Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean

doi:10.1007/s11703-010-1070-2

Front Agric Chin

2011, Vol. 5

Issue (1) : 1-14 https://doi.org/10.1007/s11703-010-1070-2

RESEARCH ARTICLE

Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean

Mohammad Anwar HOSSAIN^1,2, Mirza HASANUZZAMAN^1,3, Masayuki FUJITA¹(

)

1. Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Miki-cho, Kita-gun, Kagawa 761-0795, Japan; 2. Department of Genetics & Plant Breeding, Bangladesh Agricultural University, Mymensingh- 2202, Bangladesh; 3. Department of Agronomy, Sher-e-Bangla Agricultural University, Dhaka-1207, Bangladesh

Download: PDF(516 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

The purpose of this study was to assess the synergistic effects of exogenously applied proline and glycinebetaine (betaine) in antioxidant defense and methylglyoxal (MG) detoxification system in mung bean seedlings subjected to salt stress (200 mmol·L^-1 NaCl, 48 h). Seven-day-old mung bean seedlings were exposed to salt stress after pre-treatment with proline or betaine. Salt stress caused a sharp increase in reduced glutathione (GSH) and oxidized glutathione (GSSG) content in leaves, while the GSH/GSSG ratio and ascorbate (AsA) content decreased significantly. The glutathione reductase (GR), glutathione peroxidase (GPX), glutathione S-transferase (GST) and glyoxalase II (Gly II) activities were increased in response to salt stress, while the monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), catalase (CAT) and glyoxalase I (Gly I) activities sharply decreased with an associated increase in hydrogen peroxide (H₂O₂) and lipid peroxidation level (MDA). Proline or betaine pre-treatment had little influence on non-enzymatic and enzymatic components as compared to those of the untreated control. However, proline or betaine pre-treated salt-stressed seedlings showed an increase in AsA, GSH content, GSH/GSSG ratio and maintained higher activities of APX, DHAR, GR, GST, GPX, CAT, Gly I and Gly II involved in ROS and MG detoxification system as compared to those of the untreated control and mostly also salt-stressed plants with a simultaneous decrease in GSSG content, H₂O₂ and MDA level. These results together with our previous results suggest that coordinate induction of antioxidant defense and glyoxalase system by proline and betaine rendered the plants tolerant to salinity-induced oxidative stress in a synergistic fashion.

Keywords salt stress reactive oxygen species antioxidant defense methylglyoxal detoxification system glycinebetaine proline mung bean

Corresponding Author(s): FUJITA Masayuki,Email:fujita@ag.kagawa-u.ac.jp

Issue Date: 05 March 2011

Cite this article:

Mohammad Anwar HOSSAIN,Mirza HASANUZZAMAN,Masayuki FUJITA. Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean[J]. Front Agric Chin, 2011, 5(1): 1-14.

URL:

https://academic.hep.com.cn/fag/EN/10.1007/s11703-010-1070-2
https://academic.hep.com.cn/fag/EN/Y2011/V5/I1/1

Fig.1 Schematic illustration of possible metabolic interaction of antioxidant defense and MG detoxification systems in plant cells
Note: Abbreviations are defined in the text.

Fig.2 Reduced ascorbate (AsA) contents in mung bean seedlings induced by proline and betaine under salt stress conditions
Note: Na, P, B, Na+ P and Na+ B indicates 200 mmol·L NaCl, 5 mmol·L proline, 5 mmol·L betaine, 200 mmol·L NaCl+ 5 mmol·L proline and 200 mmol·L NaCl+ 5 mmol·L betaine treatments, respectively. Mean (±SD) is calculated from three independent experiments. Bars with different letters are significantly different at <0.05.

Fig.3 Glutathione accumulation in mung bean seedlings induced by proline and betaine under salt stress conditions
Note: A is reduced glutathione (GSH), B is oxidized glutathione (GSSG) and C is GSH/GSSG ratio. Na, P, B, Na+ P and Na+ B indicate 200 mmol·L NaCl, 5 mmol·L proline, 5 mmol·L betaine, 200 mmol·L NaCl+ 5 mmol·L proline and 200 mmol·L NaCl+ 5 mmol·L betaine treatments, respectively. Mean (±SD) is calculated from three independent experiments. Bars with different letters are significantly different at <0.05.

