Abstract
Sulfur is an essential element for all organisms. Plants utilize soil sulfate to synthesize an amino acid, cysteine, which is used for a variety of sulfur-containing compounds such as glutathione (GSH), methionine, proteins, lipids, coenzymes, and various secondary metabolites. Since animals cannot synthesize organic sulfur compounds from inorganic ones, sulfate assimilation in plants is important for the global sulfur cycle.
GSH is a tripeptide synthesized from the amino acids cysteine, glutamic acid, and glycine. By controlling the redox states of proteins and chemicals, GSH functions in many biological processes including enzymatic activity, detoxification of toxic agents, and eventually influences plant growth, development, and stress management in response to both abiotic and biotic factors. Maintaining an appropriate redox environment, for which GSH levels are crucial, is thus important for plant life.
GSH levels in plant cells are controlled by both synthesis and degradation processes. GSH is synthesized from cysteine by two-step reactions in plastids and cytosol. Since cysteine levels are relatively low in the cells, the sulfate assimilation pathway composed of sulfate uptake, sulfate reduction, and assimilation into cysteine, is a rate-limiting step in GSH synthesis. In this chapter, we review the molecular machineries and regulatory aspects of the sulfur assimilation pathway and GSH metabolism in plants.
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References
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221
Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669
Awazuhara M, Kim H, Hayashi H, Chino M, Kim SG, Fujiwara T (2002) Composition of seed storage proteins changed by glutathione treatment of soybeans. Biosci Biotechnol Biochem 66:1751–1754
Awazuhara M, Fujiwara T, Hayashi H, Watanabe-Takahashi A, Takahashi H, Saito K (2005) The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Physiol Plant 125:95–105
Bermudez MA, Paez-Ochoa MA, Gotor C, Romero LC (2010) Arabidopsis S-sulfocysteine synthase activity is essential for chloroplast function and long-day light-dependent redox control. Plant Cell 22:403–416
Bohrer AS, Yoshimoto N, Sekiguchi A, Rykulski N, Saito K, Takahashi H (2014) Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana. Front Plant Sci 5:750
Buchner P, Takahashi H, Hawkesford MJ (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773
Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41:72–78
Cao MJ, Wang Z, Wirtz M, Hell R, Oliver DJ, Xiang CB (2013) SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J 73:607–616
Chen J, Yang L, Yan X, Liu Y, Wang R, Fan T, Ren Y, Tang X, Xiao F, Cao S (2016) Zinc-finger transcription factor ZAT6 positively regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis. Plant Physiol 171:707–719
Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216
Davidian JC, Kopriva S (2010) Regulation of sulfate uptake and assimilation–the same or not the same? Mol Plant 3:314–325
Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79:331–348
Droux M, Ruffet ML, Douce R, Job D (1998) Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants – structural and kinetic properties of the free and bound enzymes. Eur J Biochem 255:235–245
Geu-Flores F, Nielsen MT, Nafisi M, Moldrup ME, Olsen CE, Motawia MS, Halkier BA (2009) Glucosinolate engineering identifies a γ-glutamyl peptidase. Nat Chem Biol 5:575–577
Geu-Flores F, Moldrup ME, Bottcher C, Olsen CE, Scheel D, Halkier BA (2011) Cytosolic γ-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell 23:2456–2469
Glaser K, Kanawati B, Kubo T, Schmitt-Kopplin P, Grill E (2014) Exploring the Arabidopsis sulfur metabolome. Plant J 77:31–45
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
Gutierrez-Marcos JF, Roberts MA, Campbell EI, Wray JL (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia Coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity. Proc Natl Acad Sci U S A 93:13377–13382
Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148:1055–1067
Harms K, von Ballmoos P, Brunold C, Hofgen R, Hesse H (2000) Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J 22:335–343
Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000a) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248:51–58
Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000b) β-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1171
Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R (2008) Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20:168–185
Hell R, Bergmann L (1990) γ-Glutamylcysteine synthetase in higher-plants – catalytic properties and subcellular-localization. Planta 180:603–612
Hell R, Jost R, Berkowitz O, Wirtz M (2002) Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22:245–257
Hell R, Khan MS, Wirtz M (2010) Cellular biology of sulfur and its functions in plants. In: Hell R, Mendel RR (eds) Cell biology of metals and nutrients, plant cell monographs 17. Springer, Berlin/Heidelberg, pp 243–279
Hernandez LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Caceres 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
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
Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663
Hirai MY, Klein M, Fujikawa Y, Yano M, Goodenowe DB, Yamazaki Y, Kanaya S, Nakamura Y, Kitayama M, Suzuki H, Sakurai N, Shibata D, Tokuhisa J, Reichelt M, Gershenzon J, Papenbrock J, Saito K (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590–25595
