Proline as a stress protectant in yeast: Physiological functions, metabolic regulations, and biotechnological applications

Applied Microbiology and Biotechnology

Volumn 81, Issue 2, 2008, Pages 211-223

  Takagi, Hiroshi ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Metabolic engineering; Proline; Saccharomyces cerevisiae; Stress tolerance

Indexed keywords

AMINES; AMINO ACIDS; BACTERIOLOGY; BEVERAGES; BIOTECHNOLOGY; CELL MEMBRANES; CELLS; ELASTICITY; ETHANOL; GENE ENCODING; NUCLEIC ACIDS; ORGANIC ACIDS; OXYGEN; PROBABILITY DENSITY FUNCTION; THEOREM PROVING; YEAST;

ALCOHOLIC BEVERAGES; BIOETHANOL PRODUCTIONS; BIOLOGICAL FUNCTIONS; BIOSYNTHETIC ACTIVITIES; BIOTECHNOLOGICAL APPLICATIONS; CELLULAR LEVELS; DEGRADATION PATHWAYS; FEEDBACK INHIBITIONS; IN VITRO; IN-VIVO; MEMBRANE STABILIZATIONS; METABOLIC ENGINEERING; METABOLIC REGULATIONS; MULTIPLE FUNCTIONS; OSMOPROTECTANT; OSMOTIC STRESSES; PHYSIOLOGICAL FUNCTIONS; PIVOTAL ROLES; PLANT CELLS; PROLINE; PROLINE ACCUMULATIONS; PROLINE LEVELS; PROTECTIVE EFFECTS; REACTIVE OXYGEN SPECIES; S. CEREVISIAE; SACCHAROMYCES CEREVISIAE; STRESS CONDITIONS; STRESS PROTECTANT; STRESS TOLERANCE; TO MANY; YEAST CELLS; YEAST SACCHAROMYCES CEREVISIAE; YEAST STRAINS;

CYTOLOGY;

ACETALDEHYDE; ALCOHOL; CARBON DIOXIDE; DNA; GLUTAMIC ACID; PROLINE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE;

AMINO ACID; BIOTECHNOLOGY; GENE EXPRESSION; METABOLISM; OSMOSIS; PHYSIOLOGICAL RESPONSE; YEAST;

AMINO ACID SYNTHESIS; BIOTECHNOLOGY; CELL VACUOLE; CELL VIABILITY; CYTOPLASM; DEGRADATION KINETICS; DESICCATION; FERMENTATION; FREEZING TOLERANCE; GENE; MEMBRANE STABILIZATION; METABOLIC ENGINEERING; METABOLIC REGULATION; MITOCHONDRION; NONHUMAN; OSMOTIC STRESS; OXIDATION KINETICS; PRO1 GENE; PROTEIN PROCESSING; PROTEIN STABILITY; PUT1 GENE; SACCHAROMYCES CEREVISIAE; SHORT SURVEY; YEAST; YEAST CELL;

PROLINE; SACCHAROMYCES CEREVISIAE;

BACTERIA (MICROORGANISMS); SACCHAROMYCES CEREVISIAE;

EID: 55649090079     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-008-1698-5     Document Type: Short Survey

References (126)

