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Initiation and Development of Chilling Injury in Leaves of Chilling-Sensitive Plants

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Abstract

Based on author’s own and literature data, possible mechanisms of initiation, development, and reparation of cell damages in chilling-sensitive plants during and after chilling are reviewed. A conception of initiation and development of chilling injury, based on a key role of oxidative stress, is put forward. Possible mechanisms of structural and functional changes in cells of chilling-sensitive plants subjected to chilling stress are discussed.

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Abbreviations

[Ca2+]cyt :

concentration of free cytosolic calcium

ROS:

reactive oxygen species

SOD:

superoxide dismutase

REFERENCES

  1. Henkel, P.A. and Kushnirenko, S.V., Kholodostoikost’ rastenii i termicheskie sposoby ee povysheniya (Plant Cold Tolerance and Its Elevation by Heat Treatments), Moscow: Nauka, 1966.

    Google Scholar 

  2. Zholkevich, V.N., Reasons of Plant Death under Low Above-Zero Temperatures, Tr. Inst. Plant Physiol., Akad. Nauk SSSR, 1955, vol. 9, pp. 3–28.

    Google Scholar 

  3. Graham, D. and Patterson, B.D., Responses of Plants to Low, Nonfreezing Temperatures: Proteins, Metabolism, and Acclimation, Annu. Rev. Plant Physiol., 1982, vol. 33, pp. 347–372.

    Article  Google Scholar 

  4. Eaks, I.I., Effect of Chilling on Respiration and Volatiles of California Lemon Fruit, J. Am. Soc. Hortic. Sci., 1980, vol. 105, pp. 865–869.

    Google Scholar 

  5. Lyons, J.M., Chilling Injury in Plants, Annu. Rev. Plant Physiol., 1973, vol. 24, pp. 445–466.

    Article  Google Scholar 

  6. Moon, B.Y., Higashi, S.I., Gombos, Z., and Murata, N., Unsaturation of the Membrane Lipids of Chloroplasts Stabilizes the Photosynthetic Machinery against Low Temperature Photoinhibition in Transgenic Tobacco Plants, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 6219–6223.

    PubMed  Google Scholar 

  7. Thompson, G.A., Molecular Changes in Membrane Lipids during Cold Stress, Environmental Stress in Plants: Biochemical and Physiological Mechanisms, NATO ASI, Ser. G: Ecol. Sci., Berlin: Springer-Verlag, 1989, vol. 19, pp. 249–257.

    Google Scholar 

  8. Platt-Aloia, K.A. and Thomson, W.W., Freeze-Fracture Evidence for Lateral Phase Separation in the Plasmalemma of Chilling-Injured Avocado Fruit, Protoplasma, 1987, vol. 136, pp. 71–80.

    Article  Google Scholar 

  9. Terzaghi, W.B., Fork, D.C., Berry, J.A., and Field, C.B., Low and High Temperature Limits to PS II: A Survey Using Transparinaric Acid, Delayed Light Emission and F0 Chlorophyll Fluorescence, Plant Physiol., 1989, vol. 91, pp. 1494–1500.

    Google Scholar 

  10. Zauralov, O.A. and Lukatkin, A.S., Kinetics of Electrolyte Exosmosis in Heat-Loving Plants under Lowered Temperatures, Fiziol. Rast. (Moscow), 1985, vol. 32, pp. 347–354 (Sov. Plant Physiol., Engl. Transl.).

    Google Scholar 

  11. Markowski, A., Augustyniak, G., and Janowiak, F., Sensitivity of Different Species of Field Crops to Chilling Temperature: 3. ATP Content and Electrolyte Leakage from Seedlings Leaves, Acta Physiol. Plant., 1990, vol. 12, pp. 167–173.

    Google Scholar 

  12. Minorsky, P.V., An Heuristic Hypothesis of Chilling Injury in Plants: A Role for Calcium as the Primary Physiological Transducer of Injury, Plant, Cell Environ., 1985, vol. 8, pp. 75–94.

