Abstract
Perennial ryegrass (Lolium perenne L.), widely used in temperate climates, is one of turf grasses that enrich cadmium (Cd). The objective of this study was to explore the physiological responses and candidate gene expression in perennial ryegrass to Cd stress. Grasses were subjected to three levels of 0, 0.2, and 0.5 mM Cd for 7 days in the greenhouse. The results indicated that soluble protein content was lower in the Cd-treated perennial ryegrass compared to untreated plants. The Cd-treated perennial ryegrass exhibited a greater level of malondialdehyde and activity of the peroxidase (POD), catalase, and superoxide dismutase (SOD) relative to the control. The Cd stress induced up-regulated expression of FeSOD, MnSOD, Chl Cu/ZnSOD, Cyt Cu/ZnSOD, APX, GPX, GR and POD at 4–24 h after treatment began for perennial ryegrass. Results suggested that the gene transcript profile was related to the enzyme activity under Cd stress.
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References
Alloways BJ (1990) In: Alloway BJ (ed) Heavy metals in soils. Blackie et Son LTD, USA, pp 100–339
Arienzo M, Adamo P, Cozzolino V (2004) The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site. Sci Total Environ 319:13–25
Beard JB (2002) Turfgrass management for golf courses, 2nd edn. Wiley, Hoboken, p 793
Bian SM, Jiang YW (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic-Amsterdam 120:264–270
Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brooks RR (1998) Plants that hyperaccumulate trace metals. CAB International, Wallingford
Brunet J, Varrault G, Zuily-Fodil Y, Repellin A (2009) Accumulation of lead in the roots of grass pea (Lathyrus sativus L.) plants triggers systemic variation in gene expression in the shoots. Chemosphere 77:1113–1120
Byrne SL, Durandeau K, Nagy I, Barth S (2010) Identification of ABC transporters from Lolium perenne L. that are regulated by toxic levels of selenium. Planta 231:901–911
Caggiano R, D’Emilio M, Macchiato M, Ragosta M (2005) Heavy metals in ryegrass species versus metal concentrations in atmospheric particulate measured in an industrial area southern Italy. Environ Monit Assess 102:67–84
Chance B, Maehly SK (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775
Chen LM, Lin CC, Kao C-H (2000) Copper toxicity in rice seedlings: changes in antioxidative enzymeactivities, H2O2 level, and cell wall peroxidase activity in roots. Bot Bull Acad Sin 41:99–103
Cho UH, Seo NH (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120
Chowdhury RS, Choudhuri MA (1985) Hydrogen peroxide metabolism as an index of water stress tolerance in jute. Physiol Plant 65:476–480
Ci DW, Jiang D, Dai TB, Jing Q, Cao WX (2009) Effects of cadmium on plant growth and physiological traits in contrast wheat recombinant inbred lines differing in cadmium tolerance. Chemosphere 77:1620–1625
Cuypers A, Karen S, Jos R, Kelly O, Els K, Tony R, Nele H, Nathalie V, Suzy VS, Frank VB, Yves G, Jan C, Jaco V (2010) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol. doi:10.1016/j.jplph.2010.07.010
Daghan H, Arslan M, Uygur V, Koleli N, Eren A (2010) The cadmium phytoextraction efficiency of SCMTII gene bearing transgenic tobacco plant. Biotechnol Biotechnol Equip 24:1974–1978
de la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Cadmium uptake and translocation in tumbleweed (Salsolakali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemosphere 55:1159–1168
Deng X, Xia Y, Hu W, Zhang H, Shen Z (2010) Cadmium-induced oxidative damage and protective effects of N-acetyl-l-cysteine against cadmium toxicity in Solanum nigrum L. J Hazard Mater 180:722–729
Dı′az J, Bernal A, Pomar F, Merino F (2001) Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. Plant Sci 161:179–188
Foito A, Byrne SL, Shepherd T, Stewart D, Barth S (2009) Transcriptional and metabolic profiles of Lolium perenne L. genotypes in response to a PEG-induced water stress. Plant Biotechnol J 7:719–732
Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a reevaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523
Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114
Goupil P, Souguir D, Ferjani E, Faure O, Hitmi A, Ledoigt G (2009) Expression of stress-related genes in tomato plants exposed to arsenic and chromium in nutrient solution. J Plant Physiol 166:1446–1452
