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In vitro Study of Interactive Effect of Cadmium and Salicylic Acid on Growth and Biochemical Parameters in Tetra and Hexaploid Wheat.

Byline: Sadia Noureen Zafar and Farrukh Javed

Abstract

In vitro cultures of plants offer a useful tool to study the adaptive mechanisms of plants in the presence of high metal concentrations. Callus cultures of tetraploid (Durum-97) and hexaploid (Shafaq-06) wheat genotypes exposed to different cadmium (Cd) concentrations (0, 100, 400, 800 and 1200 uM) and its alleviation by salicylic acid (0, 0.5 mM) were assayed for growth, antioxidant responses and Cd accumulation characters. Cadmium hampered the growth and notably enhanced antioxidant activity in all Cd regimes. We provided evidence that the two genotypes hexaploid and tetraploid are characterized by different response to cellular homeostasis and detoxification to Cd in callus culture. In particular, the high tolerance in hexploid genotype (Shafaq-06) is associated with relatively higher activity of antioxidants and Cd accumulation behaviour as indicated by Cd contents, bioconcentration factor (BCF) and stress tolerance index (STI).

However, the follow-up treatment (0.5 mM) with salicylic acid (SA) mitigated the Cd generated stress and significantly (P[?]0.05) improved the aforesaid parameters.

Keywords: Antioxidant; Cadmium; Teraploid; Hexaploid; Salicylic acid

Introduction

Unprecedented bioaccumulation of heavy metals in the environment has become a dilemma for all the living organisms including plants. This phytotoxcity is problem of paramount importance for ecological, nutritional and environmental reasons and has serious implications in agriculture as it has acquired new dimensions with the advent of the industrial era (Nagajyoti et al., 2010; Iqbal et al., 2015). Cadmium is a highly toxic metal which has no known biological function (Chen et al., 2007; 2014). Moreover, beside its primary effects, it may also provoke secondary effects that in turn may activate in convergence (Prasad and Hagemeyer, 1999), such as photosynthesis and respiration decay or interference with mineral nutrition (Jiang et al., 2004; Dong et al., 2006) and numerous serious morphological, metabolic, and physiological anomalies.

Cadmium is a non-redox metal and unable to participate in Fenton-type reactions but causes oxidative stress via overproduction of reactive oxygen species (ROS), disturbing the equilibrium between prooxidant and antioxidant homeostasis (Garnier et al., 2006) and increasing lipid peroxidation. This condition implicates the causation of multiple deteriorative disorders such as, oxidation of protein and lipids, ion leakage, oxidative DNA attack, redox imbalance, and denature of cell structure and membrane, ultimately resulting in the activation of programmed cell death (PCD) pathways (Rascio and Navari-Izzo, 2011; Sharma et al., 2012). Plants are equipped with a repertoire of mechanisms to counteract heavy metal toxicity and in response, activation of antioxidant defense mechanism is pursued (Emamverdian et al., 2015).

The enzymes superoxide dismutase (SOD), catalase (CAT), and peroxidase (POX) are involved in the detoxification of O2 and H2O2, thereby preventing the formation of OH radicals (Gill and Tuteja, 2010).

Alleviation of Cd toxicity by rebalancing the impaired prooxidant and antioxidant ratio through supplementation has gained a wide interest. Owing to considerable evidence of the injurious effects of Cd on plants, it was hypothesized that SA can assuage the toxic effects of Cd on wheat. Salicylic acid is considered as endogenous phytohormone of phenolic nature that can modulate plant responses to a wide range of abiotic or oxidative stresses or acts as an endogenous regulator that potentially affects the growth and productivity (Sakhabutdinova et al., 2003).

Tissue culture techniques offer valuable tool for studying, testing, improving and selecting plant material for tolerance to stress factors and cellular stress response (Azevedo et al., 2005; Shekhawat et al., 2010; Ahmad et al., 2013). This evaluation of the behaviour of in vitro cell cultures exposed to Cd toxicity may contribute to the knowledge that these cells may used in genetic improvement programs to withstand Cd toxicity.

