Nothing Special   »   [go: up one dir, main page]
Skip to main content
Springer Nature Link
Log in

Transgenic potato overproducing l-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity

  • Original Research Paper
  • Published:
Biotechnology Letters Aims and scope Submit manuscript

Abstract

Salt-tolerance was studied in transgenic potato. It was conferred by overexpression of ascorbate pathway enzyme (d-galacturonic acid reductase, GalUR). As genetic engineering of the GalUR gene in potato enhances its ascorbic acid content (l-AsA), and subsequently plants suffered minimal oxidative stress-induced damage, we now report on the comprehensive aptness of this engineering approach for enhanced salt tolerance in transgenic potato (Solanum tuberosum L. cv. Taedong Valley). Potatoes overexpressing GalUR grew and tuberized in continuous presence of 200 mM of NaCl. The transgenic plants maintained a higher reduced to oxidized glutathione (GSH:GSSG) ratio together with enhanced activity of glutathione dependent antioxidative and glyoxalase enzymes under salinity stress. The transgenics resisted an increase in methylglyoxal that increased radically in untransformed control plants under salinity stress. This is the first report of genetic engineering of ascorbate pathway gene in maintaining higher level of GSH homeostasis along with higher glyoxalase activity inhibiting the accumulation in methylglyoxal (a potent cytotoxic compound) under salt stress. These results suggested the engineering of ascorbate pathway enzymes as a major step towards developing salinity tolerant crop plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ASH:

Ascorbate

APx:

Ascorbate peroxidase

GalUR:

d-Galacturonic acid reductase

GPx:

Glutathione peroxidase

GR:

Glutathione reductase

Gly I:

Glyoxalase I

Gly II:

Glyoxalase II

MG:

Methylglyoxal

NADP:

Nicotinamide adenine dinucleotide phosphate

GSSG:

Oxidized glutathione

GSH:

Reduced glutathione

ROS:

Reactive oxygen species

UT:

Untransformed control

References

  • Agius F, Gonzalez-Lamothe R, Caballero JL, Mun˜oz-Blanco J, Botella MA, Valpuesta V (2003) Genetic engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181

    Article  PubMed  CAS  Google Scholar 

  • Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77:457–464

    Article  CAS  Google Scholar 

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Booth IR, Ferguson GP, Miller S, Li C, Gunasekera B, Kinghorn S (2003) Bacterial production of methylglyoxal: a survival strategy or death by misadventure? Biochem Soc Trans 31(Pt 6):1406–1408

    Article  PubMed  CAS  Google Scholar 

  • Broadbent P, Creissen GP, Kular B, Wellburn AR, Mullineaux P (1995) Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J 8:247–255

    Article  CAS  Google Scholar 

  • Conklin PL, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ 27:959–970

    Article  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Foyer CH, Shigeoka S (2001) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  Google Scholar 

  • Foyer CH, Souriau N, Perret S, Lelandaiis M, Kunert KJ, Prurost 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

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Theodoulou FL, Delrot S (2001) The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci 6:486–492

    Article  PubMed  CAS  Google Scholar 

  • Geiger PG, Lin F, Girotti AW (1993) Selenoperoxidase- mediated cytoprotection against the damaging effects of tert-butyl hydroperoxide on leukemia cells. Free Radic Biol Med 14:251–266

    Article  PubMed  CAS  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  PubMed  CAS  Google Scholar 

  • Grover A, Aggarwal PK, Kapoor A, Katiyar-Agarwal S, Agarwal M, Chandramouli A (2003) Addressing abiotic stresses in agriculture through transgenic technology. Curr Sci 84:355–367

    Google Scholar 

  • Habig WH, Jakoby WA (1981) Assays for determination of GST. Method Enzymol 77:735–740

    Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Hemavathi, Upadhyaya CP, Young KE, Nookaraju A, Kim HS, Heung JJ, Oh OM, Aswath CR, Chun SC, Kim DH, Park SW (2009) Over-expression of strawberry d-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance. Plant Sci 177:659–667

    Article  CAS  Google Scholar 

  • Hemavathi, Upadhyaya CP, Nookaraju A, Young KE, Chun SC, Kim DH, Park SW (2010a) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol Lett 32:321–330

    Article  PubMed  CAS  Google Scholar 

  • Hemavathi, Upadhyaya CP, Young KE, Nookaraju A, Kim HS, Heung JJ, Oh OM, Chun SC, Kim DH, Park SW (2010b) Biochemical analysis of enhanced tolerance in transgenic potato plants overexpressing d-galacturonic acid reductase gene in response to various abiotic stresses. Mol Breed. doi:10.1007/s11032-010-9465-6

  • Kalapos MP (1999) Methylglyoxal in living organisms: chemistry, biochemistry, toxicology and biological implications. Toxicol Lett 110:145–175

    Article  PubMed  CAS  Google Scholar 

  • Kampfenkel K, Van Montague M, Inze D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signaling during chilling and cold acclimation in plants. Physiol Plant 113:158–164

    Article  PubMed  CAS  Google Scholar 

  • Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human DHAR gene. J Plant Physiol 160:347–353

    Article  PubMed  CAS  Google Scholar 

  • Lee YP, Kim SH, Bang JW, Lee HS, Kwak SS, Kwon SY (2007) Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. Plant Cell Rep 26:591–598

