Abstract
When exposed to low non-freezing temperatures (0–10°C), the freezing tolerance of spinach increases in a time dependent fashion from an LT50 of -4°C to -14°C. Associated with the low temperature induction of freezing tolerance is the increased expression of at least 20 proteins. Three of these low temperature responsive proteins were selected for study and found to belong to two families of stress proteins, the LEA/dehydrin/Rab and the heat shock 70s. Their possible role in low temperature tolerance mechanisms and a model for the role of ATP in peptide binding activities of the 70 kDa heat shock molecular chaperones are discussed.
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References
Alber, T (1989) Mutational effects on protein stability. Ann Rev Biochem 58: 765–798
Anderson, JV, Li, Q-B, Haskell, DW, Guy, CL (1993) Structural organization of the spinach ERlumenal HSC70 gene and its expression during cold acclimation. In review.
Ausubel, FM, Brent, R, Kingston, RE, Moore, DD, Seidmon, JG, Smith, JA, Struhl, K (1989) Current Protocols in Molecular Biology, Wiley Interscience, New York.
Beckmann, RP, Mizzen, LA, Welch, WJ (1990) Interaction of Hsp 70 with newly synthesized proteins: Implications for protein folding and assembly. Science 248: 850–854
Bock, PE, Frleden, C (1978) Another look at the cold lability of enzymes. Trends Biochem Sci 3: 100–103
Bork, P, Sander, C, Valencia, A (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin and hsp70 heat shock proteins. Proc Natl Acad Sci USA 89: 7290–7294
Braell, WA, Schlossman, DM, Schmid, SL, Rothman, JE (1984) Dissociation of clathrin coats coupled to the hydrolysis of ATP: Role of an uncoating ATPase. J Cell Biol 99: 734–741
Brodsky, JL, Hamamoto, S, Feldheim, D, Schekman, R (1993) Reconstitution of protein translocation from solubilized yeast membranes reveals topological distinct roles for BiP and cytosolic Hsc70. J Cell Biol 120: 95–102
Burton, V, Mitchell, HK, Young, P, Petersen, NS (1988) Heat shock protection against cold stress of Drosophila melanogaster. Mol Cell Biol 8: 3550–3552
Carlino, A, Toledo, H, Skaleris, D, DeLisio, R, Weissbach, H, Brot, N (1992) Interactions of liver Grp78 and Escherichia coli recombinant Grp78 with ATP: multiple species and disaggregation. Proc Natl Acad Sci USA 89: 2081–2085
Chiang, H-L, Terlecky, SR, Plant, CP, Dice, JF (1989) A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246: 382–385
Chirico, WJ, Waters, MG, Blobel, G (1988) 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332: 805–810
Close, TJ, Kortt, AA, Chandler, PM (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13: 95–108
Craig, EA (1989) Essential roles of 70kDa heat inducible proteins. BioEssays 11: 48–52
Creighton, TE (1990) Understanding protein folding pathways and mechanisms. In LM Gierasch and J King ed, Protein Folding: Deciphering the Second Half of the Genetic Code. AAAS, Washington, DC, pp 157–170
Deshaies, RJ, Koch, BD, Werner-Washburne, M, Craig, EA, Schekman, R (1988) A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332: 800–805
Dickens, BF, Thompson, GA (1981) Rapid membrane response during low temperature acclimation. Correlation of early changes in the physical properties and lipid composition of Tetrahymena microsomal membranes. Biochim Biophys Acta 664: 211–218
Duck, N, McCormick, S, Winter, J (1989) Heat shock protein hsp70 cognate gene expression in vegetative and reproductive organs of Lycopersicon esculentum. Proc Natl Acad Sci USA 86: 3674–3678
Dure III, L, (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3: 363–369
Ellis, RJ, van der Vies, SM (1991) Molecular chaperones. Ann Rev Biochem 60: 321–347
Flaherty, KM, DeLuca-Flaherty, C, McKay, DB (1990) Three-dimensional structure of the ATPase fragment of a 70k heat-shock cognate protein. Nature 346: 623–628
Flaherty, KM, McKay, DB, Kabsch, W, Holmes, KC (1991) Similarity of the three-dimensional structures of actin and the ATPase fragment of a 70-kDa heat shock cognate protein. Proc Natl Acad Sci USA 88: 5041–5045
Freiden, PJ, Gaut, JR, Hendershot, LM (1992) Interconversion of three differentially modified and assembled forms of BiP. EMBO J 11: 63–70
Gaitanaris, GA, Papavassiliou, AG, Rubock, P, Silverstein, SJ, Gottesman, ME (1990) Renaturation of denatured X repressor requires heat shock proteins. Cell 61: 1013–1020
Gaut, JR, Hendershot, LM (1992) The in vivo and in vitro phosphorylation of BiP occur at different sites but have similar consequences on function. Abstract #3, Molecular chaperones: Functions in protein folding and cellular metabolism.
