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��ࡱ�>��	�����������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������[�	���)bjbj����	8Hΐΐ4o�������r	r	���������������L��D�	^ggggBBB�CDDDDDD6G��IDDQ��BB��D��gg�RD�6�6�6���g�g�C�6��C�6�6r�?T�@g�����z��t[���2vG@�ChD0�DU@�J.6RJ�@J��@�B`��6,��BBBDD�6RBBB�D������������������������������������������������������������������������JBBBBBBBBBr		{:	Title: Modulation of oxidative stress responsive enzymes and non-enzymatic components by excess cadmium in pigeon pea (Cajanus cajan Mill) cv. Upas


Running Title: Modulation of oxidative stress by excess cadmium in pigeon pea.
Authors : Pratima Sinha* and Y. K. Sharma

Corresponding author*: Dr. Pratima Sinha, Botany Department, Lucknow University Lucknow �226007 (U.P.) INDIA ,

Tel:  0522-3203201 , 09450358854; 

E- mail: pratimasinha2006@rediffmail.com
Modulation of oxidative stress responsive enzymes and non-enzymatic components by excess cadmium in pigeon pea (Cajanus cajan Mill) cv. Upas

Pratima Sinha* and Y.K. Sharma
Botany Department, Lucknow University
Lucknow �226007 (U.P.) INDIA


ABSTRACT

Heavy metal contamination of soils has markedly increased in the past few decades, the reduction in plant growth and crop production by excess heavy metals such as cadmium, cobalt, chromium, nickel and lead in contaminated soil is worldwide agriculture problem. Hence Pigeon pea (Cajanus cajan Mill) cv. Upas a very important pulse crop has been taken as a test plant, was grown in refined sand in a glass house.  Pigeon pea in excess concentration of cadmium (Cd) in the growing medium developed visual symptoms of  Cd toxicity that intensified with increasing level and duration of metal supply. The tissue concentration of cadmium increased and with increasing level of Cd supply. Decreased concentrations of chlorophylls, carotenoids and an increased carotenoids /chlorophyll ratio along with a marked increase in the activities of enzymes, viz. superoxide dismutase (SOD), ascorbate peroxidase (APOD), peroxidase (POD) and non enzymatic components- lipid peroxidation (MDA), proline, cystein, non- protein thiol (NP-SH) and electrolyte leakage suggest strong induction of oxidative stress due to excess cadmium. Decreased activity of catalase (CAT)�an iron enzyme, may suggest interference of excess cadmium in iron metabolism of plants, particularly >0.05mM Cd supply. In pigeon pea, the sufficiency value, threshold values of toxicity and Cd toxicity in leaves were < 3, 22 and 96 �g g-1 dry matter respectively which will be helpful in predicting the toxicity under field conditions. 


