Journal of Ecology and Environment

The Ecological Society of Korea (한국생태학회)
권호 표지
DOI QR코드

DOI QR Code

Over-expression of Cu/ZnSOD Increases Cadmium Tolerance in Arabidopsis thaliana

  • Cho, Un-Haing (Department of Biology, Changwon National University)
  • Published : 2007.08.30
Download PDF
⟨ Previous Next ⟩

Abstract

Over-expression of a copper/zinc superoxide dismutase (Cu/ZnSOD) resulted in substantially increased tolerance to cadmium exposure in Arabidopsis thaliana. Lower lipid peroxidation and $H_2O_2$ accumulation and the higher activities of $H_2O_2$ scavenging enzymes, including catalase (CAT) and ascorbate peroxidase (APX) in transformants (CuZnSOD-tr) compared to untransformed controls (wt) indicated that oxidative stress was the key factor in cadmium tolerance. Although progressive reductions in the dark-adapted photochemical efficiency (Fv/Fm) and quantum efficiency yield were observed with increasing cadmium levels, the chlorophyll fluorescence parameters were less marked in CuZnSOD-tr than in wi. These observations indicate that oxidative stress in the photosynthetic apparatus is a principal cause of Cd-induced phytotoxicity, and that Cu/ZnSOD plays a critical role in protection against Cd-induced oxidative stress.

