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The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants

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Abstract

Cysteine is the first organic product of sulfate assimilation and as such is the precursor of all molecules containing reduced sulfur including methionine, glutathione, and their many metabolites. In plants, 5′-adenylylsulfate (APS) reductase is hypothesized to be a key regulatory point in sulfate assimilation and reduction. APS reductase catalyzes the two-electron reduction of APS to sulfite using glutathione as an electron donor. This paper reviews the experimental basis for this hypothesis. In addition, the results of an experiment designed to test the hypothesis by bypassing the endogenous APS reductase and its regulatory mechanisms are described. Two different bacterial assimilatory reductases were expressed in transgenic Zea mays, the thioredoxin-dependent APS reductase from Pseudomonas aeruginosa and the thioredoxin-dependent 3′-phosphoadenylylsulfate reductase from Escherichia coli. Each of them was placed under transcriptional control of the ubiquitin promoter and the protein products were targeted to chloroplasts. The leaves of transgenic Z. mays lines showed significant accumulation of reduced organic thiol compounds including cysteine, γ-glutamylcysteine, and glutathione; and reduced inorganic forms of sulfur including sulfite and thiosulfate. Both bacterial enzymes appeared to be equally capable of deregulating the assimilative sulfate reduction pathway. The reduced sulfur compounds accumulated to such high levels that the transgenic plants showed evidence of toxicity. The results provide additional evidence that APS reductase is a major control point for sulfate reduction in Z. mays.

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Abbreviations

APS:

5′-adenylylsulfate

CaMV 35S:

the 35S promoter of cauliflower mosaic virus

CysC:

APS kinase

CysH:

PAPS reductase

EcPAPR:

PAPS reductase from Escherichia coli

Grx:

glutaredoxin

GSH:

reduced glutathione

GSSG:

oxidized glutathione

OAS:

O-acetylserine

PaAPR:

APS reductase from Pseudomonas aeruginosa

PAPS:

3′-phosphoadenylylsulfate

rbcS:

ribulose bisphospahte carboxylase

Trx:

thioredoxin

ZmAPR:

APS reductase from Zea mays

References

  • Abola AP, Willits MG, Wang RC, Long SR, (1999) Reduction of adenosine-5′-phosphosulfate instead of 3′-phosphoadenosine-5′-phosphosulfate in cysteine biosynthesis by Rhizobium meliloti and other members of the family Rhizobiaceae J Bacteriol 181: 5280–5287

    PubMed  CAS  Google Scholar 

  • Anderson ME, (1985) Determination of glutathione and glutathione disulfide in biological samples. In Meister A, (ed), Glutamate, Glutamine and Related Compounds. Academic Press, Orlando, FL, pp 548–545

    Chapter  Google Scholar 

  • Arisi AC, Noctor G, Foyer CH, Jouanin L, (1997) Modification of thiol contents in poplars (Populus tremula × P. alba) overexpressing enzymes involved in glutathione synthesis Planta 203: 362–372

    Article  PubMed  CAS  Google Scholar 

  • Berendt U, Haverkamp T, Prior A, Schwenn JD, (1995) Reaction mechanism of thioredoxin: 3′-phospho-adenylylsulfate reductase investigated by site-directed mutagenesis Eur J Biochem 233: 347–356

    Article  PubMed  CAS  Google Scholar 

  • Berndt C, Lillig CH, Wollenberg M, Bill E, Mansilla MC, de Mendoza D, Seidler A, Schwenn JD, (2004) Characterization and reconstitution of a 4Fe-4S adenylyl sulfate/phosphoadenylyl sulfate reductase from Bacillus subtilis J Biol Chem 279: 7850–7855

    Article  PubMed  CAS  Google Scholar 

  • Bick JA, Aslund F, Chen Y, Leustek T, (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase Proc Natl Acad Sci USA 95: 8404–8409

    Article  PubMed  CAS  Google Scholar 

  • Bick JA, Dennis JJ, Zylstra GJ, Nowack J, Leustek T, (2000) Identification of a new class of 5′-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria J Bacteriol 182: 135–142

