Response to oxidative stress induced by cadmium and copper in tobacco plants (Nicotiana tabacum) engineered with the trehalose-6-phosphate synthase gene (AtTPS1)

• Autorzy: Martins L.L. , Mourato M. P. , Baptista S. , Reis R. , Carvalheiro F. , Almeida A. M. , Fevereiro P. , Cuypers A.
• Języki publikacji: EN

Abstrakty

EN

The response of tobacco plants genetically engineered with the AtTPS1 gene to stress induced by excess Cu and Cd was evaluated in hydroponic solution (100 and 400 μM Cu and 50 and 200 μM Cd) after a 48 h exposure. Two transgenic lines, transformed with the AtTPS1 (trehalose-6-phosphate synthase) gene from Arabidopsis, with different levels of trehalose-6-phosphate synthase expression (B5H, higher and B1F, lower), and a wild type (WT) were investigated. Protein content, antioxidative enzymes (CAT, POD, SOD, and APX), glucose, fructose, lipid peroxidation, hydrogen peroxide and Cd and Cu contents were determined in leaves. The two transgenic lines were differently influenced by Cd and Cu exposure as they induced a different antioxidant enzymatic defense response. B1F and B5H plants showed a better acclimation to Cd and excess Cu compared to WT. Furthermore B1F was more tolerant than B5H to Cd and excess Cu. B1F accumulated less Cd and Cu in leaves, probably due to a more efficient exclusion mechanism. Catalase was shown to be the most important enzyme in the antioxidative system of these plants.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2014
• Tom: 36
• Numer: 03
• Opis fizyczny: p.755-765,fig.,ref.

Twórcy

autor

Martins L.L.

• UIQA, Instituto Superior de Agronomia, Universidade Tecnica de Lisboa, Lisbon, Portugal

autor

Mourato M. P.

• UIQA, Instituto Superior de Agronomia, Universidade Tecnica de Lisboa, Lisbon, Portugal

autor

Baptista S.

• UIQA, Instituto Superior de Agronomia, Universidade Tecnica de Lisboa, Lisbon, Portugal

autor

Reis R.

• UIQA, Instituto Superior de Agronomia, Universidade Tecnica de Lisboa, Lisbon, Portugal

autor

Carvalheiro F.

• Unidade de Bioenergia, LNEG-Laboratório Nacional de Energia e Geologia, Lisbon, Portugal

autor

Almeida A. M.

• IICT-Instituto de Investigação Científica Tropical, Lisbon, Portugal
• Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal

autor

Fevereiro P.

• Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal
• Departamento de Biologia Vegetal, Faculdade de Ciencias da Universidade de Lisboa, Lisbon, Portugal

autor

Cuypers A.

