Abstract
Wheat (Triticum aestivum L. cv. ‘Zyta’) seedlings were treated with 10, 100 and 200 μM Ni. Tissue Ni accumulation, length, relative water content (RWC), proline and H2O2 concentrations as well as the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (POD) and glutathione S-transferase (GST) were studied in the shoots and roots after 6 days of Ni exposure. Treatment with Ni, except for its lowest concentration, resulted in a significant reduction in wheat growth. In comparison to the shoots, the roots showed greater inhibition of elongation, which corresponded with higher accumulation of Ni in these organs. Both shoots and roots responded to Ni application with a decrease in RWC and enhancement in proline concentration. Greater dehydration of the shoot tissue was accompanied by more intense accumulation of proline. Treatment of the wheat seedlings with the highest concentration of Ni led to about 60% increase in H2O2 concentration in both studied organs. Apart from CAT, constitutive activities of antioxidative enzymes were much higher in the roots than in the shoots. Exposure of the seedlings to Ni resulted in SOD activity decline, which was more marked in the roots. While the shoots showed a substantial decrease (up to 30%) in CAT activity, in the roots the activity of this enzyme remained unchanged. After Ni application APX, POD and GST activities increased several-fold in the shoots, whereas in the roots they were not significantly altered. The results suggest that differential antioxidative responses of the shoots and roots of wheat seedlings to Ni stress might be related to diverse constitutive levels of antioxidant enzyme activities in both organs.
Similar content being viewed by others
Abbreviations
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- CDNB:
-
1-Chloro-2,4-dinitrobenzene
- GSH:
-
Reduced glutathione
- GST:
-
Glutathione S-transferase
- MBTH:
-
3-Methyl-2-benzothiazolinone hydrazone
- NBT:
-
Nitro blue tetrazolium
- POD:
-
Guaiacol peroxidase
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SOD:
-
Superoxide dismutase
References
Atta-Aly MA (1999) Effect of nickel addition on the yield and quality of parsley leaves. Sci Hort 82:9–24
Baccouch S, Chaoui A, El Ferjani E (1998) Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots. Plant Physiol Biochem 36:689–694
Baccouch S, Chaoui A, El Ferjani E (2001) Nickel toxicity induces oxidative damage in Zea mays roots. J Plant Nutr 24:1085–1097
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol 156:205–215
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Capaldi DJ, Taylor KE (1983) A new peroxidase color reaction: oxidative coupling of 3-methyl-2-benzothiazolinone hydrazone (MBTH) with its formaldehyde azine. Application to glucose and choline oxidases. Anal Biochem 129:329–336
Chen C-T, Chen T-H, Lo K-F, Chiu C-Y (2004) Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci 166:103–111
Chen L-M, Lin CC, Kao CH (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
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Edwards R, Dixon DD (2004) Metabolism of natural and xenobiotic substrates by the plant glutathione S-transferase superfamily. In: Sandermann H (eds) Molecular ecotoxicology of plants. Ecological studies, vol 170, Springer-Verlag Berlin, Heidelberg, pp 17–50
Eskew DL, Welch RM, Cary EE (1983) Nickel: an essential micronutrient for legumes and possibly all higher plants. Science 222:621–623
Farago ME, Mullen WA (1979) Plants which accumulate metals. Part IV. A possible copper-proline complex from the roots of Armeria maritima. Inorg Chim Acta 32:93–94
Gabbrielli R, Pandolfini T, Espen L, Palandri MR (1999) Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings exposed to Ni2+ toxicity. J Plant Physiol 155:639–645
Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–339
Gaspar T, Penel C, Hagege D, Greppin H (1991) Peroxidases in plant growth, differentiation, and development processes. In: Łobarzewski J, Greppin H, Penel C, Gaspar T (eds) Biochemical, molecular and physiological aspects of plant peroxidases. University M. Curie-Skłodowska, Lublin, pp. 249–280
