Abstract
Efficient phytoremediation of soils polluted with toxic elements greatly depends on the ability of selected plants to withstand the damages induced by these contaminants. Among other metabolites, glutathione (GSH) plays a fundamental dual role in tolerance as an antioxidant required for the attenuation of reactive oxygen species (ROS), such as superoxide (\({{\text{O}}_{ 2}}^{ \cdot - }\)) and hydrogen peroxide (H2O2) and as a precursor of phytochelatins (PCs). Understanding the regulatory mechanisms involved in sulphur assimilation and biothiols’ metabolism under metal and metalloid stress will provide the tools to select and obtain more tolerant plants with improved performance, where the cellular redox status and stress-related phytohormones are key players. Metal uptake and distribution depend greatly on the biothiol metabolism, and advanced metallomic analytical techniques offer the tools to characterize in detail functional aspects of metal(loid)–biothiol interaction. Therefore, we present in this chapter an insight in the impact of GSH on the cellular redox balance under metal stress, and how biothiols affect the dynamics of these contaminants in plants with possible implications for future phytoremediation approaches.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881
Ammar WB, Mediouni C, Tray B, Ghorbel MH, Jemal F (2008) Glutathione and phytochelatin contents in tomato plants exposed to cadmium. Biol Planta 52:314–320
Arruda MAZ, Azevedo RA (2009) Metallomics and chemical speciation: towards a better understanding of metal induced stress in plants. Ann Appl Biol 155:301–307
Ball L, Accotto G, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462
Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384
Batista BL, Nigar M, Mestrot A, Rocha BA, Júnior FB, Price AH, Raab A, Feldmann J (2014) Identification and quantification of phytochelatins in roots of rice to long-term exposure: evidence of individual role on arsenic accumulation and translocation. J Exp Bot 65:1467–1479
Behrens PW, Sicotte VJ, Delente J (1994) Microalgae as a source of stable isotopically labeled compounds. J Appl Phycol 6:113–121
Bluemlein K, Raab A, Meharg AA, Charnock JM, Feldmann J (2008) Can we trust mass spectrometry for determination of arsenic peptides in plants?: comparison of LC–ICP–MS and LC–ES-MS/ICP–MS with XANES/EXAFS in analysis of Thunbergia alata. Anal Bioanal Chem 390:1739–1751
Bluemlein K, Raab A, Feldmann J (2009) Stability of arsenic peptides in plant extracts: off-line versus on-line parallel elemental and molecular mass spectrometric detection for liquid chromatographic separation. Anal Bioanal Chem 393:357–366
Brammer H, Ravenscroft P (2009) Arsenic in groundwater: a threat to sustainable agriculture in South and South-East Asia. Environ Int 35:647–654
Bräutigam A, Schaumlöffel D, Krauss GJ, Wesenberg D (2009) Analytical approach for characterization of cadmium-induced thiol peptides—a case study using Chlamydomonas reinhardtii. Anal Bioanal Chem 395:1737–1747
Bräutigam A, Schaumlöffel D, Preud’Homme H, Thondorf I, Wesenberg D (2011) Physiological characterization of cadmium-exposed Chlamydomonas reinhardtii. Plant, Cell Environ 34:2071–2082
Briat J, Lebrun M (1999) Plant responses to metal toxicity. Comptes Rendus de l’Académie des Sciences-Series III-Sciences de la Vie 322:43–54
Carey AM, Lombi E, Donner E, de Jonge MD, Punshon T, Jackson BP, Guerinot ML, Price AH, Meharg AA (2012) A review of recent developments in the speciation and location of arsenic and selenium in rice grain. Anal Bioanal Chem 402:3275–3286
Carrasco-Gil S, Álvarez-Fernández A, Sobrino-Plata J, Millán R, Carpena-Ruiz RO, Leduc DL, Andrews JC, Abadía J, Hernández LE (2011) Complexation of Hg with phytochelatins is important for plant Hg tolerance. Plant, Cell Environ 34:778–791
Carrasco-Gil S, Siebner H, LeDuc DL, Webb SM, Millán R, Andrews JC, Hernández LE (2013) Mercury localization and speciation in plants grown hydroponically or in a natural environment. Environ Sci Technol 47:3082–3090
