Skip to main content
Log in

Nitric oxide acts as a signal molecule in microwave pretreatment induced cadmium tolerance in wheat seedlings

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The microwave has been widely used in the field of biology with the development of microwave technology. Previous studies suggest that suitable doses of microwave irradiation improved plant metabolism and enzymatic activities under cadmium stress and enhanced cadmium tolerance in wheat seedlings. The objective of this study was to test whether nitric oxide is involved in microwave pretreatment induced cadmium tolerance in wheat seedlings due to its nature as a second messenger in stress responses. Plant were treated with 10 s microwave pretreatment, microwave pretreatment in combination with NO scavenger, 2-(4-carboxyphenyl)-4, 4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) and their effects on the lipid peroxidation, the activities of antioxidant enzymes, the concentration of antioxidant compounds and wheat seedlings growth and development were compared. The results showed that 10 s microwave pretreatment dramatically alleviated growth suppression induced by cadmium stress, reflected by decreased malondialdehyde, hydrogen peroxide and superoxide radical production. Furthermore, the activities of antioxidant enzymes (superoxide dismutase, peroxidase, catalase, ascorbate peroxidase and glutathione reductase) and the concentration of antioxidant metabolites (ascorbate, reduced glutathione, carotenoids and nitric oxide) were increased in wheat seedlings pretreated with microwave under cadmium stress. Nevertheless, the promotive effect of microwave pretreatment induced cadmium tolerance in wheat seedlings was effectively reversed by the addition of 0.5 % (w/v) cPTIO (NO scavenger), suggesting that NO was involved in microwave pretreatment induced cadmium tolerance in wheat seedlings.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid

CAR:

Carotenoids

CAT:

Catalase

Cd:

Cadmium

cPTIO:

2-(4-Carboxyphenyl)-4,4,5,5-tetramethyl

DTNB:

5,5′-Dithiobis (2-nitrobenzoic acid)

EDTA:

Ethylenediaminetetraacetic acid

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

H2O2 :

Hydrogen peroxide

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

NO:

Nitric oxide

O 2 :

Superoxide radical

POD:

Peroxidase

ROS:

Reactive oxygen species

SNP:

Sodium nitroprusside

SOD:

Superoxide dismutase

TBA:

Thiobarbituric acid

References

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  PubMed  CAS  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

    Article  PubMed  CAS  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity on enhance activities of superoxide dismutase, peroxidase and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227

    Article  PubMed  CAS  Google Scholar 

  • Chen YP (2006) Microwave treatment of eight seconds protects cells of Isatis indigotica from enhanced UV-B radiation lesions. Photochem Photobiol 82:503–507

    PubMed  CAS  Google Scholar 

  • Chen YP, Jia JF, Han XL (2009a) Weak microwave can alleviate water deficit induced by osmotic stress in wheat seedlings. Planta 229:291–298

    Article  PubMed  CAS  Google Scholar 

  • Chen YP, Jia JF, Wang YJ (2009b) Weak microwave can enhance tolerance of wheat seedlings to salt stress. J Plant Growth Regul 8:381–385

    Article  Google Scholar 

  • Chen F, Wang F, Sun HY, Cai Y, Mao WH, Zhang GP, Eva V, Wu FB (2010) Genotype-dependent effect of exogenous nitric oxide on Cd-induced changes in antioxidative metabolism, ultrastructure, and photosynthetic performance in barley seedlings (Hordeum vulgare). J Plant Growth Regul 29:394–408

    Article  CAS  Google Scholar 

  • Cui JX, Zhou YH, Ding JG, Xia XJ, Shi K, Chen SC, Tadao A, Chen ZX, Yu JQ (2011) Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant Cell Environ 34:347–358

    Article  PubMed  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  PubMed  CAS  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  PubMed  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 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutase occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Hamada EAM (2007) Effect of microwave treatment on growth, photosynthetic pigments and some metabolites of wheat. Biol Plant 51:343–345

    Article  CAS  Google Scholar 

  • He JM, Xu H, She XP, Song XG, Zhao WM (2005) The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B induced stomatal closure in broad bean. Funct Plant Biol 32:237–247

    Article  CAS  Google Scholar 

  • Jozef K, Jirí G, Borivoj K, Frantisek S, Rogério M, Osvaldo FF (2010) Lignification and related parameters in copper-exposed Matricaria chamomilla roots: role of H2O2 and NO in this process. Plant Sci 179:383–389

    Article  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Magdalena AJ, Jolanta FW, Edward AG (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620

    Article  Google Scholar 

  • Mata CG, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  CAS  Google Scholar 