Keywords

References

  1. Asada K. 1992. Ascorbate peroxidase - a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85: 235-241 https://doi.org/10.1111/j.1399-3054.1992.tb04728.x
  2. Baryla A, Carrier P, Franck F, Coulomb C, Sahut, Havaus M. 2001. Lea chlorosis in oilseed rape plants (Brassica napus) grown on cadmium polluted soil: causes and consequences for photosynthesis and growth. Planta 212: 696-709
  3. Boominathan R, Doran PM. 2003. Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotech & Bioengin 83: 158-167 https://doi.org/10.1002/bit.10656
  4. Borsani O, Diaz P, Agius MF, Valpuesta V, Monza J. 2001. Water stress generates an oxidative stress through the induction of a specific Cu/Zn superoxide dismutase in Lotus corniculatus leaves. Plant Sci 161: 757-763 https://doi.org/10.1016/S0168-9452(01)00467-8
  5. Bowler C, Van Montagu T, Inze D. 1992. Sueroxide dismutase and stress tolerance. Annu Rev Plant Physiol 43: 83-116 https://doi.org/10.1146/annurev.pp.43.060192.000503
  6. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantity of protein utilizing the principle of proteindye binding. Anal Biochem 72: 248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  7. Buege JA, Aust SD. 1978. Microsomal lipid peroxidation. Methods Enzymol 52: 302-310 https://doi.org/10.1016/S0076-6879(78)52032-6
  8. Cakmak I, Horst WJ. 1991. Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83: 463-468 https://doi.org/10.1111/j.1399-3054.1991.tb00121.x
  9. Chance B, Maehly AC. 1955. Assay of catalase and peroxidases. Methods Enzymol 2: 764-817 https://doi.org/10.1016/S0076-6879(55)02300-8
  10. Chiang HC, Lo JC, Yeh KC. 2006. Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Tech 40: 6792-6798 https://doi.org/10.1021/es061432y
  11. Cho UH, Park JO. 2000. Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156: 1-9 https://doi.org/10.1016/S0168-9452(00)00227-2
  12. Cho UH, Seo NH. 2005. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168: 113-120 https://doi.org/10.1016/j.plantsci.2004.07.021
  13. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x
  14. De Vos CHR, Schat H, De Waal MAM, Vooijs R, Ernst WHO. 1991. Increased resistance to copper-induced damage of the root cell plasmalemma in copper-tolerant Silene cucubalus. Physiol Plantarum 82: 523-528 https://doi.org/10.1111/j.1399-3054.1991.tb02942.x
  15. De Vos CHR, Ten Boukum WM, Vooijs R, Schat H, De Kok LJ. 1993. Effect of copper on fatty acid composition and peroxidation of lipids in the roots of copper-tolerant and sensitive Silene cucubalus. Plant Physiol Bioch 31: 151-158
  16. Dhindsa RS, Dhindsa P, Thorpe TA. 1987. Leaf senescence correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32: 93-101 https://doi.org/10.1093/jxb/32.1.93
  17. Droillard M-J, Paulin A. 1990. Isozymes of superoxide dismutase in mitochondria and peroxisomes isolated from petals of carnation (Dianthus caryophyllus) during senescence. Plant Physiol 94: 1187-1192 https://doi.org/10.1104/pp.94.3.1187
  18. Elstner EF. 1991. Mechanisms of oxygen activation in different compartments of plant cells. In: Active Oxygen Species, Oxidative Stress, and Plant Metabolism (Pell EJ, Steffen KL, eds). American Society of Plant Physiologists, Rockville, pp 13-25
  19. Ezaki B, Gardner RC, Ezaki Y, Matsumoto H. 2000. Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122: 657-65 https://doi.org/10.1104/pp.122.3.657
  20. Fridovich I. 1986. Biological effects of the superoxide radical. Arch Biochem Biophys 247: 1-11 https://doi.org/10.1016/0003-9861(86)90526-6
  21. Gay C, Gebicki JM. 2000. A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284: 217-220 https://doi.org/10.1006/abio.2000.4696
  22. Halliwell B, Gutteridge JMC. 1984. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219: 1-14 https://doi.org/10.1042/bj2190001
  23. Hegedus A, Erdei S, Horvath G. 2001. Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 160: 1085-1093 https://doi.org/10.1016/S0168-9452(01)00330-2
  24. Ianneli MA, Pietrini F, Fiore L, Petrilli L, Massaci A. 2002. Antioxidant response to cadmium in Phragmites austalis plants. Plant Physiol Biochem 40: 977-982 https://doi.org/10.1016/S0981-9428(02)01455-9
  25. Imlay JA, Linn S. 1988. DNA damage and oxygen radical toxicity. Science 240: 1302-1309 https://doi.org/10.1126/science.3287616
  26. Jacob C, Courbot M, Brun A, Steinman HM, Jacquot JP, Botton B, Chalot M. 2001. Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. European J Biochem 268: 3223- 3232 https://doi.org/10.1046/j.1432-1327.2001.02216.x
  27. Kaiser W. 1976. The effect of hydrogen peroxide on $CO^{2}$ fixation of isolated intact chloroplast. Biochem Biophys Acta 440: 475-482<
