Abstract
Sulfurtransferases/rhodaneses (Str) comprise a group of enzymes widely distributed in all phyla which catalyze in vitro the transfer of a sulfur atom from suitable sulfur donors to nucleophilic sulfur acceptors. The best characterized Str is bovine rhodanese (EC 2.8.1.1) which catalyses in vitro the transfer of a sulfane sulfur atom from thiosulfate to cyanide, leading to the formation of sulfite and thiocyanate. Plants as well as other organisms contain many proteins carrying a typical rhodanese pattern or domain forming multi-protein families (MPF). Despite the presence of Str activities in many living organisms, the physiological role of the members of this MPF has not been established unambiguously. While in mammals these proteins are involved in the elimination of toxic cyanogenic compounds, their ubiquity suggests additional physiological functions. In plants, Str are localized in the cytoplasm, mitochondria, plastids, and nucleus. Str probably also transfer reduced sulfur onto substrates as large as peptides or proteins. Several studies in different organisms demonstrate a protein–protein interaction with members of the thioredoxin MPF indicating a role of Str in maintenance of the cellular redox homeostasis. The increased expression of several members of the Str MPF in various stress conditions could be a response to oxidative stress. In summary, data indicate that Str are involved in various essential metabolic reactions.
This is a preview of subscription content, access via your institution.




Abbreviations
- Acc. no.:
-
Accession number
- AR:
-
Arsenate reductase
- CAS:
-
β-Cyano-l-alanine synthase
- Cys:
-
Cysteine
- E. coli :
-
Escherichia coli
- 3-MP:
-
3-Mercaptopyruvate
- 3-MP Str:
-
3-Mercaptopyruvate Str
- Str:
-
Sulfurtransferase(s)
- TS:
-
Thiosulfate
- TS Str:
-
Thiosulfate sulfurtransferase
References
Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene biosynthesis in plant biology. Academic Press, San Diego
Adams H, Teertstra W, Koster M, Tommassen J (2002) PspE (phage-shock protein E) of Escherichia coli is a rhodanese. FEBS Lett 518:173–176
Alphey MS, Williams RA, Mottram JC, Coombs GH, Hunter WN (2003) The crystal structure of Leishmania major 3-mercaptopyruvate sulfurtransferase. A three-domain architecture with a serine protease-like triad at the active site. J Biol Chem 278:48219–48227
Azumi Y, Watanabe A (1991) Evidence for a senescence associated gene induced by darkness. Plant Physiol 95:577–583
Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schürmann P, Droux M, Buchanan BB (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101:2642–2647
Bartels A (2006) Functional characterisation of sulfurtransferase proteins in higher plants. PhD thesis, Leibniz Universität Hannover
Bartels A, Forlani F, Pagani S, Papenbrock J (2007a) Conformational studies on Arabidopsis sulfurtransferase AtStr1 analysed by spectroscopic methods. Biol Chem 388:53–59
Bartels A, Mock HP, Papenbrock J (2007b) Differential expression of Arabidopsis sulfurtransferases under various growth conditions. Plant Physiol Biochem 45:178–187
Bauer M, Papenbrock J (2002) Identification and characterization of single-domain thiosulfate sulfurtransferases from Arabidopsis thaliana. FEBS Lett 532:427–431
Bauer M, Dietrich C, Nowak K, Sierralta WD, Papenbrock J (2004) Intracellular localization of sulfurtransferases from Arabidopsis thaliana. Plant Physiol 135:916–926
Blumenthal S, Hendrickson H, Abrol Y, Conn E (1968) Cyanide metabolism in higher plants: III. The biosynthesis of β-cyanoalanine. J Biol Chem 243:5302–5307
