Skip to main content
Log in

Coordinate and non-coordinate expression of the stress 70 family and other molecular chaperones at high and low temperature in spinach and tomato

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Stress 70 molecular chaperones are found in all the major subcellular compartments of plant cells, and they are encoded by a multigene family. Twelve members of this family have been identified in spinach. The expression of the stress 70 molecular chaperones in response to heat shock is well-known and it appears that low temperature exposure can also stimulate their expression. However, it has been difficult to determine which member(s) of the family are specifically responsive to low temperature. This study was initiated to determine the levels of expression of the stress 70 family members and other selected chaperones in response to high and low temperature exposure. During heat shock of spinach, of the 10 stress 70 family members that were examined, all 10 showed increased RNA levels after one hour, and all showed down-regulation at longer durations of high temperature exposure. However, the response to low temperature was quite variable and complex. Some members were induced, some were transiently up-regulated, while others showed sustained up-regulation at a low non-freezing temperature. In comparison, the entirety of the molecular chaperone expression response of cold-sensitive tomato at the same low non-freezing temperature was even more dramatic with 11 of 15 molecular chaperones tested exhibiting elevated expression. The increased chaperone expression is consistent with the hypothesis that the biogenesis or stability of some proteins is compromised at low non-freezing temperatures. In contrast, mild freezing sufficient to cause injury of spinach did not materially activate chaperone expression.

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.

Institutional subscriptions

Similar content being viewed by others

References

  1. Anderson JV, Li QB, Haskell DW, Guy CL: Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat-shock genes during cold acclimation. Plant Physiol 104: 1359–1370 (1994).

    Google Scholar 

  2. Anderson JV, Guy CL: Spinach leaf 70-kilodalton heat-shock cognate stabilizes bovine adrenal glucose-6-phosphate dehydrogenase in vitro without apparent stable binding. Planta 196: 303–310 (1995).

    Google Scholar 

  3. Baba T, Jacq A, Brickman E, Beckwith J, Taura T, Ueguchi C, Akiyama Y, Ito K: Characterization of cold-sensitive secY mutants of Escherichia coli. J Bact 172: 7005–7010 (1990).

    Google Scholar 

  4. Bardwell JC, Craig EA: Major heat shock gene of Drosophila and Escherichia coli heat-inducible dnaK gene are homologous. Proc Natl Acad Sci USA 81: 848–852 (1984).

    Google Scholar 

  5. Barnett T, Altschuler M, McDaniel CN, Mascarenhas JP: Heat shock induced proteins in plant cells. Dev Genet 1: 331–340 (1980).

    Google Scholar 

  6. Bock PE, Frieden C: Another look at the cold lability of enzymes. Trends Biochem Sci 3: 100–103 (1978).

    Google Scholar 

  7. Boorstein WR, Ziegelhoffer T, Craig EA: Molecular evolution of the HSP70 multigene family. J Mol Evol 38: 1–17 (1994).

    Google Scholar 

  8. Boston RS, Viitanen PV, Vierling E: Molecular chaperones and protein folding in plants. Plant Mol Biol 32: 191–222 (1996).

    Google Scholar 

  9. Braulke T, Hasilik A, von Figura K: Low temperature blocks transport and sorting of cathepsin D in fibroblasts. Biol Chem Hoppe-Seyler 369: 441–449 (1988).

    Google Scholar 

  10. Cabane M, Calvet P, Vincens P, Boudet AM: Characterization of chilling-acclimation-related proteins in soybean and identi-fication of one as a member of the heat shock (HSP 70) family. Planta 190: 346–353 (1993).

    Google Scholar 

  11. Chiang H-L, Terlecky SR, Plant CP, Dice JF: A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246: 382–385 (1989).

    Google Scholar 

  12. Chilson OP, Costello LA, Kaplan NO: Effects of freezing on enzymes. Fed Proc 24: 55–65 (1965).

    Google Scholar 

  13. Corpas FJ, Trelease RN: The plant 73 kDa peroxisomal membrane protein (PMP73) is immunorelated to molecular chaperones. J Cell Biol 73: 49–57 (1997).

    Google Scholar 

  14. Denecke J, Goldman MHS, Demolder J, Seurinck J, Botterman J: The tobacco luminal binding protein is encoded by a multigene family. Plant Cell 3: 1025–1035 (1991).

