Browse > Article
http://dx.doi.org/10.5010/JPB.2005.32.3.151

Transgenic Plants with Enhanced Tolerance to Environmental Stress by Metabolic Engineering of Antioxidative Mechanism in Chloroplasts  

Kwon Suk-Yoon (Laboratory of Environmental Biotechnology, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Lee Young-Pyo (Laboratory of Environmental Biotechnology, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Lim Soon (Laboratory of Plant Cell Biotechnology, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Lee Haeng-Soon (Laboratory of Plant Cell Biotechnology, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Kwak Sang-Soo (Laboratory of Environmental Biotechnology, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Publication Information
Journal of Plant Biotechnology / v.32, no.3, 2005 , pp. 151-159 More about this Journal
Abstract
Injury caused by reactive oxygen species (ROS), known as oxidative stress, is one of the major damaging factors in plants exposed to environmental stress. Chloroplasts are specially sensitive to damage by ROS because electrons that escape from the photosynthetic electron transfer system are able to react with relatively high concentration of $O_2$ in chloroplasts. To cope with oxidative stress, plants have evolved an efficient ROS-scavenging enzymes such as superoxide dismutase (SOD) and ascorbate peroxidase (APX), and low molecular weight antioxidants including ascorbate, glutathione and phenolic compounds. To maintain the productivity of plants under the stress condition, it is possible to fortify the antioxidative mechanisms in the chloroplasts by manipulating the antioxidation genes. A powerful gene expression system with an appropriate promoter is key requisite for excellent stress-tolerant plants. We developed a strong oxidative stress-inducible peroxidase (SWPA2) promoter from cultured cells of sweetpotato (Ipomoea batatas) as an industrial platform technology to develop transgenic plants with enhanced tolerance to environmental stress. Recently, in order to develop transgenic sweetpotato (tv. Yulmi) and potato (Solanum tuberosum L. cv. Atlantic and Superior) plants with enhanced tolerance to multiple stress, the genes of both CuZnSOD and APX were expressed in chloroplasts under the control of an SWPA2 promoter (referred to SSA plants). As expected, SSA sweetpotato and potato plants showed enhanced tolerance to methyl viologen-mediated oxidative stress. In addition, SSA plants showed enhanced tolerance to multiple stresses such as temperature stress, drought and sulphur dioxide. Our results strongly suggested that the rational manipulation of antioxidative mechanism in chloroplasts will be applicable to the development of all plant species with enhanced tolerance to multiple environmental stresses to contribute in solving the global food and environmental problems in the 21st century.
Keywords
Antioxidant; chloroplast; oxidative stress; reactive oxygen species; transgneic plants;
Citations & Related Records
Times Cited By KSCI : 4  (Citation Analysis)
연도 인용수 순위
1 Tepperman JM, Dunsmuir P (1990) Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxicity. Plant Mol Biol 14:501-511   DOI
2 UNEP (2002) Global Environment Outlook 3. Earthscan, pp 1-446
3 Van Breusegem F, Slooten L, Stassart JM, Moens T, Botterman J, Van Motagu M, Inze D (1999) Overexpression of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol 40: 515-523   DOI   ScienceOn
4 Van Camp W, Willekens H, Bowler C, Van Montagu M, Inze D, Reupold-Popp P, Sandermann H, Langebartels C (1994) Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. Bio/Technology 12: 165-168   DOI
5 Van Huystee RB (1987) Some molecular aspects of plant peroxidase: Biosynthetic studies. Annu Rev Plant Physiol 38: 205-219   DOI
6 Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutases. J Plant Physiol 162: 465-472   DOI   ScienceOn
7 Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393: 365-369   DOI   ScienceOn
8 Yun BW, Huh GH, Lee HS, Kwon SY, Jo JK, Kim JS, Cho KY, Kwak SS (2000) Differential resistance to methyl viologen in transgenic tobacco plants that express sweet potato peroxidases. J Plant Physiol 156: 504-509   DOI   ScienceOn
9 Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroixidase enhances the growth of transgenic tobacco seedling during stress. Nature Biotech 15: 988- 991   DOI   ScienceOn
10 Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco ssedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41: 1229-1234   DOI   ScienceOn
11 Sen Gupta A, Heinen J, Holaday AS, Burke JJ, Allen RD (1993a) Increased resistance to oxidative stress in transgenic plants that over-express chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA 90: 1629-1633   DOI   ScienceOn