Bonomi F, Pagani S, Cerletti P, Cannella C (1977) Rhodanese-mediated sulfur transfer to succinate dehydrogenase. Eur J Biochem 72:17–24
Bordo D, Bork P (2002) The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations. EMBO Rep 3:741–746
Bordo D, Deriu D, Colnaghi R, Carpen A, Pagani S, Bolognesi M (2000) The crystal structure of a sulfurtransferase from Azotobacter vinelandii highlights the evolutionary relationship between the rhodanese and phosphatase enzyme families. J Mol Biol 298:691–704
Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, Yalovsky S, Ohad N (2004) Detection of protein–protein interactions in plants using bimolecular fluorescence complementation. Plant J 40:419–427
Burow M, Kessler D, Papenbrock J (2002) Enzymatic activity of the Arabidopsis sulfurtransferase resides in the C-terminal domain but is boosted by the N-terminal domain and the linker peptide in the full-length enzyme. Biol Chem 383:1363–1372
Cannella C, Berni R, Ricci G (1984) Determination of rhodanese activity by tetrazolium reduction. Anal Biochem 142:159–162
Chew NY (1973) Rhodanese in higher plants. Phytochemistry 12:2365–2367
Chung B-C, Lee SY, Oh SA, Rhew TH, Nam HG, Lee C-H (1997) The promoter activity of sen1, a senescence-associated gene of Arabidopsis, is repressed by sugars. J Plant Physiol 151:339–345
Colnaghi R, Cassinelli G, Drummond M, Forlani F, Pagani S (2001) Properties of the Escherichia coli rhodanese-like protein SseA: contribution of the active-site residue Ser240 to sulfur donor recognition. FEBS Lett 500:153–156
Cooper RM, Williams JS (2004) Elemental sulphur as an induced antifungal substance in plant defence. J Exp Bot 55:1947–1953
Cooper RM, Resende ML, Flood J, Rowan MG, Beale MH, Potter U (1996) Detection and cellular localization of elemental sulphur in disease-resistant genotypes of Theobroma cacao. Nature 379:159–162
Cornilescu G, Vinarov DV, Tyler EM, Merkley JL, Cornilescu CC (2006) Solution structure of a single-domain from Arabidopsis thaliana. Protein Sci 15:2836–2841
Donadio S, Shafiee A, Hutchinson R (1990) Disruption of a rhodanese like gene results in cysteine auxotrophy in Saccharopolyspora erythraea. J Bacteriol 172:350–360
Duan GL, Zhu YG, Tong YP, Cai C, Kneer R (2005) Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiol 138:461–469
Dubuis P-H, Marazzi C, Staedler E, Mauch F (2005) Sulphur deficiency causes a reduction in antimicrobial potential and leads to increased disease susceptibility of oilseed rape. J Phytopathol 153:27–36
Gemeinhardt K (1938) The thiocyanate content of plants. Ber Deut Botan Ges 56:275
Glatz Z, Bouchal P, Janiczek O, Mandl M, Ceskova P (1999) Determination of rhodanese enzyme activity by capillary zone electrophoresis. J Chromat A 838:139–148
Gliubich F, Gazerro M, Canotti G, Delbono S, Bombieri G, Berni R (1996) Active site structural features for chemically modified forms of rhodanese. J Biol Chem 271:21054–21061
Hama H, Kayahara T, Ogawa W, Tsuda M, Tsuchiya T (1994) Enhancement of serine-sensitivity by a gene encoding rhodanese-like protein in Escherichia coli. J Biochem 115:1135–1140
Hatzfeld Y, Saito K (2000) Evidence for the existence of rhodanese (thiosulfate:cyanide sulfurtransferase) in plants: preliminary characterization of two rhodanese cDNAs from Arabidopsis thaliana. FEBS Lett 470:147–150
Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256
Hildebrandt TM, Grieshaber MK (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J 275:3352–3361
Huang J, Niknahad H, Khan S, O’Brien PJ (1998) Hepatocyte-catalysed detoxification of cyanide by L-and D-cysteine. Biochem Pharmacol 55:1983–1990
