Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Endoplasmic reticulum stress regulates glutathione metabolism and activities of glutathione related enzymes in Arabidopsis

Baris Uzilday A , Rengin Ozgur A , A. Hediye Sekmen A and Ismail Turkan A B
+ Author Affiliations
- Author Affiliations

A Department of Biology, Faculty of Science, Ege University, Bornova, 35100, Izmir, Turkey.

B Corresponding author. Email: ismail.turkan@ege.edu.tr

Functional Plant Biology - https://doi.org/10.1071/FP17151
Submitted: 9 September 2016  Accepted: 30 July 2017   Published online: 1 September 2017

Abstract

Stress conditions generate an extra load on protein folding machinery in the endoplasmic reticulum (ER) and if the ER cannot overcome this load, unfolded proteins accumulate in the ER lumen, causing ER stress. ER lumen localised protein disulfide isomerase (PDI) catalyses the generation of disulfide bonds in conjugation with ER oxidoreductase1 (ERO1) during protein folding. Mismatched disulfide bonds are reduced by the conversion of GSH to GSSG. Under prolonged ER stress, GSH pool is oxidised and H2O2 is produced via increased activity of PDI-ERO1. However, it is not known how glutathione metabolism is regulated under ER stress in plants. So, in this study, ER stress was induced with tunicamycin (0.15, 0.3, 0.45 μg mL–1 Tm) in Arabidopsis thaliana (L.) Heynh. Glutathione content was increased by ER stress, which was accompanied by induction of glutathione biosynthesis genes (GSH1, GSH2). Also, the apoplastic glutathione degradation pathway (GGT1) was induced. Further, the activities of glutathione reductase (GR), dehydroascorbate reductase (DHAR), glutathione peroxidase (GPX) and glutathione S-transferase (GST) were increased under ER stress. Results also showed that chloroplastic GPX genes were specifically downregulated with ER stress. This is the first report on regulation of glutathione metabolism and glutathione related enzymes in response to ER stress in plants.

Additional keywords: ER stress, tunicamycin, unfolded protein response.


References

Au KK, Pérez‐Gómez J, Neto H, Müller C, Meyer AJ, Fricker MD, Moore I (2012) A perturbation in glutathione biosynthesis disrupts endoplasmic reticulum morphology and secretory membrane traffic in Arabidopsis thaliana. The Plant Journal 71, 881–894.
A perturbation in glutathione biosynthesis disrupts endoplasmic reticulum morphology and secretory membrane traffic in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC38XhtlSmt77E&md5=e0b6dd65a5f43be3f9f0019f86eaf682CAS |

Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. Journal of Plant Physiology 176, 192–201.
Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses.CrossRef | 1:CAS:528:DC%2BC2MXht1OitLY%3D&md5=66fe9571309ac78f3ac18bbcc4e78f1fCAS |

Birk J, Ramming T, Odermatt A, Appenzeller-Herzog C (2013) Green fluorescent protein based monitoring of endoplasmic reticulum redox poise. Frontiers in Genetics 4, 108
Green fluorescent protein based monitoring of endoplasmic reticulum redox poise.CrossRef |

Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of the protein–dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of the protein–dye binding.CrossRef | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2821bcfbf01a16b0f1b14eb3a73c5812CAS |

Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiology 141, 446–455.
Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo.CrossRef | 1:CAS:528:DC%2BD28Xmt1aktro%3D&md5=1f17403a3271f76307011e1ab5a55c45CAS |

Chang CC, Ślesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Karpiński S (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photo-oxidative stress and immune responses. Plant Physiology 150, 670–683.
Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photo-oxidative stress and immune responses.CrossRef | 1:CAS:528:DC%2BD1MXnsleit7Y%3D&md5=90bb34f381752ff64a27945042dae4d0CAS |

Chen W, Chao G, Singh KB (1996) The promoter of a H2O2‐inducible, Arabidopsis glutathione S‐transferase gene contains closely linked OBF‐and OBP1‐binding sites. The Plant Journal 10, 955–966.
The promoter of a H2O2‐inducible, Arabidopsis glutathione S‐transferase gene contains closely linked OBF‐and OBP1‐binding sites.CrossRef | 1:CAS:528:DyaK2sXnsV2ltA%3D%3D&md5=45de417fc558f47071ce269003e5b30eCAS |

