Abstract
An equal concentration (100 μM) of Cr(III)- and Cr(VI)-induced changes in activities of antioxidative enzymes and metabolites of ascorbate-glutathione cycle was studied in 7-d-old black gram (Vigna mungo L Hepper cv. Co4) seedlings for 5-d after infliction of Cr stress. Seeds were germinated and grown in the presence or absence of Cr under controlled environmental conditions. Uptake and translocation of Cr rate was relatively higher during first 12 h of treatment with both speciation of Cr, Cr(III)- and Cr(VI)-treated black gram roots retained 15 times more Cr than the shoots. Significantly increased lipid peroxidation was observed in the form of accumulation of malondialdehyde (MDA) and production of hydrogen peroxide (H2O2) molecule and superoxide (O2 ) radical after 6 h of infliction with Cr(VI) and after 12 h in Cr(III)-treated black gram roots. Superoxide dismutase (SOD) and ascorbate peroxidase (APX) activities were significantly increased under Cr(VI)-treatment after 12 and 6 h, respectively. However, catalase (CAT) and monodehydroascorbate reductase (MDHAR) activities were not significantly increased under Cr(Ill)-treatment. There was a steep increase of 2.71 μmol g-1 FW in ascorbic acid (AA) content was observed between 6 and 24 h of Cr(VI)-treatment. Oxidized glutathione (GSSG) content was steadily increased through the course of Cr(III)- and Cr(VI)-treatments, where as reduced glutathione (GSH) level was decreased after 24 h of treatment. GSH/GSSG ratio was rapidly decreased in treatment with Cr(III) than the Cr(VI). There was significant increase of 99 nmol g-1 FW in non-protein thiol (NPT) content was recorded between 6 and 24 h of Cr(VI)-treatment. The present results showed differential response to AA and H2O2 signaling by Cr(III) and Cr(VI), AA in combination with APX was more effective in mitigating oxidative stress as against the role of GSH as an antioxidant.
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Abbreviations
- AA:
-
ascorbic acid
- APX:
-
ascorbate peroxidase
- CAT:
-
Cablase
- Cr:
-
Chromium
- DHA:
-
Dehydroascorbate
- DHAR:
-
dehydroascorbate reductase
- DW:
-
dry weight
- FW:
-
fresh weight
- GR:
-
glutathione reductase
- GSH:
-
reduced glutathione
- GSSG:
-
oxidized glutathione
- MDA:
-
Malondialdehyde
- MDHA:
-
Monodehydroascorbate
- MDHAR:
-
monodehydroascorbate reductase
- NPT:
-
non-protein thiol
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
Literature cited
Able AJ, Guest Dl, Sutherland MW (1998) Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophtbora parasitica var nicotianae. Plant Physiol117: 491–499
Aebi H (1984) Catalase in vitro. Methods Enzymol105; 121–126
Ahmad SH, Reshi Z, Ahmad J, Iqbal M (2005) Morpho-anatomical responses of Trigoneila foenum graecum Linn, to induced cadmium and lead stress. J Plant Biol48(1): 64–84
Ali MB, Chun HS, Kim BK, Lee CB (2002a) Cadmium-induced changes in antioxidant enzyme activities in rice (Oryza sativa L. cv. Dongjin). J Plant Biol45(3): 134–140
All MB, Chun HS, Lee CB (2002b) Responses of antioxidant enzyme in rice (Oryza sativa L. cv. Dongjin) under mercury stress. J Plant Biol45(3): 141–147
Anderson ME (1985) Determination of glutathione and glutathione disulphide in biological samples. Methods Enzymol113: 548–555
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Bio chem44: 276–287
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol98: 1222–1227
Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium, and copper in cauliflower. Environ Poll109: 69–74
Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA100: 3525–3530
Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F, (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci57: 779–795
Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: Influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr25: 2389–2407
Dixit V, Pandey V, Shyam R (2002) Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ25: 687–690
Doulis AG, Debian N, Kingston-Smith AH, Foyer CH (1997) Differential localization of antioxidants in maize. Plant Physiol114: 1031–1037
Ellman (1959) Tissue sulfhydryl groups. Arch Biochem Biophys82(1): 70–77
Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier, Func Plant Biol32(6): 481–494
Han FX, Maruthi Sridhar BB, Monts DL, Su V (2004) Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. New Phytol162: 489–499
Heath RL, Packer K (1968) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot32: 93–101
Hoagland DR, Arnon Dl (1950) The water culture method for growing plants without soil, California Agricultural Experiment Station Circular 347, University of California, Berkeley, pp 32
Howe JA, Loeppert RH, DeRose VJ, Hunter DB, Bertsch PM (2003) Localization and speciation of chromium in Subterranean Clover using XRF, XANES, and EPR spectroscopy. Enviro Sci Technol37: 4091–4097
Hussain NA, Nakano Y, Asada K (1984) Monodehydroacorbate reductase in spinach chlorop lasts and its participitation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol25: 385–395
