Skip to main content
SpringerLink
Log in

Overproduction of a rice aldo–keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The accumulation of toxic compounds generated by the interaction between reactive oxygen species and polyunsaturated fatty acids of membrane lipids can significantly damage plant cells. A plethora of enzymes act on these reactive carbonyls, reducing their toxicity. Based on the chromosomal localization and on their homology with other stress-induced aldo–keto reductases (AKRs) we have selected three rice AKR genes. The transcription level of OsAKR1 was greatly induced by abscisic acid and various stress treatments; the other two AKR genes tested were moderately stress-inducible. The OsAKR1 recombinant protein exhibited a high nicotinamide adenine dinucleotide phosphate-dependent catalytic activity to reduce toxic aldehydes including glycolysis-derived methylglyoxal (MG) and lipid peroxidation-originated malondialdehyde (MDA). The function of this enzyme in MG detoxification was demonstrated in vivo in E. coli and in transgenic plants overproducing the OsAKR1 protein. Heterologous synthesis of the OsAKR1 enzyme in transgenic tobacco plants resulted in increased tolerance against oxidative stress generated by methylviologen (MV) and improved resistance to high temperature. In these plants lower levels of MDA were detected both following MV and heat treatment due to the activity of the OsAKR1 enzyme. The transgenic tobaccos also exhibited higher AKR activity and accumulated less MG in their leaves than the wild type plants; both in the presence and absence of heat stress. These results support the positive role of OsAKR1 in abiotic stress-related reactive aldehyde detoxification pathways and its use for improvement of stress tolerance in plants.

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

Access this article

Log in via an institution

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

AKR:

Aldo–keto reductase

MDA:

Malondialdehyde

MG:

Methylglyoxal

MsALR:

Medicago sativa aldo–keto reductase

MV:

Methylviologen

NADPH:

Nicotinamide adenine dinucleotide phosphate

qRT–PCR:

Quantitative real-time PCR

PSII:

Photosystem II

ROS:

Reactive oxygen species

SDS–PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

TBARS:

2-Thiobarbituric acid-reactive substances

References

  • Bartels D, Engelhardt K, Roncarati R, Schneider K, Rotter M, Salamini F (1991) An ABA and GA modulated gene expressed in the barley embryo encodes an aldose reductase related protein. EMBO J 10:1037–1043

    PubMed  CAS  Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl Acids Res 7:1513

    Article  PubMed  CAS  Google Scholar 

  • Bohren KM, Page JL, Shankar R, Henry SP, Gabbay KH (1991) Expression of human aldose and aldehyde reductases. J Biol Chem 266:24031–24037

    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 

  • Bukhov NG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–93

    Article  CAS  Google Scholar 

  • Chang Q, Harter TM, Rikimaru LT, Petrash JM (2003) Aldo-keto reductases as modulators of stress response. Chem Biol Interact 325:143–144

    Google Scholar 

  • Chang Q, Griest TA, Harter TM, Petrash JM (2007) Functional studies of aldo-keto reductases in Saccharomyces cerevisiae. Biochim Biophys Acta 1773:321–329

    Article  PubMed  CAS  Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal MH, El Ferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147

    Article  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Colrat S, Latche A, Guis M, Pech JC, Bouzayen M, Fallot J, Roustan JP (1999) Purification and characterization of a NADPH-dependent aldehyde reductase from mung bean that detoxifies eutypine, a toxin from Eutypa lata. Plant Physiol 119:621–626

    Article  PubMed  CAS  Google Scholar 

  • De Ronde JAD, Cress WA, Kruger GHJ, Strasser RJ, Staden JV (2004) Photosynthetic response of transgenic soybean plants containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 61:1211–1244

    Google Scholar 

  • Garretón V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516–1526

    Article  PubMed  Google Scholar 

  • Gavidia I, Perez-Bermudez P, Seitz HU (2002) Cloning and expression of two novel aldo-keto reductases from Digitalis purpurea leaves. Eur J Biochem 269:2842–2850

    Article  PubMed  CAS  Google Scholar 

  • Goff SA (1999) Rice as a model for cereal genomics. Curr Opin Plant Biol 2:86–89

    Article  PubMed  CAS  Google Scholar 

  • Gong M, Li JY, Chen SZ (1998) Abscisic acid induced thermotolerance in maize seedlings is mediated by Ca2+ and associated with antioxidant systems. J Plant Physiol 153:488–496

    CAS  Google Scholar 

  • Gounaris K, Brain AR, Quinn PJ, Williams WP (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochim Biophys Acta 766:198–208

