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Sulfur Compounds in Multiple Compensation Reactions of Abiotic Stress Responses

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Part of the book series: Proceedings of the International Plant Sulfur Workshop ((PIPSW,volume 1))

Abstract

Plants interact with sulfur in two different ways. As a macronutrient sulfur is needed for growth and development; at the same time, sulfur is an important substrate and reductant during various forms of stresses mediated by the abiotic environment. The use of sulfur compounds as substrate and/or reductant in compensation reactions of abiotic stresses including oxidative stress, heavy metal and xenobiotic exposure is discussed with special emphasis on the S-containing tri-peptide glutathione (GSH). The examples shown indicate that individual components of S metabolism are involved in different processes of abiotic stress compen‑sation. In the present review the current knowledge of GSH (i) as reductant in the compensation of oxidative stress, (ii) as reductant as well as a substrate in redox reactions, (iii) its direct and indirect involvement in posttranscriptional modification reactions, and (iv) its constitution as a substrate for chelating heavy metals and for conjugation of xenobiotic is discussed. Competition with plant development and growth is also considered.

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References

  • Almagro L, Ros LVG, Belchi-Navarro S, Bru R, Ros Barcelo A, Pedren MA (2009) Class III peroxidises in plant defence reactions. J Exp Bot 60:377–390

    Article  PubMed  CAS  Google Scholar 

  • Ammar WB, Mediouni C, Tray B, Ghorbel MH, Jemal F (2008) Glutathione and phytochelatin contents in tomato plants exposed to cadmium. Biol Plant 52:314–320

    Article  Google Scholar 

  • Anjum NA, Umar S, Ahmad A, Iqbal M, Khan NA (2008) Sulfur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regul 54:271–279

    Article  CAS  Google Scholar 

  • Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Sci 172:876–887

    Article  CAS  Google Scholar 

  • Banerjee S, Goswami R (2010) GST profile expression study in some selected plants: in silico approach. Mol Cell Biochem 336:109–126

    Article  PubMed  CAS  Google Scholar 

  • Blum R, Beck A, Korte A, Stengel A, Letzel T, Lendzian K, Grill E (2007) Function of phytochelain synthase in catabolism of glutathione-conjugates. Plant J 49:740–749

    Article  PubMed  CAS  Google Scholar 

  • Blum R, Meyer KC, Wünschmann J, Lendzian KJ, Grill E (2010) Cytosolic action of phytochelatin synthase. Plant Physiol 153:159–169

    Article  PubMed  CAS  Google Scholar 

  • Bovet L, Eggmann T, Meylan-Bettex M, Polier J, Kammer P, Marin E, Feller U, Martinoia E (2003) Transcript levels of ATMRPs after Cadmium treatment: induction of AtMRP3. Plant Cell Environ 26:371–381

    Article  CAS  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    Article  PubMed  CAS  Google Scholar 

  • Cameron JC, Pakrasi HB (2010) Essential role of glutathione in acclimation to environmental and redox perturbations in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 154:1672–1685

    Article  PubMed  CAS  Google Scholar 

  • Chen A, Komives EA, Schroeder JI (2006) An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiol 141:108–120

    Article  PubMed  CAS  Google Scholar 

  • Di Baccio D, Kopriva S, Sebastiani L, Rennenberg H (2005) Does glutathione metabolism have a role in the defence of poplar against zinc excess? New Phytol 167:73–80

    Article  PubMed  Google Scholar 

  • Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350

    Article  PubMed  CAS  Google Scholar 

  • Edwards R, Dixon PD (2005) Plant glutathione transferases. Method Enzymol 401:169–186

    Article  CAS  Google Scholar 

  • Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Eimers MC, Watmough SA, Buttle JM, Dillon PJ (2007) Drought-induced sulphate release from a wetland in south-central Ontario. Environ Monit Assess 127:399–407

    Article  PubMed  CAS  Google Scholar 

  • Ernst WHO, Krauss G-J, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulfur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143

    PubMed  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crope plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Gong J-M, Lee DA, Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci USA 100:10118–10123

    Article  PubMed  CAS  Google Scholar 

  • Grantz DA, Farrar JF (1999) Acute exposure to ozone inhibits rapid carbon translocation from source leaves of Pima cotton. J Exp Bot 50:1253–1262

    CAS  Google Scholar 

  • Grzam A, Martin MN, Hell R, Meyer AJ (2007) γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S-conjugates in Arabidopsis. FEBS Lett 581:3131–3138

    Article  PubMed  CAS  Google Scholar 

  • Haberer K, Herbinger K, Alexou M, Tausz M, Rennenberg H (2007) Antioxidative defence of old growth beech (Fagus sylvatica) under double ambient O-3 concentrations in a free-air exposure system. Plant Biol 9:215–226

    Article  PubMed  CAS  Google Scholar 

  • Haberer K, Herbinger K, Alexou M, Rennenberg H, Tausz M (2008) Effects of drought and canopy ozone exposure on antioxidants in fine roots of mature European beech (Fagus sylvatica). Tree Physiol 28:713–719

