Skip to main content
Log in

Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The present study investigates the possible regulatory role of exogenous nitric oxide (NO) in mitigating oxidative stress in wheat seedlings exposed to arsenic (As). Seedlings were treated with NO donor (0.25 mM sodium nitroprusside, SNP) and As (0.25 and 0.5 mM Na2HAsO4·7H2O) separately and/or in combination and grown for 72 h. Relative water content (RWC) and chlorophyll (chl) content were decreased by As treatment but proline (Pro) content was increased. The ascorbate (AsA) content was decreased significantly with increased As concentration. The imposition of As caused marked increase in the MDA and H2O2 content. The amount of reduced glutathione (GSH) and glutathione disulfide (GSSG) significantly increased with an increase in the level of As (both 0.25 and 0.5 mM), while the GSH/GSSG ratio decreased at higher concentration (0.5 mM). The ascorbate peroxidase and glutathione S-transferase activities consistently increased with an increase in the As concentration, while glutathione reductase (GR) activities increased only at 0.25 mM. The monodehydroascorbate reductase (MDHAR) and catalase (CAT) activities were not changed upon exposure to As. The activities of dehydroascorbate reductase (DHAR) and glyoxalase I (Gly I) decreased at any levels of As, while glutathione peroxidase (GPX) and glyoxalase II (Gly II) activities decreased only upon 0.5 mM As. Exogenous NO alone had little influence on the non-enzymatic and enzymatic components compared to the control seedlings. These inhibitory effects of As were markedly recovered by supplementation with SNP; that is, the treatment with SNP increased the RWC, chl and Pro contents; AsA and GSH contents and the GSH/GSSG ratio as well as the activities of MDHAR, DHAR, GR, GPX, CAT, Gly I and Gly II in the seedlings subjected to As stress. These results suggest that the exogenous application of NO rendered the plants more tolerant to As-induced oxidative damage by enhancing their antioxidant defense and glyoxalase system.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AO:

Ascorbate oxidase

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid

CAT:

Catalase

CDNB:

1-Chloro-2,4-dinitrobenzene

chl:

Chlorophyll

DHA:

Dehydroascorbate

DHAR:

Dehydroascorbate reductase

DTNB:

5,5′-Dithio-bis(2-nitrobenzoic acid)

EDTA:

Ethylenediaminetetraacetic acid

Gly I:

Glyoxalase I

Gly II:

Glyoxalase II

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

GPX:

Glutathione peroxidase

GST:

Glutathione S-transferase

MDA:

Malondialdehyde

MDHA:

Monodehydroascorbate

MDHAR:

Monodehydroascorbate reductase

MG:

Methylglyoxal

NO:

Nitric oxide

NTB:

2-Nitro-5-thiobenzoic acid

Pro:

Proline

ROS:

Reactive oxygen species

RWC:

Relative water content

SLG:

S-d-Lactoylglutathione

SNP:

Sodium nitroprusside

TBA:

Thiobarbituric acid

TCA:

Trichloroacetic acid

References

  • Addinsoft (2010) XLSTAT 2010: data analysis and statistics software for Microsoft Excel. Addinsoft, Paris

    Google Scholar 

  • Anjum NA, Umar S, Iqbal M, Khan NA (2011) Cadmium causes oxidative stress in mung bean by affecting the antioxidant enzyme system and ascorbate–glutathione cycle metabolism. Russ J Plant Physiol 58:92–99

    Article  CAS  Google Scholar 

  • Arnon DT (1949) Copper enzymes in isolated chloroplasts polyphenaloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Barrs HD, Weatherly PE (1962) A re-examination of relative turgidity for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of proline for water-stress studies. Plant Soil 39:205–207

    Article  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  CAS  Google Scholar 

  • Chao Y-Y, Hong C-Y, Kao C-H (2010) The decline in ascorbic acid content is associated with cadmium toxicity of rice seedlings. Plant Physiol Biochem 48:374–381

    Article  CAS  Google Scholar 

  • Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Bot Stud 52:41–46

    CAS  Google Scholar 

  • Chronopoulou EG, Labrou NE (2009) Glutathione transferases: emerging multidisciplinary tools in red and green biotechnology. Recent Pat Biotechnol 3:211–223

    Article  CAS  Google Scholar 

  • Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611

    Article  CAS  Google Scholar 

  • Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167

    Article  CAS  Google Scholar 

  • El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    Article  CAS  Google Scholar 

  • Foyer (2003) Ascorbate and glutathione metabolism in plants: H2O2-processing and signalling. In: Gitler C, Danon A (eds) Cellular implications of redox signaling. Imperial College Press, London, pp 191–212

    Chapter  Google Scholar 

  • Foyer CF, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  Google Scholar 

  • Gao HJ, Yang HQ, Wang JX (2009) Arginine metabolism in roots and leaves of apple (Malus domestica Borkh.): the tissue-specific formation of both nitric oxide and polyamines. Sci Hort 119:147–152

    Article  CAS  Google Scholar 

  • Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261

    Article  CAS  Google Scholar 

  • Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74:1201–1208

    Article  CAS  Google Scholar 

  • Gupta KJ, Igamberdiev AU, Manjunatha G, Segu S, Moran JF, Neelawarne B, Bauwe H, Kaiser WM (2011) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci 181:520–526

    Article  CAS  Google Scholar 

  • Hao GP, Zhang JH (2010) The role of nitric oxide as a bioactive signaling molecule in plants under abiotic stress. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley, Weinheim, pp 115–138

    Google Scholar 

  • Hasanuzzaman M, Fujita M (2011) Selenium pretreatment up-regulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol Trace Elem Res 143:1758–1776