    PubMed  CAS  Google Scholar 

  • Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA, Leustek T, (2001) Regulation of the plant-type 5′-adenylyl sulfate reductase by oxidative stress Biochemistry 40: 9040–9048

    Article  PubMed  CAS  Google Scholar 

  • Blaszczyk A, Brodzik R, Sirko A, (1999) Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase Plant J 20: 237–243

    Article  PubMed  CAS  Google Scholar 

  • Bui BT, Escalettes F, Chottard G, Florentin D, Marquet A, (2000) Enzyme-mediated sulfide production for the reconstitution of [2Fe-2S] clusters into apo-biotin synthase of Escherichia coli. Sulfide transfer from cysteine to biotin Eur J Biochem 267: 2688–2694

    Article  PubMed  CAS  Google Scholar 

  • Burgener M, Suter M, Jones S, Brunold C, (1998) Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves Plant Physiol 116: 1315–1322

    Article  PubMed  CAS  Google Scholar 

  • Burnell JN, (1984) Sulfate assimilation in C4 plants Plant Physiol 75: 873–875

    PubMed  CAS  Google Scholar 

  • Christensen AH, Quail PH, (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants Transgenic Res 5: 213–218

    Article  PubMed  CAS  Google Scholar 

  • Crane BR, Siegel LM, Getzoff ED, (1997) Probing the catalytic mechanism of sulfite reductase by X-ray crystallography: structures of the Escherichia coli hemoprotein in complex with substrates, inhibitors, intermediates, and products Biochemistry 36: 12120–12137

    Article  PubMed  CAS  Google Scholar 

  • Creissen G, Firmin J, Fryer M, Kular B, Leyland N, Reynolds H, Pastori G, Wellburn F, Baker N, Wellburn A, Mullineaux P, (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress Plant Cell 11: 1277–1292

    Article  PubMed  CAS  Google Scholar 

  • De Kok LJ, (1991) The internal resistance in spinach leaves to atmospheric H2S deposition is determined by metabolic processes Plant Physiol Biochem 29: 463–470

    Google Scholar 

  • Doulis AG, Debian N, Kingston-Smith AH, Foyer CH, (1997) Differential localization of antioxidants in maize leaves Plant Physiol 114: 1031–1037

    PubMed  CAS  Google Scholar 

  • Eilers T, Schwarz G, Brinkmann H, Witt C, Richter T, Nieder J, Koch B, Hille R, Hansch R, Mendel RR, (2001) Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism. J Biol Chem 276: 46989–46994

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Schofield OM, Leustek T, (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase Plant Physiol 123: 1087–1096

    Article  PubMed  CAS  Google Scholar 

  • Gerwick BC, Ku SB, Black CC, (1980) Initiation of sulfate activation: a variation in C4 photosynthesis plants Science 209: 513–515

    Article  PubMed  CAS  Google Scholar 

  • Guidotti TL, (1996) Hydrogen sulphide Occup Med (Lond) 46: 367–371

    CAS  Google Scholar 

  • 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 USA 93: 13377–13382

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Heiss S, Schafer HJ, Haag-Kerwer A, Rausch T, (1999) Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase Plant Mol Biol 39: 847–857

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hodson R, Schiff JA, (1971) The ubiquity of sulfate reduction to thiosulfate Plant Physiol 47: 269–299

    Google Scholar 

  • Houston NL, Fan C, Xiang Q-Y, Schulze J-M, Jung R, Boston RS, (2005) Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins Plant Physiol 137: 762–778

    Article  PubMed  CAS  Google Scholar 

  • Kanno N, Nagahisa E, Sato M, Sato Y, (1996) Adenosine 5′-phosphsulfate sulfotransferase from the marine macroalga Porphyra yezoensis Ueda (Rhodophyta): stabilization, purification, and properties Planta 198: 440–446

    Article  CAS  Google Scholar 

  • Kim SK, Rahman A, Bick JA, Conover RC, Johnson MK, Mason JT, Hirasawa M, Leustek T, Knaff DB, (2004) Properties of the cysteine residues and iron-sulfur cluster of the assimilatory 5′-adenylyl sulfate reductase from Pseudomonas aeruginosa Biochemistry 43: 13478–13486

