Abstract
Metabolic adaptations to heavy metal toxicity in plants are thought to be related with developmental growth stage and the type of metal by which plant is affected. In the present study, changes in ionically bound CWP, soluble peroxidase activity, H2O2 level and Malonaldehyde content in roots of cadmium and copper stressed seedlings and cadmium stressed 3–4 leaf stage plants of Brassica juncea were investigated. Cadmium inhibits root growth and reduces fresh biomass. The reduction in root growth and fresh biomass is correlated with increased lipid peroxidation and reduced tolerance. Treatment with cadmium resulted in an increase in ionically bound CWP activity in roots of seedlings but no significant change in its activity was found in roots of 3–4 leaf stage plants. Increased level of H2O2 in roots of cadmium and copper treated seedlings, show a direct correlation with increased activity of ionically bound CWP. H2O2 level in 3–4 leaf stage plant roots was found to be very low. Soluble peroxidase activity decreased in cadmium (50 and 100 μM) treated seedlings but it was ineffective to cause any change in its activity in 3–4 leaf stage plants. Copper treated seedlings showed an increase in ionically bound CWP activity, H2O2 level and MDA content. Ascorbic acid (50 mM) pretreated seedlings shows significant decrease in ionically bound CWP activity when exposed to 50 μM cadmium. Hence, it is concluded that inhibition of root growth in Brassica juncea seedlings by cadmium, is associated with CWP catalyzed H2O2 dependent reactions which are involved in metabolic adaptations to heavy-metal stress.
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Abbreviations
- CWP:
-
Cell wall peroxidase
- MDA:
-
Malonaldehyde
- ROS:
-
Reactive oxygen species
- H2O2 :
-
Hydrogen peroxide
- TMB:
-
3, 3′, 5, 5′-tetramethyl benzidine
- OFW:
-
Original fresh weight
- FW:
-
Fresh weight
References
Andrews J, Malone M, Thompson DS, Ho LC, Burton KS (2000) Peroxidase isozyme patterns in the skin of maturing tomato fruit. Plant Cell Environ 23:415–422
Bacon MA, Thompson DS, Davies WJ (1997) Can cell wall peroxidase activity explains the leaf growth response of Lolium temulentum L during drought? J Exp Bot 48:2075–2085
Barcelo AR, Munoz R, Sabater F (1987) Lupin peroxidases I. Isolation and characterization of cell wall bound isoperoxidases activity. Physiol Plant 71:448–454
Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plant 19:47–64
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Bolwell GP, Davis DR, Gerrish C, Auh CK, Murphy TM (1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol 116:1379–1385
Bos ES, Van der Doelen AA, Van Rooy N, Schuurs AHWM (1981) Tetra methylbenzidine as an ames-test negative chromogen for horse-radish peroxidase enzyme immunoassay. J Immunoassay 2:187–204
Briat JF (2002) Metal ion-activated oxidative stress and its control. In: Inze D, Montagu MV (eds) Oxidative stress in plants. Taylor and Francis, New York, pp 171–189
Carpita NC, Gilbeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the wall during growth. Plant J 3:1–30
Chaoui A, El Ferjani E (2005) Effects of cadmium and copper on antioxidant capacities, lignifiaction and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 328:23–31
Chaoui A, Mazhoudi S, Ghorbal MH, El Ferjani E (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127:139–147
Chazen O, Neumann PM (1994) Hydraulic signals from roots and rapid cell-wall hardening in growing maize (Zea mays L.) leaves are primary responses to polyethylene glycol-induced water deficits. Plant Physiol 104:1385–1392
Chen EL, Chen YA, Chen LM, Liu ZH (2002) Effect of copper on peroxidase activity and lignin content in Raphanus sativus. Plant Physiol Biochem 40:439–444
Chen L-M, Lin C-C, Kao C-H (2000) Copper toxicity in rice seedlings: changes in antioxidative enzyme activities, H2O2 level and cell wall peroxidase activity in roots. Bot Bull Acad Sin 41:99–103
Chen SL, Kao CH (1995) Cd induced changes in proline level and peroxidase activity in roots of rice seedlings. Plant Growth Regul 17:67–71
Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793
Cordoba-Pedregrosa MD, Gonzalez-reyes JA, Canadillas MD, Navas P, Cordoba F (1996) Role of apoplastic and cell awll peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol 112:1119–1125
Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171–201
De Cnodder T, Vissenberg K, Van Der Straeten D, Verbelen JP (2005) Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane–1-carboxylic acid: a matter of apoplastic reaction. New Phytol 168:541–550