12 Sen Gupta A, Webb RP, Holaday AS, Allen RD (1993b) Overexpression of superoxide dismutases protects plants from oxidative stress. Plant Physiol 103: 1067-1073   DOI
13 Slooten L, Capiau K, Van Montagu M, Sybesma C, Inze D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in the chloroplasts. Plant Physiol 107: 737-750   DOI
14 Smirnoff N, Pallanca JE (1996) Ascorbate metabolism in relation to oxidative stress. Biochem Soci Trans 24: 472-478   DOI
15 Tang L (2005) Development and characterization of transgenic potato plants with enhanced tolerance to environmental stress. Ph.D thesis, Chungnam National University, Daejeon
16 Tang L, Kwon SY, Kwak SS, Sung CK, Lee HS (2004a) Selection of transgenic potato plants expressing both CuZnSOD and APX in chloroplasts with enhanced tolerance to oxidative stress. Kor J Plant Biotechnol 31: 109-113   과학기술학회마을   DOI   ScienceOn
17 Mehler AH (1951) Studies on reaction of illuminated chloroplasts I. Mechanisms of the reaction of oxygen and other Hill reagents. Arch Biochem Biophys 33: 65-67   DOI
18 Tang L. Kwon SY, Yun DJ, Kwak SS, Lee HS (2004b) Selection of transgenic potato plants expressing NDP kinase 2 gene with enhanced tolerance to oxidative stress. Kor J Plant Biotechnol 31: 191-195   과학기술학회마을   DOI   ScienceOn
19 McKersie BD, Murnaghan J, Bowley SR (1997) Manipulating freezing tolerance in transgenic plants. Acta Physiol Plant 19: 485-495   DOI   ScienceOn
20 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   DOI
21 Moon HJ, Lee BY, Choi GT, Shin DJ, Theertha Prasad D, Lee OS, Kwak SS, Kim DH, Nam JS, Bahk JD, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) Nucleoside diphosphate kinase 2 interacts with two oxidative stress-activated mitogen-activated protein kinases to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100: 358-363   DOI   ScienceOn
22 Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880
23 Orvar BL, Ellis BE (1997) Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. Plant J 11: 1297-1305   DOI   ScienceOn
24 Oyanagui Y (1989) SOD and Active Oxygen Modulators: pharmacology and clinical trials. Nihon-Igakukan, Tokyo, pp 1-859
25 Lee HS, Kwon EJ, Jeong YJ, Kwon SY, Lee EM, Jo MH, Kim HS, Woo IS, Kwak SS (2003) Transgenic cucumber fruits that produce high level of an anti-aging superoxide dismutase. Mol Breeding 11: 213-220   DOI   ScienceOn
26 Park SY, Ryu SH, Kwon SY, Lee HS, Kim JG, Kwak SS (2003) Differential expression of six novel peroxidase cDNAs derived from sweetpotato cell cultures in response to stress. Mol Genet Genomics 269: 542-552   DOI
27 Perl A, Perl-Treves R, Galili S, Aviv D, Shalgi E, Malkin S, Galun E (1993) Enhanced oxidative-stress defence in transgenic potato expression tomato Cu,Zn superoxide dismutase. Theor Appl Genet 85: 568-576
28 Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, Allen RD, Kwak SS (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant Cell Environ 25: 873-882   DOI
29 Lee YP, Kwon SY, Bang JW, Kwak SS (2004) Characterization of transgenic tobacco plants expression of CuZnSOD, APX and DHAR in chloroplasts. Proceeding of Vision for Practical Use of Biotechnology. October 22-23, 2004. The 2004 Annual Conference of the Korean Society of Plant Biotechnology. Dong-A University. pp 99
30 Lim S, Lee HS, Kwon SY, Kwak SS (2004) Development of transgenic sweetpotato plants with enhanced tolerance to environmental stress. Proceedings of the Internatinal Workshop on Production, Utilization and Development of Sweetpotato. September 6-10,2004. Mokpo Experiment Station, NICS/RDA. pp 31-39.
31 Lim S, Yang KS, Kim YH, Kwon SY, Han SH, Lee JC, Paek KY, Lee HS, Kwak SS (2005) Transgenic sweetpotato (Ipomoea batatas Lam.) plants with enhanced tolerance to $SO_2$. Proceeding of Plant Biotechnology and Human Welfare. April 22-23, 2005. The 2005 Annual Conference of the Korean Society of Plant Biotechnology. Samsung Traning Center, Daejeon. pp 79
32 Kim KY, Kwon SY, Lee HS, Hur YK, Bang JW, Kwak SS (2003a) A novel oxidative stress-inducible peroxidase promoter from sweet potato: molecular cloning and characterization in transgenic tobacco plants and cultured cells. Plant Mol Biol 51: 831-838   DOI   ScienceOn
33 McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein. J Inorg Biochem 244: 6049-6055
34 McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111: 1177-1181   DOI
35 McKersie BD, Chen Y, De Beus M, Bowley SR, Bowler C (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol 103: 1155-1163   DOI
36 Kim MJ, Choi YH, Kim WG, Kwak SS (1997a) Antioxidative activity of urushiol components from the sap of lacquer tree (Rhus vernicifera STOKES). Kor J Plant Resour 10: 227-230
37 Kim MJ, Kim CJ, Kwak SS (1997b) Antifungal activity of urushiol components from the sap of lacquer tree (Rhus vernicifera STOKES). Kor J Plant Resour 10: 231-234
