Regulation of Cold Acclimation

A Complex Interaction of Low Temperature, Light, and Chloroplastic Redox Poise
  • Gordon R. Gray
  • Louis-Pierre Chauvin
  • Fathey Sarhan
  • Norman P. A. Huner

Abstract

Exposure to low, non-freezing temperatures induces molecular, morphological, and physiological changes in plants which result in the acquisition of freezing tolerance (Va-sil’yev, 1961; Guy, 1990; Thomashow, 1993; Hughes and Dunn, 1996). Light, through the process of photosynthesis, provides the energy required for the complex metabolic changes of cold acclimation (Dexter, 1933; Tysdall, 1933; Steponkus and Lanphear, 1968; Gusta et al., 1982; Griffith and Mclntyre, 1993). Huner and co-workers have demonstrated that the freezing tolerance of cereals is not only correlated to the capacity to keep QA, the stable quinone electron acceptor of photosystem II (PSII), in the oxidized state, but also to an increased photosynthetic capacity (PSmax) (Huner et al., 1993; Öquist et al., 1993).

Keywords

Cold Acclimation Freezing Tolerance Growth Irradiance Excitation Pressure Similar Developmental Stage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Alex LA, Simon MI (1994) Protein histidine kinases and signal transduction in prokaryotes and eukaryotes. Trends Genet 10: 133–138PubMedCrossRefGoogle Scholar
  2. Allen JF, Alexciev K, Håkansson G (1995) Regulation by redox signalling. Curr Biol 5: 869–872PubMedCrossRefGoogle Scholar
  3. Anderson JM, Chow WS, Park Y-I (1995) The grand design of photosynthesis: Acclimation of the photosyn-thetic apparatus to environmental cues. Photosynth Res 46: 129–139CrossRefGoogle Scholar
  4. Asada K, Heber U, Schreiber U (1992) Pool size of electrons that can be donated to P700+, as determined in intact leaves: Donation to P700+ from stromal components via the intersystem chain. Plant Cell Physiol 33: 927–932Google Scholar
  5. Bourret RB, Borkovich KA, Simon MI (1991) Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu Rev Biochem 60: 401–441PubMedCrossRefGoogle Scholar
  6. Bowler C, Chua N-H (1994) Emerging themes of plant signal transduction. Plant Cell 6: 1529–1541PubMedGoogle Scholar
  7. Chang C (1996) The ethylene signal transduction pathway in Arabidopsis: an emerging paradigm? Trends Biochem Sci 21: 129–133PubMedGoogle Scholar
  8. Chauvin LP, Houde M, Sarhan F (1993) A leaf-specific gene stimulated by light during wheat acclimation to low temperature. Plant Mol Biol 23: 255–265PubMedCrossRefGoogle Scholar
  9. Chauvin LP, Houde M, Sarhan F (1994) Nucleotide sequence of a new member of the freezing tolerance-associated protein family in wheat. Plant Physiol 105: 1017–1018PubMedCrossRefGoogle Scholar
  10. Danon A, Mayfield SP (1994) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266: 1717–1719PubMedCrossRefGoogle Scholar
  11. Danyluk J, Sarhan F (1990) Differential mRNA transcription during the induction of freezing tolerance in spring and winter wheat. Plant Cell Physiol 31: 609–619Google Scholar
  12. Dau H (1994) Short-term adaptation of plants to changing light intensities and its relation to photosystem II photochemistry and fluorescence emission. J Photochem Photobiol B: Biol 26: 3–27CrossRefGoogle Scholar
  13. Dexter ST (1933) Effects of several environmental factors on the hardening of plants. Plant Physiol 8:123–139PubMedCrossRefGoogle Scholar
  14. Dietz K-J, Schreiber U, Heber U (1985) The relationship between the redox state of Q A and photosynthesis in leaves at various carbon-dioxide, oxygen and light regimes. Planta 166: 219–226CrossRefGoogle Scholar
  15. Escoubas J-M, Lomas M, LaRoche J, Falkowski PG (1995) Light intensity regulation of cab gene transcription is signalled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237–10241PubMedCrossRefGoogle Scholar
