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Effect of nitrogen deficiency on antioxidant status and Cd toxicity in rice seedlings

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Abstract

Effect of nitrogen (N) deficiency on antioxidant status and Cd toxicity in rice seedlings was investigated. N deficiency resulted in a reduction of shoot growth but not root growth. The contents of N-containing compounds such as nitrate, chlorophyll, and protein decreased in leaves of rice seedlings grown under N deficiency. Accumulation of abscisic acid and H2O2 in leaves was induced by N deficiency. The content of ascorbate and the activities of ascorbate peroxidase, glutathione reductase, and catalase in N-deficient leaves were lower than their respective control leaves. However, glutathione content was not affected and superoxide dismutase activity was increased by N deficiency. Cd toxicity in N-deficient seedlings was more pronounced than that in N-sufficient ones. Pretreatment with ascorbate or L-galactono-1,4-lactone, a biosynthetic precursor of ascorbate resulted in a reduction of Cd toxicity enhanced by N deficiency. N deficiency also resulted in an enhancement of Cd uptake in rice seedlings. The possible mechanism of Cd toxicity enhanced by N deficiency is discussed.

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Abbreviations

ABA:

Abscisic acid

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid

CAT:

Catalase

DAB:

3,3-Diaminobenzidine

DHA:

Dehydroascorbate

DW:

Dry weight

ELISA:

Enzyme-linked immunosorbent assay

FW:

Fresh weight

GalL:

L-galactono-1,4-lactone

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

ROS:

Reactive oxygen species

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

References

  • Agrawal L, Chakraborty S, Jaiswal DK, Gupta S, Datta A, Chakraborty N (2008) Comparative proteomics of tuber induction, development and maturation reveal the complexity of tuberization process in potato (Solanum tuberosum L.). J Proteome Res 7:3803–3817

    Article  PubMed  CAS  Google Scholar 

  • Bennicelli RP, Stepniewski W, Zakrzhevsky DA, Balakhnina TI, Stepniewska Z, Lipiec J (1998) The effect of soil aeration on superoxide dismutase activity, malondialdehyde level, pigment content and stomatal diffusive resistance in maize seedlings. Environ Exp Bot 39:203–211

    Article  CAS  Google Scholar 

  • Bereczky Z, Wang HY, Schubert V, Ganal M, Bauer P (2003) Differential regulation of nramp and irt metal transporter genes in wild type and iron uptake mutants of tomato. J Biol Chem 278:24697–24704

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen ZS, Lee DY (1997) Evaluation of remediation techniques on two cadmium polluted soils in Taiwan. In: Iskandar IK, Adriano DC (eds) Remediation of soils contaminated with metals. Science Reviews, London, pp 209–223

    Google Scholar 

  • Cho U-H, Seo N-H (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120

    Article  CAS  Google Scholar 

  • Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Das P, Sammantaray S, Rout GR (1997) Studies on cadmium toxicity: a review. Environ Pollut 98:29–36

    Article  PubMed  CAS  Google Scholar 

  • Dey SK, Kar M (1995) Antioxidant efficiency during callus initiation from mature rice embryo. Plant Cell Physiol 36:543–549

    Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628

    Article  PubMed  CAS  Google Scholar 

  • Evans JR, Terashima I (1987) Effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14:59–68

    Article  CAS  Google Scholar 

  • Finkemeier I, Kluge C, Metwally A, Georgi M, Grotjohann N, Dietz K-J (2003) Alterations in Cd-induced gene expression under nitrogen deficiency in Hordeum vulgare. Plant Cell Environ 26:821–833

    Article  PubMed  CAS  Google Scholar 

  • Foster JG, Hess JL (1980) Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol 166:482–487

    Article  Google Scholar 

  • Garnier L, Simon-Plas F, Thuleau P, Angel J, Blein J, Ranjeva R, Montillet J-L (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969

    Article  PubMed  CAS  Google Scholar 

  • Goggin DE, Colmer TD (2005) Intermittent anoxia induces oxidative stress in wheat seminal roots: assessment of antioxidant defence system, lipid peroxidation and tissue solutes. Funct Plant Biol 32:495–506

    Article  CAS  Google Scholar 

  • Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9:597–605

    Article  PubMed  CAS  Google Scholar 

  • Graziano M, Lamattina L (2007) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–950

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hecht U, Mohr H (1990) Factors controlling nitrate and ammonium accumulation in mustard (Sinapis alba) seedlings. Physiol Plant 78:379–387

    Article  CAS  Google Scholar 

  • Hong C-Y, Chao Y-Y, Yang M-Y, Cheng S-Y, Cho S-C, Kao CH (2009) NaCl-indued expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant Soil 320:103–115

    Article  CAS  Google Scholar 

  • Hsu YT, Kao CH (2007) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 298:231–241

