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A Winning Two Pair: Role of the Redox Pairs AsA/DHA and GSH/GSSG in Signal Transduction

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Ascorbate-Glutathione Pathway and Stress Tolerance in Plants

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Abstract

For a few decades after its identification, the AsA/GSH (Halliwell–Asada) cycle has been almost exclusively considered as a scavenging system, more or less efficiently removing reactive oxygen species (ROS). The whole issue was simplistically viewed as a fight between “bad” ROS and “good” antioxidants until recently, when ROS (and reactive nitrogen species, RNS) were identified as important signalling molecules, inducing an array of defensive responses in both animal and plant systems. In this framework, antioxidants take a completely different role, becoming part of complex signalling modules. AsA and GSH are connected in many ways, forming a functional entity. Still they have their own specificity and control different aspects of plant metabolism and growth. It is increasingly clear that AsA and GSH, together with their oxidized forms, have a pivotal, multi-level regulatory role in protein function and gene expression. Remarkable progress has been recently achieved in the identification of transcription factors and other proteins, whose activity is regulated by changes in the relative amount of redox components. Additionally, participation of AsA as a co-substrate of reactions catalysed by dioxygenases (a large class of enzymes involved in hormone synthesis and post-translational protein modification), also has a relevant regulatory role.

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References

  • Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat Biotechnol 21:177–181

    Article  PubMed  CAS  Google Scholar 

  • Arrigo AP (1999) Gene expression and the thiol redox state. Free Radic Biol Med 27:936–44

    Article  PubMed  CAS  Google Scholar 

  • Arrigoni O, Arrigoni-Liso R, Calabrese G (1975) Lycorine as an inhibitor of ascorbic acid biosynthesis. Nature 256:513–514

    Article  CAS  Google Scholar 

  • Arrigoni O, Calabrese G, De Gara L, Bitonti MB, Liso R (1997a) Correlation between changes in cell ascorbate and growth of Lupinus albus seedlings. J Plant Physiol 150:302–308

    Article  CAS  Google Scholar 

  • Arrigoni O, De Gara L, Paciolla C, Evidente A, de Pinto MC, Liso R (1997b) Lycorine: a powerful inhibitor of l-galactono-γ-lactone dehydrogenase. J Plant Physiol 150:362–364

    Article  CAS  Google Scholar 

  • Asada K (2003) The water-water cycle in chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  Google Scholar 

  • Baier M, Dietz KJ (1997) The plant 2-cys peroxiredoxin BAS1 is a nuclear encoded chloroplast protein: its expression regulation, phylogenetic origin and implications for its specific physiological function in plants. Plant J 12:179–190

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–344

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Yu J, Gómez F, Fernández L, McIntosh L, Foyer CH (2006) Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation. J Exp Bot 37:1621–1631

    Article  Google Scholar 

  • Borsook H, Jeffreys CE (1936) Glutathione and ascorbic acid. Science 83:397–398

    Article  PubMed  CAS  Google Scholar 

  • Castro-Caldasa M, Milagrea I, Rodriguesa E, Gama MJ (2009) Glutathione S-transferase pi regulates UV-induced JNK signaling in SH-SY5Y neuroblastoma cells. Neurosci Lett 451:241–245

    Article  Google Scholar 

  • Chapman DJ, Ragan MA (1980) Evolution of biochemical pathways: evidence from comparative biochemistry. Annu Rev Plant Physiol 31:639–678

    Article  CAS  Google Scholar 

  • Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154:847–856

    PubMed  CAS  Google Scholar 

  • Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S, Isupov M, Littelchild JA, Smirnoff N (2006) Arabidopsis thaliana VTC4 encodes l-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem 281:15662–156670

    Article  PubMed  CAS  Google Scholar 

  • Cordoba-Pedregosa M, Gonzalez-Reyes JA, Canadillas M, Navas P, Cordoba F (1996) Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol 112:1119–1125

    PubMed  CAS  Google Scholar 

  • Cross JV, Templeton DJ (2004) Oxidative stress inhibits MEKK1 by site specific glutathionylation in the ATP-binding domain. Biochem J 381:675–683