    Google Scholar 

  13. Lukatkin, A.S., Sharkaeva, E.Sh., and Zauralov, O.A., Exosmosis of Electrolytes from Maize Leaves under Chilling Stresses, Fiziol. Rast. (Moscow), 1993, vol. 40, pp. 770–775 (Russ. Plant Physiol., Engl. Transl., pp. 665–669).

    Google Scholar 

  14. Wilson, J.M., The Mechanism of Chill-and Drought-Hardening of Phaseolus vulgaris Leaves, New Phytol., 1976, vol. 76, pp. 257–270.

    Google Scholar 

  15. Szalai, G., Janda, T., Paldi, E., and Szigeti, Z., Role of Light in the Development of Post-Chilling Symptoms in Maize, J. Plant Physiol., 1996, vol. 148, pp. 378–383.

    Google Scholar 

  16. Van Hasselt, P.R. and van Berlo, H.A.C., Photooxidative Damage to the Photosynthetic Apparatus during Chilling, Physiol. Plant., 1980, vol. 50, pp. 52–56.

    Google Scholar 

  17. Rietze, E. and Wiebe, H.-J., Diurnal Rhythm of Chilling Sensitivity of Cucumber in Light, Sci. Hortic., 1989, vol. 38, pp. 231–237.

    Article  Google Scholar 

  18. Alam, B. and Jacob, J., Overproduction of Photosynthetic Electrons Is Associated with Chilling Injury in Green Leaves, Photosynthetica, 2002, vol. 40, pp. 91–95.

    Article  Google Scholar 

  19. Janda, T., Szalai, G., Kissimov, J., Paldi, E., Marton, C., and Szigeti, Z., Role of Irradiance in the Chilling Injury of Young Maize Plants Studied by Chlorophyll Fluorescence Induction Measurements, Photosynthetica, 1994, vol. 30, pp. 293–299.

    Google Scholar 

  20. Hariyadi, P. and Parkin, K.L., Chilling Induced Oxidative Stress in Cucumber (Cucumis sativus L. cv. Calypso) Seedlings, J. Plant Physiol., 1993, vol. 141, pp. 733–738.

    Google Scholar 

  21. Prasad, T.K., Anderson, M.D., Martin, B.A., and Stewart, C.R., Evidence for Chilling-Induced Oxidative Stress in Maize Seedlings and a Regulatory Role for Hydrogen Peroxide, Plant Cell, 1994, vol. 6, pp. 65–74.

    Article  PubMed  Google Scholar 

  22. Shen, W.Y., Nada, K., and Tachibana, S., Oxygen Radical-Generation in Chilled Leaves of Cucumber (Cucumis sativus L.) Cultivars with Different Tolerances to Chilling Temperatures, J. Jpn. Soc. Hortic. Sci., 1999, vol. 68, pp. 780–787.

    Google Scholar 

  23. Lukatkin, A.S., Contribution of Oxidative Stress to the Development of Cold-Induced Damage to Leaves of Chilling-Sensitive Plants: 1. Reactive Oxygen Species Formation during Plant Chilling, Fiziol. Rast. (Moscow), 2002, vol. 49, pp. 697–702 (Russ. J. Plant Physiol., Engl. Transl., pp. 622–627).

    Google Scholar 

  24. Lukatkin, A.S., Contribution of Oxidative Stress to the Development of Cold-Induced Damage to Leaves of Chilling-Sensitive Plants: 2. The Activity of Antioxidant Enzymes during Plant Chilling, Fiziol. Rast. (Moscow), 2002, vol. 49, pp. 878–885 (Russ. J. Plant Physiol., Engl. Transl., pp. 782–788).

    Google Scholar 

  25. Takac, T., The Relationship of Antioxidant Enzymes and Some Physiological Parameters in Maize during Chilling, Plant Soil Environ., 2004, vol. 50, pp. 27–32.

