Production of reactive oxygen species by freezing stress and the protective roles of antioxidant enzymes in plants

Kwang-Hyun Baek, Daniel Z. Skinner

School of Biotechnology, Yeungnam University, Gyeongsan, South Korea.
USDA/ARS, Department of Crop and Soil Sciences, Washington State University, Pullman, USA.

DOI: 10.4236/jacen.2012.11006                

Abstract

As one of the most severe environmental stresses, freezing stress can determine native flora in nature and severely reduce crop production. Many mechanisms have been proposed to explain the damage induced by freezing-thawing cycle, and oxidative stress caused by uncontrollable production of harmful reactive oxygen species (ROS) are partially contributed to causing the injury. Plants in temperate regions have evolved a unique but effective metabolism of protecting themselves called cold acclimation. Cold-acclimating plants undergo a complex but orchestrated metabolic process to increase cold hardness triggered by exposure to low temperature and shortened photoperiod and achieve the maximum freezing tolerance by a concerted regulation and expression of a number of cold responsive genes. A complicated enzymatic system have been evolved in plants to scavenge the ROS to protect themselves from oxidative stress, therefore, cold-acclimating plants are expected to increase the de novo synthesis of the genes of antioxidant genes. Indeed, many antioxidant genes increase the expression levels in response to low temperature. Furthermore, the higher expression of many antioxidant enzymes are positively correlated to inducing higher tolerance levels against freezing. All the information summarized here can be applied for developing crop and horticultural plants to have more freezing tolerance for higher production with better quality. There have been extensive studies on the activities of antioxidant enzymes and the gene regulation, however, more researches will be required in near future to elucidate the most effective antioxidant enzymes to induce highest freezing tolerance in a crop plant in a transformation process or a breeding program.

Keywords

Antioxidant Enzymes; Cold Acclimation; Freezing Stress; Manganese Superoxide Dismutase; Reactive Oxygen Species