    Article  PubMed  CAS  Google Scholar 

  • Martins AMTBS, Cordeiro CAA, Freire AMJP (2001) In situ analysis of methylglyoxal metabolism in Saccharomyces cerevisiae. FEBS Lett 499:41–44

    Article  PubMed  CAS  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Van Montagu M, Inze D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    Article  CAS  Google Scholar 

  • Meister A (1988) Glutathione metabolism and its selective modification. J Biol Chem 263:17205–17208

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nagalakshmi S, Prasad MNV (2001) Reponses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  PubMed  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 

  • Neill S, Desikan R, Hancock J (2003) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennerberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647

    Article  CAS  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    Article  PubMed  CAS  Google Scholar 

  • Oberschall A, Deak M, Torok K, Sass L, Vass I, Kovacs I, Feher A, Dudits D, Horvath GV (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. Plant J 24:437–446

    Article  PubMed  CAS  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Janovic S, Verrier N, Graham PJ, Foyer CH (2003) Leaf vitamin C content modulates plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951

    Article  PubMed  CAS  Google Scholar 

  • Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139:1291–1303

    Article  PubMed  CAS  Google Scholar 

  • Ramaswamy O, Guha-Mukherjee S, Sopory SK (1983) Presence of glyoxalase I in pea. Biochem Int 7:307–318

    CAS  Google Scholar 

  • Roxas VP, Smith RK, Ellen ER, Allen RD (1997) Overexpression of glutathione-S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    Article  PubMed  CAS  Google Scholar 

  • Saxena M, Bisht R, Roy SD, Sopory SK, Bhalla-Sarin N (2005) Cloning and characterization of a mitochondrial glyoxalase II from Brassica juncea that is upregulated by NaCl, Zn and ABA. Biochem Biophys Res Commun 336:813–819

    Article  PubMed  CAS  Google Scholar 

  • Scaife JF (1969) Mitotic inhibition induced in human kidney cells by methylglyoxal and kethoxal. Experientia 25:178–179

    Article  PubMed  CAS  Google Scholar 

  • Sgherri CLM, Navari-Izzo F (2000) Antioxidative enzymes in wheat subjected to increasing water deficit and rewatering. J Plant Physiol 157:273–279

    CAS  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and functions of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1311

    Article  PubMed  CAS  Google Scholar 

  • Singla-Pareek SL, Reddy MK, Sopory SK (2001) Transgenic approach towards developing abiotic stress tolerance in plants. Proc Indian Natl Sci Acad B 67:265–284

    CAS  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    Article  CAS  Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19:267–290

    Article  CAS  Google Scholar 

  • Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    Article  PubMed  CAS  Google Scholar 

  • Thomas CE, McLean LR, Parker RA, Ohlweiler DF (1992) Ascorbate and phenolic antioxidant interactions in prevention of liposomal oxidation. Lipids 27:543–550

    Article  PubMed  CAS  Google Scholar 

  • Tullio MCD, Arrigoni O (2004) Hopes, disillusions and more hopes from vitamin C. Cell Mol Life Sci 61:209–219

    Article  PubMed  Google Scholar 

  • Umeda M, Hara C, Matsubayashi Y, Li HH, Liu Q, Tadokoro F, Aotsuka S, Uchimiya H (1994) Expressed sequence tags from cultured cells of rice (Oryza sativa L.) under stressed conditions: analysis of transcripts of genes engaged in ATP-generating pathways. Plant Mol Biol 25:469–478

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  PubMed  CAS  Google Scholar 

  • Wingsle G, Karpinski S (1996) Differential redox regulation by glutathione of glutathione reductase and CuZn-superoxide dismutase gene expression in Pinus sylvestris L. needles. Planta 198:151–157

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139

    Article  PubMed  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67

    Article  PubMed  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005b) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271

    Article  PubMed  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005c) Methylglyoxal detoxification by glyoxalase system: a survival strategy during environmental stresses. Physiol Mol Biol Plants 11:1–11

    CAS  Google Scholar 

  • Zhang J, Kirkham MB (1996) Enzymatic responses of the ascorbate glutathione cycle to drought in sorghum and sunflower plants. Plant Sci 113:139–147

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by Konkuk University research fund (2010). The research fellowship from Konkuk University to JV, MAG and KV as research fellow is gratefully acknowledged. This work was supported by a grant from the Next-Generation BioGreen 21 Program (No. PJ008182), Rural Development Administration, Republic of Korea.

Author information

Author notes

  1. Chandrama Prakash Upadhyaya

    Present address: Department of Botany, Guru Ghasidas Central University, Bilaspur, 495009, India

Authors and Affiliations

  1. Department of Molecular Biotechnology, Konkuk University, 1, Hwayang-dong, Gwangjin-gu, Seoul, Korea Republic

    Chandrama Prakash Upadhyaya, Jelli Venkatesh, Mayank Anand Gururani, Leonid Asnin, Kavita Sharma, Hemavathi Ajappala & Se Won Park

Authors
  1. Chandrama Prakash Upadhyaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jelli Venkatesh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mayank Anand Gururani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonid Asnin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kavita Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hemavathi Ajappala
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Se Won Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Se Won Park.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Upadhyaya, C.P., Venkatesh, J., Gururani, M.A. et al. Transgenic potato overproducing l-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol Lett 33, 2297–2307 (2011). https://doi.org/10.1007/s10529-011-0684-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10529-011-0684-7

Keywords

Search

Navigation