    Article  PubMed  CAS  Google Scholar 

  • Davidson JM, LuValle PA, Zoia O, Quaglino D Jr, Giro M (1997) Ascorbate differentially regulates elastin and collagen biosynthesis in vascular smooth muscle cells and skin fibroblasts by a pre-translational mechanism. J Biol Chem 272:345–352

    Article  PubMed  CAS  Google Scholar 

  • de Rey Pailhade MJ (1888) Sur un corps d’origine organique hydrogénant le soufre á froid. C R Acad Sci 106:1683–1684

    Google Scholar 

  • De Tullio MC (2004) How does ascorbic acid prevent scurvy? A survey of the non-antioxidant functions of vitamin C. In: Asard H, May J, Smirnoff N (eds) Vitamin C, its functions and biochemistry in animals and plants. Bios Scientific Publishers, Oxford, UK, pp 159–72

    Google Scholar 

  • De Tullio MC (2010) Antioxidants and redox regulation: changing notions in a changing world. Plant Physiol Biochem 48:289–291

    Google Scholar 

  • De Tullio MC, De Gara L, Paciolla C, Arrigoni O (1998) Dehydroascorbate-reducing proteins in maize are induced by the ascorbate biosynthesis inhibitor lycorine. Plant Physiol Biochem 36:433–440

    Article  Google Scholar 

  • De Tullio MC, Jiang K, Feldman LJ (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol Biochem 48:328–336

    Google Scholar 

  • Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468

    Article  PubMed  CAS  Google Scholar 

  • Dobzhansky T (1973) Nothing in biology makes any sense except in the light of evolution. Am Biol Teach 35:125–129

    Article  Google Scholar 

  • Fahey RC, Deena L, Di Stefano G, Meier P, Bryan RN (1980) Role of hydration state and thiolsulphide status in the control of thermal stability and protein synthesis in wheat embryo. Plant Physiol 65:1062–1066

    Article  PubMed  CAS  Google Scholar 

  • Fahey RC, Sundquist AR (1991) Evolution of glutathione metabolism. Adv Enzymol 64:1–53

    PubMed  CAS  Google Scholar 

  • Fan DP, Shi YC, Liu WQ (2009) Involvement of protein tyrosine phosphatase in signal pathway of dehydroascorbate. Plant Physiol Commun 45:843–846

    CAS  Google Scholar 

  • Firn RD, Jones GG (2009) A Darwinian view of metabolism: molecular properties determine fitness. J Exp Bot 60:719–726

    Article  PubMed  CAS  Google Scholar 

  • Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK (2008) Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signalling. J Exp Bot 59:729–737

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Garcia-Muniz N, Martinez-Izquierdo JA, Puigdomenech P (1998) Induction of mRNA accumulation corresponding to a gene encoding a cell wall hydroxyproline-rich glycoprotein by fungal elicitors. Plant Mol Biol 38:623–632

    Article  PubMed  CAS  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1987) Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci USA 84:439–443

    Article  PubMed  CAS  Google Scholar 

  • Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal binding peptides of plants, ares ynthesized from glutathione by a specific c-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci USA 86:6838–6842

    Article  PubMed  CAS  Google Scholar 

  • Groden D, Beck E (1979) H2O2 destruction by ascorbate dependent systems from chloroplasts. Biochim Biophys Acta 546:426–433

    Article  PubMed  CAS  Google Scholar 

  • Hedden P, Kamiya Y (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48:431–460

    Article  PubMed  CAS  Google Scholar 

  • Hopkins FG (1929) On glutathione: a reinvestigation. J Biol Chem 84:269–320

    CAS  Google Scholar 

  • Hopkins FG, Morgan EJ (1936) Some relations between ascorbic acid and glutathione. Biochem J 30:1446–1462

    PubMed  CAS  Google Scholar 

  • Imai T, Karita S, Shiratori G, Hattori M, Nunome T, Oba K, Hirai M (1998) l-galactono-gamma-lactone dehydrogenase from sweet potato: purification and cDNA sequence analysis. Plant Cell Physiol 39:1350–1358