Carvalho CM, Chew EH, Hashemy SI, Lu J, Holmgren A (2008) Inhibition of the human thioredoxin system a molecular mechanism of mercury toxicity. J Biol Chem 283:11913–11923
Chao DY, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku JM, Zhao F-J, Salt DE (2014) Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12:e1002009
Chen YA, Chi WC, Trinh NN, Huang LY, Chen YC, Cheng KT, Huang TL, Lin CY, Huang HJ (2014) Transcriptome profiling and physiological studies reveal a major role for aromatic amino acids in mercury stress tolerance in rice seedlings. PLoS ONE 9:e95163
Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390
Cho-Ruk K, Kurukote J, Supprung P, Vetayasuporn S (2006) Perennial plants in the phytoremediation of lead-contaminated soils. Biotechnology 5:1–4
Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trend Plant Sci 7:309–315
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Cobbett CS, May MJ, Howden R, Rolls B (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2–1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J 16:73–78
Creissen G, Firmin J, Fryer M, Kular B, Leyland N, Reynolds H, Pastori G, Wellburn F, Baker N, Wellburn ABN, Wellburn A, Mullineaux P (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11:1277–1291
Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, Opdenakker K, Nair AR, Munters E, Artois TJ, Nawrot T, Vangronsveld J, Smeets K (2010) Cadmium stress: an oxidative challenge. Biometals 23:927–940
Cuypers A, Hendrix S, Amaral dos Reis R, Deckers J, De Smet S, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E (2016) Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front Plant Sci 7:470
Davidian J, Kopriva S (2010) Regulation of sulfate uptake and assimilation—the same or not the same? Mol Plant 3:314–325
Debeljak M, van Elteren JT, Vogel-Mikuš K (2013) Development of a 2D laser ablation inductively coupled plasma mass spectrometry mapping procedure for mercury in maize (Zea mays L.) root cross-sections. Anal Chim Acta 787:155–162
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109
Domínguez-Solís JR, López-Martín MC, Ager FJ, Ynsa MD, Romero LC, Gotor C (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotechnol J 2:469–476
Duker AA, Carranza EJM, Hale M (2005) Arsenic geochemistry and health. Environ Int 31:631–641
Ekino S, Susa M, Ninomiya T, Imamura K, Kitamura T (2007) Minamata disease revisited: an update on the acute and chronic manifestations of methyl mercury poisoning. J Neurol Sci 262:131–144
Flores-Cáceres ML, Hattab S, Hattab S, Boussetta H, Banni M, Hernández LE (2015) Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants. Plant Sci 233:165–173
Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191
Galant A, Preuss ML, Cameron JC, Jez JM (2011) Plant glutathione biosynthesis: diversity in biochemical regulation and reaction products. Front Plant Sci 2:45
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212
González-Ballester D, Casero D, Cokus S, Pellegrini M, Merchant SS, Grossman AR (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell 22:2058–2084
Griffith OW, Meister A (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (Sn-butyl homocysteine sulfoximine). J Biol Chem 254:7558–7560
Gromes R, Hothorn M, Lenherr ED, Rybin V, Scheffzek K, 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
Guo J, Dai X, Xu W, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026
Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Hanikenne M (2003) Chlamydomonas reinhardtii as a eukaryotic photosynthetic model for studies of heavy metal homeostasis and tolerance. New Phytol 159:331–340
Hanikenne M, Motte P, Wu MCS, Wang T, Loppes R, Matagne RF (2005) A mitochondrial half-size ABC transporter is involved in cadmium tolerance in Chlamydomonas reinhardtii. Plant, Cell Environ 28:863–873
Herbette S, Taconnat L, Hugouvieux V (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1751–1765
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911