    Article  PubMed  CAS  Google Scholar 

  • Kopriva S, Koprivova A, (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future J Exp Bot 55: 1775–1783

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kopriva S, Buchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schurmann P, Schunemann V, Trautwein AX, Kroneck PM, Brunold C, (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron-sulfur protein J Biol Chem 276: 42881–42886

    Article  PubMed  CAS  Google Scholar 

  • Kopriva S, Buchert T, Fritz G, Suter M, Benda R, Schunemann V, Koprivova A, Schurmann P, Trautwein AX, Kroneck PM, Brunold C, (2002) The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation J Biol Chem 277: 21786–21791

    Article  PubMed  CAS  Google Scholar 

  • Koprivova A, Suter M, den Camp RO, Brunold C, Kopriva S, (2000) Regulation of sulfate assimilation by nitrogen in ArabidopsisPlant Physiol 122: 737–746

    Article  PubMed  CAS  Google Scholar 

  • Koprivova A, Melzer M, von Ballmoos P, Mandel T, Brunold C, Kopriva S, (2001) Assimilatory sulfate reduction in C3, C3–C4, and C4 species of Flaveria Plant Physiology 127: 543–550

    Article  PubMed  CAS  Google Scholar 

  • Koprivova A, Meyer AJ, Schween G, Herschbach C, Reski R, Kopriva S, (2002) Functional knockout of the adenosine 5′-phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation J Biol Chem 277: 32195–32201

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Leustek T, (1998) APS kinase from Arabidopsis thaliana: genomic organization, expression, and kinetic analysis of the recombinant enzyme Biochem Biophys Res Commun 247: 171–175

    Article  PubMed  CAS  Google Scholar 

  • Leustek T, (2002) Sulfate Metabolism. In Somerville CR, Meyerowitz EM, (eds), The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD

    Google Scholar 

  • Leustek T, Bick JA, (2000) The evolution of sulfur assimilation in plants. In C Brunold, Rennenberg H, De Kok LJ, Stulen I, Davidian J-C, (eds), Fourth Workshop on Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Paul Haupt Publishers, Wengen, Switzerland, pp 1–15

    Google Scholar 

  • Leustek T and Tarczynski MC (2003) Methods for modulating the levels of organic sulfur compounds in plants by transforming with (P)APS reductase DNA. In: USPaT Office, United States Patent and Trademark Office. Pioneer Hi-Bred International, Inc. (Des Moines, IA); Rutgers University (New Brunswick, NJ)

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Levinthal M, Schiff JA, (1968) Studies of sulfate utilization by algae. 5. Identification of thiosulfate as a major acid-volatile product formed by a cell-free sulfate reducing system from Chlorella extracts Plant Physiol 43: 555–562

    Article  PubMed  CAS  Google Scholar 

  • Lillig CH, Prior A, Schwenn JD, Aslund F, Ritz D, Vlamis-Gardikas A, Holmgren A, (1999) New thioredoxins and glutaredoxins as electron donors of 3′-phosphoadenylylsulfate reductase J Biol Chem 274: 7695–7698

    Article  PubMed  CAS  Google Scholar 

  • Lillig CH, Schiffmann S, Berndt C, Berken A, Tischka R, Schwenn JD, (2001) Molecular and catalytic properties of Arabidopsis thaliana adenylyl sulfate (APS)-kinase Arch Biochem Biophys 392: 303–310

    Article  PubMed  CAS  Google Scholar 

  • Matsumura T, Kimata-Ariga Y, Sakakibara H, Sugiyama T, Murata H, Takao T, Shimonishi Y, Hase T, (1999) Complementary DNA cloning and characterization of ferredoxin localized in bundle-sheath cells of maize leaves Plant Physiol 119: 481–488

    Article  PubMed  CAS  Google Scholar 

  • Neuenschwander U, Suter M, Brunold C, (1991) Regulation of sulfate assimilation by light and O-acetyl-L-serine in Lemna minor L Plant Physiology 97: 253–258

    PubMed  CAS  Google Scholar 

  • Neumann S, Wynen A, Truper HG, Dahl C, (2000) Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway Mol Biol Rep 27: 27–33