De Vos CHR, Schat H, Vooijs R, Ernst WHO (1989) Copper-induced damage to the permeability barrier in roots of silene cuiubalus. J Plant Physiol 135:164–179
Dietz KJ, Baier M, Kramer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. Springer, Berlin, Heidelberg New York, pp 73–97
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109
Drazkiewicz M, Skorzynska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. Biometals 17:379–387
Foreman J, Demidchik V, Bothwell JH (2003) Reactive oxygen species produced by NADPH oxidase regulates plant cell growth. Nature 27:442–446
Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Fry SC (1986) Cross-linking of matrix polymers in the growing cells of angiosperms. Annu Rev Plant Physiol 37:165–186
Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159
Goldberg R, Liberman M, Mathieu C, Pierron M, Catesson AM (1987) Development of isoperoxidases along the mung bean hypocotyl: possible involvement in the cell wall stiffening process. J Exp Bot 38:1378–1390
Guenni O, Douglas M, Baruch Z (2002) Responses to drought of five Brachiaria species. I. Biomass production, leaf growth, root distribution, water use and forage quality. Plant Soil 243:229–241
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Halliwell B (1981) Toxic effects of oxygen on plant tissues. Chloroplast metabolism: the structure and function of chloroplasts in green leaf cells. Clarenden Press, Oxford, pp 179–205
Iiyama K, Lam TBT, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104:315–320
Jouili H, El Ferjani E (2003) Changes in antioxidant and lignifying enzyme activities in sunflower roots (Helianthus annuus L.) stressed with copper excess. C R Biol 326:639–644
Katerji N, van Hoorn JW, Hamdy A, Mastrorilli M, Mou Karzel E (1997) Osmotic adjustment of sugar beets in response to soil salinity and its influence on stomatal conductance, growth and yields. Agric Water Manag 34:57–69
Kwon TW, Menzel DB, Olcott HS (1965) Reactivity of malondialdehyde with food constituents. J Food Sci 30:808–813
Lee R-B, Kim K-Y, Jung W-J, Avice J-C, Ourry A, Kim T-H (2007) Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.). J Exp Bot 58:1271–1279
Lee T-M, Lin Y-H (1995) Changes in soluble and cell wall bound peroxidase activities with growth in anoxia- treated rice (Oryza sativa L.) coleoptiles and roots. Plant Sci 106:1–7
Leon AM, Palma JM, Corpas FJ, Gomez M, Romero-Puertas MC, Chatterjee D, Mateos RM, del Rio LA, Sandalio LM (2002) Antioxidative enzymes in cultivars of pepper plants with different sensitivity of cadmium. Plant Physiol Biochem 40:813–820
Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Ann Rev Plant Physiol Plant Mol Biol 41:455–496
Lin C-C, Kao H-C (1999) NaCl induced changes in ionically bound peroxidase activity in roots of rice seedlings. Plant Soil 216:147–153
Lin C-C, Kao H-C (2001) Cell wall peroxidase activity, hydrogen peroxide level and NaCl- inhibited root growth of rice seedlings. Plant Soil 230:135–143
Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667
Lowry OH, Rosenberg NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279
Polle A, Otter T, Seifert F (1994) Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol 106:53–60
Raeymaekers T, Potters G, Asard H, Guisez Y, Horemans N (2003) Copper-mediated oxidative burst in Nicotiana tabacum L. cv. Bright Yellow 2 cell suspension cultures. Protoplasma 221:93–100
Rama Devi S, Prasad MNV (1998) Copper toxicity in Ceratophyllum demersum L. (Coontail), a free floating macrophyte: response of antioxidant enzyme and antioxidant. Plant Sci 138:157–165
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658
Schutzendubel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content and differentiation in scots pine roots. Plant Physiol 127:887–898
Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol Med 18:321–336
Thompson DS, Davies WJ, Ho LC (1998) Regulation of tomato fruit growth by epidermal cell wall enzymes. Plant Cell Environ 21:589–599
Acknowledgments
G. S. Shekhawat is thankful to Professor Aditya Shastri, Vice chancellor, Banasthali University, Rajasthan, India for kind cooperation.
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Verma, K., Shekhawat, G.S., Sharma, A. et al. Cadmium induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3–4 leaf stage plants of Brassica juncea (L.) czern. Plant Cell Rep 27, 1261–1269 (2008). https://doi.org/10.1007/s00299-008-0552-7
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DOI: https://doi.org/10.1007/s00299-008-0552-7