Fig.4 Activities of APX (A), MDHAR (B), DHAR (C), GR (D), GPX (E), GST (F) and CAT (G) in mung bean seedlings induced by proline and betaine under salt stress conditions
Note: Na, P, B, Na+ P and Na+ B indicates 200 mmol·L NaCl, 5 mmol·L proline, 5 mmol·L betaine, 200 mmol·L NaCl+ 5 mmol·L proline and 200 mmol·L NaCl+ 5 mmol·L betaine treatments, respectively. Mean (±SD) is calculated from three independent experiments. Bars with different letters are significantly different at <0.05.

Fig.5 Activities of Gly I (A) and Gly II (B) in mung bean seedlings induced by proline and betaine under salt stress conditions
Note: Na, P, B, Na+ P and Na+ B indicate 200 mmol·L NaCl, 5 mmol·L proline, 5 mmol·L betaine, 200 mmol·L NaCl+ 5 mmol·L proline and 200 mmol·L NaCl+ 5 mmol·L betaine treatments, respectively. Mean (±SD) is calculated from three independent experiments. Bars with different letters are significantly different at <0.05.

Fig.6 Changes in HO concentration (A) and lipid peroxidation (represented by MDA) (B) level in mung bean seedlings induced by proline and betaine under salt stress conditions
Note: Na, P, B, Na+ P and Na+ B indicates 200 mmol·L NaCl, 5 mmol·L proline, 5 mmol·L betaine, 200 mmol·L NaCl+ 5 mmol·L proline and 200 mmol·L NaCl+ 5 mmol·L betaine treatments, respectively. Mean (±SD) is calculated from three independent experiments. Bars with different letters are significantly different at <0.05.

