the influence of cadmium toxicity on some physiological parameters as affected by iron in rice ( ...

Journal of Plant Nutrition, 37:1202–1213, 2014Copyright C© Taylor & Francis Group, LLCISSN: 0190-4167 print / 1532-4087 onlineDOI: 10.1080/01904167.2014.881866

THE INFLUENCE OF CADMIUM TOXICITY ON SOME

PHYSIOLOGICAL PARAMETERS AS AFFECTED BY IRON

IN RICE (ORYZA SATIVA L.) PLANT

Ramazan Ali Khavari-Nejad,1,2 Farzaneh Najafi,1 and Maedeh Rezaei1

1Faculty of Biological Sciences, Kharazmi University, Tehran, Iran2Department of Biology, Islamic Azad University, Tehran, Iran

� The effects of interaction between cadmium chloride (CdCl2) and iron (Fe)- ethylenediaminete-traacetic acid (EDTA) were studied in rice plant. The seedlings of rice were treated with 0, 50, and100 μM CdCl2 supplemented with 5, 10 and 20 ppm Fe as Fe-EDTA for 30 days. Plants weregrown under controlled condition. In all the plants treated with CdCl2, growth parameters [relativeleaf growth rate (RLGR), specific leaf area (SLA), and leaf water content area (LWCA)], soluble,and unsoluble sugars contents decreased. Addition of Fe-EDTA moderated cadmium effects. UnderCdCl2 stress without Fe, malondialdehyde (MDA) content, proline content, catalase (CAT) andperoxidase (POD) activity increased, however, in solutions containing both CdCl2 and Fe-EDTA,MDA content, proline content and activities of antioxidant enzymes decreased. In 50 μM CdCl2,total protein content increased but in 100 μM decreased. With increasing Fe in solutions contain-ing CdCl2, protein content decreased. The results indicated that with increasing Fe-EDTA in CdCl2treated plants, the effects of toxicity of Cd decreased.

Keywords: Oryza sativa, cadmium, growth, iron, physiological parameters

INTRODUCTION

Cadmium (Cd) is a toxic metal and one of the main pollutants in in-dustrial area’s soil and highly toxic to plant growth and development. Cdis readily taken up by the plants and translocated to different parts ofthe plant and thus it can easily enter the food chain. Accordingly, Cd infood can cause health problems (Liu et al., 2003). Metal ions such as Cdcause physiological and morphological alterations in the plants. As well as,at the cellular level, Cd interacts with biomolecules, for example proteins(transporters or regulator proteins) and nucleic acids (Sharma et al., 2004;

Received 6 September 2011; accepted 3 January 2012.Address correspondence to Maede Rezaei, Department of Biology, Faculty of Science,Tarbiat

Moallem University, Tehran, Iran. E-mail: [email protected]

1202

Influence of Cadmium and Iron on Rice 1203

Smeets et al., 2007). The generation of toxic free radicals stimulates by cad-mium. Cd initiates oxidative stress by membrane lipids peroxidation (Smeetset al., 2007). Under Cd treatment, the absorption and translocation of metalssuch as iron (Fe), zinc (Zn), copper (Cu) and manganese (Mn) have beenstudied in agricultural crops, for example soybean (Glycine max L.), tomato(Lycopersicon esculentum L.), and wheat (Triticum aestivum L.) (Cataldo et al.,1983; Smith and Brennan, 1983; Guoping et al., 2002). Researchers observedsome differences among species, varieties and contradictions in the exper-iments (Liu et al., 2003; Guoping et al., 2002). Interaction between metalions in soil and plants, that affects its absorption, is very important. Iron isan essential ion and interfering in heavy metal toxicity, because it influencesthe absorption of heavy metal specifically or non-specifically (Sharma et al.,2004). Increase in Cd absorbtion by the roots of Fe-deficient Pisum sativum,has been studied and this subject related to Fe2+ transporter gene (IRT1)(Cohen et al., 1998). Rice is the most important cereal in the world and isused as food. In the present research, the interaction between Fe nutritionand cadmium chloride (CdCl2), with emphasis on some physiological pa-rameters in rice (Oryza sativa L.) plant, is studied. The stress level is assayedusing parameters of growth, carbohydrates content and levels of malondi-aldehyde (MDA). Furthermore, influence of the Fe–Cd interaction in riceplant is analyzed by determining proline and total protein concentrationand antioxidant enzymes activity.