Jarabak R, Westley J (1978) Steady-state kinetics of 3-mercaptopyruvate sulfurtransferase from bovine kidney Arch. Biochem Biophys 185:458–465
Kakes P, Hakvoort H (1992) Is there rhodanese activity in plants? Phytochemistry 31:1501–1505
Kende H (1993) Ethylene biosynthesis. Ann Rev Plant Physiol Plant Mol Biol 44:283–307
Klimmek O, Stein T, Pisa R, Simon J, Kroger A (1999) The single cysteine residue of the Sud protein is required for its function as a polysulfide-sulfur transferase in Wolinella succinogenes. Eur J Biochem 263:79–84
Laloi C, Rayapuram N, Chartier Y, Grienenberger JM, Bonnard G, Meyer Y (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci USA 98:14144–14149
Landrieu I, da Costa M, De Veylder L, Dewitte F, Vandepoele K, Hassan S, Wieruszeski JM, Corellou F, Faure JD, Van Montagu M, Inzé D, Lippens G (2004) A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:13380–13385
Laudenbach DE, Ehrhardt D, Green L, Grossmann A (1991) Isolation and characterization of a sulfur-regulated gene encoding a periplasmatically localized protein with sequence similarity to rhodanese. J Bacteriol 173:2751–2760
Leimkuehler S, Rajagopalan KV (2001) A sulfurtransferase is required in the transfer of cysteine sulfur in the in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J Biol Chem 276:22024–22031
Louie M, Kondor N, DeWitt JG (2003) Gene expression in cadmium-tolerant Datura innoxia: detection and characterization of cDNAs induced in response to Cd2+. Plant Mol Biol 52:81–89
Luo GX, Horowitz PM (1994) The sulfurtransferase activity and structure of rhodanese are affected by site-directed replacement of Arg-186 or Lys-249. J Biol Chem 269:8220–8225
Manning K (1988) Detoxification of cyanide by plants and hormone action. Ciba Found Symp 140:92–110
Marchand C, Le Marechal P, Meyer Y, Decottignies P (2006) Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics 6:6528–6537
Matthies A, Rajagopalan KV, Mendel RR, Leimkuehler S (2004) Evidence for the physiological role of a rhodanese-like protein for the biosynthesis of the molybdenum cofactor in humans. Proc Natl Acad Sci USA 101:5946–5951
Melino S, Cicero DO, Orsale M, Forlani F, Pagani S, Paci M (2003) Azotobacter vinelandii rhodanese: selenium loading and ion interaction studies. Eur J Biochem 270:4208–4215
Mendel RR (2007) Biology of the molybdenum cofactor. J Exp Bot 58:2289–2296
Meyer T, Burow M, Bauer M, Papenbrock J (2003) Arabidopsis sulfurtransferases: investigation of their function during senescence and in cyanide detoxification. Planta 217:1–10
Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86:419–433
Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934–11939
Nagahara N (2007) Molecular evolution of thioredoxin-dependent redox-sensing switch in mercaptopyruvate sulfurtransferase. Res Adv Biol Chem 1:19–26
Nagahara N, Katayama A (2005) Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteine-sulfenate in the maintenance of redox homeostasis. J Biol Chem 280:34569–34776
Nagahara N, Nishino T (1996) Role of amino acid residues in the active site of rat liver mercaptopyruvate sulfurtransferase. cDNA cloning, overexpression, and site-directed mutagenesis. J Biol Chem 271:27395–27401
Nagahara N, Okazaki T, Nishino T (1995) Cytosolic mercaptopyruvate sulfurtransferase is evolutionary related to mitochondrial rhodanese. J Biol Chem 270:16230–16235
Nagahara N, Ito T, Kitamura H, Nishino T (1998) Tissue and subcellular distribution of mercaptopyruvate sulfurtransferase in the rat: confocal laser fluorescence and immunoelectron microscopic studies combined with biochemical analysis. Histochem Cell Biol 110:243–250