Tetraploid Triticum durum Desf. is generally considered the hardiest of all wheats and has been regarded as an ancestral relation to modern day hexaploid bread wheat (Elias and Manthey, 2005). It seems that the amount of work done to study the effects of Cd toxicity on wheat callus tissue has not been significant. So the present study was focused to investigate different aspects related to the genotypic variations in hexaploid and tetraploid wheat calli under Cd toxicity. Meanwhile, for an in-depth understanding of the harmfulness of heavy metal as well as the mechanisms for protection and tolerance provided by SA which have been shown to vary in intensity in wheat genotypes at ploidy level.

Materials and Methods

Tetraploid (Durum-97) and hexaploid (Shafaq-06) wheat genotypes were provided by Nuclear Institute of Agriculture and Biology (NIAB) Faisalabad, Pakistan. For the induction of callus sterilized grains were cultured aseptically in test tubes containing 10 mL of MS medium (Murashige and Skoog, 1962) (solidified with agar) supplemented with (5 mg L-1) 2, 4-dichlorophenoxy acetic acid (2, 4-D). Incubation temperature was maintained at 25C with white florescent light. To study the effects of Cd toxicity alone and Cd along with SA (control, 100, 400, 800 and 1200 uM) levels of Cd (as CdCl2) and two levels (control, 0.5 mM) of salicylic acid (C7H6O3) were applied to one month old calli. Callus tissues were cultured in 100 mL Erlenmeyer (Pyrex) flasks, containing 40 mL liquid MS medium, with the same concentration of 2, 4-D as above mentioned and corresponding treatments and then placed on gyratory shaker till the termination of experiment.

Each treatment was replicated thrice and each replicate was consisted of ten flasks. After 15 days of treatment, calli were harvested and following parameters were studied.

Callus Fresh Weight/Relative Growth Rate (RGR-fresh) (g)

Fresh weight of calli was determined on analytical balance and relative fresh weight of callus growth was calculated as:

In (Final fresh weight) - In(Initial fresh weight)

Where ln denotes the natural logarithm.

Callus Dry Weight (g)

After determination of fresh weight, calli were placed in oven at 65C for a week and the dry weight was determined.

Callus Bioconcentration Factor (BCF)

The callus BCF was calculated as follows:

BCF = Cd accumulation in callus (mg/kg ) / Cd concentration in the medium (mg/kg )

Callus Stress Tolerance Index (STI)

The callus STI was calculated as follows:

STI = Average dry weight of callus (treated) / Average dry weight of callus control

Determination of Cd Contents

The dried ground material (0.5 g) of calli was digested in concentrated HNO3 (5 mL) at 100 in digestion tubes and volume of the extract was maintained up to 50 mL. Filtered extract was used for estimation of Cd contents with atomic absorption spectrophotometer.

Antioxidant Enzyme Activity Assay

Fresh samples of calli (0.5 g) were homogenized in 100 mM phosphate buffer (pH 7) containing 0.1 mM EDTA and the supernatant was used for the following antioxidant enzymes activity assay.

Superoxide Dismutase (SOD)

Superoxide dismutase activity was appraised following Giannopolitis and Ries (1977) with minor modifications. The photoreduction was measured by recording an increase in absorbance at 560 nm using UV-visible spectrophotometer (IRMECO U2020). One unit of SOD activity reflected the amount required to cause 50% inhibition of the NBT at 560 nm.

Catalase (CAT) and Peroxidase (POD)

The activities of CAT and POD enzymes were determined according to Chance and Maehly (1955) with minor modifications. For CAT, changes in absorbance of the solution every 20s were monitored at 240 nm and were expressed as umol of H2O2 decomposed per min per mg of protein. Whilst for POD, changes in absorbance of the reaction solution were recorded at 470 nm after every 20 seconds. One unit of POD activity was equivalent to change in absorbance per mg of protein.

Malanodialdehyde (MDA) and Hydrogen Peroxide (H2O2)

The level of lipid peroxidation in terms of concentration of thiobarbituric acid reactive substance (TBARS) was determined following the method of Yagi (1982). The absorbance was read at 532 nm. The absorption coefficient was calculated at 155 mmol cm-1 and expressed as nmol/MDA/g fresh weight.

MDA level (nmol) = (A532nm - A600NM)/1.56x10 5

Hydrogen peroxide (H2O2) contents were determined according to Velikova et al. (2000) and absorbance was recorded at 390 nm.

