Missing links in understanding redox signaling via thiol/disulfide modulation: How is glutathione oxidized in plants?

Frontiers in Plant Science

Volumn 4, Issue NOV, 2013, Pages

  Rahantaniaina, Marie Sylviane ^a,b   Tuzet, Andrée ^b   Mhamdi, Amna ^a   Noctor, Graham ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CEMAGREF   (France)

Author keywords

Dehydroascorbate; Glutaredoxin; Glutathione S transferase; Hydrogen peroxide; Oxidative stress

Indexed keywords

EID: 84898750982     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00477     Document Type: Review

References (105)

1. Amako, K., Ushimaru, T., Ishikawa, A., Ogishi, Y., Kishimoto, R., and Goda, K. (2006). Heterologous expression of dehydroascorbate reductase from rice and its application to determination of dehydroascorbate concentrations. J. Nutr. Sci. Vitaminol. 52, 89-95. doi: 10.3177/jnsv.52.89
2. Asada, K., and Takahashi, M. (1987). "Production and scavenging of active oxygen species in photosynthesis, " in Photoinhibition, eds D. Kyle, C. Osmond, and C. Arntzen (NewYork, NY: Elsevier Science Publishers), 227-287.
3. Barranco-Medina, S., Krell, T., Finkemeier, I., Sevilla, F., Lázaro, J. J., and Dietz, K. J. (2007). Biochemical and molecular characterization of the mitochondrial peroxiredoxin PsPrxII F from Pisum sativum. Plant Physiol. Biochem. 45, 729-739. doi: 10.1016/j.plaphy.2007.07.017
4. Barroso, J. B., Corpas, F. J., Carreras, A., Rodríguez-Serrano, M., Esteban, F. J., Fernández-Ocaòa, A., et al. (2006). Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J. Exp. Bot. 57, 1785-1793. doi: 10.1093/jxb/erj175
5. Bernier-Villamor, L., Navarro, E., Sevilla, F., and Lázaro, J. J. (2004). Cloning and characterization of a 2-Cys peroxiredoxin from Pisum sativum. J. Exp. Bot. 55, 2191-2199. doi: 10.1093/jxb/erh238
6. Bick, J. A., Aslund, F., Chen, Y., and Leustek, T. (1998). Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5'-adenylylsulfate reductase. Proc. Natl. Acad. Sci. U.S.A. 95, 8404-8409. doi: 10.1073/pnas.95.14.8404
7. Bick, J. A., Setterdahl, A. T., Knaff, D. B., Chen, Y., Pitcher, L. H., Zilinskas, B. A., et al. (2001). Regulation of the plant-type 5'-adenylyl sulfate reductase by oxidative stress. Biochemistry 40, 9040-9048. doi: 10.1021/bi010518v
8. Bors, W., Heller, W., Michel, C., and Saran, M. (1990). "Flavonoids as antioxidants: determination of radical-scavenging efficiencies, " in Oxygen Radicals in Biological Systems: Oxygen Radicals and Antioxidants, Methods in Enzymology, Vol. 186, eds L. Packer and A. N. Glazer (New York, NY: Elsevier Science Publishers), 343-355. doi: 10.1016/0076-6879(90)86128-I
9. Bréhélin, C., Meyer, E. H., de Souris, J. P., Bonnard, G., and Meyer, Y. (2003). Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: similar sequences for divergent gene expression, protein localization, and activity. Plant Physiol. 132, 2045-2057. doi: 10.1104/pp.103.022533
10. Cairns, N. G., Pasternak, M., Wachter, A., Cobbett, C. S., and Meyer, A. J. (2006). Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol. 141, 446-455. doi: 10.1104/pp.106.077982
11. Chaouch, S., Queval, G., Vanderauwera, S., Mhamdi, A., Vandorpe, M., Langlois-Meurinne, M., et al. (2010). Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE 1 in a daylength-related manner. Plant Physiol. 153, 1692-1705. doi: 10.1104/pp.110.153957