    Article  CAS  Google Scholar 

  • Grant AW, Steel G, Waugh H, Ellis EM (2003) A novel aldo-keto reductase from E. coli can increase resistance to methylglyoxal toxicity. FEMS Microbiol Lett 218:93–99

    Article  PubMed  CAS  Google Scholar 

  • Halder AB, Crabbe MJ (1984) Bovine lens aldehyde reductase (aldose reductase). Purification, kinetics and mechanism. Biochem J 219:33–39

    PubMed  CAS  Google Scholar 

  • Hegedűs A, Erdei S, Janda T, Tóth E, Horváth G, Dudits D (2004) Transgenic tobacco plants overproducing alfalfa aldose/aldehyde reductase show higher tolerance to low temperature and cadmium stress. Plant Sci 166:1329–1333

    Article  Google Scholar 

  • Hideg É, Nagy T, Oberschall A, Dudits D, Vass I (2003) Detoxification function of aldose/aldehyde reductase during drought and ultraviolet-B (280–320 nm) stresses. Plant Cell Environ 26:513–522

    Article  CAS  Google Scholar 

  • Horsch RB, Fry JE, Hoffmann EL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  • Hsieh T-H, Lee J-T, Charng Y-Y, Chan M-T (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618–626

    Article  PubMed  CAS  Google Scholar 

  • Hur J, Jung KH, Lee CH, An G (2004) Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Sci 167:417–426

    Article  CAS  Google Scholar 

  • Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for delta1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33:857–865

    Article  PubMed  CAS  Google Scholar 

  • Jez JM, Bennett MJ, Schlegel BP, Lewis M, Penning TM (1997) Comparative anatomy of the aldo–keto reductase superfamily. Biochem J 326:625–636

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kikugawa K, Tsukuda K, Kurechi T (1980) Studies on peroxidized lipids. I. Interaction of malondialdehyde with secondary amines and its relevance to nitrosamine formation. Chem Pharm Bull 28:3323–3331

    CAS  Google Scholar 

  • Kolb NA, Hunsaker LA, Vander Jagt DL (1994) Aldose reductase catalyzed reduction of acrolein: implication in cyclophasphamide toxicity. Mol Pharmacol 45:797–801

    PubMed  CAS  Google Scholar 

  • Kumar S, Dhingra A, Daniell H (2004) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves conferes enhanced salt tolerance. Plant Physiol 136:2843–2854

    Article  PubMed  CAS  Google Scholar 

  • Kwon SY, JeongYJ LeeHS, 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 methylviologen-mediated oxidative stress. Plant Cell Environ 25:873–882

    Article  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene and salicylic acid. Plant Physiol 128:682–695

    Article  PubMed  CAS  Google Scholar 

  • Lendvai A, Pettkó-Szandtner A, Csordás-Tóth E, Miskolczi P, Horváth GV, Györgyey J, Dudits D (2007) Dicot and monocot plants differ in retinoblastoma-related protein subfamilies. J Exp Bot 58:1663–1675

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Murai N (1990) Efficient plant regeneration from rice protoplasts in general medium. Plant Cell Rep 9:216–220

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Mano J, Belles-Boix E, Babiychuk E, Inzé D, Torii Y, Hiraoka E, Takimoto K, Slooten L, Asada K, Kushnir S (2005) Protection against photooxidative injury of tobacco leaves by 2-alkenal reductase. Detoxication of lipid peroxide-derived reactive carbonyls. Plant Physiol 139:1773–1783

    Article  PubMed  CAS  Google Scholar 

  • Mano J, Miyatake F, Hiraoka E, Tamoi M (2009) Evaluation of the toxicity of stress-related aldehydes to photosynthesis in chloroplasts. Planta 230:639–648

    Article  PubMed  CAS  Google Scholar 

  • Mano J, Tokushige K, Mizoguchi Hirotoshi, Fujii H, Khorobrykh S (2010) Accumulation of lipid peroxide-derived, toxic α,β-unsaturated aldehydes (E)-2-pentenal, acrolein and (E)-2-hexenal in leaves under photoinhibitory illumination. Plant Biotech 27:193–197

    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 

  • Mishra RK, Singhal GS (1992) Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. Plant Physiol 98:1–6

    Article  PubMed  CAS  Google Scholar 

  • Mundree SG, Whittaker A, Thomson JA, Farrant JM (2000) An aldose reductase homolog from the resurrection plant Xerophyta viscosa Baker. Planta 211:693–700

    Article  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 

  • Oberschall A, Deák M, Török K, Sass L, Vass I, Kovács I, Fehér A, Dudits D, Horváth GV (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stress. Plant J 24:437–446

