Plant glutathione peroxidases: Emerging role of the antioxidant enzymes in plant development and stress responses

Journal of Plant Physiology

Volumn 176, Issue , 2015, Pages 192-201

  Bela, Krisztina ^a   Horváth, Edit ^a   Gallé, Ágnes ^a   Szabados, László ^b   Tari, Irma ^a   Csiszár, Jolán ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

Antioxidant enzyme; Plant glutathione peroxidase; Reactive oxygen species; Redox regulation

Indexed keywords

ANIMALIA; ARABIDOPSIS THALIANA;

ANTIOXIDANT; GLUTATHIONE PEROXIDASE;

BIOLOGICAL MODEL; ENZYMOLOGY; METABOLISM; PHYSIOLOGICAL STRESS; PLANT; PLANT DEVELOPMENT;

ANTIOXIDANTS; GLUTATHIONE PEROXIDASE; MODELS, BIOLOGICAL; PLANT DEVELOPMENT; PLANTS; STRESS, PHYSIOLOGICAL;

EID: 84921896793     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2014.12.014     Document Type: Review

References (121)

1. Avsian-Kretchmer O., Eshdat Y., Gueta-Dahan Y., Ben-Hayyim G. Regulation of stress-induced phospholipid hydroperoxide glutathione peroxidase expression in citrus. Planta 1999, 209:469-477.
2. Baliga M.S., Wang H., Zhuo P., Schwartz J.L., Diamond A.M. Selenium and GPx-1 overexpression protect mammalian cells against UV-induced DNA damage. Biol Trace Elem Res 2007, 115:227-242.
3. Basantani M., Srivastava A. Plant glutathione transferases-a decade falls short. Can J Bot 2007, 85:443-456.
4. Beeor-Tzahar T., Ben-Hayyim G., Holland D., Faltin Z., Eshdat Y. A stress-associated citrus protein is a distinct plant phospholipid hydroperoxide glutathione peroxidase. FEBS Lett 1995, 366:151-155.
5. Bowers J.E., Chapman B.A., Rong J., Paterson A.H. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003, 422:433-438.
6. Brigelius-Flohé R., Kipp A. Glutathione peroxidases in different stages of carcinogenesis. Biochim Biophys Acta 2009, 1790:1555-1568.
7. Brigelius-Flohé R., Kipp A.P. Physiological functions of GPx2 and its role in inflammation-triggered carcinogenesis. Ann NY Acad Sci 2012, 1259:19-25.
8. Brigelius-Flohé R., Maiorino M. Glutathione peroxidases. Biochim Biophys Acta 2013, 1830:3289-3303.
9. Brugière S., Kowalski S., Ferro M., Seigneurin-Berny D., Miras S., Salvi D., et al. The hydrophobic proteome of mitochondrial membranes from Arabidopsis cell suspensions. Phytochemistry 2004, 65:1693-1707.
10. Burk R.F., Olson G.E., Winfrey V.P., Hill K.E., Yin D. Glutathione peroxidase-3 produced by the kidney binds to a population of basement membranes in the gastrointestinal tract and in other tissues. Am J Physiol Gastrointest Liver Physiol 2011, 301:G32-G38.
11. Chang C.C., Slesak I., Jordá L., Sotnikov A., Melzer M., Miszalski Z., et al. Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 2009, 150:670-683.
12. Chang Y.C., Yu Y.H., Shew J.Y., Lee W.J., Hwang J.J., Chen Y.H., et al. Deficiency of NPGPx, an oxidative stress sensor, leads to obesity in mice and human. EMBO Mol Med 2013, 5:1165-1179.
13. Chen S., Vaghchhipawala Z., Li W., Asard H., Dickman M.B. Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 2004, 135:1630-1641.
14. Churin Y., Schilling S., Börner T. A gene family encoding glutathione peroxidase homologues in Hordeum vulgare (barley). FEBS Lett 1999, 459:33-38.
15. Conrad M., Moreno S.G., Sinowatz F., Ursini F., Kolle S., Roveri A., et al. The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability. Mol Cell Biol 2005, 25:7637-7644.
16. Cosio C., Dunand C. Specific functions of individual class III peroxidase genes. J Exp Bot 2009, 60:391-408.
17. Criqui M.C., Jamet E., Parmentier Y., Marbach J., Durr A., Fleck J. Isolation and characterization of a plant cDNA showing homology to animal glutathione peroxidases. Plant Mol Biol 1992, 18:623-627.
18. Csiszár J., Gallé Á., Horváth E., Dancsó P., Gombos M., Váry Zs, et al. Different peroxidase activities and expression of abiotic stress-related peroxidases in apical root segments of wheat genotypes with different drought stress tolerance under osmotic stress. Plant Physiol Biochem 2012, 52:119-129.