    Article  CAS  Google Scholar 

  • Hu X, Zhang A, Zhang J, Jiang M (2006) Abscisic acid is a key inducer of hydrogen peroxide production in leaves of maize plants exposed to water stress. Plant Cell Physiol 47:1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Hung KT, Kao CH (2004) Hydrogen peroxide is necessary for abscisic acid-induced senescence of rice leaves. J Plant Physiol 161:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Jalil A, Selles F, Clarke JM (1994) Effect of cadmium on growth and the uptake of cadmium and other elements by durum-wheat. J Plant Nutr 17:1839–1858

    Article  CAS  Google Scholar 

  • Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz K-J (2004) The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 120:63–73

    Article  PubMed  CAS  Google Scholar 

  • Kato M, Shimizu S (1987) Chlorophyll metabolism in higher plants. VII. Chlorophyll degradation in senescing tobacco leaves: phenolic-dependent peroxidative degradation. Can J Bot 65:729–735

    Article  CAS  Google Scholar 

  • Koprivova A, Suter M, den Camp RO, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746

    Article  PubMed  CAS  Google Scholar 

  • Law MY, Stephen Y, Charles A, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and paraquat. Biochem J 210:899–903

    PubMed  CAS  Google Scholar 

  • Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulation in rice plant. Plant Cell Environ 32:408–416

    Article  PubMed  CAS  Google Scholar 

  • Logan BA, Demmig-Adams B, Rosenstiel TN, Adams WW (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 299:213–220

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academis Presss, London

    Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  PubMed  CAS  Google Scholar 

  • Mizarhi Y, Richmond AE (1972) Abscisic acid in relation to mineral deprivation. Plant Physiol 50:667–670

    Article  Google Scholar 

  • Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279–2286

    PubMed  CAS  Google Scholar 

  • Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:464–469

    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, 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 

  • O’Toole JC, Cruz RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiol 65:428–432

    Article  PubMed  Google Scholar 

  • Paoletti F, Aldinucci D, Mocali A, Capparini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154:536–541

    Article  PubMed  CAS  Google Scholar 

  • Piacentini MP, Fraternale D, Piatti E, Ricci D, Vetrano F, Dacha M, Accorsi A (2001) Senescence delay and change of antioxidant enzyme levels in Cucumis sativus L. etiolated seedlings by ELF magnetic fields. Plant Sci 161:45–53

    Article  CAS  Google Scholar 

  • Sagi M, Flurher R (2006) Production of reactive oxygen species by plant NADPH oxidase. Plant Physiol 141:336–340

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Ann Rev Plant Biol 58:47–69

    Article  CAS  Google Scholar 

  • Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314

    Article  PubMed  CAS  Google Scholar 

  • Smith IK (1985) Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol 79:104–107

    Google Scholar 

  • Tewari RK, Kumar P, Tewari N, Srivastava S, Sharma PN (2004) Macronutrient deficiencies and differential antioxidant responses-influence on the activity and expression of superoxide dismutase in maize. Plant Sci 166:687–694

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2007) Oxidative stress and antioxidant responses in young leaves of mulberry plants grown under nitrogen phosphorus or potassium deficiency. J Integr Plant Biol 49:313–322

    Article  CAS  Google Scholar 

  • Tsai Y-C, Hong C-Y, Liu L-F, Kao CH (2004) Relative importance of Na+ and Cl− in NaCl-induced antioxidant systems in roots or rice seedlings. Physiol Plant 122:86–94

    Article  CAS  Google Scholar 

  • Vysotskaya LB, Korobova AV, Kudoyarova GR (2008) Abscisic acid accumulation in the roots of nutrient-limited plants: its impact on the differential growth of roots and shoots. J Plant Physiol 165:1274–1279

    Article  PubMed  CAS  Google Scholar 

  • Wintermans JFGM, De Mots A (1965) Spectrophotometric characteristics of chlorophyll a and b and their pheophytins in ethanol. Biochim Biophys Acta 109:448–453

    Article  PubMed  CAS  Google Scholar 

  • Wu FB, Chen F, Wei K, Zhang GP (2004) Effect of cadmium on free amino acid glutathione and ascorbic acid concentrations in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance. Chemosphere 57:447–454

    Article  PubMed  CAS  Google Scholar 

  • Zabadal TJ (1974) A water potential threshold for the increase of abscisic acid in leaves. Plant Physiol 53:125–127

    Article  PubMed  CAS  Google Scholar 

  • Zhao D-Y, Tian W-Y, Li L-H, Zhang W-H (2007) Nitric oxide is involved in nitrate-induced inhibition of root elongation in Zea mays. Ann Bot 100:497–503

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported financially by the National Science Council of the Republic of China (NSC 98-2313-B002-008).

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  1. Department of Agronomy, National Taiwan University, Taipei, Taiwan, ROC

    Ya-Lin Lin, Yun-Yang Chao, Wen-Dar Huang & Ching Huei Kao

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  1. Ya-Lin Lin
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Correspondence to Ching Huei Kao.

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Lin, YL., Chao, YY., Huang, WD. et al. Effect of nitrogen deficiency on antioxidant status and Cd toxicity in rice seedlings. Plant Growth Regul 64, 263–273 (2011). https://doi.org/10.1007/s10725-011-9567-0

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