  16. Fowler DB, Gusta LV, Tyler NJ (1981) Selection for winter hardiness in wheat. III. Screening methods. Crop Sci 21: 896–901CrossRefGoogle Scholar
  17. Gray GR (1996) Cold Acclimation: A complex interaction of low temperature, light and the redox state of photo-system II. PhD thesis. The University of Western Ontario, London, CanadaGoogle Scholar
  18. Gray GR, Savitch LV, Ivanov AG, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and rye. Plant Physiol 110: 61–71PubMedGoogle Scholar
  19. Griffith M, Mclntyre HCH (1993) The interrelationship of growth and frost tolerance in winter rye. Physiol Plant 87: 335–344CrossRefGoogle Scholar
  20. Gusta LV, Chen THH (1987) The physiology of water and temperature stress. In EG Heyne, ed, Wheat and Wheat Improvement, Ed 2. ASA, CSSA, SSSA Inc., pp 115-150Google Scholar
  21. Gusta LV, Fowler DB, Tyler NJ (1982) Factors influencing hardening and survival in winter wheat. In PH Li, A Sakai, eds, Plant Cold Hardiness and Freezing Stress. Mechanisms and Crop Implications, Vol 2. Academic Press, New York, pp 23–40CrossRefGoogle Scholar
  22. Guy CL (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41: 187–223CrossRefGoogle Scholar
  23. Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100: 502–508PubMedCrossRefGoogle Scholar
  24. Guy CL, Nieme KJ, Brambl J (1985) Altered gene expression during cold acclimation of spinach. Proc Natl Acad Sci USA 82: 3673–3677PubMedCrossRefGoogle Scholar
  25. Houde M, Daniel C, Lachapelle M, Allard F, Laliberté S, Sarhan F (1995) Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J 8: 583–593PubMedCrossRefGoogle Scholar
  26. Houde M, Danyluk J, Laliberté JF, Rassart E, Dhindsa RS, Sarhan F (1992a) Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99: 1381–1387PubMedCrossRefGoogle Scholar
  27. Houde M, Dhindsa RS, Sarhan F (1992b) A molecular marker to select for freezing tolerance in Gramineae. Mol Gen Genet 234: 43–48PubMedGoogle Scholar
  28. Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47: 291–305CrossRefGoogle Scholar
  29. Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, Falk S (1996) Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of photosystem II. Physiol Plant-in pressGoogle Scholar
  30. Huner NPA, Maxwell DP, Gray GR, Savitch LV, Laudenbach DE, Falk S (1995) Photosynthetic response to light and temperature: PSII excitation pressure and redox signalling. Acta Physiol Plant 17: 167–176Google Scholar
  31. Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37: 19–39CrossRefGoogle Scholar
  32. Hurry VM, Strand Å, Tobiæson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism and carbohydrate content. Plant Physiol 109: 697–706PubMedGoogle Scholar
  33. Iuchi S, Lin ECC (1993) Adaptation of Escherichia coli to redox environments by gene expression. Mol Micro-biol 9: 9–15CrossRefGoogle Scholar
  34. Krol M, Huner NPA (1985) Growth and development at cold-hardening temperatures. Pigment and benzoquinone accumulation in winter rye. Can J Bot 63: 716–721Google Scholar
  35. Levings CS III, Siedow JN (1995) Regulation by redox poise in chloroplasts. Science 268: 695–696PubMedCrossRefGoogle Scholar
  36. Limin AE, Houde M, Chauvin LP, Fowler DB, Sarhan F (1995) Expression of the cold-induced wheat gene Wcs120 and its homologs in related species and interspecific combinations. Genome 38: 1023–1031PubMedCrossRefGoogle Scholar
  37. Maeda T, Wurgler-Murphy SM, Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242–245PubMedCrossRefGoogle Scholar
  38. Maxwell DP, Falk S, Huner NPA (1995a) Photosystem II excitation pressure and development of resistance to photoinhibition I. Light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol 107:687–694PubMedGoogle Scholar