    Google Scholar 

  15. DeRocher A, Vierling E: Cytoplasmic HSP70 homologues of pea: differential expression in vegetative and embryonic organs. Plant Mol Biol 27: 441–456 (1995).

    Google Scholar 

  16. Ellis RJ, van der Vies SM: Molecular chaperones. Annu Rev Biochem 60: 321–347 (1991).

    Google Scholar 

  17. Franks F: Biophysics and Biochemistry at Low Temperature. Cambridge University Press, Cambridge, UK (1985).

    Google Scholar 

  18. Frydman J, Nimmesgern E, Ohtsuka K, Hartl U: Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370: 111–117 (1994).

    Google Scholar 

  19. Gaitanaris GA, Papavassiliou AG, Rubock P, Silverstein SJ, Gottesman ME: Renaturation of denatured_ repressor requires heat shock proteins. Cell 61: 1013–1020 (1990).

    Google Scholar 

  20. Goode JH, Settlage SB, Wilson RF, Dewey RE: Isolation of a calnexin homolog from developing soybean seeds. Plant Physiol 108: 1341 (1995).

    Google Scholar 

  21. Günther E, Walter L: Genetic aspects of the hsp70 multigene family in vertebrates. Experientia 50: 987–1001 (1994).

    Google Scholar 

  22. Guy CL, Carter JV: Characterization of partially purified glutathione reductase from cold hardened and nonhardened spinach leaf tissue. Cryobiology 21: 454–464 (1984).

    Google Scholar 

  23. Guy CL, Haskell D: Induction of freezing tolerance in spinach is associated with the synthesis of cold acclimation induced proteins. Plant Physiol 84: 872–878 (1987).

    Google Scholar 

  24. Guy CL, Anderson JV, Haskell DW, Li QB: Caps, cors, dehydrins, and molecular chaperones: their relationship with low temperature responses in spinach. In: Cherry JH (ed) Biochemical and Cellular Mechanisms of Stress Tolerance in Plants, pp. 479–499. Springer-Verlag, Berlin (1994).

    Google Scholar 

  25. Guy CL, Li QB: The organization and evolution of the spinach stress 70molecular chaperone gene family. Plant Cell 10: 539–556 (1998).

    Google Scholar 

  26. Heschl MF, Baillie DL: The HSP70 multigene family of Caenorhabditis elegans. Comp Biochem Physiol 96: 633–637 (1990).

    Google Scholar 

  27. Hetherington SE, He J, Smillie RM: Photoinhibition at low temperature in chilling-sensitive and-resistant plants. Plant Physiol 90: 1609–1615 (1989).

    Google Scholar 

  28. Hoagland DR, Arnon DI: The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32 (1950)

    Google Scholar 

  29. Ingolia TD, Craig EA: Drosophila gene related to the major heat shock-induced gene is transcribed at normal temperatures and not induced by heat shock. Proc Natl Acad Sci USA 79: 525–529 (1982).

    Google Scholar 

  30. James P, Pfund C, Craig EA: Functional specificity among Hsp70 molecular chaperones. Science 275: 387–389 (1997).

    Google Scholar 

  31. Kalinski A, Rowley DL, Loer DS, Foley C, Buta G, Herman EM: Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs. Planta 195: 611–621 (1995).

    Google Scholar 

  32. Kamps, TL, Isleib TG, Herner RC, Sink KC: Evaluation of techniques to measure chilling injury in tomato. HortScience 22: 1309–1312 (1987).

    Google Scholar 

  33. Kang PJ, Ostermann J, Shilling J, Neupert W, Craig EA, Pfanner N: Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348: 137–143 (1990).

    Google Scholar 

  34. Key JL, Lin CY, Chen YM: Heat shock proteins of higher plants. Proc Natl Acad Sci USA 78: 3526–3530 (1981).

    Google Scholar 

  35. Ko K, Bornemisza O, Kourtz L, Ko ZW, Plaxton WC, Cashmore AR: Isolation and characterization of a cDNA clone encoding a cognate 70-kDa heat shock protein of the chloroplast envelope. J Biol Chem 267: 2986–2993 (1992).

    Google Scholar 

  36. Krishna P, Sacco M, Cherutti JF, Hill S: Cold-induced accumulation of hsp90 transcripts in Brassica napus. Plant Physiol 107: 915–923 (1995).

