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. 2010 Nov 24;16(3):259–272. doi: 10.1007/s12298-010-0028-4

Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress

Mohammad Anwar Hossain 1,2, Mirza Hasanuzzaman 1,3, Masayuki Fujita 1,
PMCID: PMC3550671  PMID: 23572976

Abstract

The present study investigates the possible mediatory role of exogenously applied glycinebetaine (betaine) and proline on reactive oxygen species (ROS) and methylglyoxal (MG) detoxification systems in mung bean seedlings subjected to cadmium (Cd) stress (1 mM CdCl2, 48 h). Cadmium stress caused a significant increase in glutathione (GSH) and glutathione disulfide (GSSG) content, while the ascorbate (AsA) content decreased significantly with a sharp increase in hydrogen peroxide (H2O2) and lipid peroxidation level (MDA). Ascorbate peroxidase (APX), glutathione S-transferase (GST), glutathione peroxidase (GPX), and glyoxalase I (Gly I) activities were increased in response to Cd stress, while the activities of catalase (CAT), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione reductase (GR) and glyoxalase II (Gly II) were sharply decreased. Exogenous application of 5 mM betaine or 5 mM proline resulted in an increase in GSH and AsA content, maintenance of a high GSH/GSSG ratio and increased the activities of APX, DHAR, MDHAR, GR, GST, GPX, CAT, Gly I and Gly II involved in ROS and MG detoxification system as compared to the control and mostly also Cd-stressed plants, with a concomitant decrease in GSSG content, H2O2 and lipid peroxidation level. These findings together with our earlier findings suggest that both betaine and proline provide a protective action against Cd-induced oxidative stress by reducing H2O2 and lipid peroxidation levels and by increasing the antioxidant defense and MG detoxification systems.

Keywords: Antioxidant defense, Glyoxalase system, Glycinebetaine, Proline, Cadmium stress, Reactive oxygen species, Mung bean

Full Text

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Acknowledgements

Thanks are due to Dr. Md. Abdul Malek, Principal Scientific Officer, Plant Breeding Division, Bangladesh Institute of Nuclear Agriculture (BINA), Bangladesh Agricultural University (BAU) campus, Mymensingh-2202, Bangladesh for providing the seeds of Vigna cultivars.

Abbreviations

AO

ascorbate oxidase

APX

ascorbate peroxidase

AsA

ascorbic acid

CAT

catalase

CDNB

1- chloro-2, 4-dinitrobenzene

DHA

dehydroascorbate

DHAR

dehydroascorbate reductase

DTNB

5,5′-dithio-bis (2-nitrobenzoic acid)