Keywords: Enzymes, cadmium, oxidative stress, non-enzymatic components, pigeon pea (Cajanus cajan Mill)
Cadmium (Cd2+) is one of the most toxic air, water and soil pollutants which penetrate into environment mainly through industrial processes and phosphate fertilizers. It can reach high levels in agricultural soils and is easily assimilated by plants [1]. The ability of plants to absorb Cd may depend on both the activity of root and the interaction between root and its environment. Cd is rapidly taken up by plant roots and can be loaded into the xylem for its transport into leaves. Most plants are sensitive to low Cd concentrations, which inhibit plant growth as a consequence of alterations in the photosynthesis rate and the uptake and distribution of macronutrients and micronutrients [2]. The uptake of Cd by plants varies not only among plant species but also among cultivars. Even the accumulation of essential nutrients in the leaves of plants is also affected by Cd treatments [3]. Cadmium toxicity is also correlated with disturbances in the uptake and distribution of macro and micronutrients in plants [4]. Abad and Jalil [5] suggested that reduced net photosynthesis in Cd-stressed plants occurs due to the reduced ability of RuBISCO to fix CO2. Apart from this, high Cd causes depression in cell culture growth and depresses the expression of cyclin B1 gene [6]. These damaging effects of Cd may probably be induced by excessive generation of various reactive oxygen species (ROS). It has been reported that toxic levels of various heavy metals induce oxidative stress in plants. Cd being a non-redox metal, is unable to participate in Fenten reaction.
Several studies have been suggested that an oxidative stress could be involved in Cd toxicity, by either inducing oxygen free radical production or by decreased enzymatic and non-enzymatic antioxidants [7]. It has been suggested that the uptake of Cd by roots and its subsequent translocation to shoots could be considerably affected by other metals existing in Cd-polluted soils such as Zn, Mn, Cu etc. Soils contaminated with Cd shows a sharp decline in crop productivity and therefore Cd serves as a serious problem for the agriculture  [8]. Although the toxic effects of cadmium on biological systems have been reported by several authors [4], the mechanisms of Cd toxicity are not completely understood yet. Pigeon pea plant is a common legume, grown throughout the year and consumed regularly. Hence, the present paper focuses the damages caused by excess Cd on the different facets of metabolism in pigeonpea by growing the plants at variable high levels of Cd in refined sand.
MATERIALS AND METHODS
	Pigeonpea (Cajanus cajan L.) var. Upas were gown in refined sand under glasshouse in polyethylene pots at ambient temperature. Just after the emergence of seedlings, complete nutrient solution containing [9]:
4mM KNO3; 4mM Ca(NO3)2; 2mM MgSO4; 1.5mM NaH2PO4; 0.1mM Fe-EDTA; 0.1mM NaCl; 30�M H3BO3 ; 1�M CuSO4; 1�M ZnSO4; 0.2�M Na2MoO4; 0.1�M CoSO4  and  0.1�M NiSO4. was supplied daily. Each pot was provided with a central drainage hole to allow free drainage of nutrient solution. Initially the seedlings were maintained in complete nutrient solution for 30 days. On 31st day, the pots were divided into six sets (5 pots in each set). One set was allowed to grow with full nutrient solution though out the experiment to serve as control. Each of the remaining five sets Cd was supplied with 0.05, 0.2, 0.3, 0.4 and 0.5 mM as cadmium sulphate with basal nutrient solution. Nutrition was supplied daily except on weekends. At d 38, i.e. 8 days after metal (Cd) supply (DAMS), some metabolic parameters concentration of chlorophylls, carotenoids, proline, cysteine, lipid peroxodation (MDA), non protien-SH  and some oxidative stress related enzymes such as catalase (CAT), peroxidase (POX), superoxide dismutase (SOD), ascorbate peroxidase (APX), and electrolyte leakage were estimated in leaves of pigeonpea. Protein was estimated in crude enzyme extract to represent the specific activity of enzymes.
 	The plants were examined periodically for visible foliar symptoms and changes in growth parameters and maintained till maturity. Plants were sampled at different stages of growth i.e. d 60 and 94 for the determination of dry matter, economic yield and concentration of Cd in different plant part to see their distribution and translocation (8 DAMS ;30 d) in pigeonpea.