Herschbach C, Rizzini L, Mult S, Hartmann T, Busch F, Peuke AD, Kopriva S, Ensminger I (2010) Over-expression of bacterial γ-glutamylcysteine synthetase (GSH1) in plastids affects photosynthesis, growth and sulphur metabolism in poplar (Populus tremula × Populus alba) dependent on the resulting γ-glutamylcysteine and glutathione levels. Plant, Cell Environ 33:1138–1151
Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH-oxidase. New Phytol 179:687–699
Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM (2007) Thiol-based regulation of redox-active glutamate-cysteine ligase from Arabidopsis thaliana. Plant Cell 19:2653–2661
Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot Article ID 87287
Hothorn M, Wachter A, Gromes R, Stuwe T, Rausch T, Scheffzek K (2006) Structural basis for the redox control of plant glutamate cysteine ligase. J Biol Chem 281:27557–27565
Howden R, Andersen CR, Goldsbrough PB, Cobbett CS (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073
Iiyama K, Lam TB, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104:315–320
Iqbal N, Khan NA, Nazar R, Teixeira da Silva JA (2012) Ethylene-stimulated photosynthesis results from increased nitrogen and sulfur assimilation in mustard types that differ in photosynthetic capacity. Environ Exp Bot 78:84–90
Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Järup L, Åkesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208
Jobe TO, Sung DY, Akmakjian G, Pham A, Komives EA, Mendoza-Cózatl DG, Schroeder JI (2012) Feedback inhibition by thiols outranks glutathione depletion: a luciferase-based screen reveals glutathione-deficient γ-ECS and glutathione synthetase mutants impaired in cadmium-induced sulfate assimilation. Plant J 70:783–795
Jones KC (1991) Contaminant trends in soils and crops. Environ Pollut 69:311–325
Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13:3145–3175
Jozefczak M, Keunen E, Schat H, Bliek M, Hernández LE, Carleer R, Remans T, Bohler S, Vangronsveld J, Cuypers A (2014) Differential response of Arabidopsis leaves and roots to cadmium: glutathione-related chelating capacity vs antioxidant capacity. Plant Physiol Biochem 83:1–9
Kabata-Pendias A (2010) Trace elements in soils and plants, 4th edn. CRC Press, Boca Raton
Keating MH, Mahaffey KR, Schoeny R, Rice G, Bullock O (1997) Mercury study report to congress, vol 1. Executive summary
Keunen E, Schellingen K, Vangronsveld J, Cuypers A (2016) Ethylene and metal stress: small molecule, big impact. Front Plant Sci 7:23
Koffler BE, Bloem E, Zellnig G, Zechmann B (2013) High resolution imaging of subcellular glutathione concentrations by quantitative immunoelectron microscopy in different leaf areas of Arabidopsis. Micron 45:119–128
Kopriva S, Rennenberg H (2004) Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55:1831–1842
Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420
Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167
Lee S, Moon JS, Ko T, Petros D, Goldsbrough PB, Korban SS (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663
Lemaire S, Keryer E, Stein M, Schepens I, Issakidis-Bourguet E, Gérard-Hirne C, Miginiac-Maslow M, Jacquot JP (1999) Heavy-metal regulation of thioredoxin gene expression in Chlamydomonas reinhardtii. Plant Physiol 120:773–778
Li Y, Dhankher OP, Carreira L, Lee D, Chen A, Schroeder JI, Balish RS, Meagher RB (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol 45:1787–1797
Li Y, Dhankher OP, Carreira L, Balish RS, Meagher RB (2005) Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial γ-glutamylcysteine synthetase. Environ Toxicol Chem 24:1376–1386
Liedschulte V, Wachter A, Zhigang A, Rausch T (2010) Exploiting plants for glutathione (GSH) production: uncoupling GSH synthesis from cellular controls results in unprecedented GSH accumulation. Plant Biotechnol J 8:807–820
Liu WJ, Wood BA, Raab A, McGrath SP, Zhao FJ, Feldmann J (2010) Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. Plant Physiol 152:2211–2221
Liu P, Cai WJ, Yu L, Yuan BF, Feng YQ (2015) Determination of phytochelatins in rice by stable isotope labeling coupled with liquid chromatography–mass spectrometry. J Agric Food Chem 63:5935–5942