EDTA

ethylene diamine tetraacetic acid

Gly I

glyoxalase I

Gly II

glyoxalase II

GR

glutathione reductase

GSH

reduced glutathione

GSSG

oxidized glutathione

GPX

glutathione peroxidase

GST

glutathione S-transferase

MDA

malondialdehyde

MDHA

monodehydroascorbate

MDHAR

monodehydroascorbate reductase

MG

methylglyoxal

NTB

2-nitro-5-thiobenzoic acid

ROS

reactive oxygen species

SLG

S-D-lactoylglutathione

TBA

thiobarbituric acid

TCA

trichloroactic acid

References

  1. Aghaei K, Ehsanpour AK, Komatsu S. Potato responds to salt stress by increased activity of antioxidant enzymes. J Integr Plant Biol. 2009;51:1095–1103. doi: 10.1111/j.1744-7909.2009.00886.x. [DOI] [PubMed] [Google Scholar]
  2. Ansel DC, Franklin MLT, De Carvalho MHC, Lameta ADA, Fodil YZ. Glutathione reductase in leaves of cowpea: cloning of two cDNAs, expression and enzymatic activity under progressive drought stress desiccation and abscisic acid treatment. Ann Bot. 2006;98:1279–1287. doi: 10.1093/aob/mcl217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aravind PA, Prasad NV. Modulation of cadmium induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem. 2005;45:107–116. doi: 10.1016/j.plaphy.2005.01.002. [DOI] [PubMed] [Google Scholar]
  4. Ashraf M, Foolad MR. Roles of glycinebetaine and proline in improving plant abiotic resistance. Environ Exp Bot. 2007;59:206–16. doi: 10.1016/j.envexpbot.2005.12.006. [DOI] [Google Scholar]
  5. Athar HR, Khan A, Ashraf M. Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ Exp Bot. 2008;63:224–231. doi: 10.1016/j.envexpbot.2007.10.018. [DOI] [Google Scholar]
  6. Bassi R, Sharma SS. Changes in proline content accompanying the uptake of zinc and copper by Lemna minor. Ann Bot. 1993;72:151–154. doi: 10.1006/anbo.1993.1093. [DOI] [Google Scholar]
  7. Bassi R, Sharma SS. Proline accumulation in wheat seedlings exposed to zinc and copper. Phytochem. 1993;33:1339–1342. doi: 10.1016/0031-9422(93)85086-7. [DOI] [Google Scholar]
  8. Booth J, Boyland E, Sims P. An enzyme from rat liver catalyzing conjugation. Biochem J. 1961;79:516–524. doi: 10.1042/bj0790516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  10. Brigelius-Flohe R, Flohe L. Is there a role of glutathione peroxidases in signaling and differentiation? Biofactors. 2003;17:93–102. doi: 10.1002/biof.5520170110. [DOI] [PubMed] [Google Scholar]
  11. Cakmak I, Strbac D, Marschner H. Activities of hydrogenperoxide scavenging enzymes in germinating wheat seeds. J Exp Bot. 1993;44:127–132. doi: 10.1093/jxb/44.1.127. [DOI] [Google Scholar]
  12. Chao UH, Seo NH. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci. 2005;168:113–120. doi: 10.1016/j.plantsci.2004.07.021. [DOI] [Google Scholar]
  13. Chao YY, Hong CY, Kao CH (2010) The decline in ascorbic acid is associated with cadmium toxicity of rice seedlings. Plant Physiol Biochem 48:374–381 [DOI] [PubMed]
  14. Chen SL, Kao CH. Glutathione reduces the inhibition of rice seedling root growth caused by cadmium. Plant Growth Regul. 1995;16:249–252. doi: 10.1007/BF00024781. [DOI] [Google Scholar]
  15. Chen TH, Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol. 2002;5:250–257. doi: 10.1016/S1369-5266(02)00255-8. [DOI] [PubMed] [Google Scholar]
  16. Chen C, Wabduragala S, Becker DF, Dickmen MB. Tomato QM-like protein protects Saccromyces cerevisiae cells against oxidative stress by regulation intracellular proline levels. Appl Environ Microbiol. 2006;72:4001–4006. doi: 10.1128/AEM.02428-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Clemens S. Evolution and function of phytochelatin synthases. J Plant Physiol. 2006;163:319–332. doi: 10.1016/j.jplph.2005.11.010. [DOI] [PubMed] [Google Scholar]
  18. Costa G, Morel JL. Water relations, gas exchange and amino acid content in Cd-treated lettuce. Plant Physiol Biochem. 1994;32:561–570. [Google Scholar]
  19. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ. Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci USA. 1986;83:3811–3815. doi: 10.1073/pnas.83.11.3811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. De Gara L, Paciolla C, De Tullio MC, Motto M, Arrigioni O. Ascorbate-dependent hydrogen peroxide detoxification and ascorbate regeneration during germination of a highly productive maize hybrid: evidence of an improved detoxification mechanism against reactive oxygen species. Physiol Plant. 2000;109:7–13. doi: 10.1034/j.1399-3054.2000.100102.x. [DOI] [Google Scholar]