MATERIALS AND METHODS

Plant Materials and Treatments

Rice (Oryza sativa L. cv. ‘Fajr’) seeds were prepared from Rice Re-search Center, Amol, Mazandaran, Iran. Seeds were sterilized in 5% sodiumhypochlorite (10 min) and washed several times with sterile distilled water.The seeds germinated on moist filter paper in a growth chamber at 27◦C tem-perature. Germinated seeds were transferred to the pots containing sand.There are some holes in the bottom of the pots to assimilate moisture ofsands to the stead. In control chamber with 16 h light periods per 24 h and200 μmol quanta m−2 s−1 light intensity, day/night temperatures of 25/18◦C,the pots were irrigated with Hoagland’s solution. The pH was adjusted to5.8. The 15 days old plants were treated with 0, 50, and 100 μM CdCl2supplemented with 5, 10, and 20 ppm Fe as Fe- ethylenediaminetetraaceticacid (EDTA) for 30 days. The experiments consist of nine treatments withfour replicates. Thus a total of 36 pots considered in a completely random-ized design. Four plants put in each pot. The nutrient solution was renewedbiweekly. To prevent cumulating additional ions while irrigation, half ofused solutions go out from bottom of the pots. The plants were grown un-der controlled environment in a greenhouse. After 45 days of experimental

1204 R. A. Khavari-Nejad et al.

period, four plants from each treatment were harvested for measurementsof biochemical and physiological parameters.

Growth Analyses

For measuring plant growth, four plants from each treatment were as-sessed by determining leaf area and shoots fresh weight. Shoots were trans-ferred into an oven to dry the tissues in 24 h at 105◦C in order to determinethe dry weights. Relative leaf growth rate (RLGR), specific leaf area (SLA)and leaf water content area (LWCA), were calculated using the equations(Evans and Hughes, 1962; Watson, 1952).

Carbohydrates Assays

Dried shoots of each treatment was homogenized in 80% ethanol andfiltered with filter paper. In soluble carbohydrate assay, for removing pig-ments from extracts, barium hydroxide [Ba(OH)2] and zinc sulfate (ZnSO4)were added to each sample. Then, mixture was centrifuged at 3000 × g for15 min. For unsoluble carbohydrate assay, substrate on filter paper was boiledfor 15 min. Then, 5% phenol and 100% sulfuric acid were added to both ofthe sample. Absorbance of extracts was measured at 485 nm (Hellubust andCraigie, 1978).

Lipid Peroxidation Assay

Lipid peroxidation levels in fresh roots were estimated as MDA content.Fresh tissues were homogenized in 0.1% trichloroacetic acid (TCA). Thehomogenate was centrifuged at 6000 × g for 5 min. 20% trichloroacetic acidin 0.5% 2-thiobarbituric acid (TBA) was added To the supernatant. Then,the mixture was included at hot bath for 30 min and quickly cooled in anice bath and centrifuged at 6000 × g for 10 min. The absorbance of thesupernatant was measured at 532 nm. Correction of the unspecific turbiditywas made by subtracting the absorbance at 600 nm. The concentration MDAwas quantified using an extinction coefficient of 0.155 μmol−1 cm−1 (Heathand Packer, 1968).

Proline Assay

Fresh shoot tissues were powdered in liquid nitrogen. The assay pow-der was mixed with 3% sulfosalicylic acid and centrifuged at 1300 × g for10 min. supernatants from each sample, acidified ninhydrin solution and100% acetic acid were blend and mixture was boiled for one hour. To stopreaction, samples were placed in ice water for at least 20 minutes and then


toluene was added. The absorbance of the reaction mixture was recorded at520 nm (Bates et al., 1973).

