Antioxidant response of Nicotiana tabacum cv. Bright Yellow 2 cells to cadmium and nickel stress
Tóm tắt
Plant cell cultures are a suitable model system for investigation of the physiological mechanisms of tolerance to environmental stress. We have determined the effects of Cd (0.1 and 0.2 mM CdCl2) and Ni (0.075 and 0.75 mM NiCl2) on Nicotiana tabacum L. cv. Bright Yellow (TBY-2) cell suspension cultures over a 72-h period. Inhibition of growth, loss of cell viability and lipid peroxidation occurred, in general, only when the TBY-2 cells were grown at 0.2 mM CdCl2 and at 0.75 mM NiCl2. At 0.1 mM CdCl2, a significant increase in growth was determined at the end of the experiment. Increases in the activities of all of the four enzymatic antioxidant defence systems tested, were induced by the two concentrations of Cd and Ni, but at different times during the period of metal exposure. Overall, the cellular antioxidant responses to Cd and Ni were similar and were apparently sufficient to avoid oxidative stress at the lower concentrations of Cd and Ni. The activities of glutathione reductase and glutathione S-transferase increased early but transiently, whereas the activities of catalase and guaiacol peroxidase increased in the latter half of the experimental period. Therefore it is likely that the metabolism of reduced glutathione was enhanced during the initial onset of the stress, while catalase and guaiacol-type peroxidase appeared to play a more important role in the antioxidant response once the stress became severe.
Tài liệu tham khảo
Asada K (1999) The water cycle in chloroplast: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292
Bai C, Reilly CC, Bruce W (2006) Wood nickel deficiency disrupts metabolism of ureides, amino acids, and organic acids of young pecan foliage. Plant Physiol 140:433–443
Basantani M, Srivastava A (2007) Plant glutathione transferases—a decade falls short. Can J Bot 85:443–456
Ben Ammar W, Nouairi I, Zarrouk M, Jemal F (2007) Cadmium stress induces changes in the lipid composition and biosynthesis in tomato (Lycopersicon esculentum Mill.) leaves. Plant Growth Regul 53:75–85
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34
Berton RS, Pires AMM, de Andrade SAL, de Abreu CA, Ambrosano EJ, da Silveira APD (2006) Nickel toxicity in common bean plants and effects on soil microbiota. Pesqui Agropecu Bras 41:1305–1312
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 quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–259
Calabrese EJ, Baldwin LA (2003) Inorganics and hormesis. Crit Rev Toxicol 33:215–304
Chiancone B, Tassoni A, Bagni N, Germana MA (2006) Effect of polyamines on in vitro anther culture of Citrus clementina Hort. Ex. Tan. Plant Cell Tissue Organ Cult 87:145–153
Dalla Vecchia F, La Rocca N, 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
Dewir YH, Chakrabarty D, Ali MB, Hahn EJ, Paek KY (2006) Lipid peroxidation and antioxidant enzyme activities of Euphorbia milii hyperhydric shoots. Environ Exp Bot 58:93–99
Durcekova K, Huttova J, Mistrik I, Olle M, Tamas L (2007) Cadmium induces premature xylogenesis in barley roots. Plant Soil 290:61–68
Fojta M, Fojtova M, Havran L, Pivonkova H, Dorcak V, Sestakova I (2006) Electrochemical monitoring of phytochelatin accumulation in Nicotiana tabacum cells exposed to sub-cytotoxic and cytotoxic levels of cadmium. Anal Chim Acta 558:171–178
Fornazier RF, Ferreira RR, Pereira GJG, Molina SMG, Smith RJ, Lea PJ, Azevedo RA (2002) Cadmium stress in sugar cane callus cultures: effect on antioxidant enzymes. Plant Cell Tissue Organ Cult 75:125–131
Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Gajewska E, Sklodowska M (2007a) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36