12. Chen, J. H., Jiang, H. W., Hsieh, E. J., Chen, H. Y., Chien, C. T., Hsieh, H. L., et al. (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. doi: 10.1104/pp.111.181875
13. Chen, Z., and Gallie, D. R. (2005). Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. Plant Physiol. 138, 1673-1689. doi: 10.1104/pp.105.062000
14. Chew, O., Whelan, J., and Millar, A. H. (2003). Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem. 278, 46869-46877. doi: 10.1074/jbc.M307525200
15. Collin, V., Lamkemeyer, P., Miginiac-Maslow, M., Hirasawa, M., Knaff, D. B., Dietz, K. J., et al. (2004). Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol. 136, 4088-4095. doi: 10.1104/pp.104.052233
16. Couturier, J., Ströher, E., Albetel, A. N., Roret, T., Muthuramalingam, M., Tarrago, L., et al. (2011). Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J. Biol. Chem. 286, 27515-27527. doi: 10.1074/jbc.M111.228726
17. Cummins, I., Cole, D. J., and Edwards, R. (1999). A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J. 18, 285-292. doi: 10.1046/j.1365-313X.1999.00452.x
18. Cummins, I., Hagan, D. O., Jablonkai, I., Cole, D. J., Hehn, A., Werck-Reichhart, D., et al. (2003). Cloning, characterization and regulation of family of phi class glutathione transferases from wheat. Plant Mol. Biol. 52, 591-603. doi: 10.1023/A:1024858218804
19. Dayer, R., Fischer, B. B., Eggen, R. I. L., and Lemaire, S. D. (2008). The peroxiredoxin and glutathione peroxidase families in Chlamydomonas reinhardtii. Genetics 179, 41-57. doi: 10.1534/genetics.107.086041
20. DeRidder, B. P., Dixon, D. P., Beussman, D. J., Edwards, R., and Goldsbrough, P. B. (2002). Induction of glutathione S-transferases in Arabidopsis by herbicide safeners. Plant Physiol. 130, 1497-1505. doi: 10.1104/pp.010066
21. Dghim, A. A., Mhamdi, A., Vaultier, M. V., Hasenfratz-Sauder, M. P., Le Thiec, D., Dizengremel, P., et al. (2013). Analysis of cytosolic isocitrate dehydrogenase and glutathione reductase 1 in photoperiod-influenced responses to ozone using Arabidopsis knockout mutants. Plant Cell Environ. 36, 1981-1991. doi: 10.1111/pce.12104
22. Díaz, M., Achkor, H., Titarenko, E., and Martínez, M. C. (2003). The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Lett. 543, 136-139. doi: 10.1016/S0014-5793(03)00426-5
23. Dietz, K. J. (2003). Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107. doi: 10.1146/annurev.arplant.54.031902.134934
24. Dietz, K. J., Horling, F., König, J., and Baier, M. (2002). The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. J. Exp. Bot. 53, 1321-1329. doi: 10.1093/jexbot/53.372.1321
25. Di Mascio, P., Kaiser, S., and Sies, H. (1989). Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch. Biochem. Biophys. 274, 532-538. doi: 10.1016/0003-9861(89)90467-0
26. Dipierro, S., and Borranccino, G. (1991). Dehydroascorbate reductase from potato tubers. Phytochemistry 30, 427-429. doi: 10.1016/0031-9422(91)83698-K
27. Dixon, D. P., Davis, B. G., and Edwards, R. (2002). Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 277, 30859-30869. doi: 10.1074/jbc.M202919200
28. Dixon, D. P., and Edwards, R. (2010). "Glutathione S-transferases, " in The Arabidopsis Book (Rockville, MD: American Society of Plant Biologists). Available online at: http://www.aspb.org/publications/arabidopsis/.