Lombi E, Scheckel KG, Kempson IM (2011) In situ analysis of metal(loid)s in plants: state of the art and artefacts. Environ Exp Bot 72:3–17
Lopes MS, Iglesia-Turiño S, Cabrera-Bosquet L, Serret MD, Bort J, Febrero A, Araus JL (2013) Molecular and physiological mechanisms associated with root exposure to mercury in barley. Metallomics 5:1305–1315
Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant, Cell Environ 35:524–533
Matschullat J (2000) Arsenic in the geosphere—a review. Sci Total Environ 249:297–312
Maughan SC, Pasternak M, Cairns N, Kiddle G, Brach T, Jarvis R, Haas F, Nieuwland J, Lim B, Müller C et al (2010) Plant homologs of the Plasmodium falciparum chloroquine-resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc Natl Acad Sci U S A 107:2331–2336
Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, 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
Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562
Mera R, Torres E, Abalde J (2014) Sulphate, more than a nutrient, protects the microalga Chlamydomonas moewusii from cadmium toxicity. Aquat Toxicol 148:92–103
Millán R, Gamarra R, Schmid T, Sierra M, Quejido A, Sánchez D, Cardona A, Fernández M, Vera R (2006) Mercury content in vegetation and soils of the Almadén mining area (Spain). Sci Total Environ 368:79–87
Miszczak A, Rosłon M, Zbroja G, Brama K, Szalacha E, Gawrońska H, Pawlak K (2013) SEC ICP MS and CZE ICP MS investigation of medium and high molecular weight complexes formed by cadmium ions with phytochelatins. Anal Bioanal Chem 405:4667–4678
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trend Plant Sci 7:405–410
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trend Plant Sci 9:490–498
Mohan TC, Castrillo G, Navarro C, Zarco-Fernandez S, Ramireddy E, Mateo C, Zamarreño AM, Paz-Ares J, Muñoz R, Garcia-Mina JM, Hernandez LE, Schmülling T, Leyva A (2016) Cytokinin determines thiol-mediated arsenic tolerance and accumulation in Arabidopsis thaliana. Plant Physiol 171:418–1426
Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Biol 52:561–591
Montero-Palmero MB, Martín-Barranco A, Escobar C, Hernández LE (2014a) Early transcriptional responses to mercury: a role for ethylene in mercury-induced stress. New Phytol 201:116–130
Montero-Palmero MB, Ortega-Villasante C, Escobar C, Hernández LE (2014b) Are plant endogenous factors like ethylene modulators of the early oxidative stress induced by mercury? Front Environ Sci 2:34
Nahar N, Rahman A, Moś M, Warzecha T, Algerin M, Ghosh S, Johnson-Brousseau S, Mandal A (2012) In silico and in vivo studies of an Arabidopsis thaliana gene, ACR2, putatively involved in arsenic accumulation in plants. J Mol Model 18:4249–4262
Nakayama M, Akashi T, Hase T (2000) Plant sulfite reductase: Molecular structure, catalytic function and interaction with ferredoxin. J Inorg Biochem 82:27–32
Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian J, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279
Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304
Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trend Plant Sci 12:125–134
Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH (2011) Glutathione. The Arabidopsis Book/American Society of Plant Biologists 9
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Márquez-García B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant, Cell Environ 35:454–484
Nriagu JO (1996) History of global metal pollution. Science 272:223–224
Nriagu J, Becker C (2003) Volcanic emissions of mercury to the atmosphere: global and regional inventories. Sci Total Environ 304:3–12
Ortega-Villasante C, Rellán-Álvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251
Ortega-Villasante C, Hernández LE, Rellán-Álvarez R, el Campo FF, Carpena-Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176:96–107
Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728
Pal R, Rai J (2010) Phytochelatins: peptides involved in heavy metal detoxification. App Biochem Biotechnol 160:945–963
Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172
Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters ABCC1 and ABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288
Paulose B, Chhikara S, Coomey J, Jung HI, Vatamaniuk O, Dhankher OP (2013) A γ-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25:4580–4595
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. Anal Biochem 363:58–69
Queval G, Jaillard D, Zechmann B, Noctor G (2011) Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant, Cell Environ 34:21–32
Rauser WE (1995) Phytochelatins and related peptides. Structure, biosynthesis, and function. Plant Physiol 109:1141–1149
Rellán-Álvarez R, Hernández LE, Abadía J, Álvarez-Fernández A (2006) Direct and simultaneous determination of reduced and oxidized glutathione and homoglutathione by liquid chromatography-electrospray/mass spectrometry in plant tissue extracts. Anal Biochem 356:254–264
Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Rio LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243
Romero-Puertas M, Rodríguez-Serrano M, Corpas F, Gomez Md, del Rio LA, Sandalio L (2004) Cadmium-induced subcellular accumulation of O2—and H2O2 in pea leaves. Plant, Cell Environ 27:1122–1134
Rouhier N, Couturier J, Jacquot JP (2006) Genome-wide analysis of plant glutaredoxin systems. J Exp Bot 57:1685–1696
Rouhier N, Couturier J, Johnson MK, Jacquot J (2010) Glutaredoxins: roles in iron homeostasis. Trend Biochem Sci 35:43–52
Sánchez-Bermejo E, Castrillo G, Del Llano B, Navarro C, Zarco-Fernández S, Martinez-Herrera DJ, Leo-del Puerto Y, Muñoz R, Cámara C, Paz-Ares J, Alonso-Blanco C, Leyva A (2014) Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat Commun 5:4617
Sandalio L, Dalurzo H, Gomez M, Romero-Puertas M, del Rio L (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126
Schädler S, Morio M, Bartke S, Rohr-Zänker R, Finkel M (2011) Designing sustainable and economically attractive brownfield revitalization options using an integrated assessment model. J Environ Manag 92:827–837
Schellingen K, Van Der Straeten D, Vandenbussche F, Prinsen E, Remans T, Vangronsveld J, Cuypers A (2014) Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression. BMC Plant Biol 14:1
Schellingen K, Van Der Straeten D, Remans T, Vangronsveld J, Keunen E, Cuypers A (2015a) Ethylene signalling is mediating the early cadmium-induced oxidative challenge in Arabidopsis thaliana. Plant Sci 239:137–146
Schellingen K, Van Der Straeten D, Remans T, Loix C, Vangronsveld J, Cuypers A (2015b) Ethylene biosynthesis is involved in the early oxidative challenge induced by moderate Cd exposure in Arabidopsis thaliana. Environ Exp Bot 117:1–11
Schnaubelt D, Queval G, Dong Y, Díaz-Vivancos P, Makgopa ME, Howell G, De Simone A, Bai J, Hannah MA, Foyer CH (2015) Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. Plant, Cell Environ 38:266–279
Semane B, Cuypers A, Smeets K, Van Belleghem F, Horemans N, Schat H, Vangronsveld J (2007) Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiol Plant 129:519–528
Serrano N, Díaz-Cruz JM, Ariño C, Esteban M (2015) Recent contributions to the study of phytochelatins with an analytical approach. Trend Anal Chem 73:129–145
Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant, Cell Environ 35:334–346
Sharma SS, Dietz K (2009) The relationship between metal toxicity and cellular redox imbalance. Trend Plant Sci 14:43–50
Sobrino-Plata J, Ortega-Villasante C, Laura Flores-Cáceres M, Escobar C, Del Campo FF, Hernández LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954
Sobrino-Plata J, Herrero J, Carrasco-Gil S, Pérez-Sanz A, Lobo C, Escobar C, Millán R, Hernández LE (2013) Specific stress responses to cadmium, arsenic and mercury appear in the metallophyte Silene vulgaris when grown hydroponically. RSC Adv 3:4736–4744
Sobrino-Plata J, Carrasco-Gil S, Abadía J, Escobar C, Álvarez-Fernández A, Hernández LE (2014a) The contribution of glutathione in Arabidopsis mercury tolerance resembles its role under cadmium stress. Metallomics 6:356–366