    Article  PubMed  CAS  Google Scholar 

  • Heizmann U, Kreuzwieser J, Schnitzler J-P, Brüggemann N, Rennenberg H (2001) Assimilate transport in the xylem sap of young oak (Quercus robur) trees. Plant Biol 3:132–138

    Article  CAS  Google Scholar 

  • Herschbach C (2003) Whole Plant regulation of sulfur nutrition of deciduous trees – influences of the environment. Plant Biol 5:233–244

    Article  CAS  Google Scholar 

  • Herschbach C, Teuber M, Eiblmeier M, Ehlting B, Ache P, Polle A, Schnitzler J-P, Rennenberg H (2010a) Changes in sulphur metabolism of grey poplar (Populus x canescens) leaves during salt stress: a metabolic link to photorespiration. Tree Physiol 30:1161–1173

    Article  PubMed  CAS  Google Scholar 

  • Herschbach C, Scheerer U, Rennenberg R (2010b) Redox states of glutathione and ascorbate in root tipps of poplar (Populus tremula x P. alba) depend on phloem transport from the shoot to the roots. J Exp Bot 61:1065–1074

    Article  PubMed  CAS  Google Scholar 

  • Herschbach C, Gessler A, Rennenberg H (2011) Long-distance transport and plant internal cycling of N- and S-compounds. Prog Bot 73:161–188

    Google Scholar 

  • Hofer N, Alexou M, Heerdt C, Low M, Werner H, Matyssek R, Rennenberg H, Haberer K (2008) Seasonal differences and within-canopy variations of antioxidants in mature spruce (Picea abies) trees under elevated ozone in a free-air exposure system. Environ Pollut 154:241–253

    Article  PubMed  CAS  Google Scholar 

  • Howden R, Goldsbrough PB, Andersen CR, Cobbett CS (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066

    Article  PubMed  CAS  Google Scholar 

  • Jaspers P, Kangasjarvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413

    Article  PubMed  CAS  Google Scholar 

  • Jin X, Yang X, Mahmood Q, Islam E, Liu D, Li H (2008) Response of antioxidant enzymes, ascorbate and glutathione metabolism towards cadmium in hyperaccumulator and nonhyperaccumulator ecotypes of Sedium alfredii H. Environ Toxicol 23:517–529

    Article  PubMed  CAS  Google Scholar 

  • Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495

    Article  PubMed  CAS  Google Scholar 

  • Kopriva S, Rennenberg H (2004) Control of sulfate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842

    Article  PubMed  CAS  Google Scholar 

  • Koprivova A, Kopriva S, Jager D, Will B, Jouanin L, Rennenberg H (2002) Evaluation of transgenic poplars over-expressing enzymes of glutathione synthesis for phytoremediation of cadmium. Plant Biol 4:664–670

    Article  CAS  Google Scholar 

  • Laisk A, Kull O, Moldau H (1989) Ozone concentration in leaf intercellular air spaces is close to zero. Plant Physiol 90:1163–1167

    Article  PubMed  CAS  Google Scholar 

  • Lan T, Yang Z-L, Yang X, Liu Y-J, Wang X-R, Zeng Q-Y (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766

    Article  PubMed  CAS  Google Scholar 

  • Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) No signals in the haze. Nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Rennenberg H, Matyssek R (2006) Effects of elevated pO3 on carbon cycle between above and belowground organs of trees. J Environ Sci (China) 18:932–936

    Article  CAS  Google Scholar 

  • Loscos J, Naya L, Ramos J, Clemente MR, Matamoros MA, Becana A (2006) A reassessment of substrate specificity and activation of phytochelatin synthases from model plants by physiologically relevant metals. Plant Physiol 140:1213–1221

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives AE, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatines, glutathione and cadmium in the phloem sap of Brassica napus. A role for-thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259

    Article  PubMed  Google Scholar 

  • Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian J-C, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148

    Article  PubMed  CAS  Google Scholar 

  • Noctor G (2006) Metabolic signalling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425

    Article  PubMed  CAS  Google Scholar 

  • Ohkama-Ohtsu N, Zhao P, Xiang C, Oliver DJ (2007) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49:878–888

    Article  PubMed  CAS  Google Scholar 

  • Olmos E, Kiddle G, Pellny TK, Kumar S, Foyer CH (2006) Modulation of plants morphology, root architecture, and cell structure by low vitamin C in Arabidopsis thaliana. J Exp Bot 57:1645–1655

    Article  PubMed  CAS  Google Scholar 

  • Öztetik E (2008) A tale of plant glutathione S-transferases: since 1970. Bot Rev 74:419–437

    Article  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 

  • Pinto DM, Blande JD, Souza SR, Nerg A-M, Holopainen JK (2010) Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmospheres: the ecological effects. J Chem Ecol 36:22–34

    Article  PubMed  CAS  Google Scholar 

  • Polle H, Rennenberg H (1993) Significance of antioxidants in plant adaptation to environmental stress. In: Fowden L, Mansfield T, Stoddard F (eds) Plant adaptation to environmental stress. Chapman & Hall, London, pp 263–273

