Abstract
The protective roles of glutathione (GSH) applied on salt stress-affected mung bean (Vigna radiata L.) seedlings were studied. The salt stress (200 mM NaCl) significantly increased the malondialdehyde (MDA), methylglyoxal (MG), H2O2, and proline (Pro) content, O2 ·− generation rate, and lipoxygenase (LOX) activity and reduced the leaf relative water content (RWC) and chlorophyll (Chl) content. The salt stress also significantly reduced the ascorbate (AsA) content, increased the endogenous GSH and glutathione disulfide (GSSG) content, and reduced the GSH/GSSG ratio. The activities of mono-dehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and catalase (CAT) decreased; and the activities of ascorbate peroxidase (APX), glutathione reductase (GR), superoxide dismutase (SOD), glutathione S-transferase (GST), and glutathione peroxidase (GPX) increased under the salt stress. The activities of glyoxalase I (Gly I) and glyoxalase II (Gly II) decreased under the salt stress (except the Gly II activity at 48 h). Mung bean seedlings which were treated with NaCl together with GSH showed an improved AsA and GSH content, GSH/GSSG ratio, higher activities of APX (only at 24 h), MDHAR, DHAR, GR, SOD (only at 24 h), CAT, GPX (only at 48 h), GST (only at 24 h), Gly I and Gly II under the salt stress compared with those treated with NaCl alone. The improved antioxidant and glyoxalase systems by GSH application decreased the MDA, H2O2, and MG content, O2 ·− generation rate, as well as increased the leaf RWC and Chl content. Thus, exogenous GSH improved the response of the mung bean seedlings to the salt stress.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- AO:
-
ascorbate oxidase
- APX:
-
ascorbate peroxidase
- AsA:
-
ascorbate
- BSA:
-
bovine serum albumin
- CAT:
-
catalase
- CDNB:
-
1-chloro-2,4-dinitrobenzene
- Chl:
-
chlorophyll
- DHA:
-
dehydroascorbate
- DHAR:
-
dehydroascorbate reductase
- DTNB:
-
5,5′-dithio-bis-(2-nitrobenzoic) acid
- EDTA:
-
ethylenediaminetetraacetic acid
- Gly:
-
glyoxalase
- GR:
-
glutathione reductase
- GSH:
-
reduced glutathione
- GSSG:
-
oxidized glutathione
- GPX:
-
glutathione peroxidase
- GST:
-
glutathione S-transferase
- LOX:
-
lipoxygenase
- MDA:
-
malondialdehyde
- MDHA:
-
monodehydroascorbate
- MDHAR:
-
monodehydroascorbate reductase
- MG:
-
methylglyoxal
- NADPH:
-
nicotinamide adenosine dinucleotide phosphate
- NTB:
-
2-nitro-5-thiobenzoic acid
- PEG:
-
polyethylene glycol
- Pro:
-
proline
- ROS:
-
reactive oxygen species
- RWC:
-
relative water content
- SLG:
-
S-D-lactoyl-glutathione
- SOD:
-
superoxide dismutase
- TBA:
-
thiobarbituric acid
- TCA:
-
trichloroacetic acid
References
Aghaleh, M., Niknam, V., Ebrahimzadeh, H., Razavi, K.: Antioxidative enzymes in two in vitro cultured Salicornia species in response to increasing salinity. — Biol. Plant. 58: 391–394, 2014.
Alam, M.M., Nahar, K., Hasanuzzaman, M., Fujita, M.: Alleviation of osmotic stress in Brassica napus, B. campestris, and B. juncea by ascorbic acid application. — Biol. Plant. 58: 697–708, 2014.
Arnon, D.T.: Copper enzymes in isolated chloroplasts polyphenal oxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.
Aziz, A., Larher, F.: Osmotic stress induced changes in lipid composition and peroxidation in leaf discs of Brassica napus L. — J. Plant Physiol. 153: 754–762, 1998.
Aziz, A., Martin-Tanguy, J., Larher, F.: Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. — Physiol. Plant. 104: 195–202, 1998.
Baier, M., Dietz, K.J.: The plant 2-cis-peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin and implications for its specific physiological function in plants. — Plant J. 12: 179–190, 1997.