Diao Y, Xu H, Li G, Yu A, Yu X, Hu W, Hu Z (2014) Cloning a glutathione peroxidase gene from Nelumbo nucifera and enhanced salt tolerance by overexpressing in rice. Molecular Biology Reports 41, 4919–4927.
Cloning a glutathione peroxidase gene from Nelumbo nucifera and enhanced salt tolerance by overexpressing in rice.CrossRef | 1:CAS:528:DC%2BC2cXmtFalsr4%3D&md5=f7ded5e582445a3453e2efce36fc7e7bCAS |

Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods in Enzymology 401, 169–186.
Plant glutathione transferases.CrossRef | 1:CAS:528:DC%2BD28XoslCisrs%3D&md5=4b5e4d762a377c9ce0006b5f41b8102aCAS |

Floerl S, Majcherczyk A, Possienke M, Feussner K, Tappe H, Gatz C, Polle A (2012) Verticillium longisporum infection affects the leaf apoplastic proteome, metabolome, and cell wall properties in Arabidopsis thaliana. PLoS One 7, e31435
Verticillium longisporum infection affects the leaf apoplastic proteome, metabolome, and cell wall properties in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC38Xjt1Kqsrw%3D&md5=d3a6332ff118b3f54102669301e4c5c5CAS |

Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21–25.
The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism.CrossRef | 1:STN:280:DC%2BC2czlsVeltA%3D%3D&md5=aa5e917cc8f2851aa0b02b36fcfdb226CAS |

Fu JY (2014) Cloning of a new glutathione peroxidase gene from tea plant (Camellia sinensis) and expression analysis under biotic and abiotic stresses. Botanical Studies (Taipei, Taiwan) 55, 1–6.

Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? Journal of Experimental Botany 64, 33–53.
Ascorbate as seen through plant evolution: the rise of a successful molecule?CrossRef | 1:CAS:528:DC%2BC38XhvV2gsbvN&md5=491538b9289fdc5ce0095bef1aad898eCAS |

Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 7130–7139.

Herbette S, Lenne C, Leblanc N, Julien JL, Drevet JR, 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. European Journal of Biochemistry 269, 2414–2420.
Two GPX‐like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities.CrossRef | 1:CAS:528:DC%2BD38XjvFGjtL8%3D&md5=038631b864cad014f080f0ded10a8223CAS |

Hossain MA, Henríquez-Valencia C, Gómez-Páez M, Medina J, Orellana A, Vicente-Carbajosa J, Zouhar J (2016) Identification of novel components of the unfolded protein response in Arabidopsis. Frontiers in Plant Science 7, 650
Identification of novel components of the unfolded protein response in Arabidopsis.CrossRef |

Hou WC, Liang HJ, Wang CC, Liu DZ (2004) Detection of glutathione reductase after electrophoresis on native or sodium dodecyl sulfate polyacrylamide gels. Electrophoresis 25, 2926–2931.
Detection of glutathione reductase after electrophoresis on native or sodium dodecyl sulfate polyacrylamide gels.CrossRef | 1:CAS:528:DC%2BD2cXnvFejtr4%3D&md5=93b49b9f495ce07fc7bbf506d3d51c2aCAS |

Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annual Review of Plant Biology 64, 477–499.
Endoplasmic reticulum stress responses in plants.CrossRef | 1:CAS:528:DC%2BC3sXosFSktbs%3D&md5=784da4879e929c798c32a5fdd06810f8CAS |

Iwata Y, Koizumi N (2012) Plant transducers of the endoplasmic reticulum unfolded protein response. Trends in Plant Science 17, 720–727.
Plant transducers of the endoplasmic reticulum unfolded protein response.CrossRef | 1:CAS:528:DC%2BC38XhtVekurjE&md5=6d3b20bdf4a803663cbb94c11561f391CAS |

Kang SG, Jeong HK, Suh HS (2004) Characterization of a new member of the glutathione peroxidase gene family in Oryza sativa. Molecules and Cells 17, 23–28.

Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of two cDNAs (ERD11 and ERD13) for dehydration‐inducible genes that encode putative glutathione S‐transferases in Arabidopsis thaliana L. FEBS Letters 335, 189–192.
Characterization of two cDNAs (ERD11 and ERD13) for dehydration‐inducible genes that encode putative glutathione S‐transferases in Arabidopsis thaliana L.CrossRef | 1:CAS:528:DyaK2cXhsFGhsb0%3D&md5=0a3cd9dfbd6c1d7fe5fe4fb708c11872CAS |

Li L, Yi H (2012) Effect of sulfur dioxide on ROS production, gene expression and antioxidant enzyme activity in Arabidopsis plants. Plant Physiology and Biochemistry 58, 46–53.
Effect of sulfur dioxide on ROS production, gene expression and antioxidant enzyme activity in Arabidopsis plants.CrossRef | 1:CAS:528:DC%2BC38Xht1emsrnP&md5=b05a324f4e767042dbdd901d40d9f018CAS |

Lin CL, Chen HJ, Hou WC (2002) Activity staining of glutathione peroxidase after electrophoresis on native and sodium dodecyl sulfate polyacrylamide gels. Electrophoresis 23, 513–516.
Activity staining of glutathione peroxidase after electrophoresis on native and sodium dodecyl sulfate polyacrylamide gels.CrossRef | 1:CAS:528:DC%2BD38XitF2gsrc%3D&md5=609ce1f3a1a75fb690ddaaea826f96feCAS |

Liu JX, Howell SH (2010) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. The Plant Cell 22, 782–796.
bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC3cXmsF2ksLo%3D&md5=43d8d03978006c74653d0b807b91627fCAS |

Liu JX, Srivastava R, Che P, Howell SH (2007) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. The Plant Cell 19, 4111–4119.
An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28.CrossRef | 1:CAS:528:DC%2BD1cXhvF2htLo%3D&md5=bfe6d8d8cde0fc70a2430ed40170835bCAS |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method.CrossRef | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c6e730b8bcaab07d1e52bd2affd3622dCAS |

Masi A, Trentin AR, Agrawal GK, Rakwal R (2015) Gamma-glutamyl cycle in plants: a bridge connecting the environment to the plant cell? Frontiers in Plant Science 6, 252
Gamma-glutamyl cycle in plants: a bridge connecting the environment to the plant cell?CrossRef |

Mauch F, Dudler R (1993) Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiology 102, 1193–1201.
Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack.CrossRef | 1:CAS:528:DyaK3sXmt1Wqsrc%3D&md5=1e71c4b034760c48091f93b17ed76599CAS |

McCormack ME, Liu X, Jordan MR, Pajerowska-Mukhtar KM (2015) An improved high-throughput screening assay for tunicamycin sensitivity in Arabidopsis seedlings. Frontiers in Plant Science 6, 663
An improved high-throughput screening assay for tunicamycin sensitivity in Arabidopsis seedlings.CrossRef |

McIlwain CC, Townsend DM, Tew KD (2006) Glutathione S-transferase polymorphisms: cancer incidence and therapy. Oncogene 25, 1639–1648.
Glutathione S-transferase polymorphisms: cancer incidence and therapy.CrossRef | 1:CAS:528:DC%2BD28XisFyhtbo%3D&md5=7c2e6c0825f0111fb402a3dbbf524b3dCAS |

Meyer Y, Belin C, Delorme-Hinoux V, Reichheld JP, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxidants & Redox Signalling 17, 1124–1160.
Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance.CrossRef | 1:CAS:528:DC%2BC38Xht1alsb%2FO&md5=83426130d8bb672ace82db43c1f0ae04CAS |

Milla MAR, Maurer A, Huete AR, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. The Plant Journal 36, 602–615.
Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways.CrossRef |

Mishiba KI, Nagashima Y, Suzuki E, Hayashi N, Ogata Y, Shimada Y, Koizumi N (2013) Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response. Proceedings of the National Academy of Sciences of the United States of America 110, 5713–5718.
Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response.CrossRef | 1:CAS:528:DC%2BC3sXntVWkt70%3D&md5=b47366f2f942b832e53efd767e64e0f5CAS |

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
Reactive oxygen gene network of plants.CrossRef | 1:CAS:528:DC%2BD2cXotF2msrg%3D&md5=b1e44594793ecc2f0efc8f03f2e75279CAS |

Moreno AA, Mukhtar MS, Blanco F, Boatwright JL, Moreno I, Jordan MR, Pajerowska-Mukhtar KM (2012) IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS One 7, e31944
IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses.CrossRef | 1:CAS:528:DC%2BC38XjtFWjtLo%3D&md5=1ff4b5613784d004736e79c61d0790bdCAS |

Nagashima Y, Mishiba KI, Suzuki E, Shimada Y, Iwata Y, Koizumi N (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Scientific Reports 1, 29
Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor.CrossRef |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.

Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiology 142, 1364–1379.
Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses.CrossRef | 1:CAS:528:DC%2BD28XhtlCns7rO&md5=e928adf53762cdf772748e02558c59e1CAS |

Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez‐Garcia B, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant, Cell & Environment 35, 454–484.
Glutathione in plants: an integrated overview.CrossRef | 1:CAS:528:DC%2BC38XjtVKnt7w%3D&md5=b73a5327bdd8e485d3106255d30f9a09CAS |

Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiology 148, 1603–1613.
A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD1cXhsVSnurbM&md5=09d326c21ce41650f7e0383c43d7b81aCAS |

Onda Y, Kawagoe Y (2011) Oxidative protein folding: selective pressure for prolamin evolution in rice. Plant Signaling & Behavior 6, 1966–1972.
Oxidative protein folding: selective pressure for prolamin evolution in rice.CrossRef | 1:CAS:528:DC%2BC38XisVSmurg%3D&md5=06f78497174a412427eedc9df761bc0aCAS |

Ozgur R, Turkan I, Uzilday B, Sekmen AH (2014) Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana. Journal of Experimental Botany 65, 1377–1390.
Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC2cXks12htLs%3D&md5=c1a73ace74f42674940d6d5e7c7a854dCAS |

Ozgur R, Uzilday B, Sekmen AH, Turkan I (2015) The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in Arabidopsis. Annals of Botany 116, 541–553.
The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in Arabidopsis.CrossRef |

Pérez-López U, Robredo A, Lacuesta M, Mena-Petite A, Munoz-Rueda A (2009) The impact of salt stress on the water status of barley plants is partially mitigated by elevated CO2. Environmental and Experimental Botany 66, 463–470.
The impact of salt stress on the water status of barley plants is partially mitigated by elevated CO2.CrossRef |

Pollard MG, Travers KJ, Weissman JS (1998) Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Molecular Cell 1, 171–182.
Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum.CrossRef | 1:CAS:528:DyaK1cXhs1yjur8%3D&md5=b19c0a6fbe6d0dc4e8c9f0e80b26a8f1CAS |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA) – Bioenergetics 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.CrossRef | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=dd10efbf539b15c48d9192fcd9e6e2baCAS |

Queval G, Noctor G (2007) A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Analytical Biochemistry 363, 58–69.
A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development.CrossRef | 1:CAS:528:DC%2BD2sXislWksbc%3D&md5=9e00e0c15a7f3bc7f1047722af4d35b1CAS |

Queval G, Thominet D, Vanacker H, Miginiac-Maslow M, Gakière B, Noctor G (2009) H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Molecular Plant 2, 344–356.
H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast.CrossRef | 1:CAS:528:DC%2BD1MXjvVWht7s%3D&md5=2b488e8c7b932d0681e2c7d2c8ff356fCAS |

Ricci G, Bello ML, Caccuri AM, Galiazzo F, Federici G (1984) Detection of glutathione transferase activity on polyacrylamide gels. Analytical Biochemistry 143, 226–230.
Detection of glutathione transferase activity on polyacrylamide gels.CrossRef | 1:CAS:528:DyaL2MXktF2itA%3D%3D&md5=706df308bf360b7f3b7035db5193eeccCAS |

Ruberti C, Kim SJ, Stefano G, Brandizzi F (2015) Unfolded protein response in plants: one master, many questions. Current Opinion in Plant Biology 27, 59–66.
Unfolded protein response in plants: one master, many questions.CrossRef | 1:CAS:528:DC%2BC2MXpt1KqsLg%3D&md5=17001600e1e73cc4fd6d1514cc0f3112CAS |

Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Harvey Millar A, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co‐silencing multiple genes results in altered metabolic sensitivity to oxidative stress. The Plant Journal 58, 53–68.
The Arabidopsis glutathione transferase gene family displays complex stress regulation and co‐silencing multiple genes results in altered metabolic sensitivity to oxidative stress.CrossRef | 1:CAS:528:DC%2BD1MXks1Cnsrg%3D&md5=ebc2e9b683e99ddefc3081ea1d9c0e67CAS |

Seppänen MM, Cardi T, Hyökki MB, Pehu E (2000) Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. Plant Science 153, 125–133.
Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids.CrossRef |

Sevier CS, Kaiser CA (2008) Ero1 and redox homeostasis in the endoplasmic reticulum. Biochimica et Biophysica Acta 1783, 549–556.
Ero1 and redox homeostasis in the endoplasmic reticulum.CrossRef | 1:CAS:528:DC%2BD1cXksVaisLc%3D&md5=caa3740692b5173afe0fbc737e773d47CAS |

