Abstract
Glutathione (GSH) is involved in not only plant developmental processes but also plant responses to abiotic stresses. A hydroponic experiment was performed to explore the protective roles of exogenous GSH in mitigating cadmium (Cd) stress in Brassica campestris L. seedlings by analyzing the morphological and physiological parameters. Results showed that Cd caused severe growth inhibition and Cd accumulation. However, application of GSH significantly mitigated toxic symptoms induced by Cd, including the improvement of the photosynthesis-, plant growth-, and root morphology-related parameters in seedlings under Cd stress. These responses were associated with a striking increase in activities of representative antioxidative enzymes and contents of corresponding non-enzymatic antioxidants. In vivo imaging of O2.- and H2O2, and the detection of lipid peroxidation further demonstrated that increased ability by GSH for Brassica campestris L. seedlings to endure Cd stress was consistent with a striking elevation of ratios of reduced to oxidized glutathione (GSH/GSSG) and ascorbic acid to dehydroascorbic acid (AsA/DHA). Additionally, GSH application increased Cd retained in roots, thus significantly decreased its translocation from root to shoot, ultimately decreased Cd accumulation in shoots. Taken together, our results proved evidence for GSH in ameliorating Cd toxicity via reducing Cd accumulation in shoots and increasing oxidation resistance. Accordingly, application of GSH could be a high-efficiency and promising strategy to decrease Cd concentration in edible parts of Brassica campestris L. in agricultural production.
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Ali B, Tao Q, Zhou Y, Gill RA, Ali S, Rafiq MT, Xu L, Zhou W (2013a) 5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicol Environ Saf 92:271–280
Ali B, Wang B, Ali S, Ghani MA, Hayat MT, Yang C, Xu L, Zhou WJ (2013b) 5-Aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity, and ultrastructural changes under cadmium stress in Brassica napus L. J Plant Growth Regul 32(3):604–661
Ali B, Huang CR, Qi ZY, Ali S, Daud MK, Geng XX, Liu HB, Zhou WJ (2013c) 5-Aminolevulinic acid ameliorates cadmium-induced morphological, biochemical, and ultrastructural changes in seedlings of oilseed rape. Environ Sci Pollut Res 20(10):7256–7267
Ali E, Maodzeka A, Hussain N, Shamsi IH, Jiang L (2015) The alleviation of cadmium toxicity in oilseed rape (Brassica napus) by the application of salicylic acid. Plant Growth Regul 75:641–655
Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324
Cai Y, Cao F, Wei K, Zhang G, Wu F (2011) Genotypic dependent effect of exogenous glutathione on Cd-induced changes in proteins, ultrastructure and antioxidant defense enzymes in rice seedlings. J Hazard Mater 192:1056–1066
Carrasco-Gil S, Estebaranz-Yubero M, Medel-Cuesta D, Millán R, Hernández LE (2012) Influence of nitrate fertilization on Hg uptake and oxidative stress parameters in alfalfa plants cultivated in a Hg-polluted soil. Environ Exp Bot 75:16–24
Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351
Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z, Cui J (2017) Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul 81:253–264
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486
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 168:309–316
Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A (2009) Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem Sci 34:85–96
Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289
Fatma M, Asgher M, Masood A, Khan NA (2014) Excess sulfur supplementation improves photosynthesis and growth in mustard under salt stress through increased production of glutathione. Environ Exp Bot 107:55–63
Feng X, Liu W, Sehar S, Zheng W, Zhang G, Wu F (2018) Application of sulfur fertilizer reduces cadmium accumulation and toxicity in tobacco seedlings (Nicotiana tabacum). Plant Growth Regul 85:165–170
Foyer CH (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
Gajewska E, Skłodowska MM, Słaba M, Mazur J (2006) Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. Biol Plantarum 50:653–659
Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120
Gill RA, Zang L, Ali B, Farooq MA, Cui P, Yang S, Ali S, Zhou W (2015) Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 120:154–164
Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol 1:22
Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Han Y, Zhang J, Chen X, Gao Z, Xuan W, Xu S, Ding X, Shen W (2008) Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol 177:155–166
Han J, Shang Q, Du Y (2009) Review: effect of environmental cadmium pollution on human health. Health 01(03):159–166
Hao G, Derakhshan B, Shi L, Campagne F, Gross SS (2006) Correction: SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc Natl Acad Sci U S A 103:1012–1017
Hasan MK, Liu C, Wang F, Ahammed GJ, Zhou J, Xu M, Yu J, Xia X (2016) Glutathione-mediated regulation of nitric oxide, S-nitrosothiol and redox homeostasis confers cadmium tolerance by inducing transcription factors and stress response genes in tomato. Chemosphere 161:536–545
Hassan MJ, Shao G, Zhang G (2005) Influence of cadmium toxicity on growth and antioxidant enzyme activity in rice cultivars with different grain cadmium accumulation. J Plant Nutr 28:1259–1270
He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z, Luo Z (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50–63
Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272
Huang B, Xu S, Xuan W, Li M, Cao Z, Liu K, Ling T, Shen W (2006) Carbon monoxide alleviates salt-induced oxidative damage in wheat seedling leaves. J Integr Plant Biol 48:249–254
Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597
Jahan MS, Ogawa K, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2008) Deficient glutathione in guard cells facilitates abscisic acid-induced stomatal closure but does not affect light-induced stomatal opening. Biosci Biotechnol Biochem 72(10):2795–2798
Jahan MS, Nozulaidi M, Khairi M, Mat N (2016) Light-harvesting complexes in photosystem II regulate glutathione-induced sensitivity of Arabidopsis guard cells to abscisic acid. J Plant Physiol 195:1–8
Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès 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 31(3):427–436
Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ Pollut 147:750–756
Jin Q, Zhu K, Cui W, Xie Y, Han B, Shen W (2013) Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system: hydrogen gas functions as a signal in plants. Plant Cell Environ 36:956–969
Khare R, Kumar S, Shukla T, Ranjan A, Trivedi PK (2017) Differential sulphur assimilation mechanism regulates response of Arabidopsis thaliana natural variation towards arsenic stress under limiting sulphur condition. J Hazard Mater 337:198–207
Knudson LL, Tibbitts TW, Edwards GE (1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiol 60:606–608
Kováčik J, Babula P, Hedbavny J, Klejdus B (2014) Hexavalent chromium damages chamomile plants by alteration of antioxidants and its uptake is prevented by calcium. J Hazard Mater 273:110–117
Li M, Liang D, Pu F, Ma F, Hou C, Lu T (2009) Ascorbate levels and the activity of key enzymes in ascorbate biosynthesis and recycling in the leaves of 22 Chinese persimmon cultivars. Sci Hortic 120:250–256
Lin Y, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206
Lux A, Martinka M, Vaculik M, White PJ (2010) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
Meister A (1994) Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269:9397
Mendoza-Cózatl DG, Moreno-Sánchez R (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modeling for plants. J Theor Biol 238:919–936
Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039
Munemasa S, Muroyama D, Nagahashi H, Nakamura Y, Mori IC, Murata Y (2013) Regulation of reactive oxygen species-mediated abscisic acid signaling in guard cells and drought tolerance by glutathione. Front Plant Sci 4(2):472
Nakamura S, Suzui N, Nagasaka T, Komatsu F, Ishioka NS, Ito-Tanabata S, Kawachi N, Rai H, Hattori H, Chino M, Fujimaki S (2013) Application of glutathione to roots selectively inhibits cadmium transport from roots to shoots in oilseed rape. J Exp Bot 64:1073–1081
Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10(3):e1003751
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, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation: methods in oxidative stress research. Plant Cell Environ 39:1140–1160
Ortega-Villasante C, Hernández LE, Rellán-álvarez R, Campo FFD, Carpena-Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176:96–107
Patsikka E, Kairavuo M, Sersen F, Aro EM, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367
Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69
Pietrini F, Lannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiol 133:829–837
Pompella A, Maellaro E, Casini AF, Comporti M (1987) Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Am J Pathol 129:295–301