Nagahara N, Ito T, Minami M (1999) Mercaptopyruvate sulfurtransferase as a defense against cyanide toxication: Molecular properties and mode of detoxification. Histol Histopathol 14:1277–1286
Nagahara N, Yoshii T, Abe Y, Matsumura T (2007) Thioredoxin-dependent enzymatic activation of mercaptopyruvate sulfurtransferase. An intersubunit disulfide bond serves as a redox switch for activation. J Biol Chem 282:1561–1569
Nakamura T, Yamaguchi Y, Sano H (2000) Plant mercaptopyruvate sulfurtransferases: molecular cloning, subcellular localization and enzymatic activities. Eur J Biochem 267:5621–5630
Nandi DL, Horowitz PM, Westley J (2000) Rhodanese as a thioredoxin oxidase. Int J Biochem Cell Biol 32:465–473
Niu JS, Yu L, Ma Z-Q, Chen P-D, Liu D-J (2002) Molecular cloning, characterization and mapping of a rhodanese like gene in wheat. Acta Genet Sin 29:266–272
Ogasawara Y, Lacourciere G, Stadtman T (2001) Formation of a selenium-substituted rhodanese by reaction with selenite and glutathione: possible role of a protein perselenide in a selenium delivery system. Proc Natl Acad Sci USA 98:9494–9498
Oh SA, Lee SY, Chung IK, Lee CH, Nam HG (1996) A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30:739–754
Okolie PN, Obasi BN (1993) Diurnal variation of cyanogenic glucosides, thiocyanate and rhodanese in cassava. Phytochemistry 33:775–778
Okubara PA, Berry PM (1999) A mRNA (Accession No. AF109156) from symbiotic root nodules of Datisca glomerata with homology to thiosulfate sulfurtransferase genes. PGR 99–027. Plant Physiol 119:1147
Pagani S, Bonomi F, Cerletti P (1984) Enzymic synthesis of the iron-sulfur cluster of spinach ferredoxin. Eur J Biochem 142:361–366
Pagani S, Eldridge M, Eady RR (1987) Nitrogenase of Klebsiella pneumoniae: rhodanese-catalyzed restoration of activity of inactive 2Fe species of the Fe protein. Biochem J 244:485–488
Palenchar PM, Buck CJ, Cheng H, Larson TJ, Mueller EG (2000) Evidence that thiI, an enzyme shared between thiamine and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate. J Biol Chem 275:8283–8286
Pantoja-Uceda D, López-Méndez B, Koshiba S, Inoue M, Rigawa T, Terada T, Shirouzu M, Tanaka A, Seki M, Shinozaki K, Yokoyama S, Güntert P (2005) Solution structure of the rhodanese homology domain At4g01050 (175–295) from Arabidopsis thaliana. Protein Sci 14:224–230
Papenbrock J, Grimm B (2001) Regulatory network of tetrapyrrole biosynthesis—studies of intracellular signalling involved in metabolic and developmental control of plastids. Planta 213:667–681
Papenbrock J, Schmidt A (2000a) Characterization of a sulfurtransferase from Arabidopsis thaliana. Eur J Biochem 267:145–154
Papenbrock J, Schmidt A (2000b) Characterization of two sulfurtransferase isozymes from Arabidopsis thaliana. Eur J Biochem 267:5571–5579
Papenbrock J, Bartels A, Hartmann F, Hartmann J, Triulzi T (2009) Reduced sulfur in the plant cell–enzymatic formation and functional roles. In: Sirko A et al (eds) Sulfur metabolism in higher plants. Backhuys Publishers, Leiden, pp 217–219
Peltier JB, Ytterberg AJ, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279:49367–49383
Piotrowski M, Schönfelder S, Weiler EW (2001) The Arabidopsis thaliana isogene NIT4 and its orthologs in tobacco encode β-cyano-l-alanine hydratase/nitrilase. J Biol Chem 276:2616–2621
Ploegman JH, Drent G, Kalk KH, Hol WGJ, Heinrikson RL, Keim P, Weng L, Russell J (1978) The covalent and tertiary structure of bovine liver rhodanese. Nature 273:124–129
Prieto JL, Perez-Castineira JR, Vega JM (1997) Thiosulfate reductase from Chlamydomonas. J Plant Physiol 151:385–389
