Abstract
Glutathione (GSH) is essential for the proper development of root nodules during the symbiotic association of legume and rhizobia. It is involved in the antioxidant defense, the detoxification of xenobiotics, and the tolerance to abiotic and biotic stresses. The high level of GSH in root nodules and the presence of an active ascorbate-glutathione (AsA-GSH) cycle suggest that GSH participates in the protection of the nitrogen-fixing process against reactive oxygen species (ROS) resulting from the active nodule metabolism. Glutathione-related enzymes also play a critical role in defense against ROS: (a) glutathione peroxidase (GPX) is a H2O2 scavenger that uses GSH as a reductant, (b) glutathione reductase (GR) reduces GSSG using NADPH as a source of reducing power and maintaining the GSH/GSSG ratio in cells, (c) glutathione-S-transferase (GST) catalyzes the nucleophilic conjugation of GSH with several electrophilic substrates, and (d) glutaredoxins (GRXs), small redox proteins from the thioredoxin (TRX) superfamily, use GSH as electron donor. In this chapter, the role of GSH and its related enzymes was analyzed in free-living rhizobia and in the symbiosis with the legumes as well as the responses to different abiotic stresses (acid pH, saline, drought, and heavy metals/metalloids).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abou-Shanab RA, Ghozlan H, Ghanem K, Moawad H (2005) Behaviour of bacterial populations isolated from rhizosphere of Diplachne fusca dominant in industrial sites. World J Microbiol Biotechnol 21:1095–1101
Alesandrini F, Mathis R, Van de Sype G, Hérouart D, Puppo A (2003) Possible roles of a cysteine protease and hydrogen peroxide in soybean nodule development and senescence. New Phytol 158:131–138
Alexander E, Pham D, Steck TR (1999) The viable but non-culturable condition is induced by copper in Agrobacteriuim Tumefaciens and Rhizobium leguminosarum. Appl Env Microbiol 65:3754–3756
Allocati N, Federici L, Masulli M, Di Llio C (2008) Glutathione transferases in bacteria. FEBS J 276:58–75
Alloway BJ (2012) Sources of heavy metals and metalloids in soils. In: Alloway BJ (ed) Heavy metals in soils. Springer, Heidelberg, pp 15–50
Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids – a review. Environ Exp Bot 75:307–324
Balestrasse KB, Gardey L, Gallego SM, Tomaro ML (2001) Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Aust J Plant Physiol 28:497–504
Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodule and roots of soybean plants. Funct Plant Biol 30:57–64
Balestrasse KB, Gallego SM, Tomaro ML (2006) Oxidation of the enzymes involved in nitrogen assimilation plays an important role in the cadmium-induced toxicity in soybean plants. Plant Soil 284:187–194
Bamborough L, Cummings SP (2008) The impact of increasing heavy metal stress on the diversity and structure of the bacterial and actinobacterial communities of metallophytic grassland soil. Biol Fertil Soils 45:273–280
Bartoli CG, Guaimet JJ, Kiddle G, Pastori GM, Di Cagno R, Theodoulou F, Foyer CH (2005) Ascorbate content of wheat leaves is not determined by maximal l-galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress. Plant Cell Environ 28:1073–1081
Becana M, Klucas RV (1992) Transition metals in legume root nodules. Iron dependent free radical production increases during nodule senescence. PNAS 89:8958–8962
Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381
Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytologist 188:960–976D
Bianucci E, Fabra A, Castro S (2008) Growth of Bradyrhizobium sp. SEMIA 6144 in response to methylglyoxal: role of glutathione. Curr Microbiol 56:371–375
Bianucci E, Fabra A, Castro S (2011) Cadmium accumulation and tolerance in Bradyrhizobium spp. (peanut microsymbionts). Curr Microbiol 62:96–100
Bianucci E, Fabra A, Castro S (2012a) Involvement of glutathione and enzymatic defense system against cadmium toxicity in Bradyrhizobium sp. strains (peanut symbionts). Biometals 25:23–32
Bianucci E, Sobrino-Plata J, Carpena-Ruiz R, Tordable MC, Fabra A, Hernández L, Castro S (2012b) Contribution of phytochelatins to cadmium tolerance in peanut plants. Metallomics 4:1119–1124