19. Csiszár J., Szabó M., Erdei L., Márton L., Horváth F., Tari I. Auxin autotrophic tobacco callus tissues resist oxidative stress: the importance of glutathione S-transferase and glutathione peroxidase activities in auxin heterotrophic and autotrophic calli. J Plant Physiol 2004, 161:691-699.
20. D'Autréaux B., Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007, 8:813-824.
21. De Gara L. Class III peroxidases and ascorbate metabolism in plants. Phytochem Rev 2004, 3:195-205.
22. 2 receptor and redox-transducer in gene activation. Cell 2002, 111:471-481.
23. den Boer B.G., Murray J.A. Triggering the cell cycle in plants. Trends Cell Biol 2000, 10:245-250.
24. De Tullio M.C. Antioxidants and redox regulation: changing notions in a changing world. Plant Physiol Biochem 2010, 48:289-291.
25. Depège N., Drevet J., Boyer N. Molecular cloning and characterization of tomato cDNAs encoding glutathione peroxidase-like proteins. Eur J Biochem 1998, 253:445-451.
26. Diao Y., Xu H., Li G., Yu A., Yu X., Hu W., et al. Cloning a glutathione peroxidase gene from Nelumbo nucifera and enhanced salt tolerance by overexpressing in rice. Mol Biol Rep 2014, 41:4919-4927.
27. Dittrich A.M., Meyer H.A., Krokowski M., Quarcoo D., Ahrens B., Kube S.M., et al. Glutathione peroxidase-2 protects from allergen-induced airway inflammation in mice. Eur Respir J 2010, 35:1148-1154.
28. Dixon D.P., Hawkins T., Hussey P.J., Edwards R. Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 2009, 60:1207-1218.
29. Dietz K.J. Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 2011, 15:1129-1159.
30. Dietz K.J., Jacob S., Oelze M.L., Laxa M., Tognetti V., de Miranda S.M., et al. The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 2006, 57:1697-1709.
31. Edwards R., Dixon D.P. Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J Biol Chem 2009, 284:21249-21256.
32. Faltin Z., Holland D., Velcheva M., Tsapovetsky M., Roeckel-Drevet P., Handa A.K., et al. Glutathione peroxidase regulation of reactive oxygen species level is crucial for in vitro plant differentiation. Plant Cell Physiol 2010, 51:1151-1162.
33. Ferreira Neto J.R.C., Pandolfi V., Guimaraes F.C., Benko-Iseppon A.M., Romero C., Silva R.L., et al. Early transcriptional response of soybean contrasting accessions to root dehydration. PLoS ONE 2013, 8:e83466. 10.1371/journal.pone.0083466.
34. Foyer C.H., Lopez-Delgado H., Dat J.F., Scott I.M. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 1997, 100:241-254.
35. Foyer C.H., Noctor G. Redox homeotasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 2005, 17:1866-1875.
36. Foyer C.H., Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 2009, 11:861-905.
37. Foyer C.H., Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 2011, 155:2-18.
38. Fu J.Y. Cloning of a new glutathione peroxidase gene from tea plant (Camellia sinensis) and expression analysis under biotic and abiotic stresses. Bot Stud 2014, 55:7.
39. Gaber A. Arabidopsis glutathione peroxidase 8 is a key enzyme in response to environmental stresses. Arab J Biotech 2011, 14:213-224.
40. Gaber A., Ogata T., Maruta T., Yoshimura K., Tamoi M., Shigeoka S. The involvement of Arabidopsis glutathione peroxidase 8 in the suppression of oxidative damage in the nucleus and cytosol. Plant Cell Physiol 2012, 53:1596-1606.
41. Gao F., Chen J., Ma T., Li H., Wang N., Li Z., et al. The glutathione peroxidase gene family in Thellungiella salsuginea: genome-wide identification, classification, and gene and protein expression analysis under stress conditions. Int J Mol Sci 2014, 15:3319-3335.
42. Garcia-Hernandez M., Berardini T.Z., Chen G., Crist D., Doyle A., Huala E., et al. TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2002, 2:239-253.
43. Herbette S., de Labrouhe D.T., Drevet J.R., Roeckel-Drevet P. Transgenic tomatoes showing higher glutathione peroxydase antioxidant activity are more resistant to an abiotic stress but more susceptible to biotic stresses. Plant Sci 2011, 180:548-553.
44. Herbette S., Lenne C., Leblanc N., Julien J.L., Drevet J.R., Roeckel-Drevet P. 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 2002, 269:2414-2420.