    Google Scholar 

  37. Lai BT, Chin NW, Stanek AE, Keh W, Lanks KW: Quantitation and intracellular localization of the 85K heat shock protein by using monoclonal and polyclonal antibodies. Mol Cell Biol 4: 2802–2810 (1984).

    Google Scholar 

  38. Lee GJ, Pokala N, Vierling E: Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270: 10432–10438 (1995).

    Google Scholar 

  39. Lelivelt MJ, Kawula TH: Hsc66, an Hsp70 homolog in Escherichia coli, is induced by cold shock but not by heat shock. J Bact 177: 4900–4907 (1995).

    Google Scholar 

  40. Levitt J: A sulfhydryl-disulfide hypothesis of frost injury and resistance in plants. J Theor Biol 3: 355–391 (1962).

    Google Scholar 

  41. Levitt J: Responses of Plants to Environmental Stresses: Chilling, Freezing and High Temperature Stresses, vol. 1, 2nd ed. Academic Press, New York (1980).

    Google Scholar 

  42. Li QB, Anderson JV, Guy CL: A cDNA clone encoding a spinach 70-kilodalton heat-shock cognate. Plant Physiol 105: 457–458 (1994).

    Google Scholar 

  43. Li X, Wu Y, Zhang D-Z, Gillikin JW, Boston RS, Franceschi VR, Okita TW: Rice prolamine protein body biogenesis: a BiP-mediated process. Science 262: 1054–1056 (1993).

    Google Scholar 

  44. Lin T-Y, Duck NB, Winter J, Folk WR: Sequences of two hsc 70 cDNAs from Lycopersicon esculentum. Plant Mol Biol 16: 475–478 (1991).

    Google Scholar 

  45. Lurie S, Klein JD: Acquisition of low-temperature tolerance in tomatoes by exposure to high-temperature stress. J Am Soc Hort Sci 116: 1007–1012 (1991).

    Google Scholar 

  46. Margolis RL, Rauch CT: Characterization of rat brain crude extract microtubule assembly: correlation of cold stability with the phosphorylation state of a microtubule-associated 64K protein. Biochemistry 20: 4451–4458 (1981).

    Google Scholar 

  47. Marivet J, Margis-Pinheiro M, Frendo P, Burkard G: Bean cyclophilin gene expression during plant development and stress conditions. Plant Mol Biol 26: 1181–1189 (1994).

    Google Scholar 

  48. Marshall JS, DeRocher AE, Keegstra K, Vierling E: Identification of heat shock protein hsp70 homologues in chloroplasts. Proc Natl Acad Sci USA 87: 374–378 (1990).

    Google Scholar 

  49. Mues GI, Munn TZ, Raese JD: A human gene family with sequence homology to Drosophila melanogaster Hsp70 heat shock genes. J Biol Chem 261: 874–877 (1986).

    Google Scholar 

  50. Nelson DE, Glaunsinger B, Bohnert HJ: Abundant accumulation of the calcium-binding molecular chaperone calreticulin in specific floral tissues of Arabidopsis thaliana. Plant Physiol 114: 29–37 (1997).

    Google Scholar 

  51. NeumannD, Nover L, Parthier B, Rieger R, ScharfK-D, Wollgiehn R, zur Nieden U: Heat shock and other stress response systems of plants. Biol Zentbl 108: 1–156 (1989).

    Google Scholar 

  52. Neven LG, Haskell DW, Guy CL, Denslow N, Klein PA, Green LG, Silverman A: Association of 70 kDa heat shock cognate proteins with acclimation to cold. Plant Physiol 99: 1362–1369 (1992).

    Google Scholar 

  53. Neven, LG, Haskell DW, Hofig A, Li QB, Guy CL: Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21: 291–305 (1993).

    Google Scholar 

  54. Nover L, Scharf KD: Heat stress proteins and transcription factors. Cell Mol Life Sci 53: 80–103 (1997).

    Google Scholar 

  55. Pace CN: Conformational stability of globular proteins. Trends Biochem Sci 15: 14–17 (1990).

    Google Scholar 

  56. Pareek A, Singla SL, Grover A: Immunological evidence for accumulation of two high-molecular-weight (104 and 90 kDa) HSPs in response to different stresses in rice and in response to high temperature stress in diverse plant genera. Plant Mol Biol 29: 293–301 (1995).