  • More HG, Magan N, Stenning BC (1992) Effect of microwave heating on quality and mycoflora of sorghum grain. J Stored Prod Res 28:251–256

    Article  Google Scholar 

  • Murphy ME, Noack E (1994) Nitric oxide assay using haemoglobin method. Method Enzymol 233:240–250

    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 

  • Palavan-Unsal N, Arisan D (2009) Nitric oxide signaling in plants. Bot Rev 75:203–229

    Article  Google Scholar 

  • Patterson BD, Mackac EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492

    Article  PubMed  CAS  Google Scholar 

  • Piyalee P, Shwetosmita N, Thorny TC, Gauri DS, Sanjib KP (2011) Cadmium stress induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.). Acta Physiol Plant 33:1737–1747

    Article  Google Scholar 

  • Predieri S, Norman MA, Krizek DT (1995) Influence of UV-B radiation on membrane lipid composition and ethylene of evolution in ‘Doyenne d’Hiver’ pear shoots grown in vitro under different photosynthetic photo fluxes. Environ Exp Bot 35:152–260

    Article  Google Scholar 

  • Qiu ZB, Li JT, Zhang YJ, Bi ZZ, Wei HF (2011) Microwave pretreatment can enhance tolerance of wheat seedlings to CdCl2 stress. Ecotoxicol Environ Saf 74:820–825

    Article  PubMed  CAS  Google Scholar 

  • Rajesh KT, Eun-Joo H, Kee-Yoeup P (2008) Modulation of copper toxicity-induced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171–181

    Google Scholar 

  • Roux D, Vian A, Girad S, Bonnet P, Paladian F, Davies E, Ledoigt G (2006) Electromagnetic fields (900 MHz) evoke consistent molecular responses in tomato plants. Physiol Plant 128:283–288

    Article  CAS  Google Scholar 

  • Shayesteh N, Barthakur NN (1996) Mortality and behaviour of two stored-product insect species during microwave irradiation. J Stored Prod Res 32:239–246

    Article  Google Scholar 

  • Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167

    Article  CAS  Google Scholar 

  • Tonamura B (1978) Test reactions for a stopped flow apparatus regulation of 2, 6-D and potassium ferricyanide by l-ascorbic acid. Anal Biochem 84:370–383

    Article  Google Scholar 

  • Vanesa T, Melina A, Lorenzo L, Raúl C (2011) Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant Cell Environ 34:909–921

    Article  Google Scholar 

  • Wang S, Tang J, Mitcham E, Hansen JD, Cavalieri RP, Bower J, Biasi B (2002) Process protocols based on radio frequency energy to control field and storage pests in in-shell walnuts. Postharvest Biol Tech 26:265–273

    Article  Google Scholar 

  • Wang Z, Zhang YX, Huang ZB, Huang L (2008) Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil 310:137–149

    Article  CAS  Google Scholar 

  • Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119

    Article  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  PubMed  CAS  Google Scholar 

  • Wu XX, Zhu WM, Zhang H, Ding HD, Zhang HJ (2011) Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill.). Acta Physiol Plant 33:1199–1209

    Article  CAS  Google Scholar 

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

    Article  PubMed  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 

  • Xu MJ, Zhu Y, Dong JF, Jin HH, Sun LN, Wang ZA, Lu ZH, Zhang M, Lu D (2012) Ozone induces flavonol production of Ginkgo biloba cells dependently on nitrate reductase-mediated nitric oxide signaling. Environ Exp Bot 75:114–119

    Article  CAS  Google Scholar 

  • Zhang JX, Kirham MB (1994) Drought stress-induced changes in activities of superoxide dismutase, catalase and peroxidase in wheat species. Plant Cell Physiol 35:785–791

    CAS  Google Scholar 

  • Zhang LG, Zhou S, Xuan Y (2009) Protective effect of nitric oxide against oxidative damage in Arabidopsis leaves under ultraviolet-B irradiation. J Plant Biol 52:135–140

    Article  Google Scholar 

  • Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Cultivation Project of the Youth Backbone Teacher of Henan Normal University and Key Subject of Biochemistry and Molecular Biology of Henan Province.

Conflict of interest

The authors declare that they have no conflicts of interest in regard to this research or its funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zong-Bo Qiu.

Additional information

Communicated by H. Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qiu, ZB., Guo, JL., Zhang, MM. et al. Nitric oxide acts as a signal molecule in microwave pretreatment induced cadmium tolerance in wheat seedlings. Acta Physiol Plant 35, 65–73 (2013). https://doi.org/10.1007/s11738-012-1048-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-012-1048-1

Keywords

Navigation