Abstract
Cadmium (Cd) is a potential environmental phytotoxicant. The generation of reactive oxygen species (ROS) due to Cd stress is responsible for the induction of oxidative stress in plants. On the other hand, SNP, a NO donor is known to have effect on Cd-induced oxidative stress in plants. We evaluated the effect of NO on the regulation of Cd stress in the rice (Oryza sativa L.) variety MSE-9. Cd treatment was given in the form of 50, 100 and 200 μM, whereas for interaction study, 100 μM of Cd and 100 μM of SNP were used. The result showed that Cd-induced oxidative stress in MSE-9 by generating ROS. However, when SNP was given with Cd stress, it was seen that SNP treatment regulated the stress metabolism in rice seedlings under Cd toxicity by generating NO. It can be said that the SNP in combination with Cd treatment might possess the way to protect rice seedlings under Cd stress.
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Abbreviations
- Cd:
-
Cadmium
- NO:
-
Nitric oxide
- SNP:
-
Sodium nitroprusside
- ROS:
-
Reactive oxygen species
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- GR:
-
Glutathione reductase
- POX:
-
Guaiacol peroxidase
- SOD:
-
Superoxide dismutase
- DTNB:
-
Dithionitrobenzoic acid
- h:
-
Hour
- TBA:
-
Thiobarbituric acid
- TCA:
-
Trichloroacetic acid
- GSH:
-
Glutathione
- ASC:
-
Ascorbate
References
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. doi:10.1146/annurev.arplant.50.1.601
Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxygenase activity and oxidative stress signaling in soybean leaves. Plant Sci 170:339–346
Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208:337–344
Beligni MV, Lamattina L (2001) Nitric oxide in plants: the history is just beginning. Plant Cell Environ 24:267–278
Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315
Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116
Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775
Chamseddine M, Wided B, Guy A, Marie-Edith H, Fatma C (2008) Cadmium and copper induction of oxidative stress and antioxidative response in tomato (Solanum lycopersicon) leaves. Plant Growth Regul. doi:10.1007/s10725-008-9324-1
Cornu JY, Denaix L, Schneider A, Pellerin S (2008) Temporal variability of solution Cd2+ concentration in metal-contaminated soils as affected by soil temperature: consequences on lettuce (Lactuca sativa L.) exposure. Plant Soil 307:51–65. doi;10.1007/s11104-008-9580-x
Cui X, Zhang Y, Chen X, Jin H, Wu X (2009) Effects of exogenous nitric oxide protects tomato plants under copper stress. Protoplasma. doi:10.1109/ICBBE.2009.5162740
Davenport SB, Gallego SM, Benavides MP, Tomaro ML (2003) Behaviour of antioxidant defense system in the adaptive response to salt stress in Helianthus annus L. cell. Plant Growth Regul 40:81–88. doi:10.1023/A:1023060211546
Davis DG, Swanson HR (2001) Activity of stress-related enzymes in the perennial weed leafy spurge (Euphorbia esula L.). Environ Exp Bot 46:95–108. doi:10.1016/S0098-8472(01)00081-8
Finkemeier I, Kluge C, Metwally A, Georgi M, Grotjohann N, Dietz KJ (2003) Alterations in Cd-induced gene expression under nitrogen deficiency in Hordeum vulgare. Plant Cell Environ 26:821–833
Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanism of acclamatory stress tolerance and signaling. Physiol Plant 100:241–254
Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314
Gould KS, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–221
Halliwell B, Foyer CH (1978) Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta 139:9–17
Hernandez LE, Cooke DT (1997) Modifications of root plasma membrane lipid composition of cadmium treated Pisum sativum. J Exp Bot 48:1375–1381
Hill AC, Bennett JH (1970) Inhibition of apparent photosynthesis by nitrogen oxides. Atmos Environ 4:341–348
Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238
Jaleel CA, Riadh K, Gopi R, Manivannan P, Ine’s J, Al-Juburi HJ, Chang-Xiang Z, Hong-Bo S, Panneerselvam R (2008) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant. doi:10.1007/s11738-009-0275-6
Jaleel CA, Gopi R, Manivannan P, Panneerselvam R (2008b) Exogenous application of triadimefon affects the antioxidant defense system of Withania somnifera Dunal. Pestic Biochem Physiol 91:170–174. doi:10.1016/j.pestbp.2008.03.006
Jaleel CA, Riadh K, Gopi R, Manivannan P, Ine`s J, Al-Juburi HJ, Chang-Xing Z, Hong-Bo S, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant. doi:10.1007/s11738-009-0275-6
Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284
Khan NA, Singh S, Nazar R (2007) Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci 193:433–442
Klepper LA (1979) Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Environ 13:537–541
Kumar P, Tewari RK, Sharma PN, (2008) Cadmium enhances generation of hydrogen peroxide and amplifies activities of catalase, peroxidases and superoxide dismutase in maize. J Agron Crop Sci. ISSN 0931-2250
Kuriakose Saritha V, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54:143–156. doi:10.1007/s10725-007-9237-4
Lamattina L, Garcı′a-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330
Leshem YY, Kuiper PJC (1996) Is there a GAS (general adaptation syndrome) response to various types of environmental stress? Biol Plant 38:1–18
Leshem YY, Haramaty E, Iluz D, Malik Z, Sofer Y, Roitman L (1997) Effect of stress nitric oxide (NO): interaction between chlorophyll fluorescence, galactolipid fluidity and lipoxygenese activity. Plant Physiol Biochem 35:573–579