Pompella A, Visvikis A, Paolicchi A, Tata VD, Casini AF (2003) The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol 66:1499–1503
Rao AR, Dayananda C, Sarada R, Shamala TR, Ravishankar GA (2007) Effect of salinity on growth of green alga Botryococcus braunii and its constituents. Bioresour Technol 98:560–564
Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Río 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
Rodriguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, Del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243
Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166
Salt DE, Rauser WE (1995) MgATP-dependent transport of Phytochelatins across the tonoplast of oat roots. Plant Physiol 107:1293–1301
Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione: metal phytoextraction and glutathione. Plant Cell Environ 35:334–346
Sgherri CLM, Navari-Izzo F (1995) Sunflower seedlings subjected to increasing water deficit stress: oxidative stress and defence mechanisms. Physiol Plantarum 93:25–30
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
Shan C, Zhang S, Li D, Zhao Y, Tian X, Zhao X, Wu Y, Wei X, Liu R (2011) Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol Plant 33:2533–2540
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
Su Y, Liu J, Lu Z, Wang X, Zhang Z, Shi G (2014) Effects of iron deficiency on subcellular distribution and chemical forms of cadmium in peanut roots in relation to its translocation. Environ Exp Bot 97:40–48
Szalai G, Kellős T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80
Tai Z, Yin X, Fang Z, Shi G, Lou L, Cai Q (2017) Exogenous GR24 alleviates cadmium toxicity by reducing cadmium uptake in switchgrass (Panicum virgatum) seedlings. Int J Environ Res Public Health 14:852
Tiwari S, Patel A, Prasad SM (2018) Kinetin alleviates chromium toxicity on growth and PS II photochemistry in Nostoc muscorum by regulating antioxidant system. Ecotox Environ Safe 161:296–304
Uraguchi S, Watanabe I, Yoshitomi A, Kiyono M, Kuno K (2006) Characteristics of cadmium accumulation and tolerance in novel cd-accumulating crops, Avena strigosa and Crotalaria juncea. J Exp Bot 57:2955–2965
Vernoux T, Wilson RC, Seeley KA, Reichheld J, Muroy S, Brown S, Maughan SC, Cobbett CS, Montagu MV, Inze D, May MJ, Sung ZR (2000) The root meristem less1/cadmium sensitive2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–109
Verougstraete V, Lison D, Hotz P (2003) Cadmium, lung and prostate cancer: a systematic review of recent epidemiological data. J Toxicol Environ Health B Crit Rev 6:227–255
Wang F, Chen F, Cai Y, Zhang G, Wu F (2011) Modulation of exogenous glutathione in ultrastructure and photosynthetic performance against Cd stress in the two barley genotypes differing in Cd tolerance. Biol Trace Elem Res 144(1–3):1275–1288
Wei S, Wang S, Li Y, Zhu J (2013) Root system responses of hyperaccumulator Solanum nigrum L. to Cd. J Soils Sediments 13:1069–1074
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179
Yuan H, Zhang Y, Huang S, Yang Y, Gu C (2015) Effects of exogenous glutathione and cysteine on growth, lead accumulation, and tolerance of Iris lactea var. chinensis. Environ Sci Pollut Res 22:2808–2816
Zeng FR, Qiu BY, Wu XJ, Niu SZ, Wu FB, Zhang GP (2012) Glutathione-mediated alleviation of chromium toxicity in Rice plants. Biol Trace Elem Res 148:255–263
Zhang H, Forman HJ (2012) Glutathione synthesis and its role in redox signaling. Semin Cell Dev Biol 23:722–728
Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012) Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mater 239-240:302–307
Zouari M, Ben Ahmed C, Zorrig W, Elloumi N, Rabhi M, Delmail D, Ben Rouina B, Labrousse P, Ben Abdallah F (2016) Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.). Ecotox Environ Safe 128:100–108
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This work was financially supported by the National Key Research and Development Program (2016YFD0800300) and China Agriculture Research System (CARS-23-A03).
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Huang, Y., Zhu, Z., Wu, X. et al. Lower cadmium accumulation and higher antioxidative capacity in edible parts of Brassica campestris L. seedlings applied with glutathione under cadmium toxicity. Environ Sci Pollut Res 26, 13235–13245 (2019). https://doi.org/10.1007/s11356-019-04745-7
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DOI: https://doi.org/10.1007/s11356-019-04745-7