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Singh, K. and Purohit, S.S. (1995) Plant productivity under environmental stress. Vedams eBooks (P) Ltd, New Delhi.
[2]	Sakai, A. and Larcher, W. (1987) Frost survival of plants. Springer-Verlag, New York. doi:10.1007/978-3-642-71745-1
[3]	Yoshida, S. and Uemura, M. (1990) Responses of the plasma membrane to cold acclimation and freezing stress. In: Larsson C. and Moller, I.M. Eds., The Plant Plasma Membrane: Structure, Function, and Molecular Biology, Springer-Verlag, Berlin Heidelberg, 293-319.
[4]	Viswanathan, C., Jianhua, Z. and Jian-Kang, Z. (2007) Cold stress regulation of gene expression in plants. Trends in Plant Science, 12, 444-451. doi:10.1016/j.tplants.2007.07.002
[5]	Allan, R.E., Pritchett, J.A. and Little, L.M. (1992) Cold injury observation. Annual Wheat Newsletter, 38, 281.
[6]	Burke, M.J., Gusta, L.V., Quamme, H.A., Weiser, C.J. and Li, P. H. (1978) Freezing and injury in plants. Annual Review of Plant Physiology, 27, 507-528. doi:10.1146/annurev.pp.27.060176.002451
[7]	Guy, C.L. (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annual Review of Plant Physiology and Plant Molecular Biology, 41, 187-223. doi:10.1146/annurev.pp.41.060190.001155
[8]	Thomashow, M.F. (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiology, 125, 89-93. doi:10.1104/pp.125.1.89
[9]	Stushnoff, C., Fowler, D.B. and Brule-Babel, A. (1984) Breeding and selection for resistance to low temperature. In: Vose, P.B. Ed., Plant Breeding: A Contemporary Basis, Pergamon Press, Oxford, 115-136.
[10]	Taiz, L. and Zeiger, E. (2006) Plant physiology. 4th Edition, Sinauer Associates, Inc., Sunderland.
[11]	Salisbury, F.B. and Ross, C.W. (1991) Plant physiology. 4th Edition, Wadsworth Publishing Company, Beverly, 481.
[12]	Gilmour, S.J., Hajela, R.K. and Thomashow, M.F. (1988) Cold acclimation in Arabidopsis thaliana. Plant Physiology, 87, 745-750.doi:10.1104/pp.87.3.745
[13]	Tseng, M.J. and Li, P.H. (1987) Changes in nucleic acid and protein synthesis during induction of cold hardiness. In: Li, P.H. Ed., Plant Cold Hardiness, Alan R. Liss, Inc., New York, 1-28.
[14]	Palva, E.T. and Pekka, H. (1997) Molecular mechanism of plant cold acclimation and freezing tolerance. In: Li, P.H. and Chen, T.H.H., Eds., Plant Cold Hardiness, Plenum Press, New York, 3-14.
[15]	Trischuk, R.G., Schilling, B.S. Wisniewski, M. and Gusta, L.V. (2006) Freezing stress: Systems biology to study cold tolerance. In: Madhava Rao, K.V., Raghavendra, A.S. and Janardhan R.K., Eds., Physiology and Molecular Biology of Stress Tolerance in Plants, Springer, Dordrecht, 131-155.
[16]	Seki, M., et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant Journal, 31, 279-292. doi:10.1046/j.1365-313X.2002.01359.x
[17]	Halliwell, B. and Gutteridge, J.M.C. (2007) Free radicals in biology and medicine. 4th Edition, Oxford University Press, New York.
[18]	Zelko, I.N., Mariani, T.J. and Folz, R.J. (2002) Superoxide dismutase multigene family: A comparison of the CuZn- SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radical Biology and Medicine, 33, 337-349. doi:10.1016/S0891-5849(02)00905-X
[19]	Fridovich, I. (1991) Molecular oxygen: Friend and foe. In: Pell, E.J. and Steffen, K.L. Eds., Active Oxygen/Oxidative Stress and Plant Metabolism, American Society of Plant Physiologists, Rockville, 1-5.
[20]	Zhang, J. and Kirkham, M.B. (1994) Drought-stress-induced changed in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiology, 35, 785-791.
[21]	Allen, R.D. (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiology, 107, 1049-1054.
[22]	Monk, L.S., Fagerstedt, K.V. and Crawford, R.M.M. (1989) Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiologia Plantarum, 76, 456-459.
[23]	Scandalios, J.G. (1993) Oxygen stress and superoxide dismutases. Plant Physiology, 101, 7-12.
[24]	Benson, E.E. and Noronha-Dutra, A.A. (1988) Chemiluminiscence in cryopreserved plant tissue cultures: The possible involvement of singlet oxygen in cryoinjury. CryoLetters, 9, 120-131.
[25]	McKersie, B.D. and Bowley, S.R. (1997) Active oxygen and freezing tolerance in transgenic plants. In: Li, P.H. and Chen, T.H.H., Eds., Plant Cold Hardiness, Plenum Press, New York, 203-214.
[26]	Park, J.I., Grant, C.N., Davies, M.J. and Dawes, I.W. (1998) The cytoplasmic Cu, Zn superoxide dismutase of Saccharomyces cerevisiae is required for resistance to freezethaw stress. Generation of free radicals during freezing and thawing. Journal of Biological Chemistry, 273, 22921- 22928. doi:10.1074/jbc.273.36.22921
[27]	Kendall, E.J. and McKersie, B.B. (1989) Free radical and freezing injury to cell membranes of winter wheat. Physiologia Plantarum, 76, 86-94. doi:10.1111/j.1399-3054.1989.tb05457.x
[28]	Davies, K.J.A. (1995) Oxidative stress: The paradox of aerobic life. In: Rice-Evans, C., Halliwell, B., Lunt, G.G., Eds., Free Radicals and Oxidative Stress: Environment, Drugs, and Food Additives, Biochemical Society Symposium 61, Portland Press, London, 1-32.
[29]	Fink, R.C. and Scandalios, J.G. (2002) Molecular evolution and structure-function relationships of the superoxide dismutase gene families in Angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Archives of Biochemistry Biophysics, 399, 19-36. doi:10.1006/abbi.2001.2739