Gajewska E, Sklodowska M (2007b) Relations between tocopherol, chlorophyll and lipid peroxides contents in shoots of Ni-treated wheat. J Plant Physiol 164:364–366
Gajewska E, Sklodowska M, Slaba M, Mazur J (2006a) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659
Gajewska E, Slaba M, Andrzejewska R, Sklodowska M (2006b) Nickel-induced inhibition of wheat root growth is related to H2O2 production, but not to lipid peroxidation. Plant Growth Regul 49:95–103
Garcia JS, Gratão PL, Azevedo RA, Arruda MAZ (2006) Metal contamination effects on sunflower (Helianthus annuus L.) growth and protein expression in leaves during development. J Agric Food Chem 54:8623–8630
Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969
Ghanati F, Ishka MR (2006) Improvement of antioxidant system and decrease of lignin by nickel treatment in tea plant. J Plant Nutr 29:1649–1661
Gomes-Junior RA, Gratão PL, Gaziola SA, Mazzafera P, Lea PJ, Azevedo RA (2007) Selenium-induced oxidative stress in coffee cell suspension cultures. Funct Plant Biol 34:449–456
Gomes-Junior RA, Moldes CA, Delite FS, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006a) Nickel elicits a fast antioxidant response in Coffea arabica cells. Plant Physiol Biochem 44:420–429
Gomes-Junior RA, Moldes CA, Delite FS, Pompeu GB, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006b) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65:1330–1337
Gratão 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
Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45
Groppa MD, Ianuzzo MP, Tomaro ML, Benavides MP (2007) Polyamine metabolism in sunflower plants under long-term cadmium or copper stress. Amino Acids 32:265–275
Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405
Hancock J, Desikan R, Harrison J, Bright J, Hooley R, Neill S (2006) Doing the unexpected: proteins involved in hydrogen peroxide perception. J Exp Bot 57:1711–1718
Hassan IA (2006) Physiological and biochemical response of potato (Solanum tuberosum L. cv. Kara) to O-3 and antioxidant chemicals: possible roles of antioxidant enzymes. Ann Appl Biol 148:197–206
Hsu YT, Kao CH (2007) Cadmium-induced oxidative damage in rice leaves is reduced by polyamines. Plant Soil 291:27–37
Jones MA, Raymond MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J Exp Bot 58:1261–1270
Kevresan S, Petrovic N, Popovic M, Kandrac J (2001) Nitrogen and protein metabolism in young pea plants as affected by different concentrations of nickel, cadmium, lead, and molybdenum. J Plant Physiol 24:1633–1644
Kim YH, Kim Y, Cho E, Kwak S, Know S, Bae J, Lee B, Men B, Huh GH (2004) Alterations in intracellular and extracellular activities of antioxidant enzymes during suspension culture of sweet potato. Phytochemistry 65:2471–2476
Kirda C, Topcu S, Cetin M, Dasgan HY, Kaman H, Topaloglu F, Derici MR, Ekici B (2007) Prospects of partial root zone irrigation for increasing irrigation water use efficiency of major crops in the Mediterranean region. Ann Appl Biol 150:281–291
Kukkola E, Rautio P, Huttunen S (2000) Stress indications in copper and nickel-exposed Scots pine seedlings. Environ Exp Bot 43:197–210
Lea PJ, Azevedo RA (2007) Nitrogen use efficiency. II. Amino acid metabolism. Ann Appl Biol 151:269–275
Li J, Jin H (2007) Regulation of brassinosteroid signalling. Trends Plant Sci 12:37–41
Liu CP, Shen ZG, Li XD (2007) Accumulation and detoxification of cadmium in Brassica pekinensis and B. chinensis. Biol Plant 51:116–120
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
Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37
Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610
Moldes CA, Medici LO, Abrahão OS, Tsai SM, Azevedo RA (2008) Biochemical responses of glyphosate resistant and susceptible soybean plants exposed to glyphosate. Acta Physiol Plant. doi:10.1007/s11738-008-0144-8
Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481
Nagata T, Nemotot Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “HeLa” cell in the cell biology of higher plants. Int Rev Cytol 132:1–30
Nakazawa R, Kameda Y, Ito T, Ogita Y, Michihata R, Takenaga H (2004) Selection and characterization of nickel-tolerant tobacco cells. Biol Plant 48:497–502
Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134
Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2007) Cadmium induced oxidative stress in soybean plants also by the accumulation of δ-aminolevulinic acid. Biometals 20:841–851
Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301
Passardi F, Theiler G, Zamocky M, Cosio C, Rouhier N, Teixera F, Margis-Pinheiro M, Ioannidis V, Penel C, Falquet Land Dunand C (2007) PeroxiBase: the peroxidase database. Phytochemistry 68:1605–1611
Pitzschke A, Fornazi C, Hirt H (2006) Reactive oxygen species signalling in plants. Antioxid Redox Signal 8:1757–1764
Rao KVM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128
Reumann S, Weber APM (2006) Plant peroxisomes respire in the light: some gaps of the photorespiratory C-2 cycle have become filled—others remain. Biochim Biophys Acta Mol Cell Res 1763:1496–1510
Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Rio LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544
Rooney CP, Zhao FJ, McGrath SP (2007) Phytotoxicity of nickel in a range of European soils: influence of soil properties, Ni solubility and speciation. Environ Pollut 145:596–605
Saito A, Higuchi K, Hirai M, Nakane R, Yoshiba M, Tadano T (2005) Selection and characterization of a nickel-tolerant cell line from tobacco (Nicotiana tabacum cv. bright yellow-2) suspension culture. Physiol Plant 125:441–453
Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177:67–80
Santa-Catarina C, Silveira V, Scherer GFE, Floh EIS (2007) Polyamine and nitric oxide levels relate with morphogenetic evolution in somatic embryopgenesis of Ocotea catharinensis. Plant Cell Tissue Organ Cult 90:93–101
Scebba F, Arduini I, Ercoli L, Sebastiani L (2006) Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol Plant 50:688–692
Skorzynska- Polit E, Krupa Z (2006) Lipid peroxidation in cadmium-treated Phaseolus coccineus plant. Arch Environ Contam Toxicol 50:482–487
Steiner N, Santa-Catarina C, Silveira V, Floh EIS, Guerra MP (2007) Polyamine effects on growth and endogenous hormones levels in Araucaria angustifolia embryogenic cultures. Plant Cell Tissue Organ Cult 89:55–62
Symons GM, Ross JJ, Jager CE, Reid JB (2008) Brassinosteroid transport. J Exp Bot 59:17–24
Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sang.) cell suspension cultures under cadmium and zinc stress. Plant Cell Tissue Organ Cult 88:201–216
Urs RR, Roberts PD, Schultz DC (2006) Localisation of hydrogen peroxide and peroxidase in gametophytes of Ceratopteris richardii (C-fern) grown in the presence of pathogenic fungi in a gnotobiotic system. Ann Appl Biol 149:327–336
Vitorello VA, Haug A (1996) Short-term aluminum uptake by tobacco cells: growth dependence and evidence for internalization in a discrete peripheral region. Physiol Plant 97:536–544
Vitória AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57:701–710
Wahid A, Ghani A (2008) Varietal differences in mung bean (Vigna radiata) for growth, yield, toxicity symptoms and cadmium accumulation. Ann Appl Biol 152:59–69
Yakimova ET, Kapchina-Toteva VM, Laarhoven LJ, Harren FM, Woltering EJ (2006) Involvement of ethylene and lipid signaling in cadmium-induced programmed cell death in tomato suspension cells. Plant Physiol 44:581–589
Yannarelli GG, Fernandez-Alvarez AJ, Santa-Cruz DM, Tomaro ML (2007) Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. Phytochemistry 68:505–512