Statistical Analysis

An analysis of variance (ANOVA) was used to analyse the data for all parameters using a computer software COSTAT (Cohort Software Berkeley, California). The least significant differences (LSD) between means were calculated using Duncan's New Multiple Range test (P[?]0.05).

Results

The growth of calli grew and proliferated with the course of time on Cd treatments (control, 100, 400, 800 and 1200 uM) were compared and revealed significant (Pless than 0.05) reductions in the calli relative growth rate (RGR) and dry weight exhibiting that Cd in culture medium inhibited the callus growth as compared to control (Fig. 1). Compared to the control RGR, reduction of 60% and 56% at 1200 uM Cd was observed in Durum-97 and Shafaq-06, respectively and greater extent of suppression was recorded in Durum-97 as compared to Shafaq-06.

Cadmium accumulation by the callus of two wheat genotypes significantly (Pless than 0.05) accelerated by the imposition of Cd stress in the medium (Table 1). However, Durum-97 accumulated more Cd contents as compared to Shafaq-06. On the other hand SA application with the elevating Cd stress declined the callus Cd accumulation in both genotypes. To assess the capability of calli to grow in the presence of a given concentration of Cd, the stress tolerance index (STI) was calculated. Plants with STI greater than 0.6 are considered tolerant (Lux et al., 2004). As presented in Table 2 Shafaq-06 showed a good tolerance to exposed Cd up to 800 uM and showed values equal/higher than 0.6. On the other hand, Durum-97 showed a lower tolerance index from 400 uM (Pless than 0.05). Upon application of SA, both genotypes showed a significant extent of improvement in STI to Cd toxicity.

The evaluation of the ability of plants to concentrate Cd from external solutions in their tissues is determined by bioconcentration factor (BCF). In Fig. 1, calli of both the genotypes showed higher values at 100 uM whilst showing a decreasing trend along with the increasing Cd concentration in the medium and differences recoded were significant (Pless than 0.05). Lower values of BCF of Shafaq-06 calli were recorded as compared to Durum-97. By the application of SA values of BCF showed suppression by the calli of both genotypes.

Malanodialdehyde (MDA) is an index of lipid peroxidation. Treatments and genotypes differed significantly (Pless than 0.05) for this parameter. Its level in Durum-97 and Shafaq-06 increased by 146% and 127%, respectively at 1200 uM in comparison with control and SA treatments efficiently reduced the stimulatory effect of Cd stress on status of lipid peroxidation (Fig. 3).

Superoxide dismutase (SOD) activity revealed a significant increase in both the genotypes. However, in Durum-97 SOD activity peaked at 400 uM whilst in Shafaq-06 it peaked at 800 uM. Declined SOD activity at 1200 uM was still higher than the control. The increase in SOD activity induced by the excessive heavy metal was alleviated by SA application. The POD activity increased gradually with Cd concentrations, but changes were not always significant and its activity elevated to 54% and 50% in Durum-97 and Shafaq-06, respectively under Cd toxicity. Salicylic acid induced a declining effect on enzyme activity upon Cd exposure. Catalase (CAT) is an important enzyme to eliminate H2O2 and O-2. The CAT activity showed an enhancement under Cd stress in SA free calli in both the genotypes (Fig. 2). The activity was significantly (P[?]0.05) higher at the elevated concentrations of Cd and peaked at highest concentrations of Cd.

However, minimal activity of CAT was observed in SA treated calli upon heavy metal exposure.

Fig. 3 reveals significant (P[?]0.05) enhancement in H2O2 contents that is manifestation of oxidative stress under SA free conditions, H2O2 contents increased by 210% in Durum-97 and 206% in Shafaq-06 at 1200 uM, which under SA treatment decreased to about 127% and 134%, respectively.

Discussion

In vitro study conducted to appraise the Cd accumulation turned out a cascade of events. Inhibition of growth exhibited by both genotypes showed differential genotypic responses suggesting that Durum-97 had higher callus Cd accumulation that caused inhibition in RGR and dry weight and resulted in callus growth inhibition. Similar results have been demonstrated in the calli of sunflower (Azevedo et al., 2005), Sesbania drummondii (Israr et al., 2006) and safflower (Namjooyan et al., 2012). Callus STI decreased with the elevating Cd concentrations in the culture medium. Though the accumulation pattern was very similar among genotypes, yet Shafaq-06 exhibited high STI as compared to the other. The superior ability of Shafaq-06 to better cope with Cd toxicity as compared to Durum-97 was elicited at the highest Cd level.