Bianucci E, Fullana C, Furlan A, Castro S (2013a) Antioxidant defense system responses and role of nitrate reductase in the redox balance maintenance in Bradyrhizobium japonicum strains exposed to cadmium. Enzyme Microb Technol 53:345–350
Bianucci E, Furlan A, Rivadeneira J, Sobrino-Plata J, Carpena-Ruiz R, Tordable MC, Fabra A, Hernández L, Castro S (2013b) Influence of cadmium on the symbiotic interaction established between peanut (Arachis hypogaea L.) and sensitive or tolerant bradyrhizobial strains. J Environ Manag 130:126–134
Bianucci E, Furlan A, Isaia A, Peralta JM, Hernández LE, Castro S (2016) Impact of arsenic in bradyrhizobia strains and in the symbiotic interaction with peanut plant. Biocell 40(1):113
Bright J, Desikan R, Tancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122
Brookes PC, Mc Grath SP (1984) Effect of metal toxicity on the size of the soil microbial biomass. Eur J Soil Sci 10:1365–2389
Broos K, Uyttebroek M, Mertens J, Smolders E (2004) A survey of symbiotic nitrogen fixation by white clover grown on metal contaminated soils. Soil Biol Biochem 36:633–640
Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207
Cárpena R, Esteban E, Lucena JJ, Peñalosa S, Vázquez P, Zornoza P, Gárate A (2006) Simbiosis y fitorrecuperación de suelos. In: Bedmar EJ, González J, Lluch C, Rodelas MB (eds) Fijación de Nitrógeno: Fundamentos y Aplicaciones. Granada, España, pp 255–268
Chen WX, Li GS, Qi YL, Wang ET, Yuan HL, Li JL (1991) Rhizobium huakuii sp. nov. isolated from the root nodules of Astragalus sinicus. Int J Syst Bacteriol 41:275–280
Clemente MR, Bustos-Sanmamed P, Loscos J, James EK, Pérez-Rontomé C, Navascués J, Gay M, Becana M (2012) Thiol synthetases of legumes: immunogold localization and differential gene regulation by phytohormones. J Exp Bot 63:3923–3934
Coba de la Peña T, Redondo FJ, Manrique E, Lucas MM, Pueyo JJ (2010) Nitrogen fixation persists under conditions of salt stress in transgenic Medicago truncatula plants expressing a cyanobacterial flavodoxin. Plant Biotechnol J 8:954–965
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182
Colville L, Kranner I (2010) Desiccation tolerant plants as model systems to study redox regulation of protein thiols. Plant Growth Regul 62:241–255
Cook D, Dreyer D, Bonnet D, Howell M, Nony E, Van den Bosch K (1995) Transient induction of a peroxidase gene in Medicago trunculata precedes infection by Rhizobium meliloti. Plant Cell 7:43–55
Corticeiro SC, Lima AI, Figueira EM (2006) The importance of glutathione in oxidative status of Rhizobium leguminosarum biovar viciae under Cd exposure. Enzym Microb Technol 40:132–137
Corticeiro S, Freitas R, Figueira E (2013) The role of GSTs in the tolerance of Rhizobium leguminosarum to cadmium. Biometals 26:879–886
Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. PNAS 83:3811–3815
Dalton DA, Langeberg L, Treneman N (1993) Correlations between the ascorbate-glutathione pathway and effectiveness in legume root nodules. Physiol Plant 87:365–370
Dalton DA, Boniface C, Turner Z, Lindahl A, Kim HJ, Jelinek L, Govindarajulu M, Finger RE, Taylor CG (2009) Physiological roles of glutathione S-transferases in soybean root nodules. Plant Physiol 150:521–530
Dary M, Chamber-Perez MA, Palomares AJ, Pajuelo E (2010) ‘In situ’ phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330
El Msehli S, Lambert A, Baldacci-Cresp F, Hopkins J, Boncompagni E, Smiti SA, Hérouart D, Frendo P (2011) Crucial role of (homo)glutathione in nitrogen fixation in Medicago truncatula nodules. New Phytol 192:496–506
Evans J, Dear B, O’Connor G (1990) Influence of an acid soil on the herbage yield and nodulation of five annual pasture legumes. Aust J Exp Agric 30:55–60
Evans PJ, Gallesi D, Mathieu C, Hernández MJ, de Felipe N, Halliwell B, Puppo A (1999) Oxidative stress occurs during soybean nodule senescence. Planta 208:73–79
Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72
Frendo P, Gallesi D, Turnbull R, Van de Sype G, Hérouart D, Puppo A (1999) Localisation of glutathione and homoglutathione in Medicago truncatula is correlated to a differential expression of genes involved in their synthesis. Plant J 17:215–219
Frendo P, Hernández-Jiménez MJ, Mathieu C, Duret L, Gallesi D, Van de Sype G, Hérouart D, Puppo A (2001) A Medicago truncatula homoglutathione synthetase is derived from glutathione synthetase by gene duplication. Plant Physiol 126:1706–1715