    Google Scholar 

  26. Wise, R.R. and Naylor, A.W., Chilling-Enhanced Photo-oxidation: The Peroxidative Destruction of Lipids during Chilling Injury to Photosynthesis and Ultrastructure, Plant Physiol., 1987, vol. 83, pp. 272–277.

    Google Scholar 

  27. Lukatkin, A.S., Contribution of Oxidative Stress to the Development of Cold-Induced Damage to Leaves of Chilling-Sensitive Plants: 3. Injury of Cell Membranes by Chilling Temperatures, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 271–274 (Russ. J. Plant Physiol., Engl. Transl., pp. 243–246).

    Google Scholar 

  28. Merzlyak, M.N., Aktivirovannyi kislorod i okislitel’nye protsessy v membranakh rastitel’noi kletki (Activated Oxygen and Oxidative Processes in Membranes of the Plant Cell), Itogi Nauki i Tekhniki, Ser. Fiziol. Rast., 1989, vol. 6.

  29. Gianinetti, A., Lorenzoni, C., and Marocco, A., Changes in Superoxide Dismutase and Catalase Activities in Response to Low Temperature in Tomato Mutants, J. Genet. Breed., 1993, vol. 47, pp. 353–356.

    Google Scholar 

  30. Pinhero, R.G., Rao, M.V., Paliyath, G., Murr, D.P., and Fletcher, R.A., Changes in Activities of Antioxidant Enzymes and Their Relationship to Genetic and Paclobutrazol-Induced Chilling Tolerance of Maize Seedlings, Plant Physiol., 1997, vol. 114, pp. 695–704.

    PubMed  Google Scholar 

  31. Tsang, W.T., Bowler, C., Herouart, D., van Camp, W., Villarroel, R., Getenello, C., van Montagu, M., and Inze, D., Differential Regulation of Superoxide Dismutases in Plants Exposed to Environmental Stress, Plant Cell, 1991, vol. 3, pp. 783–792.

    Article  PubMed  Google Scholar 

  32. Scandalios, J.G., Oxygen Stress and Superoxide Dismutases, Plant Physiol., 1993, vol. 101, pp. 7–12.

    PubMed  Google Scholar 

  33. Vladimirov, Yu.A. and Archakov, A.I., Perekisnoe okislenie lipidov v biologicheskikh membranakh (Lipid Peroxidation in Biological Membranes), Moscow: Nauka, 1972.

    Google Scholar 

  34. Bowler, C., van Montagu, M., and Inze, D., Superoxide Dismutase and Stress Tolerance, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1992, vol. 43, pp. 83–116.

    Article  Google Scholar 

  35. Gupta, A.S., Heinen, J.L., Holaday, A.S., Burke, J.J., and Allen, R.D., Increased Resistance to Oxidative Stress in Transgenic Plants That Overexpress Chloroplastic Cu/Zn Superoxide Dismutase, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 1629–1633.

    PubMed  Google Scholar 

  36. Jennings, P.H., Radical Scavengers Increase Cucumis sativus L. Seedlings Root Tolerance to Chilling, Plant Physiol., 1994, vol. 105,Suppl., p. 26.

    Google Scholar 

  37. Lukatkin, A.S. and Levina, T.E., Effect of Exogenous Modifiers of Lipid Peroxidation on Chilling Injury in Cucumber Leaves, Fiziol. Rast. (Moscow), 1997, vol. 44, pp. 397–403 (Russ. J. Plant Physiol., Engl. Transl., pp. 343–348).

    Google Scholar 

  38. Jian, L.-C., Li, J.-H., Chen, W.P., Li, P.H., and Ahlstrand, G.G., Cytochemical Localization of Calcium and Ca2+-ATPase Activity in Plant Cells under Chilling Stress: A Comparative Study between the Chilling-Sensitive Maize and the Chilling-Insensitive Winter Wheat, Plant Cell Physiol., 1999, vol. 40, pp. 1061–1071.