At the highest Cd level, lower BCF value of Shafaq-06 might be ascribed to the maintenance ability of metal influx and efflux matrix whereas marked callus growth reduction in Durum-97 attributed to cell membrane damage. Differential genotypic behaviour under Cd stress had been reported in Populus nigra clones (Iori et al., 2012).

Cytotoxic ROS production is inevitable consequence of Cd-induced oxidative stress. Reactive oxygen species (ROS) accumulation as a result of various environmental stresses is a major cause of loss crop productivity worldwide (Mittler, 2002). It has been well established that SOD, POD activity, H2O2 and MDA contents are important parameters for estimating what extent plants suffer from adverse stress (Wu et al., 2003). Cadmium stress enhanced MDA and H2O2 accumulation in calli suggesting that this increase results in oxidative stress that in turns hampered the calli growth due to greater damage to cell membrane system. A marked increase in MDA status in Durum-86 as compared to other genotype might be attributed to the greater Cd induced injury in membranes and production of more ROS.

On the contrary, Shafaq-06 showed low MDA contents signifying that reduced MDA concentration was due to efficient antioxidant enzyme activity (SOD, CAT, POD), that decreased H2O2 levels and conferred membrane stability. Similar findings have been reported previously in tomato (Shalata et al., 2001) and maize (Neto et al., 2006). However, the pragmatic approach of exogenous application of SA might induced the Cd tolerance and resulted in lesser MDA contents that could be attributed to the modifications in compartmentalization and modulation of redox balance through antioxidant activities. The decline in SOD activity at 1200 uM might indicate its impaired functionality under higher concentrations of Cd as previously reported in Alyssum (Schickler and Caspi, 1999). The activity of SOD observed to be greater in Shafaq-06 as compared to Durum-97 suggesting that the enhanced response provided a better protection against ROS (Takemura et al., 2000; Zhang et al., 2005).

It may also suggest on the ground of the results in the present study that Cd induced a reduction in the activity of SOD at higher levels. Thus this reduction might be accompanied by the accumulation of H2O2 in different compartments which may cause the inactivation of this enzyme (Vitoria et al., 2001). Similar trends in the SOD activity under Cd stress had been observed in Sesbania drummondi callus (Israr et al., 2006), B. juncea callus (Shekhawat et al., 2010) and the adapted calli of sunflower and safflower (Gallego et al., 2002; Namjooyan et al., 2012).

Table 1: Mean values of H2O2, CAT, MDA, SOD and POD with Cd alone as well as Cd in combination with salicylic acid of tetraploid (Durum-97) and hexaploid (Shafaq-06) calli with standard errors

###Cadmium+###Cadmium+Salicylic acid (0.5 mM)

Treatment Genotypes###H2O2###CAT###MDA###SOD###POD###H2O2###CAT###MDA###SOD###POD

Cadmium

Control###Durum-97###0.4840.01m###21.660.3i###37.920.8k###28.270.9j###15.730.7g###0.4090.09o###19.640.3l###41.010.8j###32.661.3j###16.820.3h

###Shafaq-06###0.4380.01n###23.950.4i###35.330.1l###26.701.0k###17.530.3gh###0.3750.01p###23.490.3i###39.490.4jk###30.150.9ij###17.910.4gh

Cd###100 Durum-97###0.9680.04e###28.250.4f###58.831.0g###41.851.5de###17.690.4gh###0.7280.03k###20.660.6kl###50.950.3h###30.230.5i###17.850.8gh

uM###Shafaq-06###0.9160.02h###26.220.1h###50.481.1h###45.651.3c###19.890.3ef###0.6750.02l###21.651.2jk###44.170.6i###35.520.4g###18.851.3g

Cd###400 Durum-97###1.010.01gh###31.640.8cd###74.020.8c###50.500.2b###24.821.2ef###0.8410.03i###24.781.0i###52.241.16g###39.830.4e###19.890.6f

uM###Shafaq-06###1.180.03d###32..610.3c###69.741.0e###48.920.8b###23.790.9e###0.7950.01j###26.190.3gh###62.360.3f###41.810.5de###20.690.7ef