Barrs, H.D., Weatherley, P.E.: A re-examination of the relative turgidity technique for estimating water deficits in leaves. — Aust. J. biol. Sci. 15: 413–428, 1962.
Bates, L.S., Waldren, R.P., Teari, D.: Rapid determination of free proline for water stress studies. — Plant Soil 39: 205–207, 1973.
Bergmann, L., Rennenberg, H.: Glutathione metabolism in plants. — In: De Kok, L.J., Stulen, I., Rennenberg, H., Brunold, C., Rauser, W.E. (ed.): Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Pp. 109–123. SPB Academic Publishers, The Hague 1993.
Bradford, M.M.: 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, 1976.
Chen, J.H., Jiang, H.W., Hsieh, E.J., Chen, H.Y., Chien. C.T., Hsieh, H.L., Lin, T.P.: 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, 2012.
Del Río, L.A., Corpas, F.J., Sandalio, L.M., Palma, J.M., Gómez, M., Barroso, J.B.: Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. — J. exp. Bot. 53: 1255–1272, 2002.
Dixon, D.P., Skipsey, M., Edwards, R.: Roles for glutathione transferases in plant secondary metabolism. — Phytochemistry 71: 338–350, 2010.
Dixon, D.P., Skipsey, M., Grundy, N.M., Edwards, R.: Stressinduced protein S-glutathionylation in Arabidopsis. — Plant Physiol. 138: 2233–2244, 2005.
Doderer, A., Kokkelink, I., Van der Veen, S., Valk, B., Schram, A., Douma, A.: Purification and characterization of two lipoxygenase isoenzymes from germinating barley. — Biochem. biophys. Acta 112: 97–104, 1992.
Elia, A.C., Galarini, R., Taticchi, M.I., Dorr, A.J.M., Mantilacci, L.: Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. — Ecotoxicol. Environ. Safety 55: 162–167, 2003.
El-Shabrawi, H., Kumar, B., Kaul, T., Reddy, M.K., Singla-Pareek, S.L., Sopory, S.K.: Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. — Protoplasma 245: 85–96, 2010.
Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. — Anal. Biochem. 70: 616–620, 1976.
Foyer, C.H., Noctor, G.: Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. — Physiol. Plant 119: 355–364, 2003.
Foyer, C.H., Theodoulou, F.L., Delrot, S.: The functions of inter- and intracellular glutathione transport systems in plants. — Trends Plant Sci. 6: 486–492, 2001.
Garg, N., Manchanda, G.: ROS generation in plants: boon or bane? — Plant Biosyst. 143: 81–96, 2009.
Gill, S.S., Anjum, N.A., Hasanuzzaman, M., Gill, R., Trivedi, D.K., Ahmad, I., Pereira E., Tuteja, N.: Glutathione reductase and glutathione: a boon in disguise for plant abiotic stress defense operations. — Plant Physiol. Biochem. 70: 204–212, 2013.
Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. — Plant Physiol. Biochem. 48: 909–930, 2010.
Grill, E., Loffler, S., Winnacker, E.L., Zenk, M.H.: Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gammaglutamylcysteine dipeptidyltranspeptidase (phytochelatin synthase). — Proc. nat. Acad. Sci. USA 86: 6838–6842, 1989.
Hajlaoui, H., Denden, M., El-Ayeb, N.: Changes in fatty acid composition, hydrogen peroxide and lipid peroxidation of salt-stressed corn (Zea mays L.) roots. — Acta Physiol. Plant. 31: 787–796, 2009.
Hasanuzzaman, M., Hossain, M.A., Da Silva, J.A.T., Fujita, M.: Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. — In: Bandi, V., Shanker, A.K., Shanker, C., Mandapaka, M. (ed.): Crop Stress and its Management: Perspectives and Strategies. Pp. 261–316. Springer, Berlin 2012.
Hasanuzzaman, M., Hossain, M.A., Fujita, M.: Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. — Plant Biotechnol. Rep. 5: 353–365, 2011a.
Hasanuzzaman, M., Hossain, M.A., Fujita, M.: Seleniuminduced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinityinduced damage in rapeseed seedlings. — Biol. Trace Element Res. 143: 1704–1721, 2011b.
Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R., Fujita, M.: Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. — Int. J. mol. Sci. 14: 9643–9684, 2013.
Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplast. I. kinetics and stoichiometry of fatty acid peroxidation. — Arch. Biochem. Biophys. 125: 189–198, 1968.
Herschbach, C., Van Der Zalm, E., Schneider, A., Jouanin, L., De Kok, L.J.: Rennenberg H.: Regulation of sulfur nutrition in wild-type and transgenic poplar by over-expressing gamma glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. — Plant Physiol. 124: 461–473, 2000.
Hossain, M.A., Fujita, M.: Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. — Physiol. mol. Biol. Plants. 16: 19–29, 2010.
Hossain, M.A., Hasanuzzaman, M., Fujita, M.: Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. — Front. Agr. China 5: 1–14, 2011.
Hossain, M.A., Hossain, M.D., Fujita, M.: Induction of pumpkin glutathione S-transferase by different stresses and its possible mechanisms. — Biol. Plant. 50: 210–218, 2006.
Hossain, M.A., Nakano, Y., Asada, K.: Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. — Plant Cell Physiol. 25: 385–395, 1984.
Huang, C., He, W., Guo, J., Chang, X., Su, P., Zhang, L.: Increased sensitivity to salt stress in ascorbate deficient Arabidopsis mutant. — J. exp. Bot. 56: 3041–3049, 2005.
Job, C., Rajjou, L., Lovigny, Y., Belghazi, M., Job, D.: Patterns of protein oxidation in Arabidopsis seeds and during germination. — Plant Physiol. 138: 790–802, 2005.
Katerji, N., Van Hoorn, J.W., Hamdy, A., Mastrorilli, M., Moukarzel, E.: Osmotic adjustment of sugar beets in response to soil salinity and its influence on stomatal conductance, growth and yield. — Agr. Water Manage. 34: 57–69, 1997.
Kattab, H.: Role of glutathione and polyadenylic acid on the oxidative defense systems of two different cultivars of canola seedlings grown under saline condition. — Aust. J. basic appl. Sci. 1: 323–332, 2007.
Khedr, A.H.A., Abbas, M.A., Wahid, A.A.A., Quick, W.P., Abogadallah, G.M.: Proline induces the expression of saltstress responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. — J. exp. Bot. 54: 2553–2562, 2003.
Lappartient, A.G., Touraine, B.: Demand-driven control of root ATP sulfurylase activity and SO4 2- uptake in intact canola. The role of phloem-translocated glutathione. — Plant Physiol. 111: 147–157, 1996.
Liu, J.J., Lin, S.H., Xu, P.L., Wang, X.J., Bai, J.G.: Effects of exogenous silicon on the activities of antioxidant enzymes and lipid peroxidation in chilling-stressed cucumber leaves. — Agr. Sci. China 8: 1075–1086, 2009.
Lynch, D.L., Thompson, J.E.: Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. — FEBS Lett. 173: 251–254, 1984.
Marrs, K.A.: The functions and regulation of glutathione S-transferases in plants. — Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 127–157, 1996.
Mishra, P., Bhoomika, K., Dubey, R.S.: Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. — Protoplasma 250: 3–19, 2013.
Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I.: Boron induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). — Environ. exp. Bot. 56: 54–62, 2006.
Moller, I.M., Jensen, P.E., Hansson, A.: Oxidative modifications to cellular components in plants. — Annu. Rev. Plant Biol. 58: 459–481, 2007.
Nahar, K., Hasanuzzaman, M., Alam, M.M., Fujita, M.: Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. — Environ. exp. Bot. 112: 44–54, 2015a.
Nahar, K., Hasanuzzaman, M., Alam, M.M., Fujita, M.: Glutathione-induced drought stress tolerance in mung bean: Coordinated roles of the antioxidant defense and methylglyoxal detoxification systems. — AoB Plants. DOI: 10.1093/aobpla/plv069, 2015b.
Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. — Plant Cell Physiol. 22: 867–880, 1981.
Naliwajski, M.R., SkŁodowska, M.: The oxidative stress and antioxidant systems in cucumber cells during acclimation to salinity. — Biol. Plant. 58: 47–54, 2014.
Paradiso, A., Berardino, R., De Pinto, M., Di Toppi, L.S., Storelli, F.T, De Gara, L.: Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. — Plant Cell Physiol. 49: 362–374, 2008.