45. Herbette S., Menn A.L., Rousselle P., Ameglio T., Faltin Z., Branlard G., et al. Modification of photosynthetic regulation in tomato overexpressing glutathione peroxidase. Biochim Biophys Acta 2005, 1724:108-118.
46. Herbette S., Roeckel-Drevet P., Drevet J.R. Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers. FEBS J 2007, 274:2163-2180.
47. Herrero E., Ros J., Bellí G., Cabiscol E. Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 2008, 1780:1217-1235.
48. Hoffmann B., Hecht H.J., Flohe L. Peroxiredoxins. Biol Chem 2002, 383:347-364.
49. Holland D., Ben-Hayyim G., Faltin Z., Camoin L., Strosberg A.D., Eshdat Y. Molecular characterization of salt-stress-associated protein in citrus: protein and cDNA sequence homology to mammalian glutathione peroxidases. Plant Mol Biol 1993, 21:923-927.
50. Hruz T., Laule O., Szabo G., Wessendorp F., Bleuler S., Oertle L., et al. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinf 2008, 2008:420747. 10.1155/2008/420747.
51. Huson D.H., Richter D.C., Rausch C., Dezulian T., Franz M., Rupp R. Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 2007, 8.
52. Imai H., Nakagawa Y. Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radical Biol Med 2003, 34:145-169.
53. Iqbal A., Yabuta Y., Takeda T., Nakano Y., Shigeoka S. Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana. FEBS J 2006, 273:5589-5597.
54. Ito J., Batth T.S., Petzold C.J., Redding-Johanson A.M., Mukhopadhyay A., Verboom R., et al. Analysis of the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J Proteome Res 2011, 10:1571-1582.
55. Johnson R.R., Cranston H.J., Chaverra M.E., Dyer W.E. Characterization of cDNA clones for differentially expressed genes in embryos of dormant and nondormant Avena fatua L. caryopses. Plant Mol Biol 1995, 28:113-122.
56. Jubany-Marí T., Alegre-Batlle L., Jiang K., Feldman L.J. Use of a redox-sensing GFP (c-roGFP1) for real-time monitoring of cytosol redox status in Arabidopsis thaliana water-stressed plants. FEBS Lett 2010, 584:889-897.
57. Jung B.G., Lee K.O., Lee S.S., Chi Y.H., Jang H.H., Kang S.S., et al. A Chinese cabbage cDNA with high sequence identity to phospholipid hydroperoxide glutathione peroxidases encodes a novel isoform of thioredoxin-dependent peroxidase. J Biol Chem 2002, 277:12572-12578.
58. Kang S.G., Jeong H.K., Suh H.S. Characterization of a new member of the glutathione peroxidase gene family in Oryza sativa. Mol Cell 2004, 17:23-28.
59. Kilili K.G., Atanassova N., Vardanyan A., Clatot N., Al-Sabarna K., Kanellopoulos P.N., et al. Differential roles of Tau class glutathione S-transferases in oxidative stress. J Biol Chem 2004, 279:24540-24551.
60. Kim S.O., Merchant K., Nudelman R., Beyer W.F., Keng T., DeAngelo J., et al. OxyR: a molecular code for redox-related signalling. Cell 2002, 109:383-396.
61. Kim Y.J., Jang M.G., Noh H.Y., Lee H.J., Sukweenadhi J., Kim J.H., et al. Molecular characterization of two glutathione peroxidase genes of Panax ginseng and their expression analysis against environmental stresses. Gene 2014, 535:33-41.
62. Kocsy G., Galiba G., Brunold C. Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plant 2001, 113:158-164.
63. Kocsy G., Tari I., Vanková R., Zechmann B., Gulyás Z., Poór P., et al. Redox control of plant growth and development. Plant Sci 2013, 211:77-91.
64. Koh C.S., Didierjean C., Navrot N., Panjikar S., Mulliert G., Rouhier N., et al. Crystal structures of a poplar thioredoxin peroxidase that exhibits the structure of glutathione peroxidases: insights into redox-driven conformational changes. J Mol Biol 2007, 370:512-529.
65. Koua D., Cerutti L., Falquet L., Sigrist C.J.A., Theiler G., Hulo N., et al. PeroxiBase: a database with new tools for peroxidase family classification. Nucleic Acids Res 2009, 37:D261-D266. 10.1093/nar/gkn680.
66. Laloi C., Dominique M.O., Marco Y., Meyers Y., Reichheld J.P. The Arabidopsis h5 gene induction by oxidative stress and its W-box mediated response to pathogen elicitor. Plant Physiol 2004, 134:1006-1016.
67. Lee O.J., Schneider-Stock R., McChesney P.A., Kuester D., Roessner A., Vieth M., et al. Hypermethylation and loss of expression of glutathione peroxidase-3 in Barrett's tumorigenesis. Neoplasia 2005, 7:854-861.