29. Dixon, D. P., Hawkins, T., Hussey, P. J., and Edwards, R. (2009). Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J. Exp. Bot. 60, 1207-1218. doi: 10.1093/jxb/ern365
30. Dixon, D. P., Skipsey, M., Grundy, N. M., and Edwards, R. (2005). Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol. 138, 2233-2244. doi: 10.1104/pp.104.058917
31. Edwards, E. A., Rawsthorne, S., and Mullineaux, P. M. (1990). Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180, 278-284. doi: 10.1007/BF00194008
32. Edwards, R., Blount, J. W., and Dixon, R. A. (1991). Glutathione and elicitation of the phytoalexin response in legume cell cultures. Planta 184, 403-409. doi: 10.1007/BF00195343
33. Eshdat, Y., Holland, D., Faltin, Z., and Ben-Hayyim, G. (1997). Plant glutathione peroxidases. Physiol. Plant. 100, 234-240. doi: 10.1111/j.1399-3054.1997.tb04779.x
34. Finkemeier, I., Goodman, M., Lamkemeyer, P., Kandlbinder, A., Sweetlove, L. J., and Dietz, K. J. (2005). The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J. Biol. Chem. 280, 12168-12180. doi: 10.1074/jbc.M413189200
35. Foyer, C. H., and Halliwell, B. (1977). Purification and properties of dehydroascorbate reductase from spinach leaves. Phytochemistry 16, 1347-1350. doi: 10.1016/S0031-9422(00)88779-8
36. Foyer, C. H., and Noctor, G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 2-18. doi: 10.1104/pp.110.167569
37. Gama, F., Bréhélin, C., Gelhaye, E., Meyer, Y., Jacquot, J. P., Rey, P., et al. (2008). Functional analysis and expression characteristics of chloroplastic Prx IIE. Plant Physiol. 133, 599-610. doi: 10.1111/j.1399-3054.2008.01097.x
38. Gama, F., Keech, O., Eymery, F., Finkemeier, I., Gelhaye, E., Gardeström, P., et al. (2007). The mitochondrial type II peroxiredoxin from poplar. Physiol. Plant. 129, 196-206. doi: 10.1111/j.1399-3054.2006.00785.x
39. Gomez, L., Vanacker, H., Buchner, P., Noctor, G., and Foyer, C. H. (2004). The intercellular distribution of glutathione synthesis and its response to chilling in maize. Plant Physiol. 134, 1662-1671. doi: 10.1104/pp.103.033027
40. Gromes, R., Hothorn, M., Lenherr, E. D., Rybin, V., Sheffzek, K., and Rausch, T. (2008). The redox switch of γ-glutamylcysteine ligase via a reversible monomer-dimer transition is a mechanism unique to plants. Plant J. 54, 1063-1075. doi: 10.1111/j.1365-313X.2008.03477.x
41. Grzam, A., Tennstedt, P., Clemens, S., Hell, R., and Meyer, A. J. (2006). Vacuolar sequestration of glutathione S-conjugates outcompetes a possible degradation of the glutathione moiety by phytochelatin synthase. FEBS Lett. 580, 6384-6390. doi: 10.1016/j.febslet.2006.10.050
42. Han, Y., Mhamdi, A., Chaouch, S., and Noctor, G. (2013a). Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant Cell Environ. 36, 1135-1146. doi: 10.1111/pce.12048
43. Han, Y., Chaouch, S., Mhamdi, A., Queval, G., Zechmann, B., and Noctor, G. (2013b). Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid. Redox Signal. 18, 2106-2121. doi: 10.1089/ars.2012.5052
44. Hausladen, A., and Kunert, K. J. (1990). Effects of artificially enhanced levels of ascorbate and glutathione on the enzymes monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase in spinach (Spinacia oleracea). Plant Physiol. 79, 384-388. doi: 10.1111/j.1399-3054.1990.tb06757.x
45. Herbette, S., Lenne, C., Leblanc, N., Julien, J. L., Drevet, J. R., and Roeckel-Drevet, P. (2002). Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur. J. Biochem. 269, 2414-2420. doi: 10.1046/j.1432-1033.2002.02905.x
46. Hicks, L. M., Cahoon, R. E., Bonner, E. R., Rivard, R. S., Sheffield, J., and Jez, J. M. (2007). Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 19, 2653-2661. doi: 10.1105/tpc.107.052597
47. Horling, F., Lamkemeyer, P., König, J., Finkemeier, I., Kandlbinder, A., Baier, M., et al. (2003). Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol. 131, 317-325. doi: 10.1104/pp.010017
48. Hossain, M. A., and Asada, K. (1984). Purification of dehydroascorbate reductase from spinach and its characterisation as a thiol enzyme. Plant Cell Physiol. 25, 85-92.
49. Iqbal, A., Yabuta, Y., Takeda, T., Nakano, Y., and Shigeoka, S. (2006). Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana. FEBS J. 273, 5589-5597. doi: 10.1111/j.1742-4658.2006.05548.x
50. Jiménez, A., Hernández, J. A., del Río, L., and Sevilla, F. (1997). Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114, 275-284.