              The concentration of photosynthetic pigments (chlorophyll a,b and carotenoids ) was determined in 80 % acetone extract according to Lichtenthaler [10]. Proline was estimated colorimetrically as ninhydrine complex in toluene [11]. 
Cysteine content was measured in supernatant using acid ninhydrin reagent at 560 nm according to the method of Gaitonde [12]  Non-protein thiol (acid soluble thiol) content in leaves was measured using Ellman,s reagent DTNB (5,5 dithiobis trinitrobenzoic acid ). The fresh material (700 mg) was homogenized in 3 ml of 6.67 % 5-sulphosalycic acid in a chilled mortar and pestle and centrifuged at 13,000 g for 10 min at 4o C. One ml of the supernatant and 9ml of reaction mixture containing 5mM EDTA and 0.6 mM DTNB in 120 mM phosphate buffer (pH 7.5) were mixed. The mixture was left for 15 min and absorbance was recorded at 412 nm following Ellman,s [13].  The readings were referred to a standard calibration curve prepared using glutathione (Sigma) for�SH. 
Lipid peroxidation was determined as the amount of malondialdehyde (MDA) produced by thiobarbituric acid (TBA) reaction as described by Heath and Packer [14]. Plant samples (500 mg) were homogenized in 5.0 ml of 0.1%(w/v) trichloro acetic acid (TCA)  and centrifuged at 10,000 x g for 20 min. Two ml of this solution was boiled for 30 min at 95 oC in a water bath with 2.0 ml of 0.5% TBA (prepared in 20% TCA) and cooled immediately on ice bath. After centrifugation at 10,000 x g, the absorbance of the supernatant was measured at 532 nm. And corrected for  non-specific absorbance by subtracting the absorbance at 600 nm. The MDA content   was calculated using extinction coefficient of 155 mM-1 cm-1.
        For the assay of catalase (CAT), peroxidase (POX) and superoxide dismutase (SOD), fresh leaf samples were homogenized with 50 mM potassium phosphate buffer (pH 7.0) and 1.0 %  polyvinyl  pyrrolidone . The homogenate was centrifuged at 20,000 x g for 20 min and the supernatant was used for assaying enzyme activity.
     The reaction mixture for CAT (E.C. 1.11.1.6), contained 0.5mmol H2O2 in 10ml 100mM phosphate buffer pH 7.0 and 1 ml enzyme extract. After 5 min reaction, H2O2 decomposed was assayed by titration the reaction mixture with 0.1 N KMnO4 according to Euler and Josephson  [15].
The activity of POX (E.C. 1.11.1.7) was assayed by the modified method of Luck   [16]. Assay mixture contained, 5ml 100mM phosphate buffer pH 6.0 ,1ml 50mM p- phenylenediamine ,1ml 3mM H2O2 and 1ml suitably diluted enzyme extract. Change in absorbance was measured at 485 nm after 5min reaction stopped by adding 2 ml of 5N H2 SO4 to the reaction mixture.  
    The activity of SOD (E.C. 1.15.1.1) was assayed in leaves by measuring the ability to inhibit the photo-chemical reduction of nitro blue tetrazolium (NBT) in 3 ml reaction mixture containg 50mM phosphate buffer pH 7.8, 13mM methionine, 75 /uM NBT, 2/uM riboflavine, 0.1mM EDTA and 0.5 ml enzyme extract adopting the method of Beauchamp and Fredovich [17]. Riboflavin was added in the last and the mixture was illuminated for 30 min. The reaction was stopped by switching off the light. Corresponding blanks were not illuminated . The absorbance of solution was measured at 560 nm and the absorbance of respective blanck was deducted.  One unit of  SOD represented  the amount that inhibited the NBT reduction by 50 % .
    The activity of APX (E.C. 1.11.1.11) was measured by the method of Nakano and Asada 
[18].Three ml of  reaction mixture  contained 50mM potassium phosphate buffer  (pH 7.0 ), 0.5 mM ascorbate, 0.1 mM  H 2O2, 0.1mM EDTA and suitable aliquot of enzyme extract. The reaction was initiated by adding H2O2 and the decrease in absorbance was recorded at each 30 sec interval for 3 min at 290 nm. The amount of ascorbate oxidized was calculated using extinction cofficient 2.8mM cm �1 and the activity was expressed as �mol ascorbate oxidized min-1mg �1 protien . 
     At 8 DAMS, plants were sampled for dry matter yield and concentration of Cd in different plant parts.  Samples collected from each treatment were washed under running tap water and rinsed with deionised water to avoid surface contamination.  Each plant part was chopped and dried in an electric oven at 70o C for 48 h and weighed for biomass determination. The oven dried material was digested using HNO3 : HClO3 ( 10:1 v/v) and  concentration of Cd was estimated in clear digest by Atomic Absorption Spectrophotometer .
      The data presented in the tables are the mean of three observations. Entire data were subjected to analysis of variance and tested for significance at p =0.05 [19].