Principato, G.B., Rosi, G., Talesa, V., Govannini, E., Uolila, L.: Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. — Biochem. biophys. Acta. 911: 349–355, 1987.
Rennenberg, H., Schmitz, K., Bergmann, L.: Long distance transport of sulfur in Nicotiana tabacum. — Planta 147: 57–82, 1979.
Roychoudhury, A., Basu, S., Sengupta, D.N.: Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of Indica rice differing in their level of salt tolerance. — J. Plant Physiol. 168: 317–328, 2011.
Schneider, A., Schatten, T., Rennenberg, H.: Exchange between phloem and xylem during long distance transport of glutathione in spruce trees (Picea abies [Karst.]L.). — J. exp. Bot. 45: 457–462, 1994.
Shringarpure, R., Davies K.J.: Protein turnover by the proteasome in aging and disease. — Free Radical Biol. Med. 32: 1084–1089, 2002.
Song, X.S., Hu, W.H., Mao, W.H., Ogweno, J.O., Zhou, Y.H., Yu, J.Q.: Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. — Plant Physiol. Biochem. 43: 1082–1088, 2005.
Srivalli, S., Khanna-Chopra, R.: Role of glutathione in abiotic stress tolerance. — In: Khan, N.A., Singh, S., Umar, S. (ed.): Sulfur Assimilation and Abiotic Stress in Plants. Pp. 207–225. Springer, Berlin 2008.
Steudle, E.: Water uptake by roots: effects of water deficit. — J. exp. Bot. 51: 1531–1542, 2000.
Sudhir, P., Murthy, S.D.S.: Effects of salt stress on basic processes of photosynthesis. — Photosynthetica 42: 481–486, 2004.
Sumithra, K., Jutur, P.P., Carmel, B.D., Reddy, A.R.: Salinityinduced changes in two cultivars of Vigna radiata: responses of antioxidative and proline metabolism. — Plant Growth Regul. 50: 11–22, 2006.
Wang, H., Liu, J., Wu, L.: Methylglyoxal-induced mitochondrial dysfunction in vascular smooth muscle cells. — Biochem. Pharmacol. 77: 1709–1716, 2009.
Wild, R., Ooi, L., Srikanth, V., Münch, G.: A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-L-cysteine assay. — Anal Bioanal. Chem. 403: 2577–2581, 2012.
Xu, L.H., Wang, W.Y., Guo, J.J., Qin, J., Shi, D.Q., Li, Y.L., Xu, J.: Zinc improves salt tolerance by increasing reactive oxygen species scavenging and reducing Na+ accumulation in wheat seedlings. — Biol. Plant. 58: 751–757, 2014.
Yadav, S.K., Singla-Pareek, S.L., Ray, M., Reddy, M.K., Sopory, S.K.: Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. — Biochem. biophys. Res. Commun. 337: 61–67, 2005.
Yadav, S.K., Singla-Pareek, S.L., Sopory, S.K.: An overview on the role of methylglyoxal and glyoxalases in plants. — Drug Metab. Drug Interact. 23: 51–68, 2008.
Yang, H., Shi, G., Wang, H., Xu, Q.: Involvement of polyamines in adaptation of Potamogeton crispus L. to cadmium stress. — Aquat. Toxicol. 100: 282–288, 2010.
Yu, C.W., Murphy, T.M., Lin, C.H.: Hydrogen peroxideinduces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. — Funct. Plant Biol. 30: 955–963, 2003.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: The first author is grateful to the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, for financial support. We acknowledge Dr Md Motiar Rohman, the Senior Scientific Officer, theBangladesh Agricultural Research Institute, for his cooperation and help in measuring enzymatic activities and other biochemical parameters. We thankfully acknowledge Dennis Murphy, Ehime University, Japan, for a critical review and English language correction.
Rights and permissions
About this article
Cite this article
Nahar, K., Hasanuzzaman, M., Alam, M.M. et al. Roles of exogenous glutathione in antioxidant defense system and methylglyoxal detoxification during salt stress in mung bean. Biol Plant 59, 745–756 (2015). https://doi.org/10.1007/s10535-015-0542-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-015-0542-x