1. H Alexandre V Ansanay-Galeote S Dequin B Blondin 2001 Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae FEBS Lett 498 98 103
2. A Ando T Nakamura Y Murata H Takagi J Shima 2007 Identification and classification of genes required for tolerance to freeze-thaw stress revealed by genome-wide screening of Saccharomyces cerevisiae deletion strains FEMS Yeast Res 7 244 253
3. +) FEBS Lett 286 13 17
4. C Andréasson EP Neve PO Ljungdahl 2004 Four permeases import proline and the toxic proline analogue azetidine-2-carboxylate into yeast Yeast 21 193 199
5. L Aravind EV Koonin 1999 Novel predicted RNA-binding domains associated with the translation machinery J Mol Evol 48 291 302
6. Atkinson DE (1977) Cellular energy metabolism and its regulation. Academic, New York
7. PV Attfield 1987 Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response FEBS Lett 225 259 263
8. JD Axcelrod J Majors MC Brandriss 1991 Proline-independent binding of PUT3 transcriptional activator protein detected by footprinting in vivo Mol Cell Biol 11 564 567
9. BR Belitsky J Brill E Bremer AL Sonenshein 2001 Multiple genes for the last step of proline biosynthesis in Bacillus subtilis J Bacteriol 183 4389 4392
10. +) in acquired osmotolerance of Saccharomyces cerevisiae J Bacteriol 171 1087 1092
11. O Borsani J Zhu PE Verslues R Sunkar JK Zhu 2005 Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis Cell 123 1279 1291
12. RA Brady LN Csonka 1988 Transcriptional regulation of the proC gene of Salmonella typhimurium J Bacteriol 170 2379 2382
13. MC Brandriss 1983 Proline utilization in Saccharomyces cerevisiae: analysis of the cloned PUT2 gene Mol Cell Biol 3 1846 1856
14. 1- pyrroline-5-carboxylate reductase J Bacteriol 174 3782 3788
15. Bremer E, Krämer R (2000) Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes in bacteria. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM, Washington, DC, pp 79-97
16. JF Carpenter JH Crowe 1988 Modes of stabilization of a protein by organic solutes during desiccation Cryobiology 25 459 470
17. HC Causton B Ren SS Koh CT Harbison E Kanin EG Jennings TI Lee HL True ES Lander RA Young 2001 Remodeling of yeast genome expression in response to environmental changes Mol Biol Cell 12 323 337
18. C Chen MB Dickman 2005 Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii Proc Natl Acad Sci USA 102 3459 3464
19. M Chen J Cao C Zheng Q Liu 2006 Directed evolution of an artificial bifunctional enzyme, γ-glutamyl kinase/γ-glutamyl phosphate reductase, for improved osmotic tolerance of Escherichia coli transformants FEMS Microbiol Lett 263 41 47
20. V Costa MA Amorim E Reis A Quintanilha P Moradas-Ferreira 1997 Mitochondrial superoxide dismutase is essential for ethanol tolerance of Saccharomyces cerevisiae in the post-diauxic phase Microbiol 143 1649 1656
21. LN Csonka 1981 Proline over-production results in enhanced osmotolerance in Salmonella typhimurium Mol Gen Genet 182 82 86
22. LN Csonka AD Hanson 1991 Prokaryotic osmoregulation: genetics and physiology Annu Rev Microbiol 45 569 606
23. LN Csonka SB Gelvin BW Goodner CS Orser D Siemieniak JL Slightom 1988 Nucleotide sequence of a mutation in the proB gene of Escherichia coli that confers proline overproduction and enhanced tolerance to osmotic stress Gene 64 199 205
24. AM Dandekar SL Uratsu 1988 A single base pair change in proline biosynthesis genes causes osmotic stress tolerance J Bacteriol 170 5943 5945
25. JR Daugherty R Rai HM el Berry TG Cooper 1993 Regulatory circuit for responses of nitrogen catabolic gene expression to the GLN3 and DAL80 proteins and nitrogen catabolite repression in Saccharomyces cerevisiae J Bacteriol 175 64 73
26. G Degols JC Jauniaux JM Wiame 1987 Molecular characterization of transposable-element-associated mutations that lead to constitutive l-ornithine aminotransferase expression in Saccharomyces cerevisiae Eur J Biochem 165 289 296
27. AJ Delauney DPS Verma 1993 Proline biosynthesis and osmoregulation in plants Plant J 4 215 223
