Abstract
Growth performance, chromium (Cr) accumulation potential and induction of antioxidative defence system and phytochelatins (PCs) were studied in hydroponically grown Brassica juncea (Indian mustard) and Vigna radiata (mungbean) at various levels of Cr treatments (0, 50, 100, 200 μM Cr). B. juncea accumulated twofolds and threefolds higher Cr in root and shoot, respectively than in V. radiata. Compared to B. juncea, V. radiata was found to be particularly sensitive to Cr as observed by the severity and development of Cr toxicity symptoms and decreased growth. Induction of PC and enzymes of antioxidant defence system were monitored as plant’s primary and secondary metal detoxifying responses, respectively. There was induction of PC and enzymes of antioxidant defence system in both the plants. PCs were induced significantly in roots and shoot of both the plants at all the levels of Cr treatments. Significantly higher activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT) and glutathione reductase (GR) were observed in shoot of B. juncea than V. radiata at all the levels of Cr treatments. Induction of PCs along with antioxidant defence system in response to Cr stress suggests the cumulative role of PCs and antioxidants in conferring tolerance against accumulated Cr in B. juncea, and thereby signifies the suitability of this plant as one of the potential remediators of Cr.
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Abbreviations
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- Cr:
-
Chromium
- DTNB:
-
5′ Dithio-bis-(2-nitrobenzoic acid)
- Fw:
-
Fresh weight
- GR:
-
Glutathione reductase
- GSH:
-
Reduced glutathione
- LSD:
-
Least significant difference
- MT:
-
Metallothioneins
- MDA:
-
Malondialdehyde
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- TBA:
-
Thiobarbituric acid reactive substances
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Alscher RG, Erturk N, Heath LS (2003) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1131–1341
Anderson ME (1985) Determination of glutathione and glutathione disulfides in biological samples. Methods Enzymol 113:548–554
Arvind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L., a free floating freshwater macrophyte. Plant Physiol Biochem 41:391–397
Asada K (1992) Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241
Baker AJM, Mc Grath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, pp 85–107
Barcelo J, Poschenrieder C (1990) Plant-water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37
Barcelo J, Poschenrieder C, Gunse B (1986) Water relations of chromium (VI) treated Bush bean plants (Phaseolus vulgaris L. cv Contender) under both normal and water stress conditions. J Exp Bot 37:178–187
Bartlett RJ (1991) Chromium cycling in soils and water: links, gaps, and methods. Environ Health Perspect 92:17–24
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 2:248–254
Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotoxicol Environ Saf 66:204–209
Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216
Cobbett CS, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Cochram WG, Cox GM (1957) Experimental designs. Wiley, New York
Dat J, Vandanabeele 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 Sci 57:779–795
Dheri GS, Brar MS, Malhi SS (2007) Comparative phytoremediation of chromium contaminated soil by fenugreek, spinach and raya. Commun Soil Sci Pl Anal 38:1655–1672
Diwan H, Ahmad A, Iqbal M (2008) Genotypic variation in the phytoremediation potential of Indian mustard for chromium. Environ Manag 41:734–741
Diwan H, Ahmad A, Iqbal M (2010) Chromium-induced modulation in the antioxidant defense system during phenological growth stages of Indian mustard. Int J Phytol 12:142–158
Dube BK, Tewari K, Chatterjee J, Chatterjee C (2003) Excess chromium alters uptake and translocation of certain nutrients in citrullus. Chemosphere 53:1147–1153
EPA US (1984) Health assessment document for chromium. Environmental Criteria and Assessment Office, EPA 600/8-83-014F. NTIS PB 85-115905. US Environmental Protection Agency, Research Triangle Park
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25
Foyer CH, Deascouveries P, Kunert KJ (1994a) Protection against oxygen radicals: important defense mechanisms studied in transgenic plants. Plant Cell Environ 17:507–523
Foyer CH, Lelandais M, Kunert KJ (1994b) Photooxidative stress in plants. Physiol Plant 92:696–717
Freeman JI, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thalpsi nickel hyperaccumulator. Plant Cell 16:2176–2191
Ghosh M, Singh SP (2005) A comparative study of cadmium phytoextraction by accumulator and weed species. Environ Pollut 133:365–371
Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494
Grill E, Thumann J, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy metal binding peptides of plants are synthesised from glutathione by a specific gamma glutamylcysteine dipeptide transpeptidase (phytochelatin synthase). Proc Natl Acad Sci USA 86:6838–6842
Gupta YP (1983) Nutritive value of food legumes. In: Arora SK (ed) Chemistry and biochemistry of legumes. Edward Arnold, London, pp 287–328
Hajiboland R (2005) An evaluation of the efficiency of cultural plants to remove heavy metals from growing medium. Plant Soil Environ 51:156–164
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Halliwell B (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chem Phys Lipids 44:327–340
Harmens H, DenHartog PR, ten Bookum WM, Verkleij JAC (1993) Increased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to increased production of phytochelatins. Plant Physiol 103:1305–1309
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts In: Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Israr M, Sahi SV, Jain J (2006) Cadmium accumulation and antioxidative responses in the Sesbania drumondii callus. Arch Environ Contam Toxicol 50:121–127
Jiang W, Liu D, Hou W (2000) Hyperaccumulation of lead by roots, hypocotyls and shoots of Brassica juncea. Biol Plant 43:603–606
Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defense system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634
Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction—the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238
Labra M, Gianazza E, Waitt R, Eberini I, Sozzi A, Regondi S, Grassi F, Agradi E (2006) Zea mays L. protein changes in response to potassium dichromate treatments. Chemosphere 62:1234–1244
Lawn RJ, Ahn CS (1985) Mung bean (Vigna radiata (L.) Wilczek/Vigna mungo (L.) Hepper. In: Summerfield RJ, Roberts EH (eds) Grain legume crops. Collins, London, pp 584–623
Lu X, Kruatrachue M, Pokethitiyook P, Homyok K (2004) Removal of cadmium and zinc by water hyacinth, Eichhornia crassipes. Sci Asia 30:93–103
Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Ogawa K, Kanematsu S, Asada K (1997) Generation of superoxide anion and localization of Cu-Zn superoxide dismutase in the vascular tissue of spinach hypocotyls and their association with lignification. Plant Cell Physiol 38:1118–1126
Panwar BS, Ahmed KS, Mittal SB (2002) Phytoremediation of nickel contaminated soils by Brassica species. Environ Dev Sustainability 4:1–6
Pawlisz AV, Kent RA, Schneider UA, Jefferson C (1997) Canadian water quality guidelines for chromium. Environ Toxicol Water Qual 12:123–183
Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt induced oxidative stress. Environ Exp Bot 53:185–193
Raab A, Feldmann J, Meharg AA (2004) The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134:1113–1122
Rao MV (1992) Cellular detoxification mechanisms to determine age dependent injury in tropical plant exposed to SO2. J Plant Physiol 140:733–740
Rauser WE (1999) Structure and function of metal chelators produced by plants. Cell Biochem Biophys 31:19–48
Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inze D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342
Rout GR, Samantaray S, Das P (2001) Differential lead tolerance of rice and black gram genotypes in hydroponic culture. Rost Výroba (Praha) 47:541–548
Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433
Salt DE, Blaylock M, Kumar PBAN, Dushenkov V, Ensley BD, Chet I, Raskin I (1996) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474
Samantary S (2002) Biochemical responses of Cr-tolerant and Cr-sensitive mung bean cultivars grown on varying levels of chromium. Chemosphere 47:1065–1072
Sanita-di-toppi L, Fossati F, Musetti R, Mikerezi I, Favali MA (2002) Effect of hexavalent chromium on maize, tomato and cauliflower plants. J Plant Nutr 25:701–717
Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392
Schmoger ME, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–801
Shanker AK, Djanaguiraman M, Sudhagar R, Chandreshekhar CN, Pathmanabhan G (2004a) Differential antioxidative response of ascorbate glutathione pathway enzymes and metabolites to chromium speciation stress in green gram [Vigna radiata (L.). Wilczek, cv CO4] roots. Plant Sci 166:1035–1043
Shanker AK, Djanaguiraman M, Sudhagar R, Jayaram R, Pathmanabhan G (2004b) Expression of metallothionein 3 (MT3) like protein mRNA in Sorghum cultivars under chromium (VI) stress. Curr Sci 86:901–902
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753
Shanker AK, Djanaguiraman M, Venkateswarlu B (2009) Chromium interactions in plants: current status and future strategies. Metallomics 1:375–383
Sharma SS, Kaul S, Metwally A, Goyal KC, Finkemeier I, Dietz KJ (2004) Cadmium toxicity to barley (Hordeum vulgare) as affected by varying Fe nutritional status. Plant Sci 166:1287–1295
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319
Shukla OP, Rai UN, Singh NK, Dubey S, Baghel VS (2007) Isolation and characterization of chromate resistant bacteria from tannery effluent. J Environ Biol 28:399–403
Simonová E, Henselová M, Masarovičová E, Kohanová J (2007) Comparison of tolerance of Brassica juncea and Vigna radiata to cadmium. Biol Plant 51:488–492
Singh RP, Tripathi RD, Dabas S, Rizvi SMH, Ali MB, Sinha SK, Gupta DK, Mishra S, Rai UN (2003) Effect of lead on growth and nitrate assimilation of Vigna radiate (L.) Wilczek seedlings in a salt affected environment. Chemosphere 52:1245–1250
Sklar FH (1980) A preliminary comparison of the uptake of chromium-51 and zinc-65 by three species of aquatic plants from Louisiana: Spirodela punctata, Eacopa caroliniana, Elodea Canadensis. Proc La Acad Sci 43:46–51
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58
Srivastava S, Tripathi RD, Dwivedi UN (2004) Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa-an angiospermic parasite. J Plant Physiol 161:665–674
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (L.f.) Royle. Environ Sci Technol 41:2930–2936
Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206
Van den Broeck K, Vandecasteele C, Geuns JMC (1998) Speciation by liquid chromatography-inductively coupled plasma-mass spectrometry of arsenic in mung bean seedlings used as a bio-indicator for the arsenic contamination. Anal Chim Acta 361:101–111
Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals—phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276:20817–20820
Vecchia FD, Rocca NL, Moro I, De Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages suffered by submerged leaves of Elodea canadensis exposed to cadmium. Plant Sci 168:329–338
WHO (1988) Chromium. Environmental health criteria. World Health Organization, Geneva
Witmer CM, Harris R, Shupack SI (1991) Oral bioavailability of chromium from a specific site. Environ Health Perspect 92:105–110
Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa T, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidise is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J 32:915–925
Yamaguchi K, Mori H, Nishimura M (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36:1157–1162
Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179:21–30
Zhang H, Jiang Y, He Z, Ma M (2005) Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol 162:977–984
Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50
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Diwan, H., Khan, I., Ahmad, A. et al. Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatments. Plant Growth Regul 61, 97–107 (2010). https://doi.org/10.1007/s10725-010-9454-0
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DOI: https://doi.org/10.1007/s10725-010-9454-0