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Arisi AC, Jouanin L, Foyer CH, (1998) Manipulation of glutathione and amino acid biosynthesis in the chloroplast Plant Physiol 118: 471–482

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ohkama-Ohtsu N, Kasajima I, Fujiwara T, Naito S, (2004) Isolation and characterization of an Arabidopsis mutant that overaccumulates O-Acetyl-L-Ser Plant Physiol 136: 3209–3222

    Article  PubMed  CAS  Google Scholar 

  • Ostrowski J, Wu JY, Rueger DC, Miller BE, Siegel LM, Kredich NM, (1989) Characterization of the cysJIH regions of Salmonella typhimurium and Escherichia coli B. DNA sequences of cysI and cysH and a model for the siroheme-Fe4S4 active center of sulfite reductase hemoprotein based on amino acid homology with spinach nitrite reductase J Biol Chem 264: 15726–15737

    PubMed  CAS  Google Scholar 

  • Papenbrock J, Schmidt A, (2000) Characterization of two sulfurtransferase isozymes from Arabidopsis thalianaEur J Biochem 267: 5571–5579

    Article  PubMed  CAS  Google Scholar 

  • Passera C, Ghisi R, (1982) ATP sulphurylase and O-acetylserine sulphhydrylase in isolated mesophyll protoplasts and bundle sheath strands of S-deprived maize leaves J Exp Bot 33: 432–438

    Article  CAS  Google Scholar 

  • Prior A, Uhrig JF, Heins L, Wiesmann A, Lillig CH, Stoltze C, Soll J, Schwenn JD, (1999) Structural and kinetic properties of adenylyl sulfate reductase from Catharanthus roseus cell cultures Biochim Biophys Acta 1430: 25–38

    PubMed  CAS  Google Scholar 

  • Ravina CG, Chang CI, Tsakraklides GP, McDermott JP, Vega JM, Leustek T, Gotor C, Davies JP, (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis Plant Physiol 130: 2076–2084

    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 

  • Renosto F, Seubert PA, Segel IH, (1984) Adenosine 5′-phosphosulfate kinase from Penicillium chrysogenum. Purification and kinetic characterization J Biol Chem 259: 2113–2123

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Vlamis-Gardikas A, Lillig CH, Berndt C, Schwenn JD, Holmgren A, Jacquot JP, (2003) Characterization of the redox properties of poplar glutaredoxin Antioxid Redox Signal 5: 15–22

    Article  PubMed  CAS  Google Scholar 

  • Russel M, Model P, Holmgren A, (1990) Thioredoxin or glutaredoxin in Escherichia coli is essential for sulfate reduction but not for deoxyribonucleotide synthesis J Bacteriol 172: 1923–1929

    PubMed  CAS  Google Scholar 

  • Schiff JA, (1983) Reduction and other metabolic reactions of sulfate. In A Läuschli, Bieleski RL, (eds), Encyclopedia of Plant Physiology, 15A. Springer, Berlin, pp 401–421

    Google Scholar 

  • Schmidt A, Trebst A, (1969) The mechanism of photosynthetic sulfate reduction by isolated chloroplasts Biochem et Biophys Acta 180: 529–535

    Article  CAS  Google Scholar 

  • Schmutz D, Brunold C, (1984) Intercellular localization of assimilatory sulfate reduction in leaves of Zea mays and Triticum aestivum Plant Physiol 74: 866–870

    PubMed  CAS  Google Scholar 

  • Schmutz D, Brunold C, (1985) Localization of nitrite and sulfite reductase in bundle sheath and mesophyll cells of maize leaves Physiol Plant 64: 523–528

    Article  CAS  Google Scholar 

  • Schwenn JD, Schriek U, (1987) PAPS-Reductase from Escherichia coli: Characterization of the enzyme as probe for thioredoxins Z. Natureforsch 42c: 93–102

    Google Scholar 

  • Schwenn JD, Krone FA, Husmann K, (1988) Yeast PAPS reductase: properties and requirements of the purified enzyme Arch Microbiol 150: 313–319

    Article  PubMed  CAS  Google Scholar 

  • Setya A, Murillo M, Leustek T, (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase Proc Natl Acad Sci USA 93: 13383–13388