Leshem YY, Wills RBH, Ku VVV (1998) Evidence for the function of the free radical gas-nitric oxide (NO)-as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833
Linger P, Ostwald A, Haensler J (2005) Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis. Biol Plant 49(4):567–576
Liu D, Kottke I (2005) Subcellular localization of Cd in the root cells of Allium sativum by electron energy loss spectroscopy. J Biosci 28(4):471–478
Liu HJ, Zhang JL, Christie P, Zhang FS (2007) Influence of external zinc and phosphorus supply on Cd uptake by rice (Oryza sativa L.) seedlings with root surface iron plaque. Plant Soil 300:105–115. doi:10.1007/s11104-007-9393-3
Luan ZQ, Cao HC, Yan BX (2008) Individual and combined phytotoxic effects of cadmium, lead and arsenic on soybean in Phaeozem. Plant Soil Environ 54(9):403–411
Maehly A, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 357
Mehlhorn H, Lelandais M, Korth HG, Foyer CH (1996) Ascorbate is the natural substrate for plant peroxidases. FEBS Lett 378:203–206. doi:10.1016/0014-5793(95)01448-9
Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Molina AS, Nievas C, Chaca MVP, Garibotto F, González U, Marsá SM, Luna C, Giménez MS, Zirulnik F (2008) Cadmium-induced oxidative damage and antioxidative defense mechanisms in Vigna mungo L. Plant Growth Regul. doi:10.1007/s10725-008-9308-1
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplast. Plant Cell Physiol 22:867–880
Neill SJ, Desikan R, Hancock JT (2002) Nitric oxide signalling in plants. New Phytol 159:11–35
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279
Noctor G, Leonardo G, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53(372):1283–1304. doi:10.1093/jexbot/53.372.1283
Orozco-Cardenas ML, Ryan CA (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol 130:487–493
Oser B, Hawks L (1985) Physiological chemistry. McGraw Hill, New York, pp 702–705
Patel MJ, Patel JN, Subramanian RB (2005) Effect of cadmium on growth and the activity of H2O2 scavenging enzymes in Colocassia esculentum. Plant Soil 273:183–188
Pedroso MC, Magalhaes JR, Durzan D (2000) Nitric oxide induces cell death in Taxus cells. Plant Sci 157:173–180
Pinto AP, Mota AM, de Varennes A, Pinto FC (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by Sorghum plants. Sci Total Environ 326:239–247
Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Int Plant Biol 50(10):1238–1246
Rodrı′guez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Rı′o LA, Sandalio L (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
Rodríguez-Serrano M, Romero-Puertas MC, Diana M, Testillano PS, Risueño MC, del Río L, Sandalio A, Luisa M (2009) Cellular response of pea plants to cadmium toxicity: cross-talk between reactive oxygen species, nitric oxide and calcium. Plant Physiol Prev. doi:10.1104/pp.108.131524
Sagisaka S (1976) The occurence of peroxide in a perennial plant Populas gelrica. Plant Physiol 57:308–309
Salin ML (1987) Toxic oxygen species and protective systems of the chloroplast. Physiol Plant 72:681–689
Sanita di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130. doi:10.1016/S0098-8472(98)00058-6
Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144
Shamsii Ih, Wei K, Zhang GP, Jilani GH, Hassan MJ (2008) Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean. Biol Plant 52(1):165–169
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53(372):1305–1319. doi:10.1093/jexbot/53.372.1305
Shingles R, Roh MH, McCarty RE (1996) Nitrate transport in chloroplast inner envelope vesicles. Plant Physiol 112:1375–1381
Siddiqui S, Meghvansi MK, Wani MA, Jabee F (2009) Evaluating cadmium toxicity in the root meristem of Pisum sativum L. Acta Physiol Plant. doi:10.1007/s11738-008-0262-3
Singh S, Eapen S, D’Souza SF (2006) Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246
Singh SP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167
Smeets K, Ruytinx J, Semane B, Belleghemc FV, Remans T, Suzy Van Sanden, Jaco V, Cuypers A (2008) Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63:1–8
Vanacker H, Carver TLW, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114. doi:10.1104/pp.117.3.1103
Wang Zi, Zhang Y, Huang Z, Huang L (2008) Antioxidative response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil 310:137–149. doi:10.1007/s11104-008-9641-1
Wellburn AR (1990) Why are atmospheric oxides of nitrogen usually phytotoxic and not alternative fertilizers? New Phytol 115:395–429
Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signalling and defence responses. Curr Opin Plant Biol 7:449–455
Yamasaki H (2000) Nitrite-dependent nitric oxide production pathway: implications for Philos. Trans R Soc Lond B Biol Sci 355:1477–1488
Zhang XZ (1992) The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. In: Zhang XZ (ed) Research methodology of crop physiology. Agriculture Press, Beijing, pp 208–211
Zhao CX, Guo LY, Jaleel CA, Hong-Bo S, Yang HB (2008) Prospects for dissecting plant-adaptive molecular mechanisms to improve wheat cultivars in drought environments. C R Biol 331:579–586. doi:10.1016/j.crvi.2008.05.006
Zottini M, Formentin E, Scattolin M, Carimi F, LoSchiavo F, Terzi M (2002) Nitric Oxide affects plant mitochondrial functionality in vivo. FEBS Lett 515:75–78
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Panda, P., Nath, S., Chanu, T.T. et al. Cadmium stress-induced oxidative stress and role of nitric oxide in rice (Oryza sativa L.). Acta Physiol Plant 33, 1737–1747 (2011). https://doi.org/10.1007/s11738-011-0710-3
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DOI: https://doi.org/10.1007/s11738-011-0710-3