51. Jubany-Mari, T., Alegre-Batlle, L., Jiang, K., and Feldman, L. J. (2010). Use of a redox-sensing GFP (c-roGFP1) for real-time monitoring of cytosol redox status in Arabidopsis thaliana water-stressed plants. FEBS Lett. 584, 889-897. doi: 10.1016/j.febslet.2010.01.014
52. Kataya, A. M. R., and Reumann, S. (2010). Arabidopsis glutathione reductase 1 is dually targeted to peroxisomes and the cytosol. Plant Signal Behav. 5, 171-175. doi: 10.4161/psb.5.2.10527
53. Kwon, E., Feechan, A., Yun, B.-W., Hwang, B.-H., Pallas, J. A., Kang, G.-J., et al. (2012). AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236, 887-900. doi: 10.1007/s00425-012-1697-8
54. Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I., and Apel, K. (2007). Cross-talk between singlet oxygen-and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104, 672-677. doi: 10.1073/pnas.0609063103
55. Lu, Y. P., Li, Z. S., Drozdowicz, Y. M., Hörtensteiner, S., Martinoia, E., and Rea, P. A. (1998). AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell 10, 267-282.
56. Mannervik, B. (1985). Glutathione peroxidases. Meths. Enzymol. 113, 490-495. doi: 10.1016/S0076-6879(85)13063-6
57. Martinoia, E., Grill, E., Tommasini, R., Kreuz, K., and Amrhein, N. (1993). ATP-dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants. Nature 364, 247-249. doi: 10.1038/364247a0
58. Marty, L., Siala, W., Schwarzländer, M., Fricker, M. D., Wirtz, M., Sweetlove, L. J., et al. (2009). The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 9109-9114. doi: 10.1073/pnas.0900206106
59. Meyer, A. J. (2008). The integration of glutathione homeostasis and redox signaling. J. Plant Physiol. 165, 1390-1403. doi: 10.1016/j.jplph.2007.10.015
60. Meyer, A. J., Brach, T., Marty, L., Kreye, S., Rouhier, N., Jacquot, J. P., et al. (2007). Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 52, 973-986. doi: 10.1111/j.1365-313X.2007.03280.x
61. Mhamdi, A., Queval, G., Chaouch, S., Vanderauwera, S., Van Breusegem, F., and Noctor, G. (2010a). Catalase in plants: a focus on Arabidopsis mutants as stress-mimic models. J. Exp. Bot. 61, 4197-4220. doi: 10.1093/jxb/erq282
62. Mhamdi, A., Hager, J., Chaouch, S., Queval, G., Han, Y., Taconnat, L., et al. (2010b). Arabidopsis GLUTATHIONE REDUCTASE 1 plays a crucial role in leaf responses to intracellular H2O2 and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol. 153, 1144-1160. doi: 10.1104/pp.110.153767
63. Michelet, L., Zaffagnini, M., Marchand, C., Collin, V., Decottignies, P., Tsan, P., et al. (2005). Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc. Natl. Acad. Sci. U.S.A. 102, 16478-16483. doi: 10.1073/pnas.0507498102
64. Nakano, Y., and Asada, K. (1987). Purification of ascorbate peroxidase in spinach chloroplasts: its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol. 28, 131-140.