Protein Assay

For determination of total protein, fresh shoots were powdered in liquidnitrogen and 50 mM Tris buffer was added to each sample. The homogenatewas centrifuged at 12000×g for 20 min in 4◦C. The supernatant was usedfor determination of enzymes activity. Extracts of proteins were mixed withreagent (25 mg coomassie brilliant blue in 12.5 ml 96% ethanol with adding25 ml 85% phosphoric acid). This mixture was diluted to 250mL with waterand solution was stable in a dark bottle at 4◦C. The absorbance of the reactionmixture was read at 595 nm. Bovine serum albumin (BSA) was used asstandard (Bradford, 1976).

Catalase Activity Assay

For determination of catalase (CAT) activity, The assay mixture con-tained 50 mM Tris buffer, 25 mM hydrogen peroxide (H2O2) and enzymeextract in a total volume of 3 mL. CAT activity was calculated with variationsof absorbance at 240 nm for 5 minutes (Pereira et al., 2002).

Peroxidase Activity Assay

For determination of POD activity, the assay mixture contained 50 mMTris buffer, 5 mM H2O2, 30 mM guaiacol and enzyme extract in a totalvolume of 3 ml. POD activity was calculated with variations of absorbance at470 nm for 5 minutes (Fielding and Hall, 1978).

Statistical Analyses

The data was analyzed using randomized design with four replications.All data were statistically analyzed by Fisher’s protected least significant dif-ference (LSD) test using SAS statistical software (SAS Institute, Cary, NC,USA).

RESULTS

Rice seedlings grown under adequate and additional Fe-EDTA in thenutrient solution and in the absence and presence of different concentra-tions of CdCl2. Results of growth analysis are shown in Table 1. In all theplants were treated with CdCl2, RLGR, and SLA were significantly decreasedas compared to that control. LWCA decreased under the Cd treatments


TABLE 1 The effects of interaction between CdCl2 and Fe on RLGR (Cm2m−2d−1), SLA (m2Kg−1) andLWCA [g(H2O) m−2]. The data are Means ± SE of four replicates. Different lowercase letters indicatesignificant difference among treatments (P = 0.05)

Fe (ppm) CdCl2 (μM) RLGR SLA LWCA

5 0 457.13 ± 32.08a 93.453 ± 7.925a 53.954 ± 3.360a50 347.96 ± 3011bc 63.962 ± 5.742bc 50.622 ± 5.321ab100 250.08 ± 32.27d 42.789 ± 3.604d 39.172 ± 4.363b

10 0 461.97 ± 24.74a 93.583 ± 3.264a 55.586 ± 1.866a50 392.48 ± 4.81abc 80.232 ± 5.312ab 52.037 ± 2.721ab100 318.33 ± 12.42dc 58.114 ± 4.365cd 48.189 ± 2.203ab

20 0 409.26 ± 43.42ab 83.877 ± 10.25a 53.541 ± 7.197a50 401.45 ± 13.05abc 84.822 ± 8.794a 51.980 ± 3.347ab100 320.01 ± 22.48bcd 58.426 ± 5.803cd 48.299 ± 1.720ab

LSD at 5% 80.789 18.482 11.649

and significantly in 100 μM CdCl2. In solutions containing both CdCl2 andFe-EDTA, growth parameters increased.

Soluble and unsoluble sugars content in shoot, are shown in Table 2.Carbohydrates concentration decreased under two levels of CdCl2 (50 and100 μM) and significantly in 100 μM. Adding Fe-EDTA (10 and 20 ppm)to solutions containing Cd, moderated cadmium effects. Increase in sugarscontent was observed at Fe treatments.

In growing seedlings of the rice, the level of lipid peroxidation wasmeasured as MDA content (Figure 1). In fresh roots, the level of lipid per-oxidation was significantly increased at 20 ppm Fe-EDTA in the absenceof Cd. CdCl2 treatments led to increase in MDA level and also correlatedsignificantly with metal concentration as compared to control. In all plants

TABLE 2 The effects of interaction between CdCl2 and Fe on soluble and insoluble sugar (mg g−1d.w.)content. The data are Means ± SE of four replicates. Different lowercase letters indicate significantdifference among treatments (P = 0.05)