Karuppanapandian T, Pritam Bala Sinha, Kamarul Haniya A, Manoharan K (2006a) Differential antioxidative responses of ascorbate-glutathione cycle enzymes and metabolites to chromium stress in green gram (Vigna radiata L. Wilczek) leaves. J Plant Biol49(6): 440–447
Karuppanapandian T, Pritam Bala Sinha, Kamarul Haniya A, Manoharan K (2008) Chromium-induced accumulation of peroxide content, stimulation of antioxidative enzymes and lipid peroxidation in green gram (Vigna racdiata L. cv. Wilczek) leaves. Afr J Biotechnol (In press)
Karuppanapandian T, Pritam Bala Sinha, Kamarul Haniya A, Premkumar C, Manoharan K (2006b) Aluminium-induced changes in antioxidative enzyme activities, hydrogen peroxide content and cell wall peroxidase activity in green gram (Vigna radiata L. cv. Wilczek) roots. J Plant Biol (India)33(3): 241–246
Karuppanapandian T, Pritam Bala Sinha, Premkumar G, Manoharan K (2006c) Chromium toxicity: correlated with increased in degradation of photosynthetic pigments and total soluble protein and increased peroxidase activity in green gram (Vigna radiata L.) seedlings. J Swamy Bot-CI23: 117–122
Kotas J, Stasicka Z (2000) Commentary: chromium occurrence in the environment and methods of its speciation. Environ Poll107: 263–283
Lee SM, Kang BS (2005) Phytochelatin is not a primary factor in determining copper tolerance. J Plant Biol48(1): 32–38
Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2, H2O2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol136(2): 3114–3123
Liu KJ, Jiang J, Shi X, Gabrys H, Walczak T, Swartz HM (1995) Low frequency EPR study of chromium(V) formation from chromium(VI) in living plants, Biochem Biophys Res Commun206; 829–834
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measuremenl with the Folin phenol reagent. J Biol Chem193: 265–275
Mittler R (2002) Oxidative stress. Trends Plant Sci7: 405–410
Morita S, Kaminaka H, Masumura T, Yanaka K (1999) Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress signaling. Plant Cell Physiol40; 417–422
Murphy AS, Eisingter WR, Shaft JE, Kochian LV, Taiz L (1999) Early copper induced leakage from Arabidopsis seedlings is mediated by iron channels and coupled to citrate efflux. Plant Physiol121: 1375–1382
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol22: 867–880
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol49: 249–279
Panda SK, Choudhury S (2005) Chromium stress in plants. Braz J Plant Physiol17(1): 95–102
Pastori G, Foyer CH, Mullineaux P (2000) Low temperature induced changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves. J Exp Sot51: 107–113
Patterson BD, MacRaf EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem139: 487–492
Pekker I, Elisha TO, Mittler R (2002) Reactive oxygen intermediates and giutathione regulate the expression of cytosolic ascorbate peroxidase during iron-mediated oxidative stress in bean. Plant Mol Biol49: 429–438
Peterson PJ, Girling CA (1981) Other trace metals,In NW Lepp, ed. Effect of heavy metal pollution on plants. Applied Science Publishers, London, pp 213–278
Potters G, Gara LD, Asard H, Horemans N (2002) Ascorbate and glutalhione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem40: 537–548
Rock ML, James B, Helz GR (2001) Hydrogen peroxide effects on Cr oxidation state and solubility in four diverse, Cr-enriched soils. Environ Sci Technol35: 4054–4059
Schaedle M, Bassham J (1977) Chloroplast giutathione reductase. Plant Physiol59: 1011–1012
Skeffington RA, Shewry PR, Eterson P (1976) Chromium uptake and transport in barley seedlings (Hordeum vu/gare L.), Planta132: 209–214
Sutherland MW, Learmonth BA (1997) The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismulase. Free Radic Res27: 283–289
Toppi LS, Musetti R, Marabottini R, Corradi MG, Vattuone Z, Favali MA, Badiani M (2004) Responses of Xanthoria parietina thalli to environmentally relevant concentrations of hexavalent chromium. Func Plant Biol31(4): 329–338
Vazquez MD, Poschenrieder C, Barcelo J (1987) Chromium VI induced structural changes in bush bean plants (Phaseolus vulgaris L.). Ann Bot59: 427–438
Wang S-H, Yang Z-M, Yang H, Lu B, Li S-Q, Lu Y-P (2004) Copperinduced stress and antioxidative responses in roots of Brassica juncea L. Bol Bull Acad Sin45: 203–212
Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inze D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C- 3 plants. EMBO J16: 4806–4816
Zayed A, Lytle CM, Terry N, Qian JH (1998) Chromium accumulation, translocation and chemical speciation in vegetable crops. Planta206: 293–299
Zayed AM, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil249: 139–156
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Karuppanapandian, T., Manoharan, K. Uptake and Translocation of Tri- and Hexa-Valent Chromium and Their Effects on Black Gram (Vigna mungo L. Hepper cv. Co4) Roots. J. Plant Biol. 51, 192–201 (2008). https://doi.org/10.1007/BF03030698
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DOI: https://doi.org/10.1007/BF03030698