65. Navrot, N., Collin, V., Gualberto, J., Gelhaye, E., Hirasawa, M., Rey, P., et al. (2006). Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stress. Plant Physiol. 142, 1364-1379. doi: 10.1104/pp.106.089458
66. Nishizawa, A., Yabuta, Y., and Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263. doi: 10.1104/pp.108.122465
67. Noctor, G., Mhamdi, A., Queval, G., and Foyer, C. H. (2013). Regulating the redox gatekeeper: vacuolar sequestration puts glutathione disulfide in its place. Plant Physiol. 163, 665-671. doi: 10.1104/pp.113.223545
68. Nutricati, E., Miceli, A., Blando, F., and De Bellis, L. (2006). Characterization of two Arabidopsis thaliana glutathione S-transferases. Plant Cell Rep. 25, 997-2005. doi: 10.1007/s00299-006-0146-1
69. Park, H. J., Cho, H.Y., and Kong, K. H. (2005). Purification and biochemical properties of glutathione S-transferase from Lactuca sativa. J. Biochem. Mol. Biol. 38, 232-237. doi: 10.5483/BMBRep.2005.38.2.232
70. Polle, A. (2001). Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling: computer simulations as a step towards flux analysis. Plant Physiol. 126, 445-462. doi: 10.1104/pp.126.1.445
71. Pulido, P., Spínola, M. C., Kirchsteiger, K., Guinea, M., Pascual, M. B., Sahrawy, M., et al. (2010). Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J. Exp. Bot. 61, 4043-4054. doi: 10.1093/jxb/erq218
72. Queval, G., Jaillard, D., Zechmann, B., and Noctor, G. (2011). Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ. 34, 21-32. doi: 10.1111/j.1365-3040.2010.02222.x
73. Queval, G., Neukermans, J., Vanderauwera, S., Van Breusegem, F., and Noctor, G. (2012). Day length is a key regulator of transcriptomic responses to both CO2 and H2O2 in Arabidopsis. Plant Cell Environ. 35, 374-387. doi: 10.1111/j.1365-3040.2011.02368.x
74. Queval, G., Thominet, D., Vanacker, H., Miginiac-Maslow, M., Gakière, B., and Noctor, G. (2009). H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol. Plant 2, 344-356. doi: 10.1093/mp/ssp002
75. Riondet, C., Desouris, J. P., Montoya, J. G., Chartier, Y., Meyer, Y., and Reichheld, J. P. (2012). A dicotyledon-specific glutaredoxin GRXC1 family with dimer-dependent redox regulation is functionally redundant with GRXC2. Plant Cell Environ. 35, 360-373. doi: 10.1111/j.1365-3040.2011.02355.x
76. Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J. E., Rodermel, S., et al. (2002). Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J. 32, 329-342. doi: 10.1046/j.1365-313X.2002.01427.x
77. Rouhier, N. (2010). Plant glutaredoxins: pivotal players in redox biology and iron-sulphur centre assembly. New Phytol. 186, 365-372. doi: 10.1111/j.1469-8137.2009.03146.x
78. Rouhier, N., Gelhaye, E., and Jacquot, J. P. (2004a). Plant glutaredoxins: still mysterious reducing systems. Cell Mol. Life Sci. 61, 1266-1277. doi: 10.1007/s00018-004-3410-y
79. Rouhier, N., Gelhaye, E., Corbier, C., and Jacquot, J. P. (2004b). Active site mutagenesis and phospholipid hydroperoxide reductase activity of poplar type II peroxiredoxin. Physiol. Plant. 120, 57-62. doi: 10.1111/j.0031-9317.2004.0203.x
80. Rouhier, N., Gelhaye, E., and Jacquot, J. P. (2002). Glutaredoxin-dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism. J. Biol. Chem. 277, 13609-13614. doi: 10.1074/jbc.M111489200
81. Rouhier, N., and Jacquot, J. P. (2005). The plant multigenic family of thiol peroxidases. Free Radic. Biol. Med. 38, 1413-1421. doi: 10.1016/j.freeradbiomed.2004.07.037
82. Rouhier, N., Villarejo, A., Srivastava, M., Gelhaye, E., Keech, O., Droux, M., et al. (2005). Identification of plant glutaredoxin targets. Antioxid. Redox Signal. 7, 919-929. doi: 10.1089/ars.2005.7.919
83. Roxas, V. P., Lodhi, S. A., Garrett, D. K., Mahan, J. R., and Allen, R. D. (2000). Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol. 41, 1229-1234. doi: 10.1093/pcp/pcd051
84. Sakamoto, A., Ueda, M., and Morikawa, H. (2002). Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett. 515, 20-24. doi: 10.1016/S0014-5793(02)02414-6
85. Schwarzländer, M., Fricker, M. D., Müller, C., Marty, L., Brach, T., Novak, J., et al. (2008). Confocal imaging of glutathione redox potential in living plant cells. J. Microsc. 231, 299-316. doi: 10.1111/j.1365-2818.2008.02030.x
86. Sen Gupta, A., Alscher, R. G., and McCune, D. (1991). Response of photosynthesis and cellular antioxidants to ozone in Populus leaves. Plant Physiol. 96, 650-655. doi: 10.1104/pp.96.2.650
87. Sen Gupta, A., Webb, R. P., Holaday, S., and Allen, R. (1993). Overexpression of superoxide dismutase protects plants from oxidative stress. lnduction of ascorbate peroxidase in superoxide dismutase-overexpressing plants. Plant Physiol. 103, 1067-1073.