    Google Scholar 

  39. Holdaway-Clarke, T.L., Walrer, N.A., Hepler, P.K., and Overall, R.L., Physiological Elevations in Cytoplasmic Free Calcium by Cold or Ion Injection Result in Transient Closure of Higher Plant Plasmodesmata, Planta, 2000, vol. 210, pp. 329–335.

    PubMed  Google Scholar 

  40. Poovaiah, B.W. and Reddy, A.S.N., Calcium Messenger System in Plants, Crit. Rev. Plant Sci., 1987, vol. 6, pp. 47–103.

    PubMed  Google Scholar 

  41. Saijo, Y., Kinoshita, K., Ishiyama, K., Hata, S., Kyozuka, J., Hayakawa, T., Nakamura, T., Shimamoto, K., Yamaya, T., and Izui, K., A Ca2+-Dependent Protein Kinase That Endows Rice Plants with Cold-and Salt-Stress Tolerance Functions in Vascular Bundles, Plant Cell Physiol., 2001, vol. 42, pp. 1228–1233.

    Article  PubMed  Google Scholar 

  42. Jouve, L., Engelmann, F., Noirot, M., and Charrier, A., Evaluation of Biochemical Markers (Sugar, Proline, Malonedialdehyde and Ethylene) for Cold Sensitivity in Microcuttings of Two Coffee Species, Plant Sci., 1993, vol. 91, pp. 109–116.

    Article  Google Scholar 

  43. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J., and Knight, M.R., Oxidative Signals in Tobacco Increase Cytosolic Calcium, Plant Cell, 1994, vol. 6, pp. 1301–1310.

    Article  PubMed  Google Scholar 

  44. Knight, H., Trewavas, A.J., and Knight, M.R., Cold Calcium Signaling in Arabidopsis Involves Two Cellular Pools and a Change in Calcium Signature after Acclimation, Plant Cell, 1996, vol. 8, pp. 489–503.

    Article  PubMed  Google Scholar 

  45. Kasamo, K., Yamaguchi, M., and Nakamura, Y., Mechanism of the Chilling-Induced Decrease in Proton Pumping across the Tonoplast of Rice Cells, Plant Cell Physiol., 2000, vol. 41, pp. 840–849.

    Article  PubMed  Google Scholar 

  46. Gehring, C.A., Irving, H.R., and Parish, R.W., Effects of Auxin and Abscisic Acid on Cytosolic Calcium and pH in Plant Cells, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, pp. 9645–9649.

    PubMed  Google Scholar 

  47. Barlow, P.W. and Adam, J.S., Anatomical Disturbances in Primary Roots of Zea mays Following Periods of Cool Temperature, Environ. Exp. Bot., 1989, vol. 29, pp. 323–336.

    Article  Google Scholar 

  48. Hayashi, Y., Nakashima, A., Hayakawa, T., Yabuta, Y., Yoshimura, K., Shigeoka, S., and Miyasaka, H., Improving Cold Tolerance of Rice by Increasing Antioxidative Capacity, Plant Cell Physiol., 2003, vol. 44,Suppl., p. 102.

    Google Scholar 

  49. Jiang, M. and Zhang, J., Effect of Abscisic Acid on Active Oxygen Species, Antioxidative Defense System and Oxidative Damage in Leaves of Maize Seedlings, Plant Cell Physiol., 2001, vol. 42, pp. 1265–1273.

    Article  PubMed  Google Scholar 

  50. Kerdnaimongkol, K., Bhatia, A., Joly, R.J., and Woodson, W.R., Oxidative Stress and Chilling Tolerance in Tomato Seedlings, Plant Physiol., 1996, vol. 111,Suppl., p. 120.

    Google Scholar 

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Translated from Fiziologiya Rastenii, Vol. 52, No. 4, 2005, pp. 608–613.

Original Russian Text Copyright © 2005 by Lukatkin.

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Lukatkin, A.S. Initiation and Development of Chilling Injury in Leaves of Chilling-Sensitive Plants. Russ J Plant Physiol 52, 542–546 (2005). https://doi.org/10.1007/s11183-005-0080-z

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