Sobrino-Plata J, Meyssen D, Cuypers A, Escobar C, Hernández LE (2014b) Glutathione is a key antioxidant metabolite to cope with mercury and cadmium stress. Plant Soil 377:369–381
Song WY, Yamaki T, Yamaji H, Ko D, Jung KH, Fuji-Kashino M, An G, Martinoia E, Lee Y, Ma JF (2014) A rice ABC transporter, OsABCC1, reduced arsenic accumulation in the grain. Proc Natl Acad Sci U S A 111:15699–15704
Sung DY, Kim TH, Komives EA, Mendoza-Cózatl DG, Schroeder JI (2009) ARS5 is a component of the 26S proteasome complex, and negatively regulates thiol biosynthesis and arsenic tolerance in Arabidopsis. Plant J 59:802–813
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Molecular, clinical and environmental toxicology. Exp Supp 101:133–164
Tognetti VB, Mühlenbock R, Van Breusegem F (2012) Stress homeostasis- the redox and auxin perspective. Plant, Cell Environ 35:321–333
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616
UNEP Chemicals Branch (2013) The global atmospheric mercury assessment: sources, emissions and transport. Geneva, Switzerland
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794
Vatamaniuk OK, Mari S, Lu Y, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci U S A 96:7110–7115
Vernoux T, Wilson RC, Seeley KA, Reichheld J, 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 12:97–109
Wachter A, Wolf S, Steininger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41:15–30
Wang SH, Zang H, Zhang Q, Jin GM, Jiang SJ, Jiang D, He QY, Li ZP (2015) Copper- induced oxidative stress and responses of the antioxidant system in roots of Medicago sativa. J Agron Crop Sci 197:418–429
Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920
Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163:273–286
Wood BA, Feldmann J (2012) Quantification of phytochelatins and their metal(loid) complexes: critical assessment of current analytical methodology. Anal Bioanal Chem 402:3299–3309
Xiang C, Oliver DJ (1998) Glutathione metabolic genes co-ordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550
Yannarelli GG, Fernández-Álvarez AJ, Santa-Cruz DM, Tomaro ML (2007) Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. Phytochemistry 68:505–512
Yoshida S, Tamaoki M, Ioki M, Ogawa D, Sato Y, Aono M, Kubo A, Saji S, Saji H, Satoh S, Nakajima N (2009) Ethylene and salicylic acid control glutathione biosynthesis in ozone-exposed Arabidopsis thaliana. Physiol Plant 136:284–298
Zechmann B (2014) Compartment-specific importance of glutathione during abiotic and biotic stress. Front Plant Sci 5:566
Zechmann B, Müller M (2010) Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma 246:15–24
Zenk MH (1996) Heavy metal detoxification in higher plants-a review. Gene 179:21–30
Zhou ZS, Yang SN, Li H, Zhu CC, Liu ZP, Yang ZM (2013) Molecular dissection of mercury-responsive transcriptome and sense/antisense genes in Medicago truncatula by high-throughput sequencing. J Hazard Mater 252:123–131
Zhu YL, Pilon-Smits EA, Jouanin L, Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–80
Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1177
Zimmer D, Kruse J, Baum C, Borca C, Laue M, Hause G, Meissner R, Leinweber P (2011) Spatial distribution of arsenic and heavy metals in willow roots from a contaminated floodplain soil measured by X-ray fluorescence spectroscopy. Sci Total Environ 409:4094–4100
Acknowledgments
This work was financially supported by the Spanish MINECO through Project No. AGL2014-53771-R.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Hernández, L.E. et al. (2016). Glutathione Metabolism in Plants Under Metal and Metalloid Stress and its Impact on the Cellular Redox Homoeostasis. In: Gupta, D., Palma, J., Corpas, F. (eds) Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer, Cham. https://doi.org/10.1007/978-3-319-44081-1_8
Download citation
DOI: https://doi.org/10.1007/978-3-319-44081-1_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-44080-4
Online ISBN: 978-3-319-44081-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)