Cd###800 Durum-97###1.220.04c###32.480.3c###80.880.2b###44.761.5c###29.450.5bd###0.9090.05g###27.930.3b###72.820.9d###39.991.0ef###25.910.5d

uM###Shafaq-06###1.310.03b###27.800.6b###62.091.0e###55.071.4a###31.920.3b###0.8920.02h###29.841.0ef###59.890.3g###42.560.8d###27.630.2cd

Cd1200###Durum-97###1.390.02a###37.070.1a###93.512.6a###48.491.2fg###30.260.3b###0.9980.04h###29.250.3f###80.250.5b###28.320.5jk###29.850.7b

uM###Shafaq-06###1.280.02b###38.300.6a###80.230.4b###39.080.6ef###34.800.6a###1.0190.06f###31.630.9cd###69.150.7e###38.430.4h###30.130.3b

Table 2: Mean values of Cd contents, RGR, Dry weight, BCF and STI with Cd alone as well as Cd in combination with salicylic acid of tetraploid (Durum-97) and hexaploid (Shafaq-06) calli with standard errors. ND: Not detectable

###Cadmium+###Cadmium+Salicylic acid (0.5 mM)

Treatment Genotypes###Cd###RGR callus###Dry weight###BCF###STI###Cd###RGR callus###Dry weight###BCF###STI

Cadmium###callus###callus

Control###Durum-97###ND###0.50 0.01b###0.2740.008c###--###--###ND###0.4900.001b###0.230.05a###--###--

###Shafaq-06###0.547 0.02a###0.2760.04c###0.500.01b###0.2690.01b

Cd 100###Durum-97###138.660.8l###0.4620.003###0.2320.004f###1.340.003a###0.7950.005###120.290.5m###0.5210.01d###0.2610.02d###1.160.004b###0.8350.02b

uM###Shafaq-06###143.50 0.8k###g0.5040.01e###0.2460.05e###1.10.004b###b0.8540.02d###109.35 0.3n###0.530.04d###0.2710.006cd###0.90.003c###0.9140.01a

Cd 400###Durum-97###203.990.4h###0.313 0.01i###0.1290.01g###0.780.04d###0.6620.01f###165.310.3j###0.4220.006g###0.2330.01f###0.690.02d###0.7190.01e

uM###Shafaq-06###190.010.5i###0.3720.007h###k 0.193.02g###0.710.005de###0.7030.008e###171.771.2j###0.4160.01g###0.2290.024f###0.650.07e###0.8730.09c

Cd 800###Durum-97###253.320.5e###0.2890.006###0.1040.003j###0.730.01de###0.5170.02h###219.660.2g###0.3350.02i###0.1740.04h###0.620.004f###0.6070.01g

uM###Shafaq-06###232.450.5f###k0.3240.003j###0.147.002i###0.690.02ef###0.6040.02g###205.670.5h###0.3440.02i###0.1880.009g###0.540.008g###0.6140.02g

Cd1200###Durum-97###336.981.8a###0.2030.01o###0.0340.009###0.640.05fg###0.3140.02k###295.990.3c###0.2060.005###0.0960.003l###0.560.003g###0.3460.02j

uM###Shafaq-06###320.980.8b###0.2380.003n###m .081.01l###0.570.008gh###0.3890.08j###291.070.3d###m0.2930.01l###0.1150.003k###0.440.001i###k0.4590.04i

Catalase (CAT) is another integral component of antioxidant system and its role in protecting the organism from damage caused by ROS is indispensable. It protects SOD against inactivation caused by the higher accumulation of H2O2 (Willekens et al., 1994; Fridovich, 1995). The progressed CAT activity with the increasing Cd levels in the culture medium had been observed in agreement with that of Leucaena leucocephalla callus (Rout et al., 1999) and Trema orientalis callus (Samantaray et al., 1999).

Peroxidase (POD) is one of the principle enzymes that play key role in the elimination of ROS. Increased activity of POD is now assigned as a biomarker of heavy metal stress; moreover, lignin biosynthesis takes place with the contribution of POD activity that builds up a physical barrier against lethal heavy metal toxicity (Hegedus et al., 2001). Salicylic acid application with the elevating Cd stress depressed the activities of CAT and POD revealing that this may be the manifestation of the beneficial effect of SA during earlier growth period, which prevented cumulative damage development response to Cd. Moreover, SA may activate Cd tolerance mechanisms different from Cd distribution and antioxidant defense. One mechanism may be the avoidance of damage and includes any mechanisms of Cd binding resulting in lowered plasmatic free Cd.