  21. Demiral T, Türkan I. Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol. 2004;161:1089–1100. doi: 10.1016/j.jplph.2004.03.009. [DOI] [PubMed] [Google Scholar]
  22. Dinakar N, Nagajyothi PC, Suresh S, Damodharam T, Suresh C. Cadmium induced changes on proline, antioxidant enzymes, nitrate and nitrite reductases in Arachis hypogaea L. J Environ Biol. 2009;30:289–294. [PubMed] [Google Scholar]
  23. Elia AC, Galarini R, Taticchi MI, Dorr AJM, Manitilacci L. Antioxidant responses and bioaccumulation in Latalurus melas under mercury exposure. Ecotoxicol Environ Saf. 2003;55:162–167. doi: 10.1016/S0147-6513(02)00123-9. [DOI] [PubMed] [Google Scholar]
  24. Eltayeb AE, Kawano N, Badawi G, Kaminaka H, Sanekata T, Morishima I. Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant. 2006;127:57–65. doi: 10.1111/j.1399-3054.2006.00624.x. [DOI] [Google Scholar]
  25. Eltayeb AL, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahar T, Inanaga S, Tanaka K. Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta. 2007;225:1255–1264. doi: 10.1007/s00425-006-0417-7. [DOI] [PubMed] [Google Scholar]
  26. Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell. 2005;17:1866–1875. doi: 10.1105/tpc.105.033589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gechev TS, Van Breusegem F, Stone JM, Denev L, Laloi C. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays. 2006;28:1091–1101. doi: 10.1002/bies.20493. [DOI] [PubMed] [Google Scholar]
  28. Gratao PL, Monteiro CC, Antunes AM, Peres LEP, Azevedo RA. Acquired tolerance to tomato (Lycopersion esculentum cv Miro-Tom) plants to cadmium-induced stress. Ann Appl Biol. 2008;153:321–333. doi: 10.1111/j.1744-7348.2008.00299.x. [DOI] [Google Scholar]
  29. Haluskova L, Valentovicova K, Huttova J, Mistrik I, Tamas L. Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tips. Plant Physiol Biochem. 2009;47:1069–1074. doi: 10.1016/j.plaphy.2009.08.003. [DOI] [PubMed] [Google Scholar]
  30. Heath RL, Packer L. Photoperoxidation in isolated chloroplast.I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;125:189–198. doi: 10.1016/0003-9861(68)90654-1. [DOI] [PubMed] [Google Scholar]
  31. Hoque MA, Banu MNA, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y. Exogenous proline and glycinebetaine ingresses NaCl-induced ascorbate-glutathione cycle enzyme activities and proline improves salt tolerance more than glycinebetaine in tobacco Bright yellow-2 suspension- cultured cells. J. Plant Physiol. 2007;164:553–561. doi: 10.1016/j.jplph.2006.10.004. [DOI] [PubMed] [Google Scholar]
  32. Hossain MA, Fujita M. Purification of glyoxalase I from onion bulbs and molecular cloning of its cDNA. Biosci Biotchnol Biochem. 2009;73:2007–2013. doi: 10.1271/bbb.90194. [DOI] [PubMed] [Google Scholar]
  33. Hossain MA, Fujita M (2010). 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 [DOI] [PMC free article] [PubMed]
  34. Hossain MA, Nakano Y, Asada K. Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol. 1984;25:385–395. [Google Scholar]
  35. Hossain MA, Hossain MZ, Fujita M. Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci. 2009;3:53–64. [Google Scholar]
  36. Hsu YT, Kao CH. Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil. 2007;298:232–241. doi: 10.1007/s11104-007-9357-7. [DOI] [Google Scholar]
  37. Hsu YT, Kao CH. Cadmium induced oxidative damage in rice leaves reduced by polyamines. Plant Soil. 2007;291:27–37. doi: 10.1007/s11104-006-9171-7. [DOI] [Google Scholar]
  38. Hu Y, Ge Y, Zhang C, Ju T, Cheng W. Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment. Plant Growth Regul. 2009;59:51–61. doi: 10.1007/s10725-009-9387-7. [DOI] [Google Scholar]
  39. 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. 2005;56:3041–3049. doi: 10.1093/jxb/eri301. [DOI] [PubMed] [Google Scholar]
  40. Huang Y, Bie Z, Liu Z, Zhen A, Wang W. Protective role of proline against salt stress is partially related to the improvement of water status and peroxidase enzyme activity in cucumber. Soil Sci Plant Nutr. 2009;55:698–704. doi: 10.1111/j.1747-0765.2009.00412.x. [DOI] [Google Scholar]