Gething, M-J, Sambrook, J (1992) Protein folding in the cell. Nature 355: 33–45
Gilmour, SJ, Artus, NN, Thomashow, MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18: 13–21
Goldstein, J, Pollitt, NS, Inouye, M (1990) Major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 87: 283–287
Guo, W, Ward, RW, Thomashow, MF (1992) Characterization of a cold-regulated wheat gene related to Arabidopsis cor47. Plant Physiol 100: 915–922
Guy, CL (1990) Cold acclimation and freezing tolerance: Role of protein metabolism. Ann Rev Plant Physiol Plant Mol Biol 41: 187–223
Guy, CL, Yelenosky, G, Sweet, HC (1981) Distribution of 14C photosynthetic assimilates in Valencia orange seedlings at 10° and 25°C. J Am Soc Hort Sci 106: 433–437
Guy, CL, Plesofsky-Vig, N, Brambl, R (1986) Heat shock protection of germinating Neurospora crassa conidiospores against intracellular freezing stress. J Bacteriol 167: 124–129
Guy, CL, Haskell, D (1987) Induction of freezing tolerance in spinach is associated with the synthesis of cold acclimation induced proteins. Plant Physiol 84: 872–878
Guy, CL, Huber, JLA, and Huber, SC (1992a) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100: 502–508
Guy, CL, Haskell, DW, Neven, LN, Klein, P, and Smelser, C (1992b) Hydration-state-responsive proteins link cold and drought stress in spinach. Planta 188: 265–270
Hahn, M, Walbot, V (1989) Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves. Plant Physiol 91: 930–938
Hardies, SC, Garvin, LD (1991) Can molecular evolution provide clues to the folding code? In BT Nail, KA Dill, ed, Conformations and Forces in Protein Folding. AAAS, Washington DC, pp 69–76
Hajela, RK, Horvath, DP, Gilmour, SJ, Thomashow, MF (1990) Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol 93: 1246–1252
Hofig, A, Neven, LG, Li, Q-B, Haskell, D, and Guy, CL (1993) Expression of a plant cold stress protein in Escherichia coli imparts enhanced freezing tolerance. Submitted.
Hopf, N, Plesofsky-Vig, N, Brambl, R (1992) The heat shock response of pollen and other tissues of maize. Plant Mol Biol 19: 623–630
Houde, M, Danyluk, J, Laibert, J-F, Rassart, E, Dhindsa, RS, Sarhan, F (1992) Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99: 1381–1387
Jones, RL, Bush, DS (1991) Gibberellic acid regulates the level of a BiP cognate in the endoplasmic reticulum of barley aleurone cells. Plant Physiol 97: 456–459
Joplin, KH, Yocum, GD, Denlinger, DL (1990) Cold shock elicits expression of heat shock proteins in the flesh fly, Sarcophaga crassipalpis. J Insect Physiol 36: 825–834
Kassenbrock, CK, Kelly, RB (1989) Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides. EMBO J 8: 141–1467
Kauzmann, W (1959) Some factors in the interpretation of protein denaturation. In CB Afinsen, ML Anson, K Bailey, JT Edsall eds, Advances in Protein Chemistry. Academic Press, New York, pp 1–63
Kim, PS, Bole, D, Arvan, P (1992) Transient aggregation of nascent thyroglobulin in the endoplasmic reticulum: Relationship to the molecular chaperone, BiP J Cell Biol 118: 541–549
King, J, Fane, B, Haase-Pettingell, C, Mitraki, A, Villafane, R, Yu, M-H (1990) Identification of amino acid sequences influencing intracellular folding pathways using temperature-sensitive folding mutations. In LM Gierasch, J King ed, Protein Folding: Deciphering the Second Half of the Genetic Code. AAAS, Washington, pp 225–240
Knittler, MR, Haas, IG (1992) Interaction of BiP with newly synthesized immunoglobulin light chain molecules: cycles of sequential binding and release. EMBO J 11: 1573–1581
Kondo, K, Inouye, M (1991) 77P7, a cold shock-inducible.gene of Saccharomyces cerevisiae. J Biol Chem 266: 17537–17544