Frendo P, Harrison J, Norman C, Hernández-Jiménez MJ, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol Plant-Microbe Interact 18:254–259
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. PNAS 103:1988–1993
Furlan A, Llanes A, Luna V, Castro S (2012) Physiological and biochemical responses to drought stress and subsequent rehydration in the symbiotic association peanut-Bradyrhizobium sp. ISRN Agron. https://doi.org/10.5402/2012/318083
Furlan A, Llanes A, Luna V, Castro S (2013) Abscisic acid mediates hydrogen peroxide production in peanut induced by water stress. Biol Plant 57:555–558
Furlan A, Bianucci E, Tordable MC, Castro S, Dietz K (2014) Antioxidant enzyme activities and gene expression patterns in peanut nodules during a drought and rehydration cycle. Funct Plant Biol 41:704–713
Furlan A, Bianucci E, Tordable MC, Kleinert A, Valentine A, Castro S (2016) Dynamic responses of photosynthesis and antioxidant system during a drought and rehydration cycle in peanut plants. Funct Plant Biol 43:337–345
Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial process in agriculture soils – a review. Soil Biol Biochem 30:1389–1414
Gogorcena Y, Iturbe-Ormaetxe I, Escuredo PR, Becana M (1995) Antioxidant defenses against activated oxygen in pea nodules subjected to water stress. Plant Physiol 108:753–759
Gómez-Sagasti MT, Marino D (2015) PGPRs and nitrogen-fixing legumes: a perfect team for efficient Cd phytoremediation? Front Plant Sci 6:81
Graham P (1992) Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions. Can J Microbiol 38:475–484
Gratão P, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494
Groten K, Vanacker H, Dutilleul C, Bastian F, Bernard S, Carzaniga R, Foyer CH (2005) The roles of redox processes in pea nodule development and senescence. Plant Cell Environ 28:1293–1304
Günther C, Schlereth A, Udvardi M, Ott T (2007) Metabolism of reactive oxygen species is attenuated in leghemoglobin-deficient nodules of Lotus japonicas. MPMI 20:1596–1603
Harrison J, Jamet A, Muglia CI, Van de Sype G, Aguilar OM, Puppo A, Frendo P (2005) Glutathione plays a functional role in growth and symbiotic capacity of Sinorhizobium meliloti. J Bacteriol 187:168–174
Howlett NG, Avery SV (1997) Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation. Appl Environ Microbiol 63:2971–2976
Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with the MTL4 and the PCS genes. Chem 66:1670–1676
Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602
International Agency of Reasearch on Cancer (IARC) (2016). On line: www.iarc.fr
Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Jubany-Mari T, Alegre-Batlle L, Jiang K, Feldman LJ (2010) Use of a redox-sensing GFP (c-roGFP1) for real-time monitoring of cytosol redox status in Arabidopsis thaliana water-stressed plants. FEBS Lett 584:889–897
Krylova VV, Dubrovo NP, Izmailov SF (2007) The effect of metabolites on the pH gradient and membrane potential of the bean peribacteroid membrane. Appl Biochem Microbiol 43:292–297
Liao M, Luo YK, Zhao X, Huang CY (2005) Toxicity of cadmium to soil microbial biomass and its activity: effect of incubation time on Cd ecological dose in a paddy soil. J Zhejiang Univ Sci B 6:324–330
Lima AIG, Corticeiro SC, Figueira EMAP (2006) Glutathione- mediated cadmium sequestration in Rhizobium leguminosarum. Enzym Microb Technol 39:763–769
Long SR (2001) Genes and signals in the Rhizobium-legume symbiosis. Plant Physiol 125:69–72
Loscos J, Matamoros MA, Becana M (2008) Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiol 146:1282–1292
Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138
Mann SS, Rate AW, Gilkes RJ (2002) Cadmium accumulation in agricultural soils in Western Australia. Water Air Soil Pollut 141:281–297
Marino D, Gonzalez EM, Arrese-Igor C (2006) Drought effects on carbon and nitrogen metabolism of pea nodules can be mimicked by paraquat: evidence for the occurrence of two regulation pathways under oxidative stresses. J Exp Bot 57:665–673
Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, González EM (2007) Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143:1968–1974