Rajjou L, Lovigny Y, Groot SP, Belghazi M, Job C, Job D (2008) Proteome-wide characterization of seed aging in Arabidopsis: a comparison between artificial and natural aging protocols. Plant Physiol 148:620–641
Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509
Ray WK, Zeng G, Potters MB, Mansuri AM, Larson TJ (2000) Characterization of a 12-kilodalton rhodanese encoded by glpE of Escherichia coli and its interaction with thioredoxin. J Bacteriol 182:2277–2284
Russell J, Weng L, Keim PS, Heinrikson RL (1978) The covalent structure of bovine liver rhodanese. J Biol Chem 253:8102–8108
Sabelli R, Iorio E, De Martino A, Podo F, Ricci A, Viticchiè G, Rotilio G, Paci M, Melino S (2008) Rhodanese-thioredoxin system and allyl sulfur compounds. FEBS J 275:3884–3899
Schenk PM, Kazan K, Rusu AG, Manners JM, Maclean DJ (2005) The SEN1 gene of Arabidopsis is regulated by signals that link plant defence responses and senescence. Plant Physiol Biochem 43:997–1005
Schievelbein H, Baumeister R, Vogel R (1969) Comparative investigations on the activity of thiosulphate-sulphur transferase. Naturwissenschaften 56:416–417
Schmidt A (1984) Occurrence of mercaptopyruvate sulfotransferase activity in photosynthetic organisms. Z Naturforsch 39c:916–921
Schmidt A, Erdle I, Gamon B (1984) Isolation and characterization of thiosulfate reductases from the green alga Chlorella fusca. Planta 162:243–249
Shimada Y, Wu GJ, Watanabe A (1998) A protein encoded by din1, a dark-inducible and senescence-associated gene of radish, can be imported by isolated chloroplasts and has sequence similarity to sulphide dehydrogenase and other small stress proteins. Plant Cell Physiol 39:139–143
Sörbo BH (1955) Rhodanese. Methods Enzymol 2:334–337
Spallarossa A, Donahue JL, Larson TJ, Bolognesi M, Bordo D (2001) Escherichia coli GlpE is a prototype sulfurtransferase for the single-domain rhodanese homology superfamily. Structure 9:1117–1125
Spallarossa A, Forlani F, Carpen A, Armirotti A, Pagani S, Bolognesi M, Bordo D (2004) The “rhodanese” fold and catalytic mechanism of 3-mercaptopyruvate sulfurtransferases: crystal structure of SseA from Escherichia coli. J Mol Biol 335:583–593
Toohey JI (1989) Sulphane sulphur in biological systems: a possible regulatory role. Biochem J 264:625–632
Vennesland B, Castric PA, Conn EE, Solomonson LP, Volini M, Westley J (1982) Cyanide metabolism. Fed Proc 41:2639–2648
Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438
Waltner M, Weiner H (1995) Conversion of a nonprocessed mitochondrial precursor protein into one that is processed by the mitochondrial processing peptidase. J Biol Chem 270:26311–26317
Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J (2004) Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65:1795–1804
Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469
Westley J (1973) Rhodanese. Adv Enzymol 39:327–368
Westley J (1981) Thiosulfate:cyanide sulfurtransferase (rhodanese). Methods Enzymol 77:285–291
Westley J, Heyse D (1971) Mechanisms of sulfur transfer catalysis sulfhydryl-catalyzed transfer of thiosulfonate sulfur. J Biol Chem 246:1468–1474
White RH (1982) Metabolism of l-[sulfane-34S]thiocystine by Escherichia coli. Biochemistry 21:4271–4275
Williams JS, Cooper RM (2004) The oldest fungicide and newest phytoalexin–a reappraisal of the fungitoxicity of elemental sulphur. Plant Pathol 53:263–279
Williams JS, Hall SA, Hawkesford MJ, Beale MH, Cooper RM (2002) Elemental sulfur and thiol accumulation in tomato and defense against a fungal vascular pathogen. Plant Physiol 128:150–159
Williams RA, Kelly SM, Mottram JC, Coombs GH (2003) 3-Mercaptopyruvate sulfurtransferase of Leishmania contains