68. Lee Y.S., Kim A.Y., Choi J.W., Kim M., Yasue S., Son H.J., et al. Dysregulation of adipose glutathione peroxidase 3 in obesity contributes to local and systemic oxidative stress. Mol Endocrinol 2008, 22:2176-2189.
69. Li G., Peng X., Wei L., Kang G. Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 2013, 529:321-325.
70. Li K., Yang Q., Wang W., Zhao X., Lou Z. GPX3 from Arabidopsis thaliana: cloning, expression, purification, crystallization and preliminary X-ray analysis. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2013, 69:1224-1226.
71. Li W.J., Feng H., Fan J.H., Zhang R.Q., Zhao N.M., Liu J.Y. Molecular cloning and expression of a phospholipid hydroperoxide glutathione peroxidase homolog in Oryza sativa. Biochim Biophys Acta 2000, 1493:225-230.
72. Liszkay A., Kenk B., Schopfer P. Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 2003, 217:658-667.
73. Loh K., Deng H., Fukushima A., Cai X., Boivin B., Galic S., et al. Reactive oxygen species enhance insulin sensitivity. Cell Metab 2009, 10:260-272.
74. Lubos E., Loscalzo J., Handy D.E. Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2011, 15:1957-1997.
75. Maiorino M., Aummann K.D., Brigelius-Flohé R., Doria D., Van den Heuvel J., McCarthy J., et al. Probing the presumed catalytic triade of selenium-containing peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PhGPx). Biol Chem Hoppe-Seyler 1995, 376:651-660.
76. Margis R., Dunand C., Teixeira F.K., Margis-Pinheiro M. Glutathione peroxidase family-an evolutionary overview. FEBS J 2008, 275:3959-3970.
77. Marmagne A., Rouet M.A., Ferro M., Rolland N., Alcon C., Joyard J., et al. Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Mol Cell Proteomics 2004, 3:675-691.
78. Meyer A.J., Brach T., Marty L., Kreye S., Rouhier N., Jacquot J.P., et al. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 2007, 52:973-986.
79. Miao Y., Lv D., Wang P., Wang X.C., Chen J., Miao C., et al. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 2006, 18:2749-2766.
80. Miao Y.C., Guo J.G., Liu E.T., Li K., Dai J., Wang P.C., et al. Osmotically stress-regulated the expression of glutathione peroxidase 3 in Arabidopsis. Chinese Sci Bull 2007, 52:127-130.
81. Miller G., Suzuki N., Ciftci-Yilmaz S., Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 2010, 33:453-467.
82. Mills G.C. Hemoglobin catabolism. I. Glutathione peroxidase, an erythrocyte enzyme which protects hemoglobin from oxidative breakdown. J Biol Chem 1957, 229:189-197.
83. Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci 2004, 9:490-498.
84. Mittova V., Theodoulou F.L., Kiddle G., Gómez L., Volokita M., Tal M., et al. Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett 2003, 554:417-421.
85. Motohashi K., Kondoh A., Stumpp M.T., Hisabori T. Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 2001, 98:11224-11229.
86. Mullineaux P.M., Karpinski S., Jiménez A., Cleary S.P., Robinson C., Creissen G.P. Identification of cDNAS encoding plastid-targeted glutathione peroxidase. Plant J 1998, 13:375-379.
87. Munné-Bosch S., Queval G., Foyer C.H. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 2013, 161:5-19.
88. Nakagawa Y. Role of mitochondrial phospholipid hydroperoxide glutathione peroxidase (PHGPx) as an antiapoptotic factor. Biol Pharm Bull 2004, 27:956-960.
89. Navrot N., Collin V., Gualberto J., Gelhaye E., Hirasawa M., Rey P., et al. Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 2006, 142:1364-1379.
90. Nikolovski N., Rubtsov D., Segura M.P., Miles G.P., Stevens T.J., Dunkley T.P., et al. Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol 2012, 160:1037-1051.
91. Noctor G., De Paepe R., Foyer C.H. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 2007, 12:125-134.
92. Noctor G., Queval G., Mhamdi A., Chaouch S., Foyer C.H. Glutathione. The Arabidopsis book 2011, 9:e0142. 10.1199/tab.0142.
93. Pagnussat G.C., Yu H.J., Ngo Q.A., Rajani S., Mayalagu S., Johnson C.S., et al. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 2005, 132:603-614.
94. 2 homeostasis and root and shoot development in rice. Plant Sci 2013, 208:93-101.