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
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004a) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704
Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004b) Root-to-shoot transport of sulfate in Arabidopsis: evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204
Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137:220–230
Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321
Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A, Rubio-Somoza I, Todesco M, Rathjen T, Saito K, Takahashi H, Dalamay T, Kopriva S (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876
Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hansch R, Mendel RR, Meyer AJ, Wirtz M, Hell R (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. Plant Cell 22:1216–1231
Kumar A, Tikoo S, Maity S, Sengupta S, Kaur A, Bachhawat AK (2012) Mammalian proapoptotic factor ChaC1 and its homologues function as γ-glutamyl cyclotransferases acting specifically on glutathione. EMBO Rep 13:1095–1101
Kumar S, Kaur A, Chattopadhyay B, Bachhawat AK (2015) Defining the cytosolic pathway of glutathione degradation in Arabidopsis thaliana: role of the ChaC/GCG family of γ-glutamyl cyclotransferases as glutathione-degrading enzymes and AtLAP1 as the Cys-Gly peptidase. Biochem J 468:73–85
Koprivova A, Suter M, Op den Camp R, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746
Kopriva S, Koprivova A (2004) Plant adenosine 50-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55:1775–1783
Koprivova A, Giovannetti M, Baraniecka P, Lee BR, Grondin C, Loudet O, Kopriva S (2013) Natural variation in the ATPS1 isoform of ATP sulfurylase contributes to the control of sulfate levels in Arabidopsis. Plant Physiol 163:1133–1141
Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106
Kuzuhara Y, Isobe A, Awazuhara M, Fujiwara T, Hayashi H (2000) Glutathione levels in phloem sap of rice plants under sulfur deficient conditions. Soil Sci Plant Nutr 46:265–270
Labrou NE, Papageorgiou AC, Pavli O, Flemetakis E (2015) Plant GSTome: structure and functional role in xenome network and plant stress response. Curr Opin Biotechnol 32:186–194
Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO42- uptake in intact canola (the role of phloem-translocated glutathione). Plant Physiol 111:147–157
Lappartient AG, Vidmar JJ, Leustek T, Glass AD, Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89–95
Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165
Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057
Long SR, Kahn M, Seefeldt L, Tsay YF, Kopriva S (2015) Chapter 16: Nitrogen and sulfur. In: Buchana BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. Wiley Blackwell, Oxford, pp 746–768
Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, Koprivova A, North K, Kopriva S, Daniel-Vedele F (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39:896–900
Lunn JE, Droux M, Martin J, Douce R (1990) Localization of ATP-sulfurylase and O-acetylserine (thiol)lyase in spinach leaves. Plant Physiol 94:1345–1352
Martin MN, Saladores PH, Lambert E, Hudson AO, Leustek T (2007) Localization of members of the γ-glutamyl transpeptidase family identifies sites of glutathione and glutathione S-conjugate hydrolysis. Plant Physiol 144:1715–1732
Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605
Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004a) A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J 38:779–789
Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004b) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signaling and regulation. J Exp Bot 55:1843–1849
Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314
Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251
Maruyama-Nakashita A, Watanabe-Takahashi A, Inoue E, Yamaya T, Saito K, Takahashi H (2015) Sulfurresponsive elements in the 3'-nontranscribed intergenic region are essential for the induction of SULFATE TRANSPORTER 2;1 gene expression in Arabidopsis roots under sulfur deficiency. Plant Cell 27:1279–1296
Maughan SC, Pasternak M, Cairns N, Kiddle G, Brach T, Jarvis R, Haas F, Nieuwland J, Lim B, Muller C, Salcedo-Sora E, Kruse C, Orsel M, Hell R, Miller AJ, Bray P, Foyer CH, Murray JA, Meyer AJ, Cobbett CS (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
May MJ, Leaver CJ (1994) Arabidopsis thaliana γ-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs. Proc Natl Acad Sci U S A 91:10059–10063
Mendoza-Cozatl 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
Miller AJ, Shen Q, Xu G (2009) Freeways in the plant: transporters for N, P and S and their regulation. Curr Opin Plant Biol 12:284–290
Nikiforova VJ, Gakiere B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55:1861–1870
Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318
Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH (2011) Glutathione. The Arabidopsis book. Am Soc Plant Biol 9: 2–32. URL: http://www.bioone.org/doi/full/10.1199/tab.0142
Noji M, Inoue K, Kimura N, Gouda A, Saito K (1998) Isoform-dependent differences in feedback regulation and subcellular localization of serine acetyltransferase involved in cysteine biosynthesis from Arabidopsis thaliana. J Biol Chem 273:32739–32745
