Agriculture and Human Values 6:42-51

[39]

Milani EA, Gardner RC, Silva FVM. 2015. Thermal resistance of Saccharomyces yeast ascospores in beers. International Journal of Food Microbiology 206:75-80

[40]

Bordet F, Romanet R, Eicher C, Grandvalet C, Klein G, et al. 2022. eGFP gene integration in HO: a metabolomic impact? Microorganisms 10:781

[41]

Win KT, Vegas J, Zhang C, Song K, Lee S. 2017. QTL mapping for downy mildew resistance in cucumber via bulked segregant analysis using next-generation sequencing and conventional methods. Theoretical and Applied Genetics 130:199-211

[42]

Huang L, Tang W, Wu W. 2022. Optimization of BSA-seq experiment for QTL mapping. G3 Genes|Genomes|Genetics 12 :jkab370

[43]

Wang X, Wang G. 2023. Application of NGS-BSA and proposal of Modified QTL-seq. Journal of Plant Biochemistry and Biotechnology 32:31-9

[44]

Greenwood BL, Luo Z, Ahmed T, Huang D, Stuart DT. 2023. Saccharomyces cerevisiae Δ9-desaturase Ole1 forms a super complex with Slc1 and Dga1. Journal of Biological Chemistry 299:104882

[45]

Qi Y, Xu N, Li Z, Wang J, Meng X, et al. 2022. Mediator engineering of Saccharomyces cerevisiae to improve multidimensional stress tolerance. Applied and Environmental Microbiology 88:e0162721

[46]

Ravishankar A, Pupo A, Gallagher JEG. 2020. Resistance mechanisms of Saccharomyces cerevisiae to commercial formulations of glyphosate involve DNA damage repair, the cell cycle, and the cell wall structure. G3Genes| Genomes| Genetics 10:2043-56

[47]

Rojas M, Farr GW, Fernandez CF, Lauden L, McCormack JC, et al. 2012. Yeast Gis2 and its human ortholog CNBP are novel components of stress-induced RNP granules. PLoS One 7:e52824

[48]

Satoh R, Tanaka A, Kita A, Morita T, Matsumura Y, et al. 2012. Role of the RNA-binding protein Nrd 1 in stress granule formation and its implication in the stress response in fission yeast. PLoS One 7:e29683

[49]

Chaves-Arquero B, Pérez-Cañadillas JM. 2023. The Nrd1-Nab3-Sen1 transcription termination complex from a structural perspective. Biochemical Society Transactions 51:1257-69

[50]

Yuan B, Zhu YF, Li K, Zhao XQ. 2025. Chromatin regulation of acetic acid stress tolerance by Ino80 in budding yeast Saccharomyces cerevisiae. Journal of agricultural and food chemistry 73:2951-60

[51]

Ye PL, Yuan B, Wang XQ, Zhang MM, et al. 2023. Modification of phosphorylation sites in the yeast lysine methyltransferase Set5 exerts influences on the mitogen-activated protein kinase Hog1 under prolonged acetic acid stress. Microbiology Spectrum 11:e0301122

[52]

Burgos ES, Walters RO, Huffman DM, Shechter D. 2017. A simplified characterization of S-adenosyl-ʟ-methionine-consuming enzymes with 1-Step EZ-MTase: a universal and straightforward coupled-assay for in vitro and in vivo setting. Chemical Science 8:6601-12

[53]

Black JJ, Sardana R, Elmir EW, Johnson AW. 2020. Bud 23 promotes the final disassembly of the small subunit processome in Saccharomyces cerevisiae. PLoS Genetics 16:e1009215

[54]

Black JJ, Johnson AW. 2022. Release of the ribosome biogenesis factor Bud23 from small subunit precursors in yeast. RNA 28:371-89

[55]

Lieber MR. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annual Review of Biochemistry 79:181-211

[56]

Heyer WD, Ehmsen KT, Liu J. 2010. Regulation of homologous recombination in eukaryotes. Annual Review of Genetics 44:113-39

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