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Fujita M (2012) Heavy metals in the environment: current status, toxic effects on plants and possible phytoremediation. In: Anjum NA, Pereira MA, Ahmad I, Duarte AC, Umar S, Khan NA (eds) Phytotechnologies: remediation of environmental contaminants. Taylor and Francis/CRC Press, Boca Raton, pp 7–73

    Chapter  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am J Plant Physiol 5:295–324

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011a) Nitric oxide modulates antioxidant defense and methylglyoxal detoxification system and reduces salinity induced damage in wheat seedling. Plant Biotecnol Rep 5:353–365

    Article  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011b) Selenium-induced upregulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704–1721

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012a) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateshwarulu B, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–315

    Chapter  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2012b) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323

    CAS  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2012c) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Gill SS, Fujita M (2013) Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 169–322

    Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  • Hossain MZ, Hossain MD, Fujita M (2006) Induction of pumpkin glutathione S-transferase by different stresses and its possible mechanisms. Biol Plant 50:210–218

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2004) Cd toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238

    Article  CAS  Google Scholar 

  • Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in ascorbate-deficient Arabidopsis mutant. J Exp Bot 56:3041–3049

    Article  CAS  Google Scholar 

  • Innocenti G, Pucciariello C, Gleuher ML, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602

    Article  CAS  Google Scholar 

  • Islam MM, Hoque MA, Okuma E, Jannat R, Banu MNA, Jahan MS, Nakamura Y, Murata Y (2009) Proline and glycinebetaine confer cadmium tolerance on tobacco bright yellow-2 cells by increasing ascorbate-glutathione cycle enzyme activities. Biosci Biotechnol Biochem 73:2320–2323

    Article  CAS  Google Scholar 

  • Ismail GSM (2012) Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303–1311

    Article  Google Scholar 

  • Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634

    Article  CAS  Google Scholar 

  • Kumar V, Yadav SK (2009) Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress in Camellia sinensis (L.) O. Kuntze. Acta Physiol Plant 31:261–269

    Article  CAS  Google Scholar 

  • Kumari A, Sheokand S, Swaraj K (2010) Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in chickpea. Braz J Plant Physiol 22:271–284

    Article  Google Scholar 

  • Li C, Li T, Zhang D, Jiang L, Shao Y (2013) Exogenous nitric oxide effect on fructan accumulation and FBEs expression in chilling-sensitive and chilling-resistant wheat. Environ Exp Bot 86:2–8

    Article  CAS  Google Scholar 

  • Liu X, Wang L, Liu L, Guo Y, Ren H (2011) Alleviating effect of exogenous nitric oxide in cucumber seedling against chilling stress. Afr J Biotechnol 10:4380–4386

    Article  Google Scholar 

  • Mantri N, Patade V, Penna S, Ford R, Pang E (2012) Abiotic stress responses in plants: present and future. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, pp 1–19

    Chapter  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Breusegem FV, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220

    Article  CAS  Google Scholar 

  • Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248:565–577

    Article  CAS  Google Scholar 

  • Mustafiz A, Sahoo KK, Singla-Pareek SL, Sopory SK (2010) Metabolic engineering of glyoxalase pathway for enhancing stress tolerance in plants. Methods Mol Biol 639:95–118

    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 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  Google Scholar 

  • Paradiso A, Berardino R, de Pinto M, di Toppi LS, Storelli FT, de Gara L (2008) Increase in ascorbate–glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49:362–374

    Article  CAS  Google Scholar 

  • Principato GB, Rosi G, Talesa V, Govannini E, Uolila L (1987) Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. Biochem Biophys Acta 911:349–355

    Article  CAS  Google Scholar 

  • Rubbo H, Radi R, Anselmi D, Kirk M, Barnes S, Butler J, Eiserich JP, Freeman BA (2000) Nitric oxide reaction with lipid peroxyl radicals spares alphatocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alphatocopherol than alpha-tocopherol/ascorbate. J Biol Chem 275:10812–10818

    Article  CAS  Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, Gupta DK, Archilla A, Romero-Puertas MC, del Río LA (2012) Reactive oxygen species and nitric oxide in plants under cadmium stress from toxicity to signaling. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 199–215

    Chapter  Google Scholar 

  • Sarma H (2011) Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. J Environ Sci Technol 4:118–138

    Article  CAS  Google Scholar 

  • Saxena M, Deb Roy S, Singla-Pareek S-L, Sopory SK, Bhalla-Sarin N (2011) Overexpression of the glyoxalase II gene leads to enhanced salinity tolerance in Brassica juncea. The Open Plant Sci J 5:23–28

    Article  CAS  Google Scholar 

  • Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346

    Article  CAS  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110

    Article  CAS  Google Scholar 

  • Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  CAS  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2008) Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Transgenic Res 17:171–180

    Article  CAS  Google Scholar 

  • Stoeva N, Berova M, Zlatev ZL (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Plant 49:293–296

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372

    Article  CAS  Google Scholar 

  • Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20

    Article  CAS  Google Scholar 

  • Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr J Bot 76:167–179

    Article  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) 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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Sopory SK (2008) An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 23:51–68

    Article  CAS  Google Scholar 

  • Yousuf PY, Hakeem KUR, Chandna R, Ahmad P (2012) Role of glutathione reductase in plant abiotic stress. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, pp 149–158

    Chapter  Google Scholar 

  • Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Mr. Mahbub Alam and Mrs. Kamrun Nahar, Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa University, Japan for critically reading of the manuscript. We also thank Mr. M.G. Mostofa of the same laboratory for his help in measuring the activity of glutathione reductase.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masayuki Fujita.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hasanuzzaman, M., Fujita, M. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22, 584–596 (2013). https://doi.org/10.1007/s10646-013-1050-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-013-1050-4

Keywords

Navigation