38 Kim YH, Kwon SY, Bang JW, Kwak SS (2003b) Photosynthetic efficiency in transgenic tobacco plants expressing both CuZnSOD and APX in chloroplasts against oxidative stress caused by highlight and chilling. Kor J Plant Biotechnol 30: 399-403   과학기술학회마을   DOI   ScienceOn
39 Kim YH, Ryu SH, Kim KY, Kwon SY, Bang JW, Kwak SS (2004) Induction of a sweetpotato anion peroxidase swpa2 gene expression by stress-related chemicals and Pectobacterium chrysanthemi. Kor J Plant Biotechnol 31: 83-88   과학기술학회마을   DOI   ScienceOn
40 Krell HW (1991) Peroxidase: an important enzyme for diagnostic test kits. In Lobarzewski J, Greppin H, Pene C, Gasper T, (eds), Molecular and Physiology Aspects of Plant Peroxidase, Univ Geneva , pp 469-478
41 Kwon SY, Ahn YO, Lee HS, Kwak SS (2001) Biochemical characterization of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Biochem Mol Biol 34: 316-321
42 Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YB, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol 160: 347-353   DOI   ScienceOn
43 Deak M, Horvath GV, Davletova S, Torok K, Sass L, Vass I, Barna B. Kiraly Z, Dudits D (1999) Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative stress damage and pathogens. Nature Biotech 17: 192-196   DOI   ScienceOn
44 Filipe P, Emerit I, Vassy J , Rigaut JP, Martin E, Freitas J, Fernandes A (1997) Epidermal localization and protective effects of topically applied superoxide dismutase. Exp Dermatol 6: 116-121   DOI   ScienceOn
45 Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109: 1047-1057   DOI   ScienceOn
46 Hong DH, Han SB, Lee CW, Park SH, Jeon YJ, Kim MJ, Kwak SS, Kim HM (1999) Cytotoxicity of urushiols isolated from sap of Korean lacquer tree (Rhus vernicifera Stokes). Arch Pharm Res 22: 638-641   DOI   ScienceOn
47 Huh GH, Lee SJ, Bae YS, Liu JR, Kwak SS (1997) Molecular cloning and characterization of anionic and neutral peroxidase cDNAs from sweet potato suspension-cultured cells and their differential expression in response to stress. Mol Gen Gen 255: 382-391   DOI
48 Kim KY, Huh GH, Lee HS, Kwon SY, Hur Y, Kwak SS (1999) Molecular characterization of two anionic peroxidase cDNAs isolated from suspension cultures of sweet potato. Mol Gen Gen 261: 941-947   DOI   ScienceOn
49 Inze D, Van Montagu M (1995) Oxidative stress in plants. Curr Opin Biotechnol 6: 153-158   DOI   ScienceOn
50 Jeong YJ (2001) Characterization of environmental stress-tolerance in transgenic tobacco plants expressing both SOD and APX in the chloroplasts. MS Thesis, Chungnam National University, Daejeon
51 Asada K (1999) The water-water cycle in chloroplasts: Scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601-639   DOI
52 Babbs CF, Pham JA, Coolbaugh RC (1989) Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol 90: 1267-1270   DOI   ScienceOn
53 Bannister JV, Bannister WH, Rotilio G (1987) Aspects of the structure, function , and applications of superoxide dismutase. CRC Crit Rev in Biochem 22: 111-180   DOI
54 Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inze D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen redicals in transgenic plants. EMBO J 10: 1723-1732
55 Bowler C, Van Camp W, Van Montagu M, Inze D (1994) Superoxide dismutase in plants. CRC Crit Rev Plant Sci 13: 199-218   DOI
56 Broadbent P, Creissen GP, Kular B, Wellburn AR, Mullineaux P (1995) Oxidative stress reponse in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J 8: 247-255   DOI   ScienceOn
57 Conklin PL, Pallanca JE, Last RL, Smirnoff N (1997) L-ascorbic acid metabolism in the ascorbate-deficient arabidopsis mutant vtc1. Plant Physiol 115: 1277-1285   DOI
58 Deutsch JC, Santhosh-Kumar CR (1996) Dihydroascorbic acid undergoes hydrolysis on solubilization which can be reversed with mercaptoethanol. J Chromatogr 724: 271-278   DOI   ScienceOn
59 Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient arabidopsis mutant. Proc Natl Acad USA 93: 9970-9974   DOI   ScienceOn
60 Crowell DN, Amasino RM (1991) Nucleotide sequence of an iron superoxide dismutase complementary DNA from soybean. Plant Physiol 96: 1393-1394   DOI   ScienceOn
61 Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107: 1049-1054   DOI
62 Allen RD, Webb RP, Schake SL (1997) Use of transgenic plants to study antioxidants defenses. Free Rad Bioi Med 23: 473-479   DOI   ScienceOn
63 Alscher RG, Hess JL (1993) Antioxidants in higher plants. CRC Press, Boca Raton, pp 1-174
64 Aono M, Saji H, Sakamoto A, Tanaka K, Kondo N, Tanaka K (1995) Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase. Plant Cell Physiol 36: 1687-1691
65 Aono M, Kubo A, Saji H, Tanaka K, Kondo N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloropalstic glutathione reductase activity. Plant Cell Physiol 34: 129-136