28. SA Des Etages DA Falvey RJ Reece MC Brandriss 1996 Functional analysis of the PUT3 transcriptional activator of the proline utilization pathway in Saccharomyces cerevisiae Genetics 142 1069 1082
29. SA Des Etages D Saxena HL Huang DA Falvey D Barber MC Brandriss 2001 Conformational changes play a role in regulating the activity of the proline utilization pathway-specific regulator in Saccharomyces cerevisiae Mol Microbiol 40 890 899
30. K Deuschle D Funck G Forlani H Stransky A Biehl D Leister E van der Graaff R Kunze WB Frommer 2004 The role of [Delta]1-pyrroline-5-carboxylate dehydrogenase in proline degradation Plant Cell 16 3413 3425
31. W Fricke E Pahlich 1990 The effect of water stress on the vacuole-extravacuole compartmentation of proline in potato cell suspension cultures Physiol Plant 78 374 378
32. T Fujita A Maggio M García-Ríos C Stauffacher RA Bressan LN Csonka 2003 Identification of regions of the tomato γ-glutamyl kinase that are involved in allosteric regulation by proline J Biol Chem 278 14203 14210
33. PD Hare WA Cress 1997 Metabolic implications of stress-induced proline accumulation in plants Plant Growth Regul 21 79 102
34. DJ Hayzer T Leisinger 1980 The gene-enzyme relationships of proline biosynthesis in Escherichia coli J Gen Microbiol 118 287 293
35. SB Helliwell S Losko CA Kaiser 2001 Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease J Cell Biol 153 649 662
36. H Hellmann D Funck D Rentsch WB Frommer 2000 Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application Plant Physiol. 123 779 789
37. AG Hinnebusch 1988 Mechanisms of gene regulation in the general control of amino acid biosynthesis in Saccharomyces cerevisiae Microbiol Rev 52 248 273
38. A Hino 2002 Safety assessment and public concerns for genetically modified food products: the Japanese experience Toxicol Pathol 30 126 128
39. R Hirasawa K Yokoigawa Y Isobe H Kawai 2001 Improving the freeze tolerance of baker's yeast by loading with trehalose Biosci Biotechnol Biochem 65 522 526
40. 1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress Plant Physiol 122 1129 1136
41. T Hottiger C De Virgilio MN Hall T Boller A Wiemken 1994 The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro Eur J Biochem 219 187 193
42. KH Hsu RC Hoseney PA Seib 1979 Frozen dough. I. Factors affecting stability of yeasted dough Cereal Chem 56 419 424
43. 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants Proc Natl Acad Sci USA 89 9354 9358
44. 1-pyrroline-5-carboxylate synthase. Alternative splice donor utilization generates isoforms with different sensitivity to ornithine inhibition J Biol Chem 274 6754 6762
45. HL Huang MC Brandriss 2000 The regulator of the yeast proline utilization pathway is differentially phosphorylated in response to the quality of the nitrogen source Mol Cell Biol 20 892 899
46. Z Ignatova LM Gierasch 2006 Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant Proc Natl Acad Sci USA 103 13357 13361
47. R Ishitani O Nureki S Fukai T Kijimoto N Nameki M Watanabe H Kondo M Sekine N Okada S Nishimura S Yokoyama 2002 Crystal structure of archaeosine tRNA-guanine transglycosylase J Mol Biol 318 665 677
48. S Izawa M Sato K Yokoigawa Y Inoue 2004 Intracellular glycerol influences resistance to freeze stress in Saccharomyces cerevisiae: analysis of a quadruple mutant in glycerol dehydrogenase genes and glycerol-enriched cells Appl Microbiol Biotechnol 66 108 114
49. JC Jauniaux M Grenson 1990 GAP1, the general amino acid permease gene of Saccharomyces cerevisiae. Nucleotide sequence, protein similarity with the other bakers yeast amino acid permeases, and nitrogen catabolite repression Eur J Biochem 190 39 44
50. M Jones JS Pierce 1964 Adsorption of amino acids from wort by yeasts J Inst Brew 70 307 315
51. T Kaino H Takagi 2008 Gene expression profiles and intracellular contents of stress protectants in Saccharomyces cerevisiae under ethanol and sorbitol stresses Appl Microbiol Biotechnol 79 273 283
