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Enhanced tolerance of transgenic potato plants overexpressing nucleoside diphosphate kinase 2 against multiple environmental stresses

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Abstract

In plants, nucleoside diphosphate kinase 2 (NDPK2) is known to regulate the expression of antioxidant genes. In this study, we developed transgenic potato plants (Solanum tuberosum L. cv. Atlantic) expressing Arabidopsis NDPK2 (AtNDPK2) gene in cytosols under the control of an oxidative stress-inducible SWPA2 promoter (referred to as SN plants) or enhanced CaMV 35S promoter (EN plants) and evaluated their tolerance to various environmental stress, including methyl viologen (MV)-mediated oxidative stress, high temperature, and salt stress. When 250 μM MV was sprayed to whole plants, plants expressing NDPK2 showed significantly an enhanced tolerance compared to non-transgenic (NT) plants. SN plants and EN plants showed 51% and 32% less visible damage than NT plants, respectively. Transcript level of AtNDPK2 gene and NDPK2 activity in SN plants following MV treatment well reflected the plant phenotype. Ascorbate peroxidase (APX) activity was also increased in MV-treated SN plants. In addition, SN plants showed enhanced tolerance to high temperature at 42°C. The photosynthetic activity of SN plants after treatment of high temperature was decreased by about 10% compared to the plants grown at 25°C, whereas that of NT plants declined by 30%. When treated with 80 mM NaCl onto the plantlets, both SN plants and EN plants also showed a significant reduced damage in root growth. These results indicate that overexpression of NDPK2 under the stress-inducible SWPA2 promoter might efficiently regulate the oxidative stress derived from various environmental stresses.

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References

  • Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radic Biol Med 50:601–639

    Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Choi G, Yi H, Lee J, Kwon YK, Soh MS, Shin B, Luka Z, Hahn TR, Song PS (1999) Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401:610–613

    Article  PubMed  CAS  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  PubMed  CAS  Google Scholar 

  • Escobar Galvis ML, Marttila S, Hakansson G, Forsberg J, Knorpp C (2001) Heat stress response in pea involves interaction of mitochondrial nucleoside diphosphate kinase with a novel 86-kilodalton protein. Plant Physiol 126:69–77

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Descourvierse P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Ishikawa T, Morimoto Y, Madhusudhan R, Sawa Y, Shibata H, Yabuta Y, Nishizawa A, Shigeoka S (2005) Acclimation to diverse environmental stresses caused by a suppression of cytosolic ascorbate peroxidase in tobacco BY-2 cells. Plant Cell Physiol 46:1264–1271

    Article  PubMed  CAS  Google Scholar 

  • Jeong MJ, Park SC, Byun MO (2001) Improvement of salt tolerance in transgenic potato plants by glyceraldehyde-3 phosphate dehydrogenase gene transfer. Molecular Cell 12: 185–189

    CAS  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  PubMed  CAS  Google Scholar 

  • Kim KY, Huh GH, Lee HS, Kwon SY, Hur Y, Kwak SS (1999) Molecular characterization of cDNAs for two anionic peroxidases from suspension cultures of sweet potato. Mol Gen Genet 261:941–947

    Article  PubMed  CAS  Google Scholar 

  • Kim KY, Kwon SY, Lee HS, Hur Y, Bang JW, Kwak SS (2003) A novel oxidative stress-inducible peroxidase promoter from sweetpotato: molecular cloning and characterization in transgenic tobacco plants and cultured cells. Plant Mol Biol 51:831–838

    Article  PubMed  CAS  Google Scholar 

  • Kim SH, Hamada T (2005) Rapid and reliable method of extracting DNA and RNA from sweetpotato, Ipomoea batatas (L). Lam. Biotechnol Lett 27:1841–1845

    Article  PubMed  CAS  Google Scholar 

  • Kwak SS, Kim SK, Lee MS, Jung KH, Park IH, Liu JR (1995) Three acidic peroxidases from suspension-cultures of sweetpotato. Phytochemistry 39:981–984

    Article  CAS  Google Scholar 

  • Kwon SY, Jeong YJ, Lee HS, Kim JS, Cho KY, Allen RD, Kwak SS (2002) Enhanced tolerance 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

    Article  Google Scholar 

  • Lee SH, Ahsani N, Lee KW, Kim DH, Lee DG, Kwak SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol. doi:10.1016/j.jplph.2007.01.003