Kondo, K, Kowalski, RZ, Inouye, M (1992) Cold shock induction of yeast NSR1 protein and its role in pre-RNA processing. J Biol Chem 267: 16259–16265
Kurkela, S, Franck, M (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis. Plant Mol Biol 15: 137–144
Ling, V, Palva, ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana ( L.) Heynh. Plant Mol Biol 20: 951–962
Langer, T, Lu, C, Echols, H, Flanagan, J, Hayer, MK, Hartl, FU (1992) Successive action of DnaK, DnaJ, and GroEL along the pathway of chaperone-mediated protein folding. Nature 356: 683–689
Levitt, J (1962) A sulfhydryl-disulfide hypothesis of frost injury and resistance in plants. J Theoret Biol 3: 355–391
Levitt, J (1980) Responses of Plants to Environmental Stresses. New York: Academic Press. 697 pp
Leustek, T, Amir-Shapira, D, Toledo, H, Brot, N, Weissbach, H (1992) Autophosphorylation of 70 kDa heat shock proteins Cell Mol Biol 38: 1–10
Lewis, MJ, Pelham, HRB (1985) Involvement of ATP in the nuclear and nucleolar functions of the 70 kd heat shock protein. EMBO J 4: 3137–3143
Knittler, MR, Haas, IG (1992) Interaction of BiP with newly synthesized immunoglobulin light chain molecules: cycles of sequential binding and release. EMBO J 11: 1573–1581
Lin, C, Thomashow, MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide. Plant Physiol 99: 519–525
Lin, Y, Gross, JK (1981) Molecular cloning and characterization of winter flounder antifreeze cDNA. Proc Natl Acad Sci USA 78: 2825–2829
Lissin, NM, Venyaminov, SY, Girshovich, AS (1990) (Mg-ATP)-dependent self-assembly of molecular chaperone GroEL. Nature 348: 339–342
Luo, M, Liu, J-H, Mohapatra, S, Hill, RD, Mohapatra, SS (1992) Characterization of a gene family encoding abscisic acid- and environmental stress-inducible proteins of alfalfa. J Biol Chem 267: 15367–15374
Maniak, M, Nellen, W (1988) A developmentally regulated membrane protein gene in Dictyostelium discoideum is also induced by heat shock and cold shock. Mol Cell Biol 8: 153–159
McCarty, JS, Walker, GC (1991) DnaK as a thermometer: Threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc Natl Acad Sci USA 88: 9513–9517
Miernyk, JA, Duck, NB, Shatters, RG, Folk, WR (1992) The 70-kilodalton heat shock cognate can act as a molecular chaperone during the membrane translocation of a plant secretory protein precursor. Plant Cell 4: 821–829
Minton, KW, Karmin, P, Hahn, GM, Minton, AP (1982) Nonspecific stabilization of stress-susceptible proteins by stress-resistant proteins: A model for the biological role of heat shock proteins. Proc Natl Acad Sci USA 79: 7107–7111
Mundy, J, Chua, NH (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 8: 2279–2286
Munro, S, Pelham, HRB (1986) An Hsp70-like protein in the ER: Identity with the 78 kd glucoseregulated protein and immunoglobulin heavy chain binding protein. Cell 46: 291–300
Neven LG, Haskell DW, Guy CL, Denslow N, Klein PA, Green LG, Silverman A (1992) Association of 70 kDa heat shock cognate proteins with acclimation to cold. Plant Physiol 99: 1362–1369
Neven, LG, Haskell, DW, Hofig, A, Li, Q-B, Guy, CL (1993) Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21: 291–305
Nilsson, B, Kuntz, ID, Anderson, S (1990) Expression and stabilization: Bovine pancreatic trypsin inhibitor folding mutants in Escherichia coii. In LM Gierasch, J King ed, Protein Folding: Deciphering the Second Half of the Genetic Code. AAAS, Washington, pp 117–122
Nordin, K, Heino, P, Palva, ET (1991) Separate signal pathways regulate the expression of a low temperature-induced gene in Arabidopsis thaliana ( L.) Heynh. Plant Mol Biol 16: 1061–1071