    Google Scholar 

  • Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40:537–548

    Article  CAS  Google Scholar 

  • Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134:1479–1487

    Article  PubMed  CAS  Google Scholar 

  • Rennenberg H (1984) The fate of excess sulfur in higher plants. Annu Rev Plant Physiol 35:121–153

    Article  CAS  Google Scholar 

  • Rennenberg H, Lamoureux G (1990) Physiological processes that modulate the concentration of glutathione in plant cells. In: Rennenberg H, Brunold Ch, De Kok LJ, Stulen I (eds) Sulfur nutrition and assimilation in higher plants; fundamental, environmental, and agricultural aspects. SPB Acadamic Publishing, The Hague, pp 53–65

    Google Scholar 

  • Rennenberg H, Loreto F, Polle A, Brilli F, Fares S, Beniwal RS, Gessler A (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8:556–571

    Article  PubMed  CAS  Google Scholar 

  • Rennenberg H, Herschbach C, Haberer K, Kopriva S (2007) Sulfur metabolism in plants: are trees different? Plant Biol 9:620–637

    Article  PubMed  CAS  Google Scholar 

  • Riikonen J, Kets K, Darbah J, Oksanen E, Sober A, Vapaavuori E, Kubiske ME, Nelson N, Karnosky DF (2008) Carbon gain and bud physiology in Populus tremuloides and Betula papyrifera grown under long-term exposure to elevated concentrations of CO2 and O3. Tree Physiol 28:243–254

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot J-P (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    Article  PubMed  CAS  Google Scholar 

  • Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-Nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143:1282–1292

    Article  PubMed  Google Scholar 

  • Sánchez-Fernández 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 mechanistically different forms of redox control. Proc Natl Acad Sci USA 94:2745–2750

    Article  PubMed  Google Scholar 

  • Sardans J, Peňuelas J, Ogaya R (2008) Drought’s impact on Ca, Fe, Mg, Mo and S concentration and accumulation patterns in the plants and soil of a Mediterranean evergreen Quercus ilex forest. Biogeochemistry 87:49–69

    Article  CAS  Google Scholar 

  • Schachtman DP, Goodger JQD (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13:281–287

    Article  PubMed  CAS  Google Scholar 

  • Schulte M (1998) Der Einfluss von erhöhtem atmospherischem CO2 auf den Kohlenstoff-, Stickstoff- und Schwefelhaushalt von Eichen. Ph.D thesis Albert-Ludwigs-University, Freiburg

    Google Scholar 

  • Seegmüller S (1998) Der Einfluss von Mykorrizen, atmospärischem Kohlendioxid und Wassermangel auf das Wachstum und die Schwefel- und Stickstoffernährung der Stieleiche (Quercus robur L.). Ph.D thesis Albert-Ludwigs-University, Freiburg

    Google Scholar 

  • Sircelj H, Tausz M, Grill D, Batic F (2005) Biochemical responses in leaves of two apple tree cultivars subjected to progressing drought. J Plant Physiol 162:1308–1318

    Article  PubMed  CAS  Google Scholar 

  • Steinkamp R, Rennenberg H (1985) Degradation of glutathione in plant cells: evidence against the participation of a γ-glutamyltranspeptidase. Z Naturforsch 40c:29–33

    CAS  Google Scholar 

  • Szalai G, Kellös T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80

    Article  CAS  Google Scholar 

  • Tardieu F, Parent B, Simonneau T (2010) Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes. Plant Cell Environ 3:636–647

    Article  Google Scholar 

  • Tausz M, Sircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  PubMed  CAS  Google Scholar 

  • Topa MA, McDermitt DJ, Yun SC (2004) Do elevated ozone and variable light alter carbon transport to roots in sugar maple? New Phytol 162:173–186

    Article  Google Scholar 

  • Vatamaniuk OK, Mari S, Lu Y-P, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. J Biol Chem 275:31451–31459

    Article  PubMed  CAS  Google Scholar 

  • Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631

    Article  PubMed  CAS  Google Scholar 

  • Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86:345–362

    Article  PubMed  CAS  Google Scholar 

  • Wojas S, Hennig J, Plaza S, Geisler M, Siemianowski O, Sklodowska A, Ruszczynska A, Bulska E, Antosiewicz DM (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Pollut 157:2781–2789

    Article  PubMed  CAS  Google Scholar 

  • Wolf AE, Dietz K-J, Schröder P (1996) Degradation of glutathione S-conjugates by a carboxypeptidase in the plant vacuole. FEBS Lett 384:31–34

    Article  PubMed  CAS  Google Scholar 

  • Xiang CB, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550

    PubMed  CAS  Google Scholar 

  • Zhao FY, Zhang H (2006) Salt and paraquat stress tolerance results from co-expression of the Suaeda salsa glutathione S-transferase and catalase in transgenic rice. Plant Cell Tissue Organ Cult 86:349–358

    Article  CAS  Google Scholar 

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Rennenberg, H., Herschbach, C. (2012). Sulfur Compounds in Multiple Compensation Reactions of Abiotic Stress Responses. In: De Kok, L., et al. Sulfur Metabolism in Plants. Proceedings of the International Plant Sulfur Workshop, vol 1. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4450-9_25

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