Fe (ppm) CdCl2 (μM) Soluble sugar Unsoluble sugar

5 0 73.99 ± 5.93a 24.69 ± 5.21a50 58.73 ± 10.64ab 18.20 ± 2.33abc

100 31.17 ± 5.52c 7.67 ± 3.79c

10 0 74.85 ± 10.66a 24.80 ± 3.72a50 64.31 ± 6.48ab 20.35 ± 2.01ab

100 33.87 ± 6.82c 7.78 ± 1.87c

20 0 75.07 ± 5.76a 25.08 ± 1.84a50 66.95 ± 9.23a 22.15 ± 2.45ab

100 40.24 ± 5.66bc 11.89 ± 3.47bcLSD at 5% 22.95 9.749


FIGURE 1 The effects of interaction between CdCl2 and Fe on lipid peroxidation (μmol g−1f.w.).Bars with different letters indicate significant difference a P< 0.05 [Fisher’s protected least significantdifference (LSD) test].

treated with solutions containing both CdCl2 and Fe- EDTA, reduction inperoxidation was observed.

Proline concentration enhanced in 50 and 100 μM CdCl2 as well as in 10and 20 ppm Fe-EDTA. As shown in Figure 2, increasing in proline content

FIGURE 2 The effects of interaction between CdCl2 and Fe on proline content (μg g−1f.w.). Bars withdifferent letters indicate significant difference a P< 0.05 [Fisher’s protected least significant difference(LSD) test].


FIGURE 3 The effects of interaction between CdCl2 and Fe on protein content (μg g−1f.w.). Bars withdifferent letters indicate significant difference a P< 0.05 [Fisher’s protected least significant difference(LSD) test].

in plants grown in different levels of Cd was significant. Interaction betweenCd and Fe led to decline in proline content.

Figure 3 shows that total protein content are higher in plants treated withFe-EDTA (10 and 20 ppm). In shoots, the level of protein content enhancedwith increasing in Cd concentration (50 μM), however, decreased at higherconcentration of Cd (100 μM) as compared to control. Reduction of totalprotein concentration was observed in solutions containing both Fe-EDTAand CdCl2.

Antioxidative enzyme activities in the plants exposed to stress are shownin Figures 4 and 5. The CAT activity increased in plants treated with CdCl2and this increment was significantly as compared to non-stressed plants. Theactivity of CAT was stimulated at exposure of Fe. Inhibition in CAT activitywas observed at plants treated with Cd and Fe. CdCl2 induced a typicalincrease in POD activity and this was significant. Elevation in POD activitywas observed in seedlings growing in presence of Fe-EDTA whereas PODactivity was decreased in interaction between Cd and Fe.

DISCUSSION

In this research, the response of rice (Oryza sativa) plant to exposure ironand toxicity of cadmium was studied. There were differences in Cd uptakeand accumulation between plant species and among genotypes of a givenspecies such as researchers have reported differences between rice cultivars


FIGURE 4 The effects of interaction between CdCl2 and Fe on catalase activity (�OD min−1g−1f.w.).Bars with different letters indicate significant difference a P< 0.05 [Fisher’s protected least significantdifference (LSD) test].

in Cd uptake (Liu et al., 2003; Shah et al., 2001). Cadmium and iron havemany chemical diversity and the cellular antitoxin pathways are distinct. Forexample, surplus Cd and Fe deposit in the epidermisand in the mesophyllof barley leaves, respectively. Researchers reported that Fe and Cd partly af-fect to likeness biochemical mechanisms and cause parallel stress responses(Sharma et al., 2004) that with our results in this research have accordant,such as, production of reactive oxygen species. Decreasing effects of Cd ongrowth and cell death have been reported in different plants (Smeets et al.,2007; Clijster and Van Assche, 1985). The results showed that the toxicityof Cd levels have significant effects on the growth parameters. RLGR, SLA,and LWCA decrease under the Cd stress levels. Addition of Fe-EDTA en-hances growth parameters. The effects of Cd toxicity in growth inhibitionare associated with restriction of photosynthesis, chlorophyll metabolism andnitrogen metabolism and reduction of water and essential element uptake(Meda et al., 2007). Cd in plants cells disarranges intracellular signaling pro-cesses and hormonal balance (Meda et al., 2007). Our results indicated that,in 50 and 100 μM CdCl2, both soluble and unsoluble sugars contents weredecreased. With increasing Fe-EDTA, cadmium effects moderated. Sugars inplants play an important role in osmotic adjustment. Environmental stressesincluding salinity, wounding, drought and infection via viruses can causevariation of sugar levels (Rolland et al., 2002). Increasing in lipid peroxida-tion in plants grown in different levels of CdCl2 as well as in Fe-EDTA ob-served. Heavy metals such as Cd, nickel (Ni), and Zn induce oxidative stress