Results and Discussion
In pigeonpea, the characteristic effects of excess Cd were discernible (at 0.5 mM Cd) at d 33 (3 days after metal supply) when subjected excess levels of Cd. In addition to growth depression the old leaves developed chlorosis initiated from the apex and margins of the leaf lamina. At d 37 (7 DAMS) stem of pigeonpea developed black spots. In severe toxicity (0.5 mM) chlorotic spots became necrotic (pale yellow), enlarge in size, coalesced and a major portion of lamina turned necrotic. At this stage, the black spots on stem coalesced and whole stem became black. Further growth of plants was checked. At later stages the affected leaves turned dry, distorted with rudimentary leaves at the top. These effects were more pronounced at 0.5 mM Cd and less so at lower levels (< 0.5 mM) of Cd. No flower and pods were formed at 0.5 to 0.2 mM Cd. At 0.1 mM Cd only a few flowers were formed which became dry and shed prematurely. The symptoms are somewhat similar to those described for some other plant species   and might also resemble Fe deficiency type symptoms [20]. The toxicity symptoms observed in plants in presence of excessive amount of heavy metal may be due to a range of interaction at the cellular level [21]. The growth inhibition (Table 1) by Cd resulted in reduced biomass [22] and might be the result of Cd on the photosynthesis rate. This reduction might also be due to the decrease in chlorophyll concentration produced by the Cd treatment [23; 24]. Cd can induce oxidative stress indirectly by producing disturbances in chloroplasts. Thus Cd produces degradation of chlorophyll and carotenoids (Table 2) as well as an inhibition of their biosynthesis [25] which can produce disturbances in the electron transport rates of PS I and PS II leading to the generation of oxygen free radicals [ 24; 4].
	Cd has been reported to interact with the water balance [4 ;26] as it affects the plasma membrane permeability causing a reduction in water content. Excess Cd stimulated the accumulation of prolines (Table 2), might be due to higher Cd uptake [27]. Significance of proline in Cd stressed plants lies in its contribution to water balance maintenance, protection of enzymes and biomolecules as well as detoxification of reactive oxygen species. Proline mediated alleviation of water deficit could substantially contribute to the Cd tolerance of plants [28].Cadmium produces alterations in the functionality of membranes by inducing lipid peroxidation (Table 2)  [29] and disturbances in chloroplast metabolism by inhibiting chlorophyll biosynthesis and reducing the activity of enzymes involved in CO2 fixation . The increase in cysteine and NP-SH contents (Table 2)  at 0.5 mM   was marked in leaves. The induction in this level of nonprotein thiols (NP-SH) paralleled with Cd. The increase in the NP-SH content which represents the free �SH groups of S containing amino acids glutathione, phytochelatins, etc., have been reported as components of the detoxification mechanism on exposure to heavy metal stress [29]. The induction in the level of free � SH groups as a result of Cd supply also indicates the behavior of pigeon pea plants against the Cd injury.
The increased activity antioxidative enzymes in excess Cd exposed plants appear to serve as an important component of antioxidant defence mechanism of plants to combat metal induced oxidative injury [8].	Catalase activity in pigeonpea leaves was reduced (Table 2)  by increasing concentration of Cd in the nutrient solution. The decline in catalase activity has been associated with Cd toxicity as has been suggested by other workers [ 30; 8]. Catalase is associated with peroxisomes and these organelles contain proteases, some of which are induced by senescence, catalase being a target of the peroxisomal protease activity [22]. The possibility of Cd-dependent changes in the transcriptional regulation of catalase can also be not ruled out [24 ; 31]. SOD is a key enzyme in protecting cell against oxidative stress. The enzyme catalyses (Table 2)   dismutation  of O2- to H2O2 and O2. This shows that antioxidative enzymes show variations in Cd stress, as has been suggested by many workers [30; 32]. Low concentration of total proteins in Cd treated pigeon pea leaves might be due to disturbed nitrogen metabolism in such conditions which consequently affects the synthesis of protein.
In Cd toxic conditions the accumulation of H2O2 and other oxygen free radicals are high resulting in higher peroxidase activity (Table 2)   in pigeonpea leaves, this shows that the cells are not competent enough to remove the toxic levels of H2O2 from the cell. Some of these radicals may function as important signalling molecules that alter gene expression and modulate the activity of specific defence proteins [4]. 
In excess Cd, another protein scavenger of hydrogen peroxide, ascorbate peroxidase (APX) (Table 2)  was also found to be reduced  in pigeonpea leaves. These ROS can oxdize proteins, lipids and nucleic acids often leading to alterations in cell structure and mutagenesis [4]. In Cd-induced pigeonpea leaves the activity of ascorbate peroxidase (APX) is also reduced might be due to H2O2 accumulation and growth retardation as has been seen in poplar roots [33].
In leaves of pigeonpea at excess Cd, the concentration of melandehyde, as a result of increased lipid peroxidation was increased (Table 2). These observations are similar to that of Barazani et al., (34), who have also reported DNA damage, oxidation of protein and reduction in the cell due to excess Cd.
	In pigeonpea the nutritional status of leaves was altered by Cd excess. The concentration of Fe was reduced in leaves (Table 1). These might suggest that Cd interferes mainly with the translocation of micronutrients (1). Metal translocation is dependent on the production of phytochelatins which have a variable affinity for specific metals and could determine the metal translocation to the shoot (Sandalio et al., 8). The changes in iron concentration is in consonance with the findings on Cd-induced disturbances in the element composition of pea [23; 30].
	Antioxidative enzymes are considered to be an important defence system of plants against oxidative stress caused by metals (1). Since the peroxidase enzymes (Table 2) are related to free radical formation, it is evident that Cd induces the development of free radical reactions. The primary stress reaction and rapid changes appear in plants due to excess Cd. The relationship between metal sensitivity and lipid peroxidation was clearly illustrated in response to Cd, indicates that Cd toxicity resulted in the increased peroxidation of ROS. Excess Cd treatment had  increased APX activities in root of maize plants [34]. These results suggest that introduction of a cysteine synthase gene into tobacco plants resulted not only in high level production of sulfur-containing compounds that detoxify cadmium, but also in active elimination of cadmium toxicity from plant bodies.
Conclusion 
It is concluded that at lower levels of Cd accumulation of osmoprotectant proline and NP-SH and activities of antioxidant enzymes CAT, POX, SOD and APX could have protected the pigeon  pea plants from the deleterious effect of Cd. However, excess Cd supply of affected adversely the metabolism resulting in a decline in the boldness and quality of seeds. In pigeon pea, the sufficiency value, threshold values of toxicity and Cd toxicity in leaves were < 3, 22 and 96 �g g-1 dry matter respectively which will be helpful in predicting the toxicity under field conditions. 