    Google Scholar 

  • Lim S, Kim YH, Kim SH, Kwon SY, Lee HS, Kim JS, Cho KW, Pack KY, Kwak SS (2007) Enhanced tolerance of transgenic sweetpotato plants that express both CuZnSOD and APX in chloroplasts to methyl viologen-mediated oxidative stress and chilling. Mol Breed 19:227–239

    Article  CAS  Google Scholar 

  • Mckerisie BD, Murnaghan J, Jones KS, Bowley SR (2000) Iron-superoxide dismutase expression in transgenic alfalfa increased winter survival without a detectable increase in photosynthetic oxidative stress tolerance. Plant Physiol 122:1427–1437

    Article  Google Scholar 

  • Moisyadi S, Dharmasiri S, Harrington HM, Lukas TJ (1994) Characterization of a low molecular mass autophosphorylating protein in cultured sugarcane cells and its identification as a nucleoside diphosphate kinase. Plant Physiol 104:1401–1409

    Article  PubMed  CAS  Google Scholar 

  • Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak SS, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun DJ (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358–363

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Otero AS (2000) NM23/nucleoside diphosphate kinase and signal transduction. J Bioenerg Biomembr 32:269–275

    Article  PubMed  CAS  Google Scholar 

  • Payton P, Allen R, Trolinder N, Holaday A (1997) Over-expression of chloroplast-targeted Mn Superoxide dismutase in cotton does not alter the reduction of photosynthesis after short exposures to low temperature and high light intensity. Photosynth Res 52: 233–244

    Article  CAS  Google Scholar 

  • Perl A, Perl-Treves R, Dalili S (1993) Enhanced oxidative stress defence in transgenic potato expressing Cu,Zn superoxide dismutase. Theor Appl Genet 85:568–576

    Article  CAS  Google Scholar 

  • Ross H (1986) Potato breeding: problems and perspectives. In Parey P (ed) Journal of Plant Breedings Suppl 13. Advances in Plant Breeding. Berlin and Hamburg pp. 132

  • Tang L, Kwon SK, Kwak SS, Sung CK, Lee HS (2004) Selection of transgenic potato plants expressing NDP kinase 2 gene with enhanced tolerance to oxidative stress. Kor J Plant Biotechnol 31:191–195

    Article  Google Scholar 

  • Tang L, Kwon SK, Kim SH, Kim JS, Choi JS, Cho KY, Cung CK, Kwak SS, Lee HS (2006) Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep 25:1380–1386

    Article  PubMed  CAS  Google Scholar 

  • Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472

    Article  PubMed  CAS  Google Scholar 

  • Yang KA, Moon HJ, Kim GT, Lim CJ, Hong JC, Lim CO, Yun DJ (2003) NDP kinase 2 regulates expression of antioxidant genes in Arabidopsis. Proc Jpn Acad Ser B 79(B):86–91

    Article  CAS  Google Scholar 

  • Yano A, Umeda M, Uchimiya H (1995) Expression of functional proteins of cDNA encoding rice nucleoside diphosphate kinase (NDK) in Escherichia coli and organ-related alteration of NDK activities during rice seed germination (Oryza sativa L.). Plant Mol Biol 27:1053–1058

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Shinmyo A (2000) Transgene expression systems in plants, a natural bioreactor. J Biosci Bioeng 90:353–362

    PubMed  CAS  Google Scholar 

  • Zimmermann S, Baumann A, Jaekel K, Marbach I, Engelberg D, Frohnmeyer H (1999) UV-responsive genes of Arabidopsis revealed by similarity to the Gcn4-mediated UV response in yeast. J Biol Chem 274:17017–17024

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by grants from BioGreen21 Program (code #20070301034015), Rural Development Administration, Korea, from the Environmental Biotechnology National Core Research Center, KOSEF/MOST, Korea, and from the Korea Foundation for International Cooperation of Science and Technology (KICOS).

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Correspondence to Haeng-Soon Lee.

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Tang, L., Kim, M.D., Yang, KS. et al. Enhanced tolerance of transgenic potato plants overexpressing nucleoside diphosphate kinase 2 against multiple environmental stresses. Transgenic Res 17, 705–715 (2008). https://doi.org/10.1007/s11248-007-9155-2

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  • DOI: https://doi.org/10.1007/s11248-007-9155-2

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