  41. Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y. Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol. 2010;166:1587–1597. doi: 10.1016/j.jplph.2009.04.002. [DOI] [PubMed] [Google Scholar]
  42. Jain M, Choudhary D, Kale RK, Sarin NB. Salt and glyphosate-induced increase in glyoxalase I activity in cell lines of groundnut (Arachis hypogaea) Physiol Plant. 2002;114:499–505. doi: 10.1034/j.1399-3054.2002.1140401.x. [DOI] [PubMed] [Google Scholar]
  43. Kalapos MP, Garzo T, Antoni F, Mandl J. Accumulation of S-D-lactoylglutathione and transient decrease of glutathione level caused by methylglyoxal load in isolated hepatocytes. Biochim Biophys Acta. 1992;1135:159–64. doi: 10.1016/0167-4889(92)90132-U. [DOI] [PubMed] [Google Scholar]
  44. Khedr AHA, Abbas MA, Wahid AAA, Quick WP, Abogadallah GM. Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot. 2003;54:2553–2562. doi: 10.1093/jxb/erg277. [DOI] [PubMed] [Google Scholar]
  45. Kocsy G, Laurie R, Szalai G, Szilagyi V, Simon-Sarkadi L, Galiba G. Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stresses. Physiol Plant. 2005;124:227–35. doi: 10.1111/j.1399-3054.2005.00504.x. [DOI] [Google Scholar]
  46. Kumar V, Yadav SK. Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress and Camellia sinensis (L.) O.Kuntze. Acta Physiol Plant Plant. 2009;31:261–269. doi: 10.1007/s11738-008-0227-6. [DOI] [Google Scholar]
  47. Kuriakose SV, Prasad MNV. Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul. 2008;54:143–156. doi: 10.1007/s10725-007-9237-4. [DOI] [Google Scholar]
  48. Kuzniak E, Sklodowska M. Compartment-specific role of the ascorbate-glutathione cycle in the response to tomato leaf cells to Botrytis cinerea infection. J Exp Bot. 2005;413:921–933. doi: 10.1093/jxb/eri086. [DOI] [PubMed] [Google Scholar]
  49. Larson RA. The antioxidants of higher plants. Phytochem. 1988;27:969–978. doi: 10.1016/0031-9422(88)80254-1. [DOI] [Google Scholar]
  50. Ma QQ, Wang W, Li YH, Li DQ, Zou Q. Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. J Plant Physiol. 2006;163:165–175. doi: 10.1016/j.jplph.2005.04.023. [DOI] [PubMed] [Google Scholar]
  51. Mallick N, Mohn FH. Reactive oxygen species: response of algal cells. J Plant Physiol. 2000;157:183–193. [Google Scholar]
  52. May MJ, Leaver CJ. Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol. 1993;103:621–627. doi: 10.1104/pp.103.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Mehta SK, Gaur JP. Heavy-metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol. 1999;143:253–259. doi: 10.1046/j.1469-8137.1999.00447.x. [DOI] [Google Scholar]
  54. Mittler R, Vanderauwera S, Gollery M, Breusegem FV. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490–498. doi: 10.1016/j.tplants.2004.08.009. [DOI] [PubMed] [Google Scholar]
  55. Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981;22:867–880. [Google Scholar]
  56. Noctor G. Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ. 2006;29:409–425. doi: 10.1111/j.1365-3040.2005.01476.x. [DOI] [PubMed] [Google Scholar]
  57. Noctor G, Foyer CH. Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol. 1998;49:249–279. doi: 10.1146/annurev.arplant.49.1.249. [DOI] [PubMed] [Google Scholar]
  58. Noctor G, Arisi A, Jouanin L, Kunert KJ, Rennenberg H, Foyer C. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot. 1998;49:623–647. doi: 10.1093/jexbot/49.321.623. [DOI] [Google Scholar]
  59. Noctor G, Gomez L, Vanaker H, Foyer CH. Interactions between biosynthesis, compartmetnation and transport in the control of glutathione homeostasis and signaling. J Exp Bot. 2002;53:1283–1304. doi: 10.1093/jexbot/53.372.1283. [DOI] [PubMed] [Google Scholar]
  60. Nouairi I, Ammar WB, Youssef NB, Miled DDB, Ghorbal MH, Zarrouk M. Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiol Plant. 2009;31:237–247. doi: 10.1007/s11738-008-0224-9. [DOI] [Google Scholar]
  61. Okuma E, Soeda K, Fukuda M, Tada M, Murata Y. Negative correlation between the ratio of K+ to Na+ and proline accumulation in tobacco suspension cells. Soil Sci Plant Nutr. 2002;48:753–757. [Google Scholar]
  62. Okuma E, Murakami Y, Shimoishi Y, Tada M, Murata Y. Effects of exogenous application of proline and betaine on the growth of tobacco cultured cells under saline conditions. Soil Sci Plant Nutr. 2004;50:301–1305. [Google Scholar]