Hannaway D, Fransen S, Cropper J, Teel M, Chaney M, Griggs T, Halse R, Hart J, Cheeke P, Hansen D, Klinger R, Lane W. Perennial ryegrass (Lolium perenne L.). In: A pacific northwest extension publication, vol PNW 502. Oregon State University, Washington State University, University of Idaho. 1999
Heath RN, Packer H (1968) Photoperoxidation in isolated chloroplasts. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hiscox TD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissues without maceration. Can J Bot 57:1332–1334
Hoagland C, Arnon D (1950) The solution-culture method for growing plants without soil. Calif Agric Exp Circ 247
Lee JM, Roche JR, Donaghy DJ, Thrush A, Sathish P (2010) Validation of reference genes for quantitative RT-PCR studies of gene expression in perennial ryegrass (Lolium perenne L.). BMC Mol Biol 11:1471–2199
Liu W, Shu WS, Lan CY (2004) Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin Sci Bull 49:29–32
Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132:272–281
Milone MT, Cristina S, Clijsters H, Navari-Izzo F (2003) Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50:265–276
Pawlak S, Firych A, Rymer K, Deckert J (2009) Cu, Zn-superoxide dismutase is differently regulated by cadmium and lead in roots of soybean seedlings. Acta Physiologiae Plantarum 31:741–747
Polle A, Eiblemeier M, Sheppard L, Murray M (1997) Responses of antioxidative enzymes to evaluated CO2 in leaves of beech (Fagus sylvatica L.) seedlings grownunder a range of nutrient regimes. Plant Cell Environ 20:1317–1321
Reinheckel T, Noack H, Lorenz S, Wiswedel I, Augustin W (1998) Comparison of protein oxidation and aldehyde formation during oxidative stress in isolated mitochondria. Free Radic Res 29:297–305
Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M (2004) Nitric oxide signalling functions in plant-pathogen interactions. Cell Microbiol 6:795–803
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Schutzendubel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen per oxide content, and differentiation in Scot Pine roots. Plant Physiol 127:887–898
Shah K, Kumar RG, Verma A, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes ingrowing rice seedlings. Plant Sci 161:1135–1144
Singh PK, Tewari RK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–112
Smeets K, Ruytinx J, Semane B, Van Belleghem F, Remans T, Van Sanden SJ, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–3
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58
Soleimani M, Hajabbasi MA, Afyuni M, Mirlohi A, Borggaard OK, Holm PE (2010) Effect of Endophytic Fungi on cadmium tolerance and bioaccumulation by Festuca Arundinacea and Festuca Pratensis. Int J Phytoremediation 12:535–549
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
Van Assche F, Clijsters H (1990) A biological test system for the evaluation of the phytotoxicity of metal-contaminated soils. Environ Pollut 66:157–172
Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242
Vogel-Mikuš K, Regvar M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Simčič J, Pelicon P, Budnar M (2008) Spatial distribution of cadmium in leaves of metal hyperaccumulating Thlaspi praecox using micro-PIXE. New Phytol 179:712–721
Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–212
Yamaguchi H, Fukuoka H, Arao T, Ohyama A, Nunome T, Miyatake K, Negoro S (2010) Gene expression analysis in cadmium-stressed roots of a low cadmium-accumulating solanaceous plant, Solanum torvum. J Exp Bot 61:423–437
Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189
Zhang JX, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791
Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavymetal 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
Zhang FQ, Zhang HX, Wang GP, Xu LL, Shen ZG (2009) Cadmium-induced accumulation of hydrogen peroxide in the leaf apoplast of Phaseolus aureus and Vicia sativa and the roles of different antioxidant enzymes. J Hazard Mater 168:76–84
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Luo, H., Li, H., Zhang, X. et al. Antioxidant responses and gene expression in perennial ryegrass (Lolium perenne L.) under cadmium stress. Ecotoxicology 20, 770–778 (2011). https://doi.org/10.1007/s10646-011-0628-y
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DOI: https://doi.org/10.1007/s10646-011-0628-y