    Article  PubMed  CAS  Google Scholar 

  • Sirko A, Blaszczyk A, Liszewska F, (2004) Overproduction of SAT and/or OASTL in transgenic plants: a survey of effects J Exp Bot 55: 1881–1888

    Article  PubMed  CAS  Google Scholar 

  • Stulen I, Posthumus F, Amância S, Masselink-Beltman I, Müller M, De Kok LJ, (2000) Mechanism of H2S phytotoxicity. In C Brunold, Rennenberg H, De Kok LJ, Stulen I, Davidian J-C, (eds), Fourth Workshop on Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Paul Haupt Publishers, Wengen, Switzerland, pp 381–383

    Google Scholar 

  • Suter M, von Ballmoos P, Kopriva S, den Camp RO, Schaller J, Kuhlemeier C, Schurmann P, Brunold C, (2000) Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5′-phosphosulfate reductase are identical enzymes J Biol Chem 275: 930–936

    Article  PubMed  CAS  Google Scholar 

  • Tarczynski MC, Martin MN, Shen B, Li C, Leustek T, Falco C, Glassman K, Ranch J and Allen B (2003) Sulfate reduction limits methionine and cysteine content in maize seed. In: Plant Biology 2003. American Society of Plant Biologists, Honolulu, HI, USA

  • Thomas D, Barbey R, Henry D, Surdin-Kerjan Y, (1992) Physiological analysis of mutants of Saccharomyces cerevisiae impaired in sulphate assimilation J Gen Microbiol 138: 2021–2028

    PubMed  CAS  Google Scholar 

  • Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A, Leustek T, (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa Plant J 32: 879–889

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wagner W, Follmann H, Schmidt A, (1978) Multiple functions of thioredoxins Z Naturforsch 33: 517–520

    CAS  Google Scholar 

  • Weber M, Suter M, Brunold C, Kopriva S, (2000) Sulfate assimilation in higher plants characterization of a stable intermediate in the adenosine 5′-phosphosulfate reductase reaction Eur J Biochem 267: 3647–3653

    Article  PubMed  CAS  Google Scholar 

  • Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S, (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors Plant J 37: 269–281

    Article  PubMed  CAS  Google Scholar 

  • Williams SJ, Senaratne RH, Mougous JD, Riley LW, Bertozzi CR, (2002) 5′-adenosinephosphosulfate lies at a metabolic branch point in mycobacteria J Biol Chem 277: 32606–32615

    Article  PubMed  CAS  Google Scholar 

  • Wirtz M, Hell R, (2003) Production of cysteine for bacterial and plant biotechnology: application of cysteine feedback-insensitive isoforms of serine acetyltransferase Amino Acids 24: 195–203

    PubMed  CAS  Google Scholar 

  • Youssefian S, Nakamura M, Orudgev E, Kondo N, (2001) Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine(thiol) lyase modifies plant responses to oxidative stress Plant Physiol 126: 1001–1011

    Article  PubMed  CAS  Google Scholar 

  • Ziegler I, (1974) Malate dehydrogenase in Zea mays: properties and inhibition by sulfite Biochim Biophys Acta 364: 28–37

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The research was funded by the United States National Science Foundation IBN-9817594 (TL), MCB-0094062 (MNM), and Pioneer Hi-Bred International, Inc. The authors wish to acknowledge Kimberly Glassman for vector construction and Jerry Ranch for Zea mays transformation.

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  1. Department of Plant Biology and Pathology, Biotechnology Center for Agriculture and the Environment, Rutgers University, New Brunswick, NJ, 08901-8520, USA

    Melinda N. Martin & Thomas Leustek

  2. Pioneer Hi-Bred International Inc., A DuPont Company, Trait & Development, 7300 NW 62nd Avenue, P.O. Box 1004, Johnston, IA 50131-1004, USA

    Mitchell C. Tarczynski & Bo Shen

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  1. Melinda N. Martin
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Correspondence to Thomas Leustek.

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Martin, M.N., Tarczynski, M.C., Shen, B. et al. The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth Res 86, 309–323 (2005). https://doi.org/10.1007/s11120-005-9006-z

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