    Google Scholar 

  57. Pelham HR: Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46: 959–961 (1986).

    Google Scholar 

  58. Powles SB: Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44 (1984).

    Google Scholar 

  59. Prasad TK, Stewart CR: cDNA clones encoding Arabidopsis thaliana and Zea mays mitochondrial chaperonin HSP60 and gene expression during seed germination and heat shock. Plant Mol Biol 18: 873–885 (1992).

    Google Scholar 

  60. Privalov PL: Cold denaturation of proteins. CRC Rev Biochem Mol Biol 25: 281–305 (1990).

    Google Scholar 

  61. Rassow J, von Ahsen O, Bömer U, Pfanner N: Molecular chaperones: towards a characterization of the heat-shock protein 70 family. Trends Cell Biol 7: 129–133 (1997).

    Google Scholar 

  62. Rubin DM, Mehta AD, Zhu J, Shoham S, Chen X, Wells QR, Palter KB: Genomic structure and sequence analysis of Drosophila melanogaster HSC70 genes. Gene 128: 155–163 (1993).

    Google Scholar 

  63. Sabehat A, Weiss D, Lurie S: The correlation between heat shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiol 110: 536–541 (1996).

    Google Scholar 

  64. Saito T, Ishiguro S, Ashida H, Kawamukai M, Matsuda H, Ochiai H, Nakagawa T: Cloning and sequence analysis of genes for cyclophilin from Arabidopsis thaliana. Plant Cell Physiol 36: 377–382 (1995).

    Google Scholar 

  65. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  66. Schilke B, Forster J, Davis J, James P, Walter W, Laloraya S, Johnson J, Miao B, Craig E: The cold sensitivity of a mutant of Saccharomyces cerevisiae lacking a mitochondrial heat shock protein 70 is suppressed by loss of mitochondrial DNA. J Cell Biol 134: 603–613 (1996).

    Google Scholar 

  67. Seaton BL, Vickery LE: A gene encoding a DnaK/hsp70 homolog in Escherichia coli. Proc Natl Acad Sci USA 91: 2066–2070 (1994).

    Google Scholar 

  68. Sheffield WP, Shore GC, Randall SK: Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence. J Biol Chem 265: 11069–11076 (1990).

    Google Scholar 

  69. Steponkus PL: Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35: 543–584 (1984).

    Google Scholar 

  70. Sukamaran NP, Weiser CJ: An excised leaflet test for evaluating potato frost tolerance. HortScience 7: 467–468.

  71. Sun SW, Chung MC, Lin TY: The structure and expression of an hsc70 gene from Lycopersicon esculentum. Gene 170: 237–241 (1996).

    Google Scholar 

  72. Tavaria M, Gabriele T, Kola I, Anderson RL: A hitchhiker's guide to the human Hsp70 family. Cell Stress Chaperones 1: 23–28 (1996).

    Google Scholar 

  73. Tissieres A, Mitchell HK, Tracy UM: Protein synthesis in salivary glands of D. melanogaster. Relation to chromosome puffs. J Mol Biol 84: 389–398 (1974).

    Google Scholar 

  74. Walker MA, Smith DM, Pauls KP, McKersie BD: A chlorophyll fluorescence screening test to evaluate chilling tolerance in tomato. HortScience 25: 334–339 (1990).

    Google Scholar 

  75. Walther-Larsen H, Brandt J, Collinge DB, Thordal-Christensen H: A pathogen-induced gene of barley encodes a HSP90 homologue showing striking similarity to vertebrate forms resident in the endoplasmic reticulum. Plant Mol Biol 21: 1097–1108 (1993).

    Google Scholar 

  76. Watts FZ, Walters AJ, Moore AL: Characterization of PHSP1, a cDNA encoding a mitochondrial HSP70 from Pisum sativum. Plant Mol Biol 18: 23–32 (1992).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, QB., Haskell, D.W. & Guy, C.L. Coordinate and non-coordinate expression of the stress 70 family and other molecular chaperones at high and low temperature in spinach and tomato. Plant Mol Biol 39, 21–34 (1999). https://doi.org/10.1023/A:1006100532501

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006100532501

Navigation