  28. Kamikana H, Morita S, Tokumoto M, Masamura T, Tanka K. 1999. Differential gene expression of rice superoxide dismutase isoforms to oxidative and environmental stresses. Free Radical Res 31: 219-225 https://doi.org/10.1080/10715769900301541
  29. Kliebenstein DJ, Monde R-A, Last RL. 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118: 637-650 https://doi.org/10.1104/pp.118.2.637
  30. Kupper H, Mijovilovich A, Meyer-Klaucke W, Kroneck PMH. 2004. Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges Ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol 134: 748-757 https://doi.org/10.1104/pp.103.032953
  31. Lee EH, Bennett JH. 1982. Superoxide dismutase A possible protective enzyme against ozone injury in snap beans (Phaseolus vulgaris L.). Plant Physiol 69: 1444-1449 https://doi.org/10.1104/pp.69.6.1444
  32. Lee DH, Lee CB. 2000 Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159: 75-85 https://doi.org/10.1016/S0168-9452(00)00326-5
  33. Lozano-Rodriguez E, Hermandez LE, Bonay P, Carpena Euiz RO. 1997. Distribution of Cd in shoot and root tissues of maize and pea plants: Physiological disturbances. J Exp Bot 306: 123-128
  34. Maksymiec W, Krupa Z. 2006. The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57: 187-194 https://doi.org/10.1016/j.envexpbot.2005.05.006
  35. McCord JM, Fridovich I. 1969. Superoxide dismutase: An enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244: 6049-6055
  36. McKersie BD, Murnaghan J, Jones KS, Bowley SR. 2000. Iron-superoxide dismutase expression in transgenic alfalfa increases winter survival without a detectable increase in photosynthetic oxidative stress tolerance. Plant Physiol 122: 1427-1437 https://doi.org/10.1104/pp.122.4.1427
  37. Mishra NP, Mishra RK, Singhal GS. 1993. Changes in the activities of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiol 102: 903-910 https://doi.org/10.1104/pp.102.3.903
  38. Pandolfini T, Gabbrielli R, Comparini C. 1992. Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ 15: 719-725 https://doi.org/10.1111/j.1365-3040.1992.tb01014.x
  39. Pietrini F, Iannelli MA, Pasqualini S, Massacci A. 2003. Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (CAv.) Trin. Ex Steudel. Plant Physiol 133: 829-837 https://doi.org/10.1104/pp.103.026518
  40. Pilon-Smits EAG, Zhu Y, Sears T, Terry N. 2000. Overexpression of glutathione reductase in Brassica juncea: Effects on cadmium accumulation and tolerance. Physiol Plant 110: 455-460 https://doi.org/10.1111/j.1399-3054.2000.1100405.x
  41. Pilon-Smits EAG, Zhu Y, Sears T, Terry N. 2000. Overexpression of glutathione reductase in Brassica juncea: Effects on cadmium accumulation and tolerance. Physiol Plant 110: 455-460 https://doi.org/10.1111/j.1399-3054.2000.1100405.x
  42. Pitcher LH, Brennan E, Hurley A, Dunsmuir P, Tepperman JM, Zilinskas BA. 1991. Overproduction of petunia chloroplastic copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco. Plant Physiol 97: 452-455 https://doi.org/10.1104/pp.97.1.452
  43. Polle A. 1997. Defense against photooxidative damage in plants. In: Oxidative Stress and the Molecular Biology of Antioxidants Defense (Scandalios J, ed). Cold Spring Harbor Laboratory Press. pp. 623-666
  44. Rao MV, Hale BA, Ormond DP. 1995. Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiol 109: 421-432 https://doi.org/10.1104/pp.109.2.421
  45. Rauser WE. 1987. Changes in glutathione content of maize seedlings exposed to cadmium. Plant Sci 51: 171-175 https://doi.org/10.1016/0168-9452(87)90190-7
  46. Reddy AM, Kumar SG, Jyothsnakumari G, Thimmanaik S, Sudhakar C. 2005. Lead induced changes in antioxidant metabolism of horsegram (Macrotyloma uniflorum (Lam.) Verdc.) and bengalgram (Cicer arietinum L.). Chemosphere 60: 97-104 https://doi.org/10.1016/j.chemosphere.2004.11.092
  47. Schutzendubel A, Schwanz P, Teichnan T, Gross K. 2001. Cadmiuminduced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127: 887-898 https://doi.org/10.1104/pp.010318
  48. Somashekaraiah BV, Padmaja K, Prasad ARK. 1992. Phytoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85: 85-89 https://doi.org/10.1111/j.1399-3054.1992.tb05267.x
  49. Thomas DJ, Thomas JB, Prier SD, Nasso NE, Herbert SK. 1999. Iron superoxide dismutase protects against chilling damage in the Cyanobacterium synechococcus species. Plant Physiol 120: 275-282 https://doi.org/10.1104/pp.120.1.275
  50. Wu G, Wilen RW, Robertson AJ, Gusta LV. 1999. Isolation chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol 120: 513-520 https://doi.org/10.1104/pp.120.2.513
  51. Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H. 2002. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species on plant cells. Plant Physiol 128: 63-72 https://doi.org/10.1104/pp.010417
  52. Zhang F-Q, Wang Y-S, Lou Z-P, Dong J-D. 2007. Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67: 44-50 https://doi.org/10.1016/j.chemosphere.2006.10.007