1	Aghaei K, Ehsanpour A A, Komatsu S (2009). Potato responds to salt stress by increased activity of antioxidant enzymes. J Integr Plant Biol , 51(12): 1095–1103 doi: 10.1111/j.1744-7909.2009.00886.x pmid:20021557
2	Ahmad P, Jaleel C A, Sharma R (2010a). Antioxidant defense system, lipid Peroxidation, proline-metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. Russ J Plant Physiol , 57(4): 509–517 doi: 10.1134/S1021443710040084
3	Ahmad R, Kim Y H, Kim M D, Kwon S Y, Cho K, Lee H S, Kwak S S (2010b). Simultaneous expression of choline oxidase, superoxide dismutase and ascorbate peroxidase in potato plant chloroplasts provides synergistically enhanced protection against various abiotic stresses. Physiol Plant , 138(4): 520–533 doi: 10.1111/j.1399-3054.2010.01348.x pmid:20059737
4	Apel K, Hirt H (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol , 55(1): 373–399 doi: 10.1146/annurev.arplant.55.031903.141701 pmid:15377225
5	Aravind P A, Prasad M N (2005). Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant Physiol Biochem , 43(2): 107–116 15820657 doi: 10.1016/j.plaphy.2005.01.002
6	Asada K (1999). The water–water cycle in chloroplasts: Scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol , 50(1): 601–639 doi: 10.1146/annurev.arplant.50.1.601 pmid:15012221
7	Athar H R, Khan A, Ashraf M (2008). Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ Exp Bot , 63(1-3): 224–231 doi: 10.1016/j.envexpbot.2007.10.018
8	Ben Ahmed C, Ben Rouina B, Sensoy S, Boukhriss M, Ben Abdullah F (2010). Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem , 58(7): 4216–4222 doi: 10.1021/jf9041479 pmid:20210359
9	Bradford M 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(1-2): 248–254 doi: 10.1016/0003-2697(76)90527-3 pmid:942051
10	Creighton D J, Migliorini M, Pourmotabbed T, Guha M K (1988). Optimization of efficiency in the glyoxalase pathway. Biochemistry , 27(19): 7376–7384 doi: 10.1021/bi00419a031 pmid:3207683
11	Dalton D A, Boniface C, Turner Z, Lindahl A, Kim H J, Jelinek L, Govindarajulu M, Finger R E, Taylor C G (2009). Physiological roles of glutathione S-transferases in soybean root nodules. Plant Physiol , 150(1): 521–530 doi: 10.1104/pp.109.136630 pmid:19279195
12	Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000). Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci , 57(5): 779–795 10892343 doi: 10.1007/s000180050041
13	De Gara L, Paciolla C, De Tullio M C, Motto M, Arrigioni O (2000). 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 , 109(1): 7–13 doi: 10.1034/j.1399-3054.2000.100102.x
14	Demiral T, Türkan I (2004). Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? J Plant Physiol , 161(10): 1089–1100 doi: 10.1016/j.jplph.2004.03.009 pmid:15535118
15	Desingh R, Kanagaraj G (2007). Influence of salinity stress on photosynthesis and antioxidative systems in two cotton varieties. Gen Appl Plant Physiol , 33: 221–234
16	El-Shabrawi H, Kumar B, Kaul T, Reddy M K, Singla-Pareek S L, Sopory S K (2010). Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma , 245(1-4): 85–96 doi: 10.1007/s00709-010-0144-6 pmid:20419461
17	Eltayeb A E, Kawano N, Badawi G, Kaminaka H, Sanekata T, Morishima I, Shibahara T, Inanaga S, Tanaka K (2006). Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant , 127(1): 57–65 doi: 10.1111/j.1399-3054.2006.00624.x
18	Eltayeb A E, Kawano N, Badawi G H, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007). Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta , 225(5): 1255–1264 doi: 10.1007/s00425-006-0417-7 pmid:17043889
19	Eshdat Y, Holland D, Faltin Z, Ben-Hayyim G (1997). Plant glutathione peroxidases. Physiol Plant , 100(2): 234–240 doi: 10.1111/j.1399-3054.1997.tb04779.x
20	Fujita M, Hossain M Z (2003). Modulation of pumpkin glutathione S-transferases by aldehydes and related compounds. Plant Cell Physiol , 44(5): 481–490 doi: 10.1093/pcp/pcg060 pmid:12773634
21	Gueta-Dahan Y, Yaniv Z, Zilinskas B A, Ben-Hayyim G (1997). Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta , 203(4): 460–469 doi: 10.1007/s004250050215 pmid:9421931
22	Halusková L, Valentovicová K, Huttová J, Mistrík I, Tamás L (2009). Effect of abiotic stresses on glutathione peroxidase and glutathione S-transferase activity in barley root tips. Plant Physiol Biochem , 47(11-12): 1069–1074 doi: 10.1016/j.plaphy.2009.08.003 pmid:19733091