FIGURE 5 The effects of interaction between CdCl2 and Fe on peroxidase activity (�OD min−1g−1f.w.).Bars with different letters indicate significant difference a P< 0.05 [Fisher’s protected least significantdifference (LSD) test].

with the oxidation of lipids in plant cells and accumulating reactive oxy-gen species (ROS), which include hydrogen peroxide (H2O2), superoxideradical (O2

o−) and hydroxyl radical (OHo) in plants (Sinha and Saxena,2006; Schutzendubel and Polle, 2002). Free radicals cause various dam-age to the cells membrane, organelles and biomolecules such as nucleicacids, proteins and lipids (Shah et al., 2001; Sinha and Saxena, 2006). Withthe breakdown of Fe homeostatic mechanisms in cells, oxidative stress isgenerated by free Fe (Sharma et al., 2004). Enhancement in the prolineconcentration observed under Cd and Fe treatments separation in our ex-periments. Proline content is higher in many plants and algae treated withheavy metals (Siripornadulsil et al., 2002). Similar to our results, increasein accumulation of proline in the Bacopa monniera is reported under Cu, Al,Zn, and Cd stress (Sinha and Saxena, 2006). Proline induces the cadmiumtolerance and reduces free radical damage through detoxification and re-acting with hydroxyl radicals (Sinha and Saxena, 2006; Siripornadulsil et al.,2002). In the present study, total protein content in low Cd concentrationincreased, but in high Cd concentration, decreased as compared to control.Protein content was enhanced in 10 and 20 ppm Fe-EDTA. Under heavymetals stress, such as Cd, several proteins for example, heat shock proteins(Hsp) and pathogenesis related (PR) proteins are expressed (Aina et al.,2007; Hensel et al., 1999). Cd binds with the thiolic group of proteins suchas phytochelatins with low molecular weight and metallothioneins. Proteinand Cd complexes are accumulated in the vacuole by ABC transporters,


accordingly the activity of free Cd decreased (Sanita di Toppi and Gab-brielli, 1999). Some researchers demonstrated that plant species respondto Cd stress with diminution of soluble protein content (Aina et al., 2007;Hsu and Kao, 2003). In the present experiment, exposure of Cd increasedCAT and POD activities as compared to the control grown plants. Antiox-idant enzymes like CAT and POD are able to neuter hydrogen peroxide(H2O2) and thus play an important role in restricting of oxidative stressand scavenging ROS. Producing O2 and H2O are result-quenching H2O2