95. Passaia G., Queval G., Bai J., Margis-Pinheiro M., Foyer C.H. The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana. J Exp Bot 2014, 65:1403-1413.
96. Passardi F., Penel C., Dunand C. Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 2004, 9:534-540.
97. Potters G., Horemans N., Jansen M.A.K. The cellular redox state in plant stress biology-a charging concept. Plant Physiol Biochem 2010, 48:292-300.
98. Ramos J., Matamoros M.A., Naya L., James E.K., Rouhier N., Sato S., et al. The glutathione peroxidase gene family of Lotus japonicus: characterization of genomic clones, expression analyses and immunolocalization in legumes. New Phytol 2009, 181:103-114.
99. Rhee S.Y., Beavis W., Berardini T.Z., Chen G., Dixon D., Doyle A., et al. The Arabidopsis Information Resource, TAIR: a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 2003, 31:224-228.
100. Rodriguez Milla M.A., Maurer A., Rodriguez Huete A., Gustafson J.P. Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 2003, 36:602-615.
101. Rouhier N., Jacquot J.P. The plant multigenic family of thiol peroxidases. Free Radical Biol Med 2005, 38:1413-1421.
102. Roxas V.P., Smith R.K., Allen E.R., Allen R.D. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 1997, 15:988-991.
103. Sánchez-Fernández R., Fricker M., Corben L.B., White N.S., Sheard N., Leaver C.J., et al. Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci USA 1997, 94:2745-2750.
104. Schafer F.Q., Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biol Med 2001, 30:1191-1212.
105. Seiler A., Schneider M., Forster H., Roth S., Wirth E.K., Culmsee C., et al. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab 2008, 8:237-248.
106. Shabala S. Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 2009, 60:709-712.
107. Sugimoto M., Oono Y., Gusev O., Matsumoto T., Yazawa T., Levinskikh M.A., et al. Genome-wide expression analysis of reactive oxygen species gene network in Mizuna plants grown in long-term spaceflight. BMC Plant Biol 2014, 14:4.
108. Sugimoto M., Sakamoto W. Putative phospholipid hydroperoxide glutathione peroxidase gene from Arabidopsis thaliana induced by oxidative stress. Genes Genet Syst 1997, 72:311-316.
109. Suzuki N., Koussevitzky S., Mittler R., Miller G. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 2012, 35:259-270.
110. Szalai G., Kellos T., Galiba G., Kocsy G. Glutathione as an antioxidant and a regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 2009, 28:66-80.
111. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 2013, 30:2725-2729.
112. Thompson J.D., Higgins D.G., Gibson T.J. Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
113. Toppo S., Flohe L., Ursini F., Vanin S., Maiorino M. Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme. Biochim Biophys Acta 2009, 1790:1486-1500.
114. Vernoux T., Wilson R.C., Seeley K.A., Reichheld J.P., Muroy S., Brown S., et al. The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 2000, 12:97-110.
115. Welinder K.G., Justesen A.F., Kjaersgard I.V.H., Jensen R.B., Rasmussen S.K., Jespersen H.M., Duroux L. Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur J Biochem 2002, 269:6063-6081.
116. Xu X.M., Lin H., Maple J., Björkblom B., Alves G., Larsen J.P., Møller S.G. The Arabidopsis DJ-1a protein confers stress protection through cytosolic SOD activation. J Cell Sci 2010, 123:1644-1651.
117. Yang R., Jarvis D.E., Chen H., Beilstein M.A., Grimwood J., Jenkins J., et al. The reference genome of the halophytic plant Eutrema salsugineum. Front Plant Sci 2013, 4:46.
118. Yang X.D., Li W.J., Liu J.Y. Isolation and characterization of a novel PHGPx gene in Raphanus sativus. Biochim Biophys Acta 2005, 1728:199-205.
119. Yang X.D., Dong C.J., Liu J.Y. A plant mitochondrial phospholipid hydroperoxide glutathione peroxidase: its precise localization and higher enzymatic activity. Plant Mol Biol 2006, 62:951-962.
120. 2 tolerances in Arabidopsis. PLoS ONE 2013, 8:e73989. 10.1371/journal.pone.0073989.
121. Zybailov B., Rutschow H., Friso G., Rudella A., Emanuelsson O., Sun Q., van Wijk K.J. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 2008, 3:e1994.