23	Hare P D, Cress W A, van Staden J (1998). Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ , 21(6): 535–553 doi: 10.1046/j.1365-3040.1998.00309.x
24	Heath R L, Packer L (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys , 125(1): 189–198 doi: 10.1016/0003-9861(68)90654-1 pmid:5655425
25	Hernández J A, Jimenez A, Millineaus P, Sevilla F (2000). Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ , 23(8): 853–862 doi: 10.1046/j.1365-3040.2000.00602.x
26	Hoque M A, Banu M N A, Nakamura Y, Shimoishi Y, Murata Y (2008). Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol , 165(8): 813–824 doi: 10.1016/j.jplph.2007.07.013 pmid:17920727
27	Hoque M A, Banu M N A, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2007). 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 , 164(11): 553–561 doi: 10.1016/j.jplph.2006.10.004 pmid:16650912
28	Hossain M A, Fujita M (2009). Purification of glyoxalase I from onion bulbs and molecular cloning of its cDNA. Biosci Biotechnol Biochem , 73(9): 2007–2013 doi: 10.1271/bbb.90194 pmid:19734676
29	Hossain M A, 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(1): 19–29 doi: 10.1007/s12298-010-0003-0
30	Hossain M A, 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 (in press) doi: 10.1007/s12298-010-0028-4
31	Hossain M A, Hossain M Z, Fujita M (2009). Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci , 3(2): 53–64
32	Hossain M A, Nakano Y, Asada K (1984). Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol , 25(3): 385–395
33	Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005). Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. J Exp Bot , 56(422): 3041–3049 doi: 10.1093/jxb/eri301 pmid:16263910
34	Huang Y, Bie Z, Liu Z, Zhen A, Wang W (2009). 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 , 55(5): 698–704 doi: 10.1111/j.1747-0765.2009.00412.x
35	Jain M, Choudhary D, Kale R K, Bhalla-Sarin N (2002). Salt- and glyphosate-induced increase in glyoxalase I activity in cell lines of groundnut (Arachis hypogaea). Physiol Plant , 114(4): 499–505 doi: 10.1034/j.1399-3054.2002.1140401.x pmid:11975722
36	Ji W, Zhu Y, Li Y, Yang L, Zhao X, Cai H, Bai X (2010). Over-expression of a glutathione S-transferase gene, GsGST, from wild soybean (Glycine soja) enhances drought and salt tolerance in transgenic tobacco. Biotechnol Lett , 32(8): 1173–1179 doi: 10.1007/s10529-010-0269-x pmid:20383560
37	Khan M A, Panda S K (2008). Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiol Plant , 30(1): 81–89 doi: 10.1007/s11738-007-0093-7
38	Khan N A, Syeed S, Masood A, Nazar R, Iqbal N (2010). Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity. Int J Plant Biol , 1: 1–8
39	Khedr A H A, Abbas M A, Wahid A A A, Quick W P, Abogadallah G M (2003). Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot , 54(392): 2553–2562 doi: 10.1093/jxb/erg277 pmid:14512386
40	Kocsy G, Laurie R, Szalai G, Szilágyi V, Simon-Sarkadi L, Galiba G, de Ronde J A (2005). Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stresses. Physiol Plant , 124(2): 227–235 doi: 10.1111/j.1399-3054.2005.00504.x
41	Kumar V, Yadav S K (2009). Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress and Camellia sinensis (L.) O. Kuntze. Acta Physiol Plant , 31(2): 261–269 doi: 10.1007/s11738-008-0227-6
42	Lin S H, Liu Z J, Xu P L, Fang Y Y, Bai J G (2010). Paraquat pre-treatment increases activities of antioxidant enzymes and reduces lipid peroxidation in salt-stressed cucumber leaves. Acta Physiol Plant (in press) doi: 10.1007/s11738-010-0547-1
43	Mallick N, Mohn F H (2000). Reactive oxygen species: response of algal cells. J Plant Physiol , 157(2): 183–193
44	Martins A M T B S, Cordeiro C A A, Ponces Freire A M (2001). In situ analysis of methylglyoxal metabolism in Saccharomyces cerevisiae. FEBS Lett , 499(1-2): 41–44 doi: 10.1016/S0014-5793(01)02519-4 pmid:11418108
45	May M J, Leaver C J (1993). Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol , 103(2): 621–627 pmid:12231968
46	McNeil S D, Nuccio M L, Ziemak M J, Hanson A D (2001). Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc Natl Acad Sci USA , 98(17): 10001–10005 doi: 10.1073/pnas.171228998 pmid:11481443
47	Meloni D A, Martinez C A (2010). Glycinebetaine improves salt tolerance in vinal (Prosopis ruscifolia Griesbach) seedlings. Braz J Plant Physiol , 21: 233–241