  63. Paradiso A, Berardino R, de Pinto M, di Toppi LS, Storelli FT, de Gara L. Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol. 2008;49:362–374. doi: 10.1093/pcp/pcn013. [DOI] [PubMed] [Google Scholar]
  64. Park EJ, Jeknic Z, Chen THH. Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol. 2006;47:706–714. doi: 10.1093/pcp/pcj041. [DOI] [PubMed] [Google Scholar]
  65. Popova LP, Maslenkova LT, Yordanova RY, Ivanova AP, Krantev AP, Szalai G, Janda T. Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem. 2009;47:224–231. doi: 10.1016/j.plaphy.2008.11.007. [DOI] [PubMed] [Google Scholar]
  66. Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y. Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol. 2004;134:1479–1487. doi: 10.1104/pp.103.033548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Principato GB, 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. 1987;911:349–355. doi: 10.1016/0167-4838(87)90076-8. [DOI] [PubMed] [Google Scholar]
  68. Reisinger S, Schiavon M, Norman T, Pilon-Smits EAH. Heavy metal tolerance and accumulation in Indian mustard (Brassica juncea L.) expressing bacterial gamma-glutamylcysteine synthetase or glutathione synthetase. Int J Phytoremed. 2008;10:1–15. doi: 10.1080/15226510802100630. [DOI] [PubMed] [Google Scholar]
  69. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodriguez-Serrano M, del Rio LA, Palma JM. Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol. 2006;170:43–52. doi: 10.1111/j.1469-8137.2006.01643.x. [DOI] [PubMed] [Google Scholar]
  70. Romero-Puertas M, Corpas FJ, Rodriguez-Serrano M, Gomez M, del Rio AL, Sandalio LM. Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol. 2007;164:1346–1357. doi: 10.1016/j.jplph.2006.06.018. [DOI] [PubMed] [Google Scholar]
  71. Saxena M, Bisht R, Roy DS, Sopory SK, Bhalla-Sarinn M. Cloning and characterization of a mitochondrial glyoxalase II from Brassica juncea that is upregulated by NaCl, Zn and ABA. Biochem Biophys Res Commun. 2005;336:813–819. doi: 10.1016/j.bbrc.2005.08.178. [DOI] [PubMed] [Google Scholar]
  72. Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R. Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol. 2001;127:887–898. doi: 10.1104/pp.010318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Schützendübel A, Nikolova P, Rudolf C, Polle A. Cadmium and H2O2-induced oxidative stress in Populus × canescens roots. Plant Physiol Biochem. 2002;40:577–584. doi: 10.1016/S0981-9428(02)01411-0. [DOI] [Google Scholar]
  74. Sekmen AH, Türkan I, Takio S. Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant. 2007;131:399–411. doi: 10.1111/j.1399-3054.2007.00970.x. [DOI] [PubMed] [Google Scholar]
  75. Semane B, Cuypers A, Smeets K, Van Belleghem F, Horemans F, Schat H, Vangronsveld J. Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiol Plant. 2007;129:519–528. doi: 10.1111/j.1399-3054.2006.00822.x. [DOI] [Google Scholar]
  76. Shalata A, Mittova V, Volokita M, Guy M, Tal M. Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant. 2001;112:487–494. doi: 10.1034/j.1399-3054.2001.1120405.x. [DOI] [PubMed] [Google Scholar]
  77. Shao G, Chen M, Wang W, Zhang G. The effect of salinity pretreatment on Cd accumulation and Cd-induced stress in BADH-transgenic and nontransgenic rice seedlings. J Plant Growth Regul. 2008;27:205–210. doi: 10.1007/s00344-008-9047-6. [DOI] [Google Scholar]
  78. Singla-Pareek SL, Ray M, Reddy MK, Sopory SK. Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proc Natl Acad Sci USA. 2003;100:14672–14677. doi: 10.1073/pnas.2034667100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK. Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol. 2006;140:613–623. doi: 10.1104/pp.105.073734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK. Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Transgenic Res. 2008;17:171–180. doi: 10.1007/s11248-007-9082-2. [DOI] [PubMed] [Google Scholar]
  81. Siripornadulsil S, Traina S, Verma DPS, Sayre RT. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell. 2002;14:2837–2847. doi: 10.1105/tpc.004853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Smeets K, Ruytinx J, Semane B, Belleghem FV, Remans T, Sanden SV, Vangronsveld J, Cupers A. Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot. 2008;63:1–8. doi: 10.1016/j.envexpbot.2007.10.028. [DOI] [Google Scholar]
  83. Smirnoff N. Ascorbic acid: metabolism and functions of a multifaceted molecule. Curr Opin Plant Biol. 2000;3:229–235. [PubMed] [Google Scholar]