Marquez-Garcia B, Shaw D, Cooper JW, Karpinska B, Dorcas Quain M, Makgopa EM, Kunert K, Foyer CH (2015) Redox markers for drought-induced nodule senescence, a process occurring after drought-induced senescence of the lowest leaves in soybean (Glycine max). Ann Bot 116:495–510
Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888
Matamoros MA, Dalton DA, Clemente MR, Rubio MC, Ramos J, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 133:1–11
Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N, Moore M, James EK, Dietz KJ, Becana M (2015) Function of glutathione peroxidases in legume root nodules. J Exp Bot 66:2979–2990
Maughan S, Foyer CH (2006) Engineering and genetic approaches to modulating the glutathione network in plants. Physiol Plant 126:382–397
Mehra RK, Mulchandani P (1995) Glutathione-mediated transfer of Cu(I) into phytochelatins. Biochem J 307:697–705
Meister A, Anderson ME (1983) Glutathione Ann Rev Biochem 52:711–760
Mendoza-Cozatl DG, Jobe TO, Hauser F, Schroeder JL (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562
Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–986
Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat Y, Saindrenan P, Issakidis-Bourguet E, Gouia H, Renou JP, Noctor G (2010) Arabidopsis glutathione reductase 1 is essential for the metabolism of intracellular H2O2 and to enable appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153:1144–1160
Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766
Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Clemente MR, Brewin NJ, Becana M (2000) Glutathione and homoglutathione synthetases of legumes nodules. Cloning, expression, and subcellular localization. Plant Physiol 124:879–888
Muglia CI, Grasso DH, Aguilar OM (2007) Rhizobium tropici response to acidity involves activation of glutathione synthesis. Microbiology 153:1286–1296
Muglia C, Comai G, Spegazzini E, Riccillo PM, Aguilar OM (2008) Glutathione produced by Rhizobium tropici is important to prevent early senescence in common bean nodules. FEMS Microbiol Lett 286:191–198
Müller J, Wiemken A, Boller T (2001) Redifferentiation of bacteria isolated from Lotus japonicus root nodules colonized by Rhizobium sp. NGR234. J Exp Bot 2:2181–2186
Munns D (1986) Acid soil tolerance in legumes and rhizobia. Adv Plant Nutr 2:63–91
Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379
Naya L, Ladrera R, Ramos J, Gonzáez EM, Arrese-Igor C, Minchin FR, Becana M (2007) The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant Physiol 144:1104–1114
Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648
Ott T, van Dongen JT, Günther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535
Paudyal SP, Aryal RR, Chauhan SVS, Maheshwari DK (2007) Effect of heavy metals on growth of Rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World J 5:27–32
Ponsone L, Fabra A, Castro S (2004) Interactive effects of acidity and aluminium on the growth, lipopolysaccharide and glutathione contents in two nodulating peanut rhizobia. Symbiosis 36:193–204
Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143
Pucciariello C, Innocenti G, Van de Velde W, Lambert A, Hopkins J, Clément M, Ponchet M, Pauly N, Goormachtig S, Holsters M, Puppo A, Frendo P (2009) (Homo)glutathione depletion modulates host gene expression during the symbiotic interaction between Medicago truncatula and Sinorhizobium meliloti. Plant Physiol 151:1186–1196
Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rontomé C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118
Ramos J, Naya L, Gay M, Abian J, Becana M (2008) Functional characterization of an unusual phytochelatin synthase, LjPCS3, of Lotus japonicus. Plant Physiol 148:536–545
Rauser WE, Meuwly P (1995) Retention of cadmium in roots of maize seedlings. Role of complexation by phytochelatins and related thiol peptides. Plant Physiol 109:195–202
Reichman SM (2007) The potential use of legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593
Ricillo PM, Muglia CI, Bruijn F, Roe AJ, Booth IR, Aguilar OM (2000) Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J Bacteriol 182:1748–1753
Rubio MC, Bustos-Sanmamed P, Clemente MR, Becana M (2009) Effects of salt stress on the expression of antioxidant genes and proteins in the model legume Lotus japonicus. New Phytol 181:851–859