Conclusion

The studies led to conclusion that the positive SA effect on Cd-challenged calli of tetra and hexaploid wheat could have many hypothetical explanations. On the basis of antioxidant profile and STI, BCF, MDA levels, we can safely conclude that hexalopid wheat (Shafaq-06) performs better upon exposure to heavy metal stress and SA prevented cumulative damage development in response to endogenous Cd accumulation. This suggests that SA could be used as a potential growth regulator to improve the plant growth under Cd stress.

Acknowledgements

The first author acknowledges the financial grant from Higher Education Commission of Pakistan for her Ph.D. indigenous fellowship.

References

Ahmad, K., Z.I. Khan, S. Ashraf, A. Ejaz, M. Shaheen, S.H. Raza, F. Abbas and H.M. Tahir, 2013. Effect of sewage water irrigation on the uptake of some essential minerals in canola (Brassica napus L.): A potential forage crop for ruminants. Pak. J. Life Soc. Sci., 11: 42-47

Azevedo, H., C.G.G. Pinto and C. Santos, 2005. Cadmium effects in sunflower: Membrane permeability and changes in catalase and peroxidase activity in leaves and calluses. J. Plant Nutr., 28: 2233- 2241

Chance, B. and A.C. Maehly, 1955. Assay of catalase and peroxidase. Method Enzymol., 2: 764-775

Chen, F., W. Feibo, J. Dong, E. Vincze, G. Zhang, F. Wang, Y. Huang and K. Wei, 2007. Cadmium translocation and accumulation in developing barley grains. Planta, 227: 223-232

Chen, M., L. Cao, X. Song, X. Wang, Q. Qian and W. Liu, 2014. Effect of iron plaque and selenium on cadmium uptake and translocation in rice seedlings (Oryza sativa) grown in solution culture. Int. J. Agric. Biol., 16: 1159-1164

Dong, J., F. Wu and G. Zhang, 2006. Influence of cadmium on antioxidant capacity and four microelement concentrations in tomato seedlings (Lycopersicon esculentum). Chemosphere, 64: 1659-1666

Elias, E.M. and F.A. Manthey, 2005. End products: present and future uses. In: Durum Wheat Breeding Current Approaches and Future Strategies, pp: 63-86. Royo, C., M.M. Nachit, N. DiFonzo, J.L. Araus, W.H. Pfeiffer and G.A. Slafer (eds.). Food Products Press, New York, USA

Emamverdian, A., Y. Ding, F. Mokhberdoran and Y. Xie, 2015. Heavy metal stress and some mechanisms of plant defense response. Sci. World J., 12: 187-190

Fridovich, I., 1995. Superoxide radical and superoxide dismutases. Annu. Rev. Biochem., 64: 97-112

Gallego, S.M., M.P. Benavides and M.L. Tomaro, 2002. Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci., 121: 151-159

Garnier, J., A. Cebron, G. Tallec, G. Billen, M. Sebilo and A. Martinez, 2006. Nitrogen behaviour and nitrous oxide emission in the tidal Seine River estuary (France) as influenced by human activities in the upstream watershed. Biogeochemistry, 77: 305-326

Giannopolitis, C.N. and S.K. Ries, 1977. Superoxidae dismutase. I. Occurrence in higher plants. Plant Physiol., 59: 309-314

Gill, S.S. and N. Tuteja, 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biolchem., 48: 909-930

Hegedus, A., S. Erdei and G. Horvath, 2001. Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci., 160: 1085-1093

Iori, V., F. Pietrini, A. Massacci and M. Zacchini, 2012. Induction of metal binding compounds and antioxidative defense in callus cultures of two black poplar (P. nigra) clones with different tolerance to cadmium. Plant Cell Tissue Org. Cult., 108: 17-26

Israr, M., S.V. Sahi and J. Jain, 2006. Cadmium accumulation and antioxidative responses in the Sesbania drummondii callus. Arch. Environ. Contam. Toxicol., 50: 121-127

Iqbal, M.M., G. Murtaza, Z.A. Saqib and R. Ahmad, 2015. Growth and physiological responses of two rice varieties to applied lead in salt affected soils. Int. J. Agric. Biol., 17: 901-910