Gonnelli C, Galardi F, Gabbrielli R (2001) Nickel and copper tolerance and toxicity in three Tuscan populations of Silene paradoxa. Physiol Plant 113:507–514
Gratão PL, Polle A, Lea PJ, Azevedo A (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494
Haag-Kerwer A, Schafer HJ, Heiss S, Walter C, Rausch T (1999) Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. J Exp Bot 50:1827–1835
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 246:7130–7139
Hao F, Wang X, Chen J (2006) Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158
Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102
Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468
Hodgson MA, Fridovich I (1975) The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: inactivation of the enzyme. Biochemistry 40:5294–5303
Hsiao TC (1973) Plant responses to water stress. Ann Rev Plant Physiol 24:519–570
Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438
Leonard SS, Harris GK, Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Rad Biol Med 37:1921–1942
Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128
Maehly AC, Chance B (1954) The assay of catalases and peroxidases. In: Glick D (ed) Methods of biochemical analysis, vol 1, Interscience Publishers Inc., New York, pp 357–425
Maheshwari R, Dubey RS (2007) Nickel toxicity inhibits ribonuclease and protease activities in rice seedlings: protective effects of proline. Plant Growth Regul 51:231–243
Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Ann Rev Plant Physiol Plant Mol Biol 47:127–158
Marrs KA, Walbot V (1997) Expression and RNA splicing of the maize glutathione S-transferase Bronze2 gene is regulated by cadmium and other stresses. Plant Physiol 113:93–102
Matysik J, Alia, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532
Minami M, Yoshikawa H (1979) A simplified assay method of superoxide dismutase activity for clinical use. Clin Chim Acta 92:337–342
Mishra S, Agrawal SB (2006) Interactive effects between supplemental ultraviolet-B radiation and heavy metals on the growth and biochemical characteristics of Spinacia oleracea L. Braz J Plant Physiol 18:307–314
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nepovím A, Podlipná R, Soudek P, Schröder P, Vaněk T (2004) Effects of heavy metals and nitroaromatic compounds on horseradish glutathione S-transferase and peroxidase. Chemosphere 57:1007–1015
Pandey N, Sharma CP (2002) Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci 163:753–758
Pandolfini T, Gabbrielli R, Ciscato M (1996) Nickel toxicity in two durum wheat cultivars differing in drought sensitivity. J Plant Nutr 19:1611–1627
Parida BK, Chhibba IM, Nayyar VK (2003) Influence of nickel-contaminated soils on fenugreek (Trigonella corniculata L.) growth and mineral composition. Sci Hort 98:113–119
Prasad SM, Dwivedi R, Zeeshan M (2005) Growth, photosynthetic electron transport, and antioxidant responses of young soybean seedlings to simultaneous exposure of nickel and UV-B stress. Photosynthetica 43:177–185
Samarakoon AB, Rauser WE (1979) Carbohydrate levels and photoassimilate export from leaves of Phaseolus vulgaris exposed to excess cobalt, nickel, and zinc. Plant Physiol 63:1165–1169
Santoro A, Lioi MB, Monfregola J, Salzano S, Barbieri R, Ursini MV (2005) L-Carnitine protects mammalian cells from chromosome aberrations but not from inhibition of cell proliferation induced by hydrogen peroxide. Mutation Res 587:16–25
Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277
Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847
Smart RE, Bingham GE (1974) Rapid estimation of relative water content. Plant Physiol 53:258–260
Tripathy BC, Bhatia B, Mohanty P (1981) Inactivation of chloroplast photosynthetic electron-transport activity by Ni2+. Biochim Biophys Acta 638:217–224
Acknowledgements
This work was partly supported by University of Łódź Grant No 505/402. The authors are grateful to Dr. Z. Nita (Hodowla Roślin Strzelce Sp. z o.o., Poland) for supplying the wheat seeds.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gajewska, E., Skłodowska, M. Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54, 179–188 (2008). https://doi.org/10.1007/s10725-007-9240-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-007-9240-9