via CAT (Shah et al., 2001). Smeets et al. (2007) reported an addition inCAT transcription but no meaningful variation in CAT enzymatic activity inthe Arabidopsis thaliana observed. Some authors also reported an enhance-ment in CAT activity in certain plant species treated with heavy metals Zn,Cu, lead (Pb) (Prasad et al., 1999). Decline in the activities of CAT andPOD was observed in rice roots by Cd stress (Guo et al., 2007). Inhibition ofCAT enzyme synthesis causes decrease in its activity in some stress such asenvironmental and heavy metals stresses (MacRae and Ferguson, 1985). Anincrease in the POD activity was observed in Cd (Shah et al., 2001) and Custresses (Chen et al., 2000). Also, CAT and POD activities under water stress(Zhang and Kirkham, 1994) and toxicity of Fe (Sinha and Saxena, 2006)have been reported. Metal chelator of 2,2′-bipyridine (BP) lessen Cd toxicityin rice leaves. Increase in activities of antioxidative enzymes and decreasein lipid peroxidation is associated with 2,2′-bipyridine (Fang et al., 2001).In the present research, decline of Cd toxicity in interaction with Fe in riceplant was observed. Our results show that in solutions containing both CdCl2and Fe-EDTA, growth parameters and carbohydrates content increased. Inplants grown in different levels of Fe-EDTA and CdCl2, reduction in levels ofMDA, proline, and total protein concentrations and activities of antioxidantenzymes that include CAT and POD, was observed. In the ecosystem, therewere interactions between different metals, synergistic or antagonistic. Smithand Brennan (1983) observed a synergistic interaction between Cd and Zn,whereas Cataldo et al. (1983) reported antagonistic interaction between Cdand Fe, Mn, Cu, Zn. Fe nutrition interferes in absorbance and heavy metaltoxicity. Decreasing of Cd uptake and diffusion is correlated with antago-nism effects between Cd and Fe contents (Sharma et al., 2004). Heavy metalof Cd can causes the inhibition uptake of Fe by interfering with transportersor competition. The graminaceous plants root excrete phytosiderophores(PS) under Fe deficiency which can chelate with Fe(III) and to form Fe-PScomplex. Also, phytosiderophores are not particular for Fe(III) and linkewith metals such as Mn, Ni, Zn, Cu and Cd (Meda et al., 2007). Increasein releasing of phytosiderophores in the present of toxic metals has beenreported. Researchers believed that when protons or other divalent cationspresent in soil, formation of Cd-PS complex is incoherent. Restriction of Cduptake by phytosiderophore demonstrated as a mechanism to protect maizeroots from toxic effects of Cd (Hill et al., 2002). Despite inability of Cd in


competition with Fe(III), exposure of Cd decreases the uptake rate of Fe-PScomplex.

REFERENCES

Aina, R., M. Labra, P. Fumagalli, C. Vannini, M. Marsoni, U. Cucchi, M. Bracale, S. Sgorbati, and S.Citterio. 2007. Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryzasativa L. roots. Environmental and Experimental Botany 59: 381–392.

Bates, L. S., R. P. Waldren, and I. D. Teare. 1973. Rapid determination of free proline of water stressstudies. Plant and Soil 39: 205–207.

Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities ofprotein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248–254.

Cataldo, D. A., T. R. Garland, and R. E. Wildung. 1983. Cadmium uptake kinetics in intact soybean plants.Plant Physiology 73: 844–848.

Chen, L. M., C. C. Lin, and C. H. Kao. 2000. Copper toxicity in rice seedling: Changes in antioxidativeenzyme activities, H2O2 level, and cell wall peroxidase activity in roots. Botanical Bulletin of AcademiaSinica 41: 99–103.

Clijster, H., and F. Van Assche. 1985. Inhibition of photosynthesis by heavy metals. Photosynthesis Research7: 31–40.

Cohen, C. K., T. C. Fox, D. F. Garevin, and L. V. Kochian. 1998. The role of iron deficiencystress responses in stimulating heavy-metal transport in plants. Plant Physiology 116: 1063–1072.

Evans, G. C., and A. P. Hughes. 1962. Plant growth and the aerial environment III on the computationof unit leaf rate. New Phytologist 61: 322–327.

Fang, C. H., W. J. Wu, C. C. Lin, and C. H. Kao. 2001. Cadmium toxicity of rice leaves is mediated throughlipid peroxidation. Plant Growth Regulation 33: 205–213.

Fielding, J. L., and J. L. Hall. 1978. A biochemical and cytochemical study of peroxidase activity in rootsof Pisum sativum �. Distribution of enzymes in relation to root development. Journal of ExperimentalBotany 29: 983–991.

Guo, B., Y. C. Liang, Y. G. Zhu, and F. J. Zhao. 2007. Role of salicylic acid in alleviating oxidativedamage in rice roots (Oryza sativa) subjected to cadmium stress. Environmental Pollution 147: 743–749.

Guoping, Z., F. Motohiro, and S. Hitoshi. 2002. Influence of cadmium on mineral concentrations andyield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crops Research77: 93–98.

Heath, R. L., and L. Packer. 1968. Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometryof fatty acid peroxidation. Archives of Biochemistry and Biophysics 125: 189–198.

Hellubust, J. A., and J. S. Craigie. 1978. Handbook of Physiological and Biochemical Methods. Cambridge, UK:Cambridge University Press.