52. T Kaino T Tateiwa S Mizukami-Murata J Shima H Takagi 2008 Self-cloning baker's yeasts that accumulate proline enhance freeze tolerance in doughs Appl Environ Microbiol 74 5845 5849
53. O Kandror N Bretschneider E Kreydin D Cavalieri AL Goldberg 2004 Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones Mol Cell 13 771 781
54. S Kaul SS Sharma IK Mehta 2008 Free radical scavenging potential of L-proline: evidence from in vitro assays Amino Acids 34 315 320
55. 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants Plant Physiol 108 1387 1394
56. Y Kawahara T Ohsumi Y Yoshihara S Ikeda 1989 Proline in the osmoregulation of Brevibacterium lactofermentum Agric Biol Chem 53 2475 2479
57. T Kiyosue Y Yoshiba K Yamaguchi-Shinozaki K Shinozaki 1996 A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis Plant Cell 8 1323 1335
58. Kodama K (1993) Sake-brewing yeasts. In: Rose AH, Harrison JS (eds) The yeasts. vol. 3. Academic, London, United Kingdom, pp 129-168
59. N Krishnan MB Dickman DF Becker 2008 Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress Free Radic Biol Med 44 671 681
60. Kunkee RE, Bisson LF (1993) Wine-making yeast. In: Rose AH, Harrison JS (eds) The yeast. vol. 5, 2nd edn. Academic, San Diego, California, pp 94-99
61. W Li MC Brandriss 1992 Proline biosynthesis in Saccharomyces cerevisiae: molecular analysis of the PRO1 gene, which encodes γ-glutamyl kinase J Bacteriol 174 4148 4156
62. B List RA Lerner CF Barbas III 2000 Proline-catalyzed direct asymmetric aldol reactions J Am Chem Soc 122 2395 2396
63. ZL Liu 2006 Genomic adaptation of ethanologenic yeast to biomass conversion inhibitors Appl Microbiol Biotechnol 73 27 36
64. A Maggio S Miyazaki P Veronese T Fujita JI Ibeas B Damsz ML Narasimhan PM Hasegawa RJ Joly RA Bressan 2002 Does proline accumulation play an active role in stress-induced growth reduction Plant J 31 699 712
65. S Mani B Van De Cotte M Van Montagu N Verbruggen 2002 Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis Plant Physiol 128 73 83
66. C Marco-Marín F Gil-Ortiz I Pérez-Arellano J Cervera I Fita V Rubio 2007 A novel two-domain architecture within the amino acid kinase enzyme family revealed by the crystal structure of Escherichia coli glutamate 5-kinase J Mol Biol 367 1431 1446
67. K Matsuura H Takagi 2005 Vacuolar functions are involved in stress-protective effect of intracellular proline in Saccharomyces cerevisiae J Biosci Bioeng 100 538 544
68. S Maxwell GE Davis 2000 Differential gene expression in p53-mediated apoptosis-resistant vs. apoptosis-sensitive tumor cell lines Proc Natl Acad Sci USA 97 13009 13014
69. L Meric S Lambert-Guilois O Neyreneuf D Richard-Molard 1995 Cryoresistance of baker's Saccharomyces cerevisiae in frozen dough: contribution of cellular trehalose Cereal Chem 72 609 615
70. WJ Middelhoven 1964 The pathway of arginine breakdown in Saccharomyces cerevisiae Biochim Biophys Acta 93 650 652
71. AP Mohanty J Matysik 2001 Effect of proline on the production of single oxygen Amino Acids 21 195 200
72. Y Morita S Nakamori H Takagi 2002 Effect of proline and arginine metabolism on freezing stress of Saccharomyces cerevisiae J Biosci Bioeng 94 390 394
73. Y Morita S Nakamori H Takagi 2003 l-proline accumulation and freeze tolerance of Saccharomyces cerevisiae are caused by a mutation in the PRO1 gene encoding γ-glutamyl kinase Appl Environ Microbiol 69 212 219
74. T Nanjo M Kobayashi Y Yoshiba Y Kakubari K Yamaguchi-Shinozaki K Shinozaki 1999 Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana FEBS Lett 461 205 210
75. T Nanjo M Fujita M Seki T Kato S Tabata K Shinozaki 2003 Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase Plant Cell Physiol 44 541 548
76. M Nomura H Takagi 2004 Role of the yeast acetyltransferase Mpr1 in oxidative stress: regulation of oxygen reactive species caused by a toxic proline catabolism intermediate Proc Natl Acad Sci USA 101 12616 12621
77. AB Northrup DW MacMillan 2004 Two-step synthesis of carbohydrates by selective aldol reactions Science 305 1752 1755