• Environmental Biology, Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium

Bibliografia

• Aebi HE (1983) Catalase. In: Bergmeyer US (ed) Methods in enzymatic analysis, vol III. Oxireductases, transferases. Verlag Chemie, Weinheim, pp 273–277
• Ali MB, Yu KW, Hahn EJ, Paek KY (2005) Differential responses of anti-oxidants enzymes, lipoxygenase activity, ascorbate content and the production of saponins in tissue cultured root of mountain Panax ginseng C.A. Mayer and Panax quinquefolium L. in bioreactor subjected to methyl jasmonate stress. Plant Sci 169(1):83–92
• Almeida AM, Villalobos E, Araújo SS, Leyman BVDP, Alfaro-Cardoso L, Fevereiro PS, Torné JM, Santos DM (2005) Transformation of tobacco with an Arabidopsis thaliana gene involved in trehalose biosynthesis increases tolerance to several abiotic stresses. Euphytica 146:165–176
• Almeida AM, Cardoso LA, Santos DM, Torne JM, Fevereiro PS (2007a) Trehalose and its applications in plant biotechnology. Vitro Cell Dev Biol Plant 43(3):167–177
• Almeida AM, Santos M, Villalobos E, Araujo SS, van Dijck P, Leyman B, Cardoso LA, Santos D, Fevereiro PS, Torne JM (2007b) Immunogold localization of trehalose-6-phosphate synthase in leaf segments of wild-type and transgenic tobacco plants expressing the AtTPS1 gene from Arabidopsis thaliana. Protoplasma 230(1–2):41–49
• Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
• Bailey NJC, Oven M, Holmes E, Nicholson JK, Zenk MH (2003) Metabolomic analysis of the consequences of cadmium exposure in Silene cucubalus cell cultures via H-1 NMR spectroscopy and chemometrics. Phytochemistry 62(6):851–858
• Benaroudj N, Lee DH, Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276(26):24261–24267
• Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein–dye binding. Anal Biochem 72(1–2):248–254
• Burzyński M, Żurek A (2007) Effects of copper and cadmium on photosynthesis in cucumber cotyledons. Photosynthetica 45(2):239–244
• Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88(11):1707–1719
• Cortina C, Culiáñez-Macià FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169(1):75–82
• Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57(3):449–459
• Cuypers A, Vangronsveld J, Clijsters H (2002) Peroxidases in roots and primary leaves of Phaseolus vulgaris copper and zinc phytotoxicity: a comparison. J Plant Physiol 159(8):869–876
• Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair A, Munters E, Artois T, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23(5):927–940
• Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Sanden SV, Belleghem FV, Guisez Y, Colpaert J, Vangronsveld J (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168(4):309–316
• De Vos CHR, Schat H, Dewaal MAM, Vooijs R, Ernst WHO (1991) Increased resistance to copper-induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiol Plant 82(4):523–528
• Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53(3):247–257
• Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266
• Djebali W, Gallusci P, Polge C, Boulila L, Galtier N, Raymond P, Chaibi W, Brouquisse R (2008) Modifications in endopeptidase and 20S proteasome expression and activities in cadmium treated tomato (Solanum lycopersicum L.) plants. Planta 227(3):625–639
• Drazkiewicz M, Skorzynska-Polit E, Krupa Z (2003) Response of the ascorbate–glutathione cycle to excess copper in Arabidopsis thaliana (L.). Plant Sci 164(2):195–202
• Fernandes JC, Henriques FS (1991) Biochemical, physiological, and structural effects of excess copper in plants. Bot Rev 57(3):246–273
• Gajewska E, Sklodowska M, Slaba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50(4):653–659
• Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930
• Gorinova N, Nedkovska M, Todorovska E, Simova-Stoilova L, Stoyanova Z, Georgieva K, Demirevska-Kepova K, Atanassov A, Herzig R (2007) Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity. Environ Pollut 145(1):161–170
• 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
• Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11
• He ZLL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19(2–3):125–140
• Hottiger T, Boller T, Wiemken A (1987) Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett 220(1):113–115
• Khatun S, Ali MB, Hahn E-J, Paek K-Y (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro grown plants. Environ Exp Bot 64(3):279–285
• Kovácik J, Backor M (2008) Oxidative status of Matricaria chamomilla plants related to cadmium and copper uptake. Ecotoxicology 17(6):471–479
• Luo Y, Li W-M, Wang W (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot 63(1–3):378–384
• Maksymiec W (1997) Effect of copper on cellular processes in higher plants. Photosynthetica 34(3):321–342
• Martins LL, Mourato MP (2006) Effect of excess copper on tomato plants: growth parameters, enzyme activities, chlorophyll and mineral content. J Plant Nutr 29:2179–2198
• Mazhoudi S, Chaoui A, Ghorbal MH, El Ferjani E (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum, Mill). Plant Sci 127(2):129–137
• Mithofer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5
• Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410
• Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481
• Mourato MP, Martins LL, Campos-Andrada MP (2009) Physiological responses of Lupinus luteus to different copper concentrations. Biol Plant 53(1):105–111
• Nery DDCM, da Silva CG, Mariani D, Fernandes PN, Pereira MD, Panek AD, Eleutherio ECA (2008) The role of trehalose and its transporter in protection against reactive oxygen species. Biochim Biophys Acta 1780(12):1408–1411
• Oku K, Watanabe H, Kubota M, Fukuda S, Kurimoto M, Tsujisaka Y, Komori M, Inoue Y, Sakurai M (2003) NMR and quantum chemical study on the OH…Pi and CH…O Interactions between trehalose and unsaturated fatty acids: implication for the mechanism of antioxidant function of trehalose. J Am Chem Soc 125(42):12739–12748
• Rubio MC, Gonzalez EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115(4):531–540
• Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
• Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365
• 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
• Sharma SS, Dietz K-J (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14(1):43–50
• Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167(3):541–550
• Singh N, Ma LQ, Srivastava M, Rathinasabapathi B (2006) Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L and Pteris ensiformis L. Plant Sci 170(2):274–282
• Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A, Vangronsveld J (2005) Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43(5):437–444
• Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden S, Vangronsveld J, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63(1–3):1–8
• Valluru R, Van den Ende W (2008) Plant fructans in stress environments: emerging concepts and future prospects. J Exp Bot 59(11):2905–2916
• Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60(1):9–18
• Vangronsveld J, Clijsters H (1994) Toxic effects of metals. In: Farago ME (ed) Plants and the chemical elements. Biochemistry, uptake, tolerance and toxicity. VCH Verlagsgesellschaft, Weinheim, pp 149–177
• Wingler A (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60(5):437–440
• Yannarelli GG, Gallego SM, Tomaro ML (2006) Effect of UV-B radiation on the activity and isoforms of enzymes with peroxidase activity in sunflower cotyledons. Environ Exp Bot 56(2):174–181
• Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36(5):409–430

Identyfikatory

DOI

10.1007/s11738-013-1453-0