48	Mittova V, Tal M, Volokita M, Guy M (2003a). Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ , 26(6): 845–856 doi: 10.1046/j.1365-3040.2003.01016.x pmid:12803612
49	Mittova V, Theodoulou F L, Kiddle G, Gómez L, Volokita M, Tal M, Foyer C H, Guy M (2003b). Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett , 554(3): 417–421 doi: 10.1016/S0014-5793(03)01214-6 pmid:14623104
50	Molinari H B C, Marur C J, Bespalhok J C, Kobayashi A K, Pileggi M, Pereira F P P, Vieira L G E (2004). Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. × Poncirus trifoliate L. Raf.) overproducing proline. Plant Sci , 167(6): 1375–1381 doi: 10.1016/j.plantsci.2004.07.007
51	Munns R (2005). Genes and salt tolerance: bringing them together. New Phytol , 167(3): 645–663 doi: 10.1111/j.1469-8137.2005.01487.x pmid:16101905
52	Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol , 22(5): 867–880
53	Newaz K, Ashraf M (2010). Exogenous application of glycinebetaine modulates activities of antioxidants in maize plants subjected to salt stress. J Agron Crop Sci , 196(1): 28–37 doi: 10.1111/j.1439-037X.2009.00385.x
54	Noctor G, Arisi A, Jouanin L, Kunert K J, Rennenberg H, Foyer C (1998). Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot , 49(321): 623–647 doi: 10.1093/jexbot/49.321.623
55	Noctor G, Foyer C H (1998). Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol , 49(1): 249–279 doi: 10.1146/annurev.arplant.49.1.249 pmid:15012235
56	Noctor G, Gomez L, Vanacker H, Foyer C H (2002). Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot , 53(372): 1283–1304 doi: 10.1093/jexbot/53.372.1283 pmid:11997376
57	Paradiso A, Berardino R, de Pinto M C, Sanità di Toppi L, Storelli M M, Tommasi F, De Gara L (2008). Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol , 49(3): 362–374 doi: 10.1093/pcp/pcn013 pmid:18234716
58	Parida A K, Jha B (2010). Antioxidative defense potential to salinity in the euhalophyte Salicornia brachiata. J Plant Growth Regul , 29(2): 137–148 doi: 10.1007/s00344-009-9129-0
59	Pérez-López U, Robredo A, Lacuesta M, Sgherri C, Mu?oz-Rueda A, Navari-Izzo F, Mena-Petite A (2009). The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO₂. Physiol Plant , 135(1): 29–42 doi: 10.1111/j.1399-3054.2008.01174.x pmid:19121097
60	Potters G, Horemans N, Bellone S, Caubergs R J, Trost P, Guisez Y, Asard H (2004). Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol , 134(4): 1479–1487 doi: 10.1104/pp.103.033548 pmid:15047900
61	Ray S, Dutta S, Halder J, Ray M (1994). Inhibition of electron flow through complex I of the mitochondrial respiratory chain of Ehrlich ascites carcinoma cells by methylglyoxal. Biochem J , 303: 69–72 pmid:7945267
62	Raza H, Athar H R, Ashraf M, Hameed A (2007). Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance. Environ Exp Bot , 60(3): 368–376 doi: 10.1016/j.envexpbot.2006.12.009
63	Saha P, Chatterjee P, Biswas A K (2010). NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata L. Wilczek). Indian J Exp Biol , 48(6): 593–600 pmid:20882762
64	Saxena M, Bisht R, Roy S D, Sopory S K, Bhalla-Sarin N (2005). Cloning and characterization of a mitochondrial glyoxalase II from Brassica juncea that is upregulated by NaCl, Zn, and ABA. Biochem Biophys Res Commun , 336(3): 813–819 doi: 10.1016/j.bbrc.2005.08.178 pmid:16153601
65	Secenji M, Hideg E, Bebes A, Gy?rgyey J (2010). Transcriptional differences in gene families of the ascorbate-glutathione cycle in wheat during mild water deficit. Plant Cell Rep , 29(1): 37–50 doi: 10.1007/s00299-009-0796-x pmid:19902215
66	Sekmen A H, Türkan I, Takio S (2007). Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant , 131(3): 399–411 doi: 10.1111/j.1399-3054.2007.00970.x pmid:18251879
67	Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001). Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: The root antioxidative system. Physiol Plant , 112(4): 487–494 doi: 10.1034/j.1399-3054.2001.1120405.x pmid:11473708
68	Shalata A, Neumann P M (2001). Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot , 52(364): 2207–2211 pmid:11604460
69	Singla-Pareek S L, Reddy M K, Sopory S K, Sopory S K (2003). Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proc Natl Acad Sci USA , 100(25): 14672–14677 doi: 10.1073/pnas.2034667100 pmid:14638937
70	Singla-Pareek S L, Yadav S K, Pareek A, Reddy M K, Sopory S K (2006). Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol , 140(2): 613–623 doi: 10.1104/pp.105.073734 pmid:16384901