Acknowledgement
Authors are grateful to by the Indian Council of Agricultural Research under the All India  Coordinated Research Project on ��Micro and secondary nutrients and pollutant elements in
soils and plants�  for financial assistance.
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Table 1. Effect of variable Cd on dry matter, yield, Cd and Fe concentration in different part of pigeonpea

                        mM CdLSD p=0.05Control0.050.10.20.40.5         d 38    (DAMS 8)               Dry weight: g plant-12.95 1.54 (-48)1.5 (-49)1.33 (-55)1.32 (-55)1.2 (-20)0.08         d 60  (DAMS 30)7.14 3.13 (-56)2.12 (-70)2.08 (-71)1.40 (-80)1.15 (-84)0.11         d 90 (DAMS 63)17.097.35 (-57)3.29 (-79)3.11 (-81)2.57 (-85)1.99 (-88)0.21                  Total pod + inflorescence weight: g plant-14.681.30--------d 38Cd concentration: �g  g-1 dry matterLeaves:2501622012082121.32Stem:518241011291121.14Roots:815951551641171.36d 38Iron concentration: �g g-1 dry matterLeaves:34829220115098894.02Stem:2402131881631521382.22Roots:3552502472302291882.31
Table 2. Effect of variable Cd on concentration of chlorophylls, carotenoid, lipid peroxidation (MDA),  cystein, proline, and specific activity of some enzymes in  leaves  of  pigeonpea.

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