[30]	Smith, M.W. and Doolittle, R.F. (1992) A comparison of evolutionary rates of the two major kinds of superoxide dismutase. Journal of Molecular Evolution, 34, 175-184. doi:10.1007/BF00182394
[31]	Asada, K. (1999) The water-water cycle in chloroplast: Scavenging of active oxygens and dissipation of excess photons. Annul Review of Plant Physiology and Plant Molecular Biology, 50, 601-639. doi:10.1146/annurev.arplant.50.1.601
[32]	Apel, K. and Hirt, H. (2004) Reactive oxygen species: Metabolism, oxidation stress, and signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology, 55, 373-399.
[33]	Levine A., Tenhaken, R., Dixon, R. and Lamb, C. (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593. doi:10.1016/0092-8674(94)90544-4
[34]	O’Kane, D., Gill, V., Boyd, P. and Burdon, R. (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta, 198, 371-377. doi:10.1007/BF00620053
[35]	Shinozaki, K. and Yamajuchi-Shinozaki, K. (1997) Gene expression and signal transduction in water-stress response. Plant Physiology, 115, 327-334. doi:10.1104/pp.115.2.327
[36]	Wu, G., Shortt, B.J., Lawrence, E.B., Fitzsimmons, J.L.K.C., Levine, E.B., Raskin, I. and Shah, D.M. (1997) Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants. Plant Physiology, 115, 427- 435.
[37]	Prasad, T.K., Anderson, M.D., Martin, B.A. and Stewart, C.R. (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell, 6, 65-74.
[38]	Prasad, T.K., Anderson, M.D. and Stewart, C.R. (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiology, 105, 619-627.
[39]	Mittler, R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405-410. doi:10.1016/S1360-1385(02)02312-9
[40]	Baek, K.H. and Skinner, D.Z. (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near isogenic wheat lines. Plant Science, 165, 1221- 1227. doi:10.1016/S0168-9452(03)00329-7
[41]	Miao, Z. and Gaynor, J.J. (1993) Molecular cloning, characterization and expression of Mn-superoxide dismutase from the rubber tree (Hevea brasiliensis). Plant Molecular Biology, 23, 267-277. doi:10.1007/BF00029003
[42]	Zhu, D. and Scandalios, J.G. (1993) Maize mitochondrial manganese superoxide dismutases are encoded by a differentially expressed multigene family. Proceedings of the National Academy Sciences of United States of America, 90, 9310-9314. doi:10.1073/pnas.90.20.9310
[43]	Wu, G., Wilen, R.W., Robertson, A.J. and Gusta, L.V. (1999) Isolation, chromosomal localization, and differenttial expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiology, 120, 513-520. doi:10.1104/pp.120.2.513
[44]	Baek, K.H. and Skinner, D.Z. (2006) Differential expression of manganese superoxide dismutase sequence variants in near isogenic lines of wheat during cold acclimation. Plant Cell Reports, 25, 223-230. doi:10.1007/s00299-005-0073-6
[45]	Baek, K.H. and Skinner, D.Z. (2006) Differential mRNA stability to endogenous ribonucleases of the coding region and 3’ untranslated regions of wheat (Triticum aestivum l.) manganese superoxide dismutase genes. Plant Cell Reports, 25, 133-139. doi:10.1007/s00299-005-0046-9
[46]	Carlioz, A. and Touati, D. (1986) Isolation of superoxide dismutase mutants in Escherichia coli is superoxide necessary for aerobic life? EMBO, 5, 623-630.
[47]	Van Loon, A.P., Pesold-Hurt, B. and Shatz, G. (1986) A yeast mutant lacking mitochondrial manganese-superoxide dismutase is hypersensitive to oxygen. Proceedings of the National Academy Sciences of United States of America, 83, 3820-3824. doi:10.1073/pnas.83.11.3820
[48]	Bowler, C., Alliotte, T., Bulcke, M.V.D., Bauw, G., Vandekerckhove, J., Montagu, M. V. and Inze, D. (1989) A plant manganese superoxide dismutase is efficiently imported and correctly processed by yeast mitochondria. Proceedings of the National Academy of Sciences of United States of America, 86, 3237-3241. doi:10.1073/pnas.86.9.3237
[49]	McKersie, B.D., Chen, Y., De Beus, M., Bowley, S.R., Bowler, C., Inze, D., D’Halluin, K. and Botterman, J. (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiology, 103, 1155-1163. doi:10.1104/pp.103.4.1155
[50]	Clare, D. A., Rabinowitch, H. D. and Fridovich, I. (1984) Superoxide dismutase and chilling injury in Chlorella ellipsoidea. Archives of Biochemistry and Biophysics, 231, 158-168. doi:10.1016/0003-9861(84)90372-2
[51]	Basu, U., Good, A.G. and Taylor, G.J. (2001) Transgenic Brassica napus plants overexpressing aluminum-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminum. Plant, Cell, and Environment, 24, 1269-1278. doi:10.1046/j.0016-8025.2001.00783.x
[52]	Van Breusegem, F., Slooten, V., Stassart, J.M., Botterman, J., Moens, T., van Montagu, M. and Inze, D. (1999) Effects of overproduction of tobacco MnSOD in maize chloroplasts on foliar tolerance to cold and oxidative stress. Journal of Experimental Botany, 50, 71-78.
[53]	Baek, K.H. and Skinner, D.Z. (2010) Molecular cloning and expression of sequence variants of manganese superoxide dismutase genes from wheat. Korean Journal of Environmental Agriculture, 29, 77-85. doi:10.5338/KJEA.2010.29.1.077
[54]	Holmberg, N. and Bülow, L. (1998) Improving stress tolerance in plants by gene transfer. Trends in Plant Science, 3, 61-66. doi:10.1016/S1360-1385(97)01163-1