71	Singla-Pareek S L, Yadav S K, Pareek A, Reddy M K, Sopory S K (2008). Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Transgenic Res , 17(2): 171–180 doi: 10.1007/s11248-007-9082-2 pmid:17387627
72	Smirnoff N (2000). Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol , 3(3): 229–235 pmid:10837263
73	Sobhanian H, Motamed N, Jazii F R, Nakamura T, Komatsu S (2010). Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C₄ plant. J Proteome Res , 9(6): 2882–2897 doi: 10.1021/pr900974k pmid:20397718
74	Song X S, Hu W H, Mao W H, Ogweno J O, Zhou Y H, Yu J Q (2005). Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. Plant Physiol Biochem , 43(12): 1082–1088 doi: 10.1016/j.plaphy.2005.11.003 pmid:16386429
75	Sudhakar C L, Akshm A, Giridarakumar S (2001). Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci , 161(3): 613–619 doi: 10.1016/S0168-9452(01)00450-2
76	Sumithra K, Jutur P P, Carmel B D, Reddy A R (2006). Salinity-induced changes in two cultivars of vigna rediata: responses of antioxidative and proline metabolism. Plant Growth Regul , 50(1): 11–22 doi: 10.1007/s10725-006-9121-7
77	Tanou G, Molassiotis A, Diamantidis G (2009). Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot , 65(2-3): 270–281 doi: 10.1016/j.envexpbot.2008.09.005
78	Thornalley P J (1990). The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J , 269(1): 1–11 pmid:2198020
79	Thornalley P J (1996). Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification: a role in pathogenesis and antiproliferative chemotherapy. Gen Pharmacol , 27(4): 565–573 doi: 10.1016/0306-3623(95)02054-3 pmid:8853285
80	Veena, Reddy V S, Sopory S K (1999). Glyoxalase I from Brassica juncea: molecular cloning, regulation and its over-expression confer tolerance in transgenic tobacco under stress. The Plant J , 17: 385–395
81	Wang W, Vinocur B, Altman A (2003). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta , 218(1): 1–14 doi: 10.1007/s00425-003-1105-5 pmid:14513379
82	Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2010). Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol , 52(4): 400–409 doi: 10.1111/j.1744-7909.2010.00921.x pmid:20377702
83	Wu L, Juurlink B H J (2002). Increased methylglyoxal and oxidative stress in hypertensive rat vascular smooth muscle cells. Hypertension , 39(3): 809–814 doi: 10.1161/hy0302.105207 pmid:11897769
84	Xu J, Yin H X, Li X (2009). Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep , 28(2): 325–333 doi: 10.1007/s00299-008-0643-5 pmid:19043719
85	Yadav S K, Singla-Pareek S L, Ray M, Reddy M K, Sopory S K (2005a). Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun , 337(1): 61–67 doi: 10.1016/j.bbrc.2005.08.263 pmid:16176800
86	Yadav S K, Singla-Pareek S L, Reddy M K, Sopory S K, Sopory S K (2005b). Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett , 579(27): 6265–6271 doi: 10.1016/j.febslet.2005.10.006 pmid:16253241
87	Yoshimura K, Miyao K, Gaber A, Takeda T, Kanaboshi H, Miyasaka H, Shigeoka S (2004). Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J , 37(1): 21–33 doi: 10.1046/j.1365-313X.2003.01930.x pmid:14675429
88	Yu C W, Murphy T M, Sung W W, Lin C H (2002). H₂O₂ treatment induces glutathione accumulation and chilling tolerance in mung bean. Funct Plant Biol , 29(9): 1081–1087 doi: 10.1071/PP01264
89	Zhu J K (2002). Salt and drought stress signal transduction in plants. Annu Rev Plant Biol , 53(1): 247–273 doi: 10.1146/annurev.arplant.53.091401.143329 pmid:12221975

[1]	Qingjuan NIE, Zhigang WANG, Zhibin REN, Dazhuang HUANG. Effect of salt stress on the physiological and photosynthetic characteristics of Weigela florida[J]. Front Agric Chin, 2011, 5(4): 655-661.
[2]	WU Qiangsheng, ZOU Yingning, XIA Renxue. Effect of Glomus versiforme inoculation on reactive oxygen metabolism of Citrus tangerine leaves exposed to water stress[J]. Front. Agric. China, 2007, 1(4): 438-443.
[3]	WANG Suping, JIA Yongxia, GUO Shirong, ZHOU Guoxian. Effects of polyamines on K+, Na+ and Cl– content and distribution in different organs of cucumber (Cucumis sativus L.) seedlings under NaCl stress[J]. Front. Agric. China, 2007, 1(4): 430-437.
[4]	Xuezheng WANG,Hua WANG,Fengzhi WU,Bo LIU. Effects of cinnamic acid on the physiological characteristics of cucumber seedlings under salt stress[J]. Front. Agric. China, 2007, 1(1): 58-61.

Viewed

Full text

Abstract

Cited

Shared

Discussed