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Iwabuchi M, Ogawa K (2003) The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: Detection using biotinylated glutathione. Plant Cell Physiol 44:655–660

    Article  PubMed  CAS  Google Scholar 

  • Jain A, Martenson J, Mehta T, Krauss AN, Auld PAM, Meister A (1992) Ascorbic acid prevents oxidative stress in glutathione-deficient mice: Effects on lung type 2 cell lamellar bodies, lung surfactant, and skeletal muscle. Proc Natl Acad Sci USA 89:5093–5097

    Article  PubMed  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ, Foyer CH (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antiox Redox Sign 5:23–32

    Article  CAS  Google Scholar 

  • Klapheck S, Zimmer I, Cosse H (1990) Scavenging of hydrogen peroxide in the endosperm of Ricinus communis by ascorbate peroxidase. Plant Cell Physiol 31:1005–1013

    CAS  Google Scholar 

  • Kosower EM, Kosower NS (1969) Lest I forget thee, glutathione…. Nature 224:117–120

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Grill D (1993) Content of low molecular weight thiols during the imbibition of pea seeds. Physiol Plant 88:557–562

    Article  CAS  Google Scholar 

  • Liso R, Calabrese G, Bitonti MB, Arrigoni O (1984) Relationship between ascorbic acid and cell division. Exp Cell Res 150:314–320

    Article  PubMed  CAS  Google Scholar 

  • Lorence A, Chevone BI, Mendes P, Nessler CL (2004) myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205

    Article  PubMed  CAS  Google Scholar 

  • Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR (2001) Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc Natl Acad Sci USA 98:2262–2267

    Article  PubMed  CAS  Google Scholar 

  • Marrs K (1996) The functions and regulation of glutathione S transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  PubMed  CAS  Google Scholar 

  • Mårtensson JM, Meister A (1991) Glutathione deficiency decreases tissue ascorbate levels in newborn rats: ascorbate spares glutathione and protects. Proc Natl Acad Sci USA 88:4656–46560

    Article  PubMed  Google Scholar 

  • Marx JL (1985) Oxygen free radicals linked to many diseases. Science 235:529–531

    Article  Google Scholar 

  • Meister A (1994) Glutathione, ascorbate, and cellular protection. Cancer Res Suppl 54:1969–1975

    Google Scholar 

  • Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447

    Article  PubMed  CAS  Google Scholar 

  • Morell S, Follmann H, De Tullio M, Häberlein I (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Lett 414:567–571

    Article  PubMed  CAS  Google Scholar 

  • Mori T, Itoh S, Ohgiya S, Ishizaki K, Kamataki T (1997) Regulation of CYP1A and CYP3A mRNAs by ascorbic acid in guinea pigs. Arch Biochem Biophys 348:268–277

    Article  PubMed  CAS  Google Scholar 

  • Mueller LA, Goodman CD, Silady RA, Walbot V (2000) AN9, a Petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid binding protein. Plant Physiol 123:1561–1570

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1980) Spinach chloroplasts scavenge hydrogen peroxide on illumination. Plant Cell Physiol 21:1295–1307

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–278

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283–1304

    Article  PubMed  CAS  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-JovanovicS VPJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer F, Casanueva E, Kamar J, Guerra A, Perichart O, Vadillo-Ortega F (1998) Modulation of 72-kilodalton type IV collagenase (matrix metalloproteinase-2) by ascorbic acid in cultured human amnion-derived cells. Biol Reprod 59:326–329

    Article  PubMed  CAS  Google Scholar 

  • Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Curr Opin Plant Biol 6:379–389

    Article  PubMed  CAS  Google Scholar 

  • Prescott AG, John P (1996) Dioxygenases: molecular structure and role in plant metabolism. Annu Rev Plant Physiol Plant Mol Biol 47:245–271

    Article  PubMed  CAS  Google Scholar 

  • Rocklin AM, Tierney DL, Kofman V, Brunhuber NM, Hoffman BM, Christoffersen RE, Reich NO, Lipscomb JD, Que L (1999) Role of the nonheme Fe(II) center in the biosynthesis of the plant hormone ethylene. Proc Natl Acad Sci USA 96:7905–7909

