Skip to main content
Log in

Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains

  • Genomics, transcriptomics, proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

An understanding of the genetic basis underlying the phenotypic variations of yeast strains would guide the breeding of this useful microorganism. Here, comparative functional genomics (CFG) of two bioethanol Saccharomyces cerevisiae strains (YJS329 and ZK2) with different stress tolerances and ethanol fermentation performances were performed. Our analysis indicated that different patterns of gene expression in the central carbon metabolism, antioxidative factors, and membrane compositions of these two strains are the main contributors to their various traits. Some of the differently expressed genes were directly caused by the genomic structural variations between YJS329 and ZK2. Moreover, CFG of these two strains also led to novel insights into the mechanism of stress tolerance in yeast. For example, it was found that more oleic acid in the plasma membrane contributes to the acetic acid tolerance of yeast. Based on the genetic information particular to each strain, strategies to improve their adaptability and ethanol fermentation performances were designed and confirmed. Thus, CFG could not only help reveal basis of phenotypic diversities but also guide the genetic breeding of industrial microorganisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akache B, Wu KQ, Turcotte B (2001) Phenotypic analysis of genes encoding yeast zinc cluster proteins. Nucleic Acids Res 29(10):2181–2190

    Article  CAS  Google Scholar 

  • Akao T, Yashiro I, Hosoyama A, Kitagaki H, Horikawa H, Watanabe D, Akada R, Ando Y, Harashima S, Inoue T, Inoue Y, Kajiwara S, Kitamoto K, Kitamoto N, Kobayashi O, Kuhara S, Masubuchi T, Mizoguchi H, Nakao Y, Nakazato A, Namise M, Oba T, Ogata T, Ohta A, Sato M, Shibasaki S, Takatsume Y, Tanimoto S, Tsuboi H, Nishimura A, Yoda K, Ishikawa T, Iwashita K, Fujita N, Shimoi H (2011) Whole-genome sequencing of sake yeast Saccharomyces cerevisiae kyokai no. 7. DNA Res 18(6):423–434

    Article  CAS  Google Scholar 

  • Anderson MJ, Barker SL, Boone C, Measday V (2012) Identification of RCN1 and RSA3 as ethanol-tolerant genes in Saccharomyces cerevisiae using a high copy barcoded library. FEMS Yeast Res 12(1):48–60

    Article  CAS  Google Scholar 

  • Argueso JL, Carazzolle MF, Mieczkowski PA, Duarte FM, Netto OV, Missawa SK, Galzerani F, Costa GG, Vidal RO, Noronha MF, Dominska M, Andrietta MG, Andrietta SR, Cunha AF, Gomes LH, Tavares FC, Alcarde AR, Dietrich FS, McCusker JH, Petes TD, Pereira GA (2009) Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production. Genome Res 19(12):2258–2270

    Article  CAS  Google Scholar 

  • Auesukaree C, Damnernsawad A, Kruatrachue M, Pokethitiyook P, Boonchird C, Kaneko Y, Harashima S (2009) Genome-wide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. J Appl Genet 50(3):301–310

    Article  CAS  Google Scholar 

  • Benjaphokee S, Hasegawa D, Yokota D, Asvarak T, Auesukaree C, Sugiyama M, Kaneko Y, Boonchird C, Harashima S (2012) Highly efficient bioethanol production by a Saccharomyces cerevisiae strain with multiple stress tolerance to high temperature, acid and ethanol. N Biotechnol 29(3):379–386

    Article  CAS  Google Scholar 

  • Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ (2011) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7(2):e1001287

    Article  CAS  Google Scholar 

  • Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12(2):323–337

    CAS  Google Scholar 

  • Dunn B, Richter C, Kvitek DJ, Pugh T, Sherlock G (2012) Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res 22(5):908–924

    Article  CAS  Google Scholar 

  • Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24(4):469–486

    Article  CAS  Google Scholar 

  • Fujita K, Matsuyama A, Kobayashi Y, Iwahashi H (2006) The genome-wide screening of yeast deletion mutants to identify the genes required for tolerance to ethanol and other alcohols. FEMS Yeast Res 6(5):744–750

    Article  CAS  Google Scholar 

  • Hirasawa T, Yamada K, Nagahisa K, Dinh TN, Furusawa C, Katakura Y, Shioya S, Shimizu H (2009) Proteomic analysis of responses to osmotic stress in laboratory and sake-brewing strains of Saccharomyces cerevisiae. Process Biochem 44(6):647–653

    Article  CAS  Google Scholar 

  • Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14(16):1511–1527

    Article  CAS  Google Scholar 

  • Kvitek DJ, Will JL, Gasch AP (2008) Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 4(10):e1000223

    Article  Google Scholar 

  • Landolfo S, Zara G, Zara S, Budroni M, Ciani M, Mannazzu I (2010) Oleic acid and ergosterol supplementation mitigates oxidative stress in wine strains of Saccharomyces cerevisiae. Int J Food Microbiol 141(3):229–235

    Article  CAS  Google Scholar 

  • Lewis JA, Elkon IM, McGee MA, Higbee AJ, Gasch AP (2010) Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics 186(4):1197–1205

    Article  CAS  Google Scholar 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25(15):1966–1967

    Article  CAS  Google Scholar 

  • Mahmud SA, Hirasawa T, Shimizu H (2010) Differential importance of trehalose accumulation in Saccharomyces cerevisiae in response to various environmental stresses. J Biosci Bioeng 109(3):262–266

    Article  CAS  Google Scholar 

  • Melamed D, Pnueli L, Arava Y (2008) Yeast translational response to high salinity: global analysis reveals regulation at multiple levels. RNA 14(7):1337–1351

    Article  CAS  Google Scholar 

  • Mira NP, Palma M, Guerreiro JF, Sa-Correia I (2010) Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microb Cell Factories 9:79

    Article  Google Scholar 

  • Mira NP, Henriques SF, Keller G, Teixeira MC, Matos RG, Arraiano CM, Winge DR, Sa-Correia I (2011) Identification of a DNA-binding site for the transcription factor Haa1, required for Saccharomyces cerevisiae response to acetic acid stress. Nucleic Acids Res 39(16):6896–6907

    Article  CAS  Google Scholar 

  • Mulford KE, Fassler JS (2011) Association of the Skn7 and Yap1 transcription factors in the Saccharomyces cerevisiae oxidative stress response. Eukaryot Cell 10(6):761–769

    Article  CAS  Google Scholar 

  • Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L, Sanderson BW, Hattem GL, Li R (2010) Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468(7321):321–325

    Article  CAS  Google Scholar 

  • Redón M, Guillamón JM, Mas A, Rozès N (2011) Effect of growth temperature on yeast lipid composition and alcoholic fermentation at low temperature. Eur Food Res Technol 232(3):517–527

    Article  Google Scholar 

  • Rossouw D, Olivares-Hernandes R, Nielsen J, Bauer FF (2009) Comparative transcriptomic approach to investigate differences in wine yeast physiology and metabolism during fermentation. Appl Environ Microbiol 75(20):6600–6612

    Article  CAS  Google Scholar 

  • Sanda T, Hasunuma T, Matsuda F, Kondo A (2011) Repeated-batch fermentation of lignocellulosic hydrolysate to ethanol using a hybrid Saccharomyces cerevisiae strain metabolically engineered for tolerance to acetic and formic acids. Bioresour Technol 102(17):7917–7924

    Article  CAS  Google Scholar 

  • Tao X, Zheng D, Liu T, Wang P, Zhao W, Zhu M, Jiang X, Zhao Y, Wu X (2012) A novel strategy to construct yeast Saccharomyces cerevisiae strains for very high gravity fermentation. PLoS One 7(2):e31235

    Article  CAS  Google Scholar 

  • Teixeira MC, Raposo LR, Mira NP, Lourenco AB, Sa-Correia I (2009) Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Appl Environ Microbiol 75(18):5761–5772

    Article  CAS  Google Scholar 

  • Teste MA, Duquenne M, François J, Parrou JL (2009) Validation of reference genes for quantitative expression analysis by real-time RT-PCR in Saccharomyces cerevisiae. BMC Mol Biol 10:99

    Article  Google Scholar 

  • Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, Amon A (2007) Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317(5840):916–924

    Article  CAS  Google Scholar 

  • Wang B, Guo G, Wang C, Lin Y, Wang X, Zhao M, Guo Y, He M, Zhang Y, Pan L (2010) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic Acids Res 38(15):5075–5087

    Article  CAS  Google Scholar 

  • Wang PM, Zheng DQ, Liu TZ, Tao XL, Feng MG, Min H, Jiang XH, Wu XC (2012) The combination of glycerol metabolic engineering and drug resistance marker-aided genome shuffling to improve very-high-gravity fermentation performances of industrial Saccharomyces cerevisiae. Bioresour Technol 108:203–210

    Article  Google Scholar 

  • Yang J, Bae JY, Lee YM, Kwon H, Moon HY, Kang HA, Yee S, Kim W, Choi W (2011) Construction of Saccharomyces cerevisiae strains with enhanced ethanol tolerance by mutagenesis of the TATA-binding protein gene and identification of novel genes associated with ethanol tolerance. Biotechnol Bioeng 108(8):1776–1787

    Article  CAS  Google Scholar 

  • Yazawa H, Kamisaka Y, Kimura K, Yamaoka M, Uemura H (2011) Efficient accumulation of oleic acid in Saccharomyces cerevisiae caused by expression of rat elongase 2 gene (rELO2) and its contribution to tolerance to alcohols. Appl Microbiol Biotechnol 91(6):1593–1600

    Article  CAS  Google Scholar 

  • You KM, Rosenfield CL, Knipple DC (2003) Ethanol tolerance in the yeast Saccharomyces cerevisiae is dependent on cellular oleic acid content. Appl Environ Microbiol 69(3):1499–1503

    Article  CAS  Google Scholar 

  • Zheng DQ, Wu XC, Tao XL, Wang PM, Li P, Chi XQ, Li YD, Yan QF, Zhao YH (2011) Screening and construction of Saccharomyces cerevisiae strains with improved multi-tolerance and bioethanol fermentation performance. Bioresour Technol 102(3):3020–3027

    Article  CAS  Google Scholar 

  • Zheng DQ, Wang PM, Chen J, Zhang K, Liu TZ, Wu XC, Li YD, Zhao YH (2012) Genome sequencing and genetic breeding of a bioethanol Saccharomyces cerevisiae strain YJS329. BMC Genomics 13(1):479

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the State Key Laboratory of Motor Vehicle Biofuels Technology of China, Henan Tianguan Group, Co., Ltd.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xue-Chang Wu or Pin-Mei Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 298 kb)

ESM 2

(XLS 737 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zheng, DQ., Liu, TZ., Chen, J. et al. Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Appl Microbiol Biotechnol 97, 2067–2076 (2013). https://doi.org/10.1007/s00253-013-4698-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-4698-z

Keywords

Navigation