Tolin S, Arrigoni G, Trentin AR, Veljovic‐Jovanovic S, Pivato M, Zechman B, Masi A (2013) Biochemical and quantitative proteomics investigations in Arabidopsis ggt1 mutant leaves reveal a role for the gamma‐glutamyl cycle in plant’s adaptation to environment. Proteomics 13, 2031–2045.
Biochemical and quantitative proteomics investigations in Arabidopsis ggt1 mutant leaves reveal a role for the gamma‐glutamyl cycle in plant’s adaptation to environment.CrossRef | 1:CAS:528:DC%2BC3sXovFaktL0%3D&md5=5174ae59566294d81f8b6a39caadffaaCAS |

Townsend DM (2007) S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Molecular Interventions 7, 313
S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response.CrossRef | 1:CAS:528:DC%2BD1cXitVWisbw%3D&md5=eb50353d12135b2e699ed3ba897b7e9eCAS |

Tu BP, Weissman JS (2004) Oxidative protein folding in eukaryotes mechanisms and consequences. Journal of Cell Biology 164, 341–346.
Oxidative protein folding in eukaryotes mechanisms and consequences.CrossRef | 1:CAS:528:DC%2BD2cXhtVaiu7g%3D&md5=6448e642370a6e3ad65034e110e2e1e9CAS |

Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS Journal 274, 1152–1171.
Cellular response to unfolded proteins in the endoplasmic reticulum of plants.CrossRef | 1:CAS:528:DC%2BD2sXjtlWnu7o%3D&md5=6402ebfb0b45b2f4d4952c8af11dc46cCAS |

Vanacker H, Carver TL, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiology 123, 1289–1300.
Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction.CrossRef | 1:CAS:528:DC%2BD3cXmtVehur0%3D&md5=9ae8ff89861e9ecaf4cc00ef922f02dfCAS |

Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, May MJ (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. The Plant Cell 12, 97–110.
The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development.CrossRef | 1:CAS:528:DC%2BD3cXhtVWqs7o%3D&md5=8eb77cd8edd9131aee939d1f6e635f07CAS |

Walley J, Xiao Y, Wang JZ, Baidoo EE, Keasling JD, Shen Z, Dehesh K (2015) Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proceedings of the National Academy of Sciences of the United States of America 112, 6212–6217.
Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum.CrossRef | 1:CAS:528:DC%2BC2MXnt1Wgsb8%3D&md5=f1f9ab90c5bfc4b3440f9f987e87f801CAS |

Watanabe N, Lam E (2008) BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis. Journal of Biological Chemistry 283, 3200–3210.
BAX inhibitor-1 modulates endoplasmic reticulum stress-mediated programmed cell death in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD1cXhtlyjt7g%3D&md5=37b66dfed862694802a0ae1eaecc6530CAS |

Xiang C, Oliver DJ (1998) Glutathione metabolic genes co-ordinately respond to heavy metals and jasmonic acid in Arabidopsis. The Plant Cell 10, 1539–1550.
Glutathione metabolic genes co-ordinately respond to heavy metals and jasmonic acid in Arabidopsis.CrossRef | 1:CAS:528:DyaK1cXmsVKiu7s%3D&md5=a2a0cb171fabedc6fb4b8833c8294bc7CAS |

Yang XD, Li WJ, Liu JY (2005) Isolation and characterization of a novel PHGPx gene in Raphanus sativus. Biochimica et Biophysica Acta (BBA) – Gene Structure and Expression 1728, 199–205.
Isolation and characterization of a novel PHGPx gene in Raphanus sativus.CrossRef | 1:CAS:528:DC%2BD2MXjs1CmtLs%3D&md5=c10de95a25f3166192053c708c1103a4CAS |

Ye Z, Zhang J, Ancrum T, Manevich Y, Townsend DM, Tew KD (2017) S-Glutathionylation of endoplasmic reticulum proteins impacts unfolded protein response sensitivity. Antioxidants & Redox Signaling 26, 247–261.
S-Glutathionylation of endoplasmic reticulum proteins impacts unfolded protein response sensitivity.CrossRef | 1:CAS:528:DC%2BC2sXitlCnt7w%3D&md5=d39b094dd76db087611b7fb48abc0cc2CAS |



Supplementary MaterialSupplementary Material (17 KB) Export Citation