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inzé D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistichally different forms of redox control. Proc Natl Acad Sci USA 94:2745–2749

    Article  PubMed  CAS  Google Scholar 

  • Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212

    Article  PubMed  CAS  Google Scholar 

  • Schmidt S, Sunyaev S, Bork P, Dandekar T (2003) Metabolites: a helping hand for pathway evolution? Trends Biochem Sci 28:336–341

    Article  PubMed  CAS  Google Scholar 

  • Schultz C, Gilson F, Oxley D, Youl J, Bacic A (1998) GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci 3:426–431

    Article  Google Scholar 

  • Schwarzländer M, Fricker MD, Müller C, Marty L, Brach T, Novak J, Sweetlove LJ, Hell R, Meyer AJ (2008) Confocal imaging of glutathione redox potential in living plant cells. J Microsc 231:299–316

    Article  PubMed  Google Scholar 

  • Seitz G, Gebhardt S, Beck JF, Bohm W, Lode HN, Niethammer D, Bruchelt G (1998) Ascorbic acid stimulates DOPA synthesis and tyrosine hydroxylase gene expression in the human neuroblastoma cell line SK-N-SH. Neurosci Lett 244:33–36

    Article  PubMed  CAS  Google Scholar 

  • Serpe MD, Nothnagel EA (1994) Effects of Yariv phenylglicosides on Rosa cell suspensions: evidence for the involvement of arabinogalactan proteins in cell proliferation. Planta 193:542–550

    Article  CAS  Google Scholar 

  • Sies H (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27:916–21

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Conklin P, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    Article  PubMed  CAS  Google Scholar 

  • Sommer-Knudsen J, Bacic A, Clarke AE (1998) Hydroxyproline-rich plant glycoproteins. Phytochemistry 47:483–497

    Article  CAS  Google Scholar 

  • Stasolla C (2010) Redox regulation of in vitro embryogenesis. Plant Physiol Biochem doi. doi:10.1016/j.plaphy.2009.10.007

    Google Scholar 

  • Szent-Giörgyi A (1963) Lost in the twentieth century. Annu Rev Biochem 36:1–15

    Article  Google Scholar 

  • Townsend DM, Tew KD, Tapiero H (2003) The importance of glutathione in human disease. Biomed Pharmacother 57:145–155

    Article  PubMed  CAS  Google Scholar 

  • Townsend DM, Manevich Y, He L, Hutchens S, Pazoles CJ, Tew KD (2009) Novel role for Glutathione S-Transferase π: regulator of protein S-glutathionylation following oxidative and nitrosative stress. J Biol Chem 284:436–445

    Article  PubMed  CAS  Google Scholar 

  • Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D, May MJ, Sung ZR (2000) 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 12:97–110

    PubMed  CAS  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:65–69

    Google Scholar 

  • Wingate VMP, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210

    Article  PubMed  CAS  Google Scholar 

  • Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) the biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Abant Izzet Baysal University, Bolu, Turkey

    Günce Şahin

  2. Plant Biology and Pathology, Aldo Moro University, Bari, Italy

    Mario C. De Tullio

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  1. Günce Şahin
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  2. Mario C. De Tullio
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Correspondence to Mario C. De Tullio .

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Editors and Affiliations

  1. Biotechnology Center in Southern Taiwan, Academia Sinica, Huandong Rd., Sinshih, Tainan, 74146, Taiwan R.O.C.

    Naser A. Anjum

  2. Biotechnology Center in Southern Taiwan, Academia Sinica, Huandong Rd., Sinshih, Tainan, 74146, Taiwan R.O.C.

    Ming-Tsair Chan

  3. Dept. Botany, Hamdard University, New Delhi, 110062, India

    Shahid Umar

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Şahin, G., De Tullio, M.C. (2010). A Winning Two Pair: Role of the Redox Pairs AsA/DHA and GSH/GSSG in Signal Transduction. In: Anjum, N., Chan, MT., Umar, S. (eds) Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9404-9_9

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