  84. Song XS, Hu WH, Mao WH, Ogweno JO, Zhou YH, Yu JQ. Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. Plant Physiol Biochem. 2005;43:1082–1088. doi: 10.1016/j.plaphy.2005.11.003. [DOI] [PubMed] [Google Scholar]
  85. Subbarao GV, Wheeler RM, Levine LH, Stutte GW. Glycinebetaine accumulation, ionic and water relations of red-beet at contrasting levels of sodium supply. J Plant Physiol. 2001;158:767–776. doi: 10.1078/0176-1617-00309. [DOI] [PubMed] [Google Scholar]
  86. Sun RL, Zhou QX, Sun FH, Jin CX. Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot. 2007;60:468–476. doi: 10.1016/j.envexpbot.2007.01.004. [DOI] [Google Scholar]
  87. Tamas L, Dudikova J, Durcekova K, Haluskova L, Huttova J, Mistrik I, Olle M. Alteration of the gene expression, lipid peroxidation, proline and thiol content along the barley root exposed to cadmium. J Plant Physiol. 2008;165:1193–1203. doi: 10.1016/j.jplph.2007.08.013. [DOI] [PubMed] [Google Scholar]
  88. Tamás L, Mistrík I, Huttová J, Halusková L, Valentovicová K, Zelinová V. Role of reactive oxygen species-generating enzymes and hydrogen peroxide during cadmium, mercury and osmotic stresses in barley root tip. Planta. 2010;231:221–231. doi: 10.1007/s00425-009-1042-z. [DOI] [PubMed] [Google Scholar]
  89. Tamura T, Hara K, Yamaguchi Y, Koizumi N, Sano H. Osmotic stress tolerance of transgenic tobacco expressing a gene encoding a membrane-located receptor-like protein from tobacco plants. Plant Physiol. 2003;131:454–462. doi: 10.1104/pp.102.011007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Veena, Reddy VS, Sopory SK. Glyoxalase I from Brassica juncea: molecular cloning, regulation and its over-expression confer tolerance in transgenic tobacco under stress. Plant J. 1999;17:385–395. doi: 10.1046/j.1365-313X.1999.00390.x. [DOI] [PubMed] [Google Scholar]
  91. Wang Z, Zhang Y, Huang Z, Huang L. Antioxidant response of metal-accumulator and non-accumulator plants under cadmium stress. Plant Soil. 2008;310:137–149. doi: 10.1007/s11104-008-9641-1. [DOI] [Google Scholar]
  92. Wang Z, Zhang L, Xiao Y, Chen W, Tang K. Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol. 2010;52:400–409. doi: 10.1111/j.1744-7909.2010.00921.x. [DOI] [PubMed] [Google Scholar]
  93. Witzel K, Weidner A, Surabhi GK, Börner A, Mock HP. Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot. 2009;60:3546–3557. doi: 10.1093/jxb/erp198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Xiang C, Oliver DJ. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic aicd in Arabidopsis. Plant Cell. 1998;10:1539–1550. doi: 10.1105/tpc.10.9.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Xu J, Yin HX, Li X. Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep. 2009;28:325–353. doi: 10.1007/s00299-008-0643-5. [DOI] [PubMed] [Google Scholar]
  96. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK. Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun. 2005;337:61–67. doi: 10.1016/j.bbrc.2005.08.263. [DOI] [PubMed] [Google Scholar]
  97. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK. Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett. 2005;579:6265–6271. doi: 10.1016/j.febslet.2005.10.006. [DOI] [PubMed] [Google Scholar]
  98. Yang X, Lu C. Photosynthesis is improved by exogenous glycinebetaine in salt-stressed maize plants. Physiol Plant. 2005;124:343–352. doi: 10.1111/j.1399-3054.2005.00518.x. [DOI] [Google Scholar]
  99. Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta. 2007;225:719–733. doi: 10.1007/s00425-006-0380-3. [DOI] [PubMed] [Google Scholar]
  100. Yu CW, Murphy TM, Lin CH. Hydrogen peroxide-induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol. 2003;30:955–963. doi: 10.1071/FP03091. [DOI] [PubMed] [Google Scholar]
  101. Zhao ZQ, Cai YL, Zhu YG, Kneer R. Cadmium-induced oxidative stress and protection by L-Galactono-1, 4-lactone in winter wheat (Triticum aestivum L.) Plant Nutr Soil Sci. 2005;168:759–763. doi: 10.1002/jpln.200520513. [DOI] [Google Scholar]
  102. Zhu YL, Pilon-Smits EAH, Tarun A, Weber SU, Jouanin L, Terry N. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol. 1999;121:1169–1177. doi: 10.1104/pp.121.4.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]

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