Strategies of Freezing Tolerance in Yeast: Genes’ Rapid Response for Accumulation of Stress Protectants

Author(s): Maryam Z. Khajavi, Abhishek D. Tripathi, Kianoush Khosravi-Darani*.

Journal Name: Current Nutrition & Food Science

Volume 15 , Issue 6 , 2019

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Graphical Abstract:


Production of frozen ready-to-bake bakery products has gained significant attention during the past few years. However, the freezing process during the production of frozen bakery products may decrease the quality especially in the case of suppression of the activity of baker yeast. Great improvements in the quality of frozen bakery products may be achieved by increasing the stability of yeast during freezing storage. Many microorganisms have different kinds of mechanisms to suppress environmental, freezing or thawing stresses. In this review paper, reported strategies which are used for rising tolerance of microorganisms, especially yeast, are reviewed. One of the introduced protective procedures is the accumulation of special intra-cellular metabolites by some microorganisms. Two main key metabolites in this regard are trehalose and proline (which act as an osmoprotectant and decrease the melting point of DNA), which are introduced in this review article. Also, cloning strategies for increasing their bioaccumulation are pointed out, and their mechanisms of action are described. Finally, overexpression of SNR84 gene as an another microbial strategy for surviving in harsh environmental conditions is (small nucleolar RNAs) mentioned, which leads to ribosomal pseudouridines (responsible for freezing tolerance and decreasing growth rate of organisms).

Keywords: Bioaccumulation, freezing & thawing, intra-cellular metabolites, overexpression, ready-to-bake products, suppress environmental stress, yeast activity.