88. Shimaoka, T., Miyake, C., and Yokota, A. (2003). Mechanism of the reaction catalyzed by dehydroascorbate reductase from spinach chloroplasts. Eur. J. Biochem. 270, 921-928. doi: 10.1046/j.1432-1033.2003.03452.x
89. Shimaoka, T., Yokota, A., and Miyake, C. (2000). Purification and characterization of chloroplast dehydroascorbate reductase fom spinach leaves. Plant Cell Physiol. 41, 1110-1118. doi: 10.1093/pcp/pcd035
90. Smith, I. K., Kendall, A. C., Keys, A. J., Turner, J. C., and Lea, P. J. (1985). The regulation of the biosynthesis of glutathione in leaves of barley (Hordeum vulgare L.). Plant Sci. 41, 11-17. doi: 10.1016/0168-9452(85)90059-7
91. Su, T., Xu, J., Li, Y., Lei, L., Zhao, L., Yang, H., et al. (2011). Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23, 364-380. doi: 10.1105/tpc.110.079145
92. Tang, Z. X., and Yang, H. L. (2013). Functional divergence and catalytic properties of dehydroascorbate reductase family proteins from Populus tomentosa. Mol. Biol. Rep. 40, 5105-5114. doi: 10.1007/s11033-11013-2612-5
93. Tarrago, L., Laugier, E., Zaffagnini, M., Marchand, C., Le Maréchal, P., Rouhier, N., et al. (2009). Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J. Biol. Chem. 284, 18963-18971. doi: 10.1074/jbc.M109.015487
94. Tripathi, B. N., Bhatt, I., and Dietz, K. J. (2009). Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma 235, 3-15. doi: 10.1007/s00709-009-0032-0
95. Urano, J., Nakagawa, T., Maki, Y., Masumura, T., Tanaka, K., Murata, N., et al. (2000). Molecular cloning and characterization of a rice dehydroascorbate reductase. FEBS Lett. 466, 107-111. doi: 10.1016/S0014-5793(99)01768-8
96. Vanacker, H., Carver, T. L. W., and Foyer, C. H. (2000). Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol. 123, 1289-1300. doi: 10.1104/pp.123.4.1289
97. Wagner, U., Edwards, R., Dixon, D. P., and Mauch, F. (2002). Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515-532. doi: 10.1023/A:1015557300450
98. Wang, Z., Xiao, Y., Chen, W., Tang, K., and Zhang, L. (2010). Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J. Integr. Plant Biol. 52, 400-409. doi: 10.1111/j.1744-7909.2010.00921.x
99. Wells, W. W., Xu, D. P., Yang, Y., and Rocque, P. A. (1990). Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J. Biol. Chem. 265, 15361-15364.
100. Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., Van Montagu, M., et al. (1997). Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J. 16, 4806-4816. doi: 10.1093/emboj/16.16.4806
101. Winterbourn, C. C. (2013). The biological chemistry of hydrogen peroxide. Methods Enzymol. 528, 3-25. doi: 10.1016/B978-0-12-405881-1.00001-X
102. Yang, X., Sun, W., Liu, J. P., Liu, Y. J., and Zeng, Q. Y. (2009). Biochemical and physiological characterization of a tau class glutathione transferase from rice (Oryza sativa). Plant Physiol. Biochem. 47, 1061-1068. doi: 10.1016/j.plaphy.2009.07.003
103. Yin, L., Wang, S., Eltayeb, A. E., Uddin, M. I., Yamamoto, Y., Tsuji, W., et al. (2010). Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231, 609-621. doi: 10.1007/s00425-009-1075-3
104. Yoshida, S., Tamaoki, M., Shikano, T., Nakajima, N., Ogawa, D., Ioki, M., et al. (2006). Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol. 47, 304-308. doi: 10.1093/pcp/pci246
105. Zaffagnini, M., Bedhomme, M., Lemaire, S. D., and Trost, P. (2012). The emerging roles of protein glutathionylation in chloroplasts. Plant Sci. 185-186, 86-96. doi: 10.1016/j.plantsci.2012.01.005