Ouellet, F, Houde, M, Sarhan, F (1993) Purification, characterization and cDNA cloning of the 200 kDa protein induced by cold acclimation in wheat Plant Cell Physiol 34: 59–65
Orr, W, Lu, B, White, TC, Robert, LS, Singh, J (1992) Complementary DNA sequence of a low temperature-induced Brassica napus gene with homology to the Arabidopsis thaliana kin1 gene. Plant Physiol 98: 1532
Pace, CN (1990) Conformational stability of globular proteins. Trends Biochem Sci 15: 14–17
Paiieros, DR, Welch, WJ, Fink, AL (1991) Interaction of hsp70 with unfolded proteins: Effects of temperature and nucleotides on the kinetics of binding. Proc Natl Acad Sci USA 88: 5719–5723
Pearce, RS (1988) Extracellular ice and cell shape in frost-stressed cereal leaves: A low-temperature scanning-electron-microscopy study. Planta 175: 313–324
Pelham, HRB (1986) Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46: 959–961
Petersen, NS, Young, P, Burton, V (1990) Heat shock mRNA accumulation during recovery from cold shock in Drosophila melanogaster. Insect Biochem 20: 679–684
Privalov, PL (1990) Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25: 281–305
Rubin, DM, Mehta, AD, Zhu, J, Shoham, S, Chen, X, Wells, QR, Palter, KB (1993) Genomic structure and sequence analysis of Drosophila melanogaster HSC70 genes. Gene (in press).
Sakai, A, Larcher, W (1987) Frost Survival of Plants: Responses and Adaptation to Freezing Stress. Springer-Verlag, Berlin, pp 321
Sato, N (1992) Cloning of a low-temperature-induced gene Iti2 from the cyanobacterium Anabaena variabilis M3 that is homologous to a-amylases. Plant Mol Biol 18: 165–170
Schmid, SL, Braell, WA, Rothman, JE (1985) ATP catalyzes the sequestration of clathrin during enzymatic uncoating. J Biol Chem 260: 10057–10062
Sherman, MY, Goldberg, AL (1992) Heat shock in Escherichia coli alters the protein-binding properties of the chaperonin groEL by inducing its phosphorylation. Nature 357: 167–169
Skowyra, D, Georgopoulos, C, Zylicz, M (1990) TheE coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell 62: 939–944
Snutch, TP, Heschl, MFP, Baillie, DL (1988) The Caenorhabditis elegans hsp70 gene family: a molecular genetic characterization. Gene 64: 241–255
Steponkus, PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Ann Rev Plant Physiol 35: 543–584
Sutton, F, Ding, X, Kenefick, DG (1992) Group 3 LEA gene HVA1 regulation by cold acclimation and deacclimation in two barley cultivars with varying freeze resistance. Plant Physiol 99: 338–340
VanBogelen, RA, Neidhardt, FC (1990) Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci 87: 5589–5593
Vierling, E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579–620
Weiser CJ (1970) Cold resistance and injury in woody plants. Science 169: 1269–1278
Willimsky, G, Bang, H, Fischer, G, Marahiel, MA (1992) Characterization of cspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperature. J Bacteriol 174: 6326–6335
Zylicz, M, LeBowitz, JH, McMacken, R, Georgopolous, C (1983) The dnaK protein of Escherichia coli possesses an ATPase and autophosphorylating activity and is essential in an in vitro DNA replication system. Proc Natl Acad Sci USA 80: 6431–6435
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Guy, C.L., Anderson, J.V., Haskell, D.W., Li, QB. (1994). Caps, Cors, Dehydrins, and Molecular Chaperones: Their Relationship with Low Temperature Responses in Spinach. In: Cherry, J.H. (eds) Biochemical and Cellular Mechanisms of Stress Tolerance in Plants. NATO ASI Series, vol 86. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79133-8_29
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DOI: https://doi.org/10.1007/978-3-642-79133-8_29
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