Jiang, X.J., Y.M. Luo, Q. Liu, S.L. Liu and Q.G. Zhao, 2004. Effects of cadmium on nutrient uptake and translocation by Indian mustard. Environ. Geochem. Health, 26: 319-324

Lux, A, A. Sottnikova, J. Opatrna and M. Greger, 2004. Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiol. Plant., 120: 537-545

Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci., 7: 405-410

Murashige, T. and F. Skoog, 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant., 15: 473-497

Nagajyoti, P.C., K.D. Lee and S.V.M. Sreekanth, 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem Lett., 8: 199-216

Namjooyan, S., R. Khavari-Nejad and F. Bernard, 2012. The effect of cadmium on growth and antioxidant responses in the safflower (Carthamus tinctorius L. ) callus. Turk. J. Agric. For., 36: 145-152

Neto, A.D., J.T. Prisco, J. Eneas-Filho, C.E.B. Abreu and E. Gomes-Filho, 2006. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt sensitive maize genotypes. J. Environ. Exp. Bot., 56: 87-94

Prasad, M.N.V. and J. Hagemeyer, 1999. Heavy Metal Stress in Plants: From Molecules to Ecosystems. New York, USA

Rascio, N. and F. Navari-Izzo, 2011. Heavy metal accumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci., 180: 169-181

Rout, G.R., S. Samantaray and P. Das, 1999. Chromium, nickel and zinc tolerance in Leucaena leucocephalla. Silvae Genet., 48: 151-157

Sakhabutdinova, A., D.R. Fatkutdinova, M.V. Bezrukova and F.M. Shakirova, 2003. Salicylic acid prevents the damaging action of stress factors on wheat plants. Bulg. J. Plant Physiol., 21: 314-319

Samantaray, S., G.R. Rout and P. Das, 1999. Chromium and nickel tolerance of Trema orientalis (Blume) L. in tissue culture. Acta Physiol. Plant., 21: 27-35

Schickler, H. and H. Caspi, 1999. Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiol. Plant., 105: 39-44

Shalata, A., V. Mittova, M. Volokita, M. Guy and M. Tal, 2001. Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the antioxidative system. Physiol. Plant., 112: 487-494

Sharma, P., A.B. Jha, R.S. Dubey and M. Pessarakli, 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot., 221: 1-26

Shekhawat, G.S., K. Verma, S. Jana, K. Singh, P. Teotia and A. Prasad, 2010. In vitro biochemical evaluation of cadmium tolerance mechanism in callus and seedlings of Brassica juncea. Protoplasma, 239: 31-38

Takemura, T., N. Hanagata, Z. Dubinsky and I. Karube, 2002. Molecular characterization and response to salt stress of mRNAs encoding cytosolic Cu/Zn superoxide dismutase and catalase from Bruguiera gymnorrhiza. Trees, 16: 94-99

Velikova, V., I. Yordanov and A. Edreva, 2000. Oxidative stress and some antioxidant systems in acid rain treated bean plants: Protective role of exogenous polyamines. Plant Sci., 151: 59-66

Vitoria, A.P., P.J. Lea and R.A. Azevedo, 2001. Antioxidant enzymes responses to cadmium in radish tissues. Phytochimistry, 57: 701-710

Willekens, H., W.V. Camp, M.V. Montago, D. Inze, C. Langebartels and H. Sandermann, 1994. Ozone, sulphurdioxide and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol., 106: 1007-1014

Wu, F.B., G.P. Zhang and P. Dominy, 2003. Four barley genotypes respond differently to cadmium: Lipid peroxidation and activity of antioxidant capacity. Environ. Exp. Bot., 50: 67-77

Yagi, K., 1982. Assay for serum lipid peroxide level and its clinical significance. In: Lipid Peroxides in Biology and Medicine, pp: 223- 242. Yagi, K. (ed.). Academic Press, New York, USA

Zhang, H., Y. Jiang, Z. He and M. Ma, 2005. Cadmium accumulation and oxidativeburst in garlic (Allium sativum). Plant Physiol., 162: 977-984
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Author:Zafar, Sadia Noureen; Javed, Farrukh
Publication:International Journal of Agriculture and Biology
Article Type:Report
Date:Aug 31, 2016
Words:5007
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