Schröder P, Lyubenova L, Huber C (2009) Do heavy metals and metalloids influence the detoxification of organic xenobiotics in plants? Environ Sci Pollut Res 16:795–804
Sengupta D, Ramesh G, Mudalkar S, Kumar KRR, Kirti PB, Reddy AR (2012) Molecular cloning and characterization of γ-Glutamyl cysteine Synthetase (VrγECS) from roots of Vigna radiata (L.) Wilczek under progressive drought stress and recovery. Plant Mol Biol Report 30:894–903
Shah K, Nongkynrih JM (2007) Metal hyperaccumulator and bioremediation. Biol Plant 51:618–634
Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131
Shvaleva A, Coba T, Peña D, Rincón A, Lucas MM, Pueyo JJ (2010) Flavodoxin overexpression reduces cadmium-induced damage in alfalfa root nodules. Plant Soil 326:109–121
Sobolev D, Begonia MFT (2008) Effects of heavy metal contamination upon soil microbes: lead- induced changes in general and denitrifying microbial communities as evidenced by molecular markers. Int J Environ Res Public Health 5:450–456
Sobrevals L, Müller P, Fabra A, Castro S (2006) Role of glutathione in growth and symbiotic properties of Bradyrhizobium sp (peanut microsymbiont) under different environmental stresses. Can J Microbiol 52:606–616
Sriprang R, Hayashi M, Yamashita M, Ono H, Saeki K, Murooka Y (2002) A novel bioremedia- tion system for heavy metals using the symbiosis between leguminous plant and genetically engineered rhizobia. J Biotechnol 99:279–293
Sriprang R, Hayashi M, Ono H, Takagi M, Hirata K, Murooka Y (2003) Enhanced accumulation of Cd2+ by a Mesorhizobium sp. transformed with a gene from Arabidopsis thaliana coding for phytochelatin synthase. Appl Environ Microbiol 69:1791–1796
Stougaard J (2000) Regulators and regulation of legume root nodule development. Plant Physiol 124:531–540
Van de Wiel C, Scheres B, Franssen H, Van Lierop MJ, Van Lammeren A, Van Kammen A, Bisseling T (1990) The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J 9:1–7
Vance CP (2008) Carbon and nitrogen metabolism in legumes nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp 293–320
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372
Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, van Montagu M, Inzé D et al. (2000) The ROOT MERISTEM LESS1⁄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
Wang Y, Zhang Z, Pan Zhang P, Cao Y, Hu T, Yan (2016) Rhizobium symbiosis contribution to short-term salt stress tolerance in alfalfa (Medicago sativa L.). Plant Soil 402:247–261
Wani PA, Khan MS, Zaidi A (2006) An evaluation of the effects of heavy metals on the growth, seed yield and grain protein of lentil in pots. Ann Appl Biol 27:23–24
Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163
Wingate VP, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210
World Health Organization (WHO) (2010) Online: www.who.int
Younis M (2007) Response of lablab perpureus–rhizobium symbiosis to heavy metals in pot and field experiments. World J Agric Sci 3:111–122
Zenk MH (1996) Heavy metal detoxification in higher plants – a review. Gene 179:21–30
Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50
Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228
Zhu YL, Pilon-Smits AH, Jouarin L, Terry N (1999) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–80
Ziemacki G, Viviano G, Merli F (1989) Heavy metals: sources and environmental presence. Ann Ist Super Sanita 25:531–536
Acknowledgment
This work was supported by Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto (SECYT-UNRC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), and Ministerio de Ciencia y Tecnología Córdoba. E. Bianucci and A. Furlan are members of the research career from CONICET.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Bianucci, E., Furlan, A., Castro, S. (2017). Importance of Glutathione in the Legume-Rhizobia Symbiosis. In: Hossain, M., Mostofa, M., Diaz-Vivancos, P., Burritt, D., Fujita, M., Tran, LS. (eds) Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-66682-2_17
Download citation
DOI: https://doi.org/10.1007/978-3-319-66682-2_17
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-66681-5
Online ISBN: 978-3-319-66682-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)