78. K Omori S Suzuki Y Imai S Komatsubara 1991 Analysis of the Serratia marcescens proBA operon and feedback control of proline biosynthesis J Gen Microbiol 137 509 517
79. K Omori S Suzuki Y Imai S Komatsubara 1992 Analysis of the mutant proBA operon from a proline-producing strain of Serratia marcescens J Gen Microbiol 138 693 699
80. F Omura A Fujita K Miyajima N Fukui 2005 Engineering of yeast Put4 permease and its application to lager yeast for efficient proline assimilation Biosci Biotechnol Biochem 69 1162 1171
81. CS Orser BW Goodner M Johnston SB Gelvin LN Csonka 1988 The Escherichia coli proB gene corrects the proline auxotrophy of Saccharomyces cerevisiae pro1 mutants Mol Gen Genet 212 124 128
82. AK Påhlman K Granath R Ansell S Hohmann L Adler 2001 The yeast glycerol 3-phosphatases Gpp1p and Gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress J Biol Chem 276 3555 3563
83. H Pan S Agarwalla DT Moustakas J Finer-Moore RM Stroud 2003 Structure of tRNA pseudouridine synthase TruB and its RNA complex: RNA recognition through a combination of rigid docking and induced fit Proc Natl Acad Sci USA 100 12648 12653
84. J Panadero C Pallotti S Rodríguez-Vargas F Randez-Gil JA Prieto 2006 A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae J Biol Chem 281 4638 4645
85. 1- pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants Mol Gen Genet 253 334 341
86. I Perez-Arellano V Rubio J Cervera 2005 Dissection of Escherichia coli glutamate 5-kinase: functional impact of the deletion of the PUA domain FEBS Lett 579 6903 6908
87. B Poolman E Glaasker 1998 Regulation of compatible solute accumulation in bacteria Mol Microbiol 29 397 407
88. CSV Rajendrakumar T Suryanarayana AR Reddy 1997 DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process FEBS Lett 410 201 205
89. S Ramón-Maiques A Marina F Gil-Ortiz I Fita V Rubio 2002 Structure of acetylglutamate kinase, a key enzyme for arginine biosynthesis and a prototype for the amino acid kinase enzyme family, during catalysis Structure 10 329 342
90. AS Rudolph JH Crowe 1985 Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline Cryobiology 22 367 377
91. R Russnak D Konczal SL McIntire 2001 A family of yeast proteins mediating bidirectional vacuolar amino acid transport J Biol Chem 276 23849 23857
92. D Samuel TKS Kumar G Ganesh G Jayaraman PW Yang MM Chang VD Trivedi SL Wang KC Hwang DK Chang C Yu 2000 Proline inhibits aggregation during protein refolding Protein Sci 9 344 352
93. T Sato Y Ohsumi Y Anraku 1984 Substrate specificities of active transport systems for amino acids in vacuolar membrane vesicles of Saccharomyces cerevisiae J Biol Chem 259 11505 11508
94. SH Saum V Müller 2007 Salinity-dependent switching of osmolyte strategies in a moderately halophilic bacterium: glutamate induces proline biosynthesis in Halobacillus halophilus J Bacteriol 189 6968 6975
95. B Schade G Jansen M Whiteway KD Entian DY Thomas 2004 Cold adaptation in budding yeast Mol Biol Cell 15 5492 5502
96. B Schobert H Tschesche 1978 Unusual solution properties of proline and its interaction with proteins Biochim Biophys Acta 541 270 277
97. AP Seddon KY Zhao A Meister 1989 Activation of glutamate by γ-glutamate kinase: formation of γ-cis-cycloglutamyl phosphate, an analog of γ-glutamyl phosphate J Biol Chem 264 11326 11335
98. T Sekine A Kawaguchi Y Hamano H Takagi 2007 Desensitization of feedback inhibition of the Saccharomyces cerevisiae γ-glutamyl kinase enhances proline accumulation and freezing tolerance Appl Environ Microbiol 73 4011 4019
99. M Shimazu T Sekito K Akiyama Y Ohsumi Y Kakinuma 2005 A family of basic amino acid transporters of the vacuolar membrane from Saccharomyces cerevisiae J Biol Chem 280 4851 4857
100. P Sivakumar P Sharmila PP Saradhi 1998 Proline suppresses rubisco activity in higher plants Biochem Biophys Res Commun 252 428 432
101. N Smirnoff QJ Cumbes 1989 Hydroxyl radical scavenging activity of compatible solutes Phytochemistry 28 1057 1060