Hensel, G., G. Kunze, and I. Kunze. 1999. Expression of the tobacco gene CBP20 in response to devel-opmental stage, wounding, salicylic acid and heavy metals. Plant Science 148: 165–174.

Hill, K. A., L. W. Lion, and B. A. Ahner. 2002. Reduced Cd accumulation in Zea mays: A protective rolefor phytosiderophores? Environmental Science and Technology 36: 5363–5368.

Hsu, Y. T., and C. H. Kao. 2003. Changes in protein and amino acid contents in two cultivarsof rice seedlings with different apparent tolerance to cadmium. Plant Growth Regulation 40:147–155.

Liu, J., K. Li, J. Xu, J. Liang, X. Lu, J. Yang, and Q. Zhu. 2003. Interaction of Cd and five mineralnutrients for uptake and accumulation in different rice cultivars and genotypes. Field Crops Research83: 271–281.

MacRae, E. A., and I. B. Ferguson. 1985. Changes in catalase activity and hydrogen peroxide concentrationin plants in response to low temperature. Physiologia Plantarum 65: 51–56.

Meda, A. R., E. B. Scheuermann, U. E. Prechsl, B. Erenoglu, G. Schaaf, H. Hayen, G. Weber, and N. Wiren.2007. Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiology 143:1761–1773.


Pereira, G. J. G., S. M. G. Molina, P. J. Lea, and R. A. Azevedo. 2002. Activity of antioxidant enzymes inresponse to cadmium in Crotalaria juncea. Plant and Soil 239: 123–132.

Prasad, K. V. S. K., S. P. Paradha, and P. Sharmila. 1999. Concerted action of antioxidant enzymes andcurtailed growth under zinc toxicity in Brassica juncea. Environmental and Experimental Botany 42:1–10.

Rolland, F., B. Moore, and J. Sheen. 2002. Sugar sensing and signaling in plants. The Plant Cell 14:185–205.

Sanita di Toppi, L., and R. Gabbrielli. 1999. Response to cadmium in higher plants. Environmental andExperimental Botany 41: 105–130.

Schutzendubel, A., and A. Polle. 2002. Plant responses to abiotic stresses: heavy metal-induced oxidativestress and protection by mycorrhization. Journal of Experimental Botany 53: 1351–1365.

Shah, K., R. G. Kumar, S. Verma, and R. S. Dubey. 2001. Effect of cadmium on lipid peroxidation,superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. PlantScience 161: 1135–1144.

Sharma, S. S., S. Kaul, A. Metwally, K. C. Goyal, I. Finkemeier, and K. J. Dietz. 2004. Cadmium toxicity tobarley (Hordeum vulgare) as affected by varying Fe nutritional status. Plant Science 166: 1287–1295.

Sinha, S., and R. Saxena. 2006. Effect of iron on lipid peroxidation, and enzymatic and non-enzymatic an-tioxidants and bacoside-A content in medicinal plant Bacopa monnieri L. Chemosphere 62: 1340–1350.

Siripornadulsil, S., S. Traina, D. P. Verma, and R. T. Sayre. 2002. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. The Plant Cell 14: 2837–2847.

Smeets, K., J. Ruytinx, B. Semane, F. V. Belleghem, T. Remans, S. V. Sanden, J. Vangronsveld, and A.Cuypers. 2007. Cadmium-induced transcriptional and enzymatic alterations related to oxidativestress. Environmental and Experimental Botany 63: 1–8.

Smith, G. C., and E. G. Brennan. 1983. Cadmium–zinc interaction in tomato plants. Phytopathology 73:879–882.

Watson, D. J. 1952. The physiological basis of variation in yield. Advances in Agronomy 4: 101–145.Zhang, J., and M. B. Kirkham. 1994. Drought-stress-induced changes in activities of superoxide dismutase,

catalase and peroxidase in wheat species. Plant and Cell Physiology 35: 785–791.

Copyright of Journal of Plant Nutrition is the property of Taylor & Francis Ltd and its contentmay not be copied or emailed to multiple sites or posted to a listserv without the copyrightholder's express written permission. However, users may print, download, or email articles forindividual use.

the influence of cadmium toxicity on some physiological parameters as affected by iron in rice ( ...

Documents