    Article  PubMed  CAS  Google Scholar 

  • Ray S, Dutta S, Halder J, Ray M (1994) Inhibition of electron flow through complex I of the mitochondrial respiratory chain of Ehrlich ascites carcinoma cells by methylglyoxal. Biochem J 303:69–72

    PubMed  CAS  Google Scholar 

  • Rodrigues SM, Andrade MO, Gomes AP, Damatta FM, Baracat-Pereira MC, Fontes EP (2006) Arabidopsis and tobacco plants ectopically expressing the soybean antiquitin-like ALDH7 gene display enhanced tolerance to drought, salinity, and oxidative stress. J Exp Bot 57:1909–1918

    Article  PubMed  CAS  Google Scholar 

  • Roncarati R, Salamini F, Bartels D (1995) An aldose reductase homologous gene from barley: regulation and function. Plant J 7:809–822

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Shimamoto K, Kyozuka J (2002) Rice as a model for comparative genomics of plants. Annu Rev Plant Biol 53:399–419

    Article  PubMed  CAS  Google Scholar 

  • Simpson PJ, Tantitadapitak C, Reed AM, Mather OC, Bunce CM, White SA, Ride JP (2009) Characterization of two novel aldo-keto reductases from Arabidopsis: expression patterns, broad substrate specificity, and an open active-site structure suggest a role in toxicant metabolism following stress. J Mol Biol 392:465–480

    Article  PubMed  CAS  Google Scholar 

  • Sree BK, Rajendrakumar SV, Reddy AR (2000) Aldose reductase in rice (Oryza sativa L.): stress response and developmental specificity. Plant Sci 160:149–157

    Article  Google Scholar 

  • Srivastava S, Watowich SJ, Petrash JM, Srivastava SK, Bhatnagar A (1999) Structural and kinetic determinants of aldehyde reduction by aldose reductase. Biochemistry 38:42–54

    Article  PubMed  CAS  Google Scholar 

  • Srivastava SK, Ramana KV, Bhatnagar A (2005) Role of aldose reductase and oxidative damage in diabetes and the consequent potential for therapeutic options. Endocrin Rev 26:380–392

    Article  CAS  Google Scholar 

  • Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35:452–464

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:46–51

    Article  Google Scholar 

  • Thompson LK, Blaylock R, Sturtevant JM, Brudwig GW (1989) Molecular basis of heat denaturation of photosystem II. Biochemistry 28:6686–6695

    Article  PubMed  CAS  Google Scholar 

  • Vander Jagt DL, Robinson B, Taylor KK, Hunsaker LA (1992) Reduction of trioses by NADPH-dependent aldo-keto reductases. Aldose reductase, methylglyoxal, and diabetic complications. J Biol Chem 267:4364–4369

    PubMed  CAS  Google Scholar 

  • Xiang C, Miao ZH, Lam E (1996) Coordinated activation of as-1 type elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide. Plant Mol Biol 32:415–426

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Sugimoto Y (2010) Effect of protein modifcation by malondialdehyde on the interaction between the oxygen-evolving complex 33 kDa protein and photosystem II core proteins. Planta 231:1077–1088

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugimoto Y (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat stressed plants. Plant Physiol Biochem 46:786–793

    Article  PubMed  CAS  Google Scholar 

  • Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Authors would like to acknowledge the help of Dr. Éva Hideg in the theoretical and practical aspects of the photosythetic measurements. This research was supported by the Hungarian National Office for Research and Technology (NKTH) (NKFP Grant No. 4-064-2004), OMFB Grant No. 00514/2007 and by the Baross Gábor Program 2009 (Grant No. REG_DA_KFI_09 ALDEHID9). Gábor V. Horváth is grateful for the support of the “János Bólyai” Research Fellowship.

Author information

Authors and Affiliations

  1. Institute of Plant Biology, Biological Research Center, Hungarian Academy of Sciences, Temesvári krt. 62, 6726, Szeged, Hungary

    Zoltán Turóczy, Petra Kis, Katalin Török, Mátyás Cserháti, Ágnes Lendvai, Dénes Dudits & Gábor V. Horváth

Authors
  1. Zoltán Turóczy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petra Kis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katalin Török
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mátyás Cserháti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ágnes Lendvai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dénes Dudits
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gábor V. Horváth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gábor V. Horváth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Turóczy, Z., Kis, P., Török, K. et al. Overproduction of a rice aldo–keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification. Plant Mol Biol 75, 399–412 (2011). https://doi.org/10.1007/s11103-011-9735-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9735-7

Keywords

Search

Navigation