102. CJ Smith AH Deutch KE Rushlow 1984 Purification and characteristics of a γ-glutamyl kinase involved in Escherichia coli proline biosynthesis J Bacteriol 157 545 551
103. +-induced down-regulation of the Saccharomyces cerevisiae Gap1p permease involves its ubiquitination with lysine-63-linked chains J Cell Sci 112 1375 1383
104. M Stanbrough B Magasanik 1995 Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae J Bacteriol 177 94 102
105. 1-pyrroline-5-carboxylate synthetase mRNA or protein Plant Physiol 120 923 931
106. N Strizhov E Abrahám L Okrész S Blickling A Zilberstein J Schell C Koncz L Szabados 1997 Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis Plant J 12 557 569
107. M Sugiura M Kisumi 1985 Proline-hyperproducing strains of Serratia marcescens: enhancement of proline analog-mediated growth inhibition by increasing osmotic stress Appl Environ Microbiol 49 782 786
108. RA Sumrada TG Cooper 1984 Nucleotide sequence of the Saccharomyces cerevisiae arginase gene (CAR1) and its transcription under various physiological conditions J Bacteriol 160 1078 1087
109. 1-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean Plant Physiol 99 1642 1649
110. H Takagi F Iwamoto S Nakamori 1997 Isolation of freeze-tolerant laboratory strains of Saccharomyces cerevisiae from proline-analogue-resistant mutants Appl Microbiol Biotechnol 47 405 411
111. H Takagi K Sakai K Morida S Nakamori 2000 Proline accumulation by mutation or disruption of the proline oxidase gene improves resistance to freezing and desiccation stresses in Saccharomyces cerevisiae FEMS Microbiol Lett 184 103 108
112. H Takagi M Takaoka A Kawaguchi Y Kubo 2005 Effect of l-proline on sake brewing and ethanol stress in Saccharomyces cerevisiae Appl Environ Microbiol 71 8656 8662
113. H Takagi F Matsui A Kawaguchi H Wu H Shimoi Y Kubo 2007 Construction and analysis of self-cloning sake yeasts that accumulate proline J Biosci Bioeng 103 377 380
114. Y Terao S Nakamori H Takagi 2003 Gene dosage effect of l-proline biosynthetic enzymes on L-proline accumulation and freeze tolerance in Saccharomyces cerevisiae Appl Environ Microbiol 69 6527 6532
115. JM Thevelein S Hohmann 1995 Trehalose synthase: guard to the gate of glycolysis in yeast Trends Biochem Sci 20 3 10
116. KC Thomas SH Hynes WM Ingledew 1994 Effects of particulate materials and osmoprotectants on very-high-gravity ethanolic fermentation by Saccharomyces cerevisiae Appl Environ Microbiol 60 1519 1524
117. DM Tomenchok MC Brandriss 1987 Gene-enzyme relationships in the proline biosynthetic pathway of Saccharomyces cerevisiae J Bacteriol 169 5364 5372
118. EW Trotter CMF Kao L Berenfeld D Botstein GA Petsko JV Gray 2002 Misfolded proteins are competent to mediate a subset of the response to heat shock in Saccharomyces cerevisiae J Biol Chem 177 44817 44825
119. T Umezawa M Fujita Y Fujita K Yamaguchi-Shinozaki K Shinozaki 2006 Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future Curr Opin Biotech 17 113 122
120. M Vandenbol JC Jauniaux M Grenson 1989 Nucleotide sequence of the Saccharomyces cerevisiae PUT4 proline-permease-encoding gene: similarities between CAN1, HIP1 and PUT4 permeases Gene 83 153 159
121. P Van Dijck D Colavizza P Smet JM Thevelein 1995 Differential importance of trehalose in stress resistance in fermenting and nonfermenting Saccharomyces cerevisiae cells Appl Environ Microbiol 61 109 115
122. N Verbruggen XJ Hua M May M Van Montagu 1996 Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator Proc Natl Acad Sci USA 93 8787 8791
123. SS Wang MC Brandriss 1986 Proline utilization in Saccharomyces cerevisiae: analysis of the cloned PUT1 gene Mol Cell Biol 6 2638 2645
124. M Yamada H Morishita K Urano N Shiozaki K Yamaguchi-Shinozaki K Shinozaki Y Yoshiba 2005 Effects of free proline accumulation in petunias under drought stress J Exp Bot 56 1975 1981
125. 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress Plant J 7 751 760
126. 1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants J Biol Chem 270 20491 20496