  39. Maxwell DP, Laudenbach DE, Huner NPA (1995b) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109: 787–795PubMedGoogle Scholar
  40. Monroy AF, Dhindsa RS (1995) Low-temperature signal transduction: Induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. Plant Cell 7: 321–331PubMedGoogle Scholar
  41. Ögren E (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184: 538–544CrossRefGoogle Scholar
  42. Öquist G, Hurry VM, Huner NPA (1993) Low-temperature effects on photosynthesis and correlation with freezing tolerance in spring and winter cultivars of wheat and rye. Plant Physiol 101: 245–250PubMedGoogle Scholar
  43. Ota IM, Varshavsky A (1993) A yeast protein similar to bacterial two-component regulators. Science 262: 566–568PubMedCrossRefGoogle Scholar
  44. 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: 59–65PubMedGoogle Scholar
  45. Parkinson JS (1993) Signal transduction schemes of bacteria. Cell 73: 857–871PubMedCrossRefGoogle Scholar
  46. Pearce RS, Dunn MA, Rixon JE, Harrison P, Hughes MA (1996) Expression of cold-inducible genes and frost hardiness in the crown meristem of young barley (Hordeum vulgare L. cv. Igri) plants grown in different environments. Plant Cell Environ 19: 275–290CrossRefGoogle Scholar
  47. Pollock CJ, Lloyd EJ (1987) The effect of low growth temperature upon starch, sucrose and fructan synthesis in leaves. Ann Bot 60: 231–235Google Scholar
  48. Roberts DWA (1984) The effect of light on development of the rosette growth habit of winter wheat. Can J Bot 62: 818–822CrossRefGoogle Scholar
  49. Savitch LV, Maxwell DP, Huner NPA (1996) Photosystem II excitation pressure and photosynthetic carbon metabolism in Chlorella vulgaris. Plant Physiol 111: 127–136PubMedGoogle Scholar
  50. Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In E-D Shulze, MM Caldwell, eds, Ecophysiology of photosynthesis. Springer-Verlag, Berlin, pp 49–70Google Scholar
  51. Steponkus PL, Lanphear FO (1968) The role of light in cold acclimation of Hedera helix L. var. Thorndale. Plant Physiol 43: 151–156PubMedCrossRefGoogle Scholar
  52. Stushnoff C, Fowler DB, Brûelé-Babel A (1984) Breeding and selection for resistance to low temperature. In PB Vose, SG Blixt, eds, Crop Breeding. A Contemporary Basis. Pergamon Press, New York, pp 115–136CrossRefGoogle Scholar
  53. Thomashow MF (1993) Genes induced during cold acclimation in higher plants. In PL Steponkus, ed, Advances Low-Temperature Biology, Vol 2. JAI Press, London, pp 183–210Google Scholar
  54. Trewavas A, Gilroy S (1991) Signal transduction in plant cells. Trends Genet. 7: 356–361PubMedGoogle Scholar
  55. Tysdal HM (1933) Influence of light, temperature, and soil moisture on the hardening process in alfalfa. J Agr Res 46:483–515Google Scholar
  56. Vanlerberghe GC, Day DA, Wiskich JT, Vanlerberghe AE, Mclntosh L (1995) Alternative oxidase activity in tobacco leaf mitochondria. Dependence on tricarboxylic acid cycle-mediated redox regulation and pyru-vate activation. Plant Physiol 109: 353–631PubMedGoogle Scholar
  57. Vasil’yev IM (1961) Wintering of Plants. American Institute of Biological Sciences, Washington DCGoogle Scholar
  58. Verhey SD, Lomax TL (1993) Signal transduction in vascular plants. J Plant Growth Regul 12: 179–195CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Gordon R. Gray
    • 1
  • Louis-Pierre Chauvin
    • 2
  • Fathey Sarhan
    • 2
  • Norman P. A. Huner
    • 1
  1. 1.Department of Plant SciencesThe University of Western OntarioLondonCanada
  2. 2.Departement des Sciences biologiquesUniversité du Québec à MontréalMontréalCanada

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