Noji M, Saito K (2002) Molecular and biochemical analysis of serine acetyltransferase and cysteine synthase towards sulfur metabolic engineering in plants. Amino Acids 22:231–243
Ohkama-Ohtsu N, Radwan S, Peterson A, Zhao P, Badr AF, Xiang C, Oliver DJ (2007a) Characterization of the extracellular γ-glutamyl transpeptidases, GGT1 and GGT2, in Arabidopsis. Plant J 49:865–877
Ohkama-Ohtsu N, Zhao P, Xiang C, Oliver DJ (2007b) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49:878–888
Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148:1603–1613
Ohkama-Ohtsu N, Sasaki-Sekimoto Y, Oikawa A, Jikumaru Y, Shinoda S, Inoue E, Kamide Y, Yokoyama T, Hirai MY, Shirasu K, Kamiya Y, Oliver DJ, Saito K (2011) 12-oxo-phytodienoic acid-glutathione conjugate is transported into the vacuole in Arabidopsis. Plant Cell Physiol 52:205–209
Orlowski M, Meister A (1970) The γ-glutamyl cycle: a possible transport system for amino acids. Proc Natl Acad Sci U S A 67:1248–1255
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
Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012
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, Thominet D, Vanacker H, Miginiac-Maslow M, Gakiere B, Noctor G (2009) H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol Plant 2:344–356
Rotte C, Leustek T (2000) Differential subcellular localization and expression of ATP sulfurylase and 5'-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol 124:715–724
Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian JC, Fourcroy P, Berthomieu P (2008) Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol 147:897–911
Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450
Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera Littoralis. Plant J 55:774–786
Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci U S A 93:13383–13388
Shibagaki N, Grossman AR (2010) Binding of cysteine synthase to the STAS domain of sulfate transporter and its regulatory consequences. J Biol Chem 285:25094–25102
Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486
Storozhenko S, Belles-Boix E, Babiychuk E, Herouart D, Davey MW, Slooten L, Van Montagu M, Inze D, Kushnir S (2002) γ-glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing, and biochemical properties. Plant Physiol 128:1109–1119
Su T, Xu J, Li Y, Lei L, Zhao L, Yang H, Feng J, Liu G, Ren D (2011) Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23:364–380
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JD, Engler G, VanMontagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107
Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182
Takahashi H, Buchner P, Yoshimoto N, Hawkesford MJ, Shiu SH (2011a) Evolutionary relationships and functional diversity of plant sulfate transporters. Front Plant Sci 2:119
Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011b) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184
Takahashi H, Buchner P, Yoshimoto N, Hawkesford MJ, Shiu SH (2012) Evolutionary relationships and functional diversity of plant sulfate transporters. Front Plant Sci 2:a119
Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5'-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740
Vidmar JJ, Tagmount A, Cathala N, Touraine B, Davidian JCE (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett 475:65–69
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 CL, Oliver DJ (1996) Cloning of the cDNA and genomic clones for glutathione synthetase from Arabidopsis thaliana and complementation of a gsh2 mutant in fission yeast. Plant Mol Biol 31:1093–1104
Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008a) Physiological roles of the beta-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146:310–320
Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K (2008b) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20:2484–2496
Wawrzynska A, Lewandowska M, Sirko A (2010) Nicotiana tabacum EIL2 directly regulates expression of at least one tobacco gene induced by sulphur starvation. J Exp Bot 61:889–900
Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19:625–639
Wirtz M, Berkowitz O, Droux M, Hell R (2001) The cysteine synthase complex from plants – mitochondrial serine acetyltransferase from Arabidopsis thaliana carries a bifunctional domain for catalysis and protein-protein interaction. Eur J Biochem 268:686–693
Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10:1539–1550
Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T, Hase T (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122:887–894
Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473
Yoshimoto N, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131:1511–1517
Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:378–388
Zhang B, Pasini R, Dan H, Joshi N, Zhao YH, Leustek T, Zheng ZL (2014) Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status. Plant J 77:185–197
Zuber H, Davidian JC, Aubert G, Aime D, Belghazi M, Lugan R, Heintz D, Wirtz M, Hell R, Thompson R, Gallardo K (2010) The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol 154:913–926
Acknowledgement
This work was supported by Japan Society for the Promotion of Science KAKENHI grant Number 15KT0028 (for N.O.O. and A.M.N.) and 24380040 (for A.M.N.).
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Maruyama-Nakashita, A., Ohkama-Ohtsu, N. (2017). Sulfur Assimilation and Glutathione Metabolism in Plants. 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_13
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