Rudolph AS, Crowe JH. Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. Cryobiology 1985; 22(4): 367-77.
Rajendrakumar CSV, Suryanarayana T, Reddy AR. DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process. FEBS Lett 1997; 410(2-3): 201-5.
Samuel D, Kumar TKS, Ganesh G, et al. Proline inhibits aggregation during protein refolding. Protein Sci 2000; 9(2): 344-52.
Hong Z, Lakkineni K, Zhang Z, et al. Removal of feedback inhibition of $Δ$1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 2000; 122(4): 1129-36.
Chen C, Dickman MB. Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci USA 2005; 102(9): 3459-64.
Sekine T, Kawaguchi A, Hamano Y, et al. Desensitization of feedback inhibition of the Saccharomyces cerevisiae γ-glutamyl kinase enhances proline accumulation and freezing tolerance. Appl Environ Microbiol 2007; 73(12): 4011-9.
Kaino T, Tateiwa T, Mizukami-Murata S, et al. Self-cloning baker’s yeasts that accumulate proline enhance freeze tolerance in doughs. Appl Environ Microbiol 2008; 74(18): 5845-9.
Sasano Y, Haitani Y, Hashida K, et al. Enhancement of the proline and nitric oxide synthetic pathway improves fermentation ability under multiple baking-associated stress conditions in industrial baker’s yeast. Microb Cell Fact 2012; 11(1): 40.
Sasano Y, Haitani Y, Ohtsu I, et al. Proline accumulation in baker’s yeast enhances high-sucrose stress tolerance and fermentation ability in sweet dough. Int J Food Microbiol 2012; 152(1): 40-3.
Sasano Y, Takahashi S, Shima J, et al. Antioxidant N-acetyltransferase Mpr1/2 of industrial baker’s yeast enhances fermentation ability after air-drying stress in bread dough. Int J Food Microbiol 2010; 138(1): 181-5.
Trotter EW, Kao CM-F, Berenfeld L, et al. Misfolded proteins are competent to mediate a subset of the responses to heat shock in Saccharomyces cerevisiae. J Biol Chem 2002; 277(47): 44817-25.
Steensels J, Snoek T, Meersman E, et al. Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiol Rev 2014; 38(5): 947-95.
Rose MD, Broach JR. Cloning genes by complementation in yeast. Methods Enzymol 1991; 194: 195-230.
Tsolmonbaatar A, Hashida K, Sugimoto Y, et al. Isolation of baker’s yeast mutants with proline accumulation that showed enhanced tolerance to baking-associated stresses. Int J Food Microbiol 2016; 238: 233-40.
Elbein AD, Pan YT, Pastuszak I, et al. New insights on trehalose: a multifunctional molecule. Glycobiology 2003; 13(4): 17R-27R.
Grba S, Oura E, Suomalainen H. On the formation of glycogen and trehalose in baker’s yeast. Appl Microbiol Biotechnol 1975; 2(1): 29-37.
Gélinas P, Fiset G, LeDuy A, et al. Effect of growth conditions and trehalose content on cryotolerance of bakers’ yeast in frozen doughs. Appl Environ Microbiol 1989; 55(10): 2453-9.
Shima J, Hino A, Yamada-Iyo C, et al. Stress tolerance in doughs of Saccharomyces cerevisiae trehalase mutants derived from commercial bakers yeast. Appl Environ Microbiol 1999; 65(7): 2841-6.
Nakamura T, Takagi H, Shima J. Effects of ice-seeding temperature and intracellular trehalose contents on survival of frozen Saccharomyces cerevisiae cells. Cryobiology 2009; 58(2): 170-4.
Chi Z, Liu J, Zhang W. Trehalose accumulation from soluble starch by Saccharomycopsis fibuligera sdu. Enzyme Microb Technol 2001; 28(2-3): 240-5.
Berg JM, Stryer L, Tymoczko JL. Stryer Biochemie. Switzerland: Springer-Verlag 2015.
Grosjean H. DNA and RNA modification enzymes. Austin, TX: Landes Biosci 2009.
Cantara WA, Crain PF, Rozenski J, et al. The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res 2010; 39(Suppl. 1): D195-201.
Lane BG. Historical perspectives on RNA nucleoside modifications.In: Modification and Editing of RNA. Washington, DC: ASM Press 1998; pp. 1-20.
Cohn WE, Volkin E. Nucleoside-5 -phosphates from ribonucleic acid. Nature 1951; 167(4247): 483-4.
Davis FF, Allen FW. Ribonucleic acids from yeast which contain a fifth nucleotide. J Biol Chem 1957; 227(2): 907-15.
Wrzesinski J, Bakin A, Ofengand J, et al. Isolation and properties of Escherichia coli 23S-RNA pseudouridine 1911, 1915, 1917 synthase (RluD). IUBMB Life 2000; 50(1): 33-7.
Raychaudhuri S, Niu L, Conrad J, et al. Functional effect of deletion and mutation of the Escherichia coli ribosomal RNA and tRNA pseudouridine synthase RluA. J Biol Chem 1999; 274(27): 18880-6.
Ma X, Yang C, Alexandrov A, et al. Pseudouridylation of yeast U2 snRNA is catalyzed by either an RNA-guided or RNA-independent mechanism. EMBO J 2005; 24(13): 2403-13.
Ni J, Tien AL, Fournier MJ. Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell 1997; 89(4): 565-73.
Schattner P, Barberan-Soler S, Lowe TM. A computational screen for mammalian pseudouridylation guide H/ACA RNAs. RNA 2006; 12(1): 15-25.
Balakin AG, Smith L, Fournier MJ. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 1996; 86(5): 823-34.
Brown JWS, Clark GP, Leader DJ, et al. Multiple snoRNA gene clusters from Arabidopsis. RNA 2001; 7(12): 1817-32.
Kiss T. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 2002; 109(2): 145-8.
Tycowski KT, Steitz JA. Non-coding snoRNA host genes in Drosophila: expression strategies for modification guide snoRNAs. Eur J Cell Biol 2001; 80(2): 119-25.
Schattner P, Decatur WA, Davis CA, et al. Genome-wide searching for pseudouridylation guide snoRNAs: analysis of the Saccharomyces cerevisiae genome. Nucleic Acids Res 2004; 32(14): 4281-96.
Smith CM, Steitz JA. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell 1997; 89(5): 669-72.
Lin X, Zhang C-Y, Bai X-W, et al. Improvement of stress tolerance and leavening ability under multiple baking-associated stress conditions by overexpression of the SNR84 gene in baker’s yeast. Int J Food Microbiol 2015; 197: 15-21.
Shima J, Takagi H. Stress-tolerance of baker’s-yeast (Saccharomyces cerevisiae) cells: stress-protective molecules and genes involved in stress tolerance. Biotechnol Appl Biochem 2009; 53(3): 155-64.
Attfield PV. Stress tolerance: the key to effective strains of industrial baker’s yeast. Nat Biotechnol 1997; 15(13): 1351-7.
Morimoto RI. Cells in stress: transcriptional activation of heat shock genes. Science 1993; 259(5100): 1409-10.
Ge J, Yu Y-T. RNA pseudouridylation: new insights into an old modification. Trends Biochem Sci 2013; 38(4): 210-8.
Ganot P, Bortolin M-L, Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 1997; 89(5): 799-809.
Newby MI, Greenbaum NL. A conserved pseudouridine modification in eukaryotic U2 snRNA induces a change in branch-site architecture. RNA 2001; 7(6): 833-45.
Venema J, Tollervey D. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast 1995; 11(16): 1629-50.

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Article Details

Year: 2019
Page: [531 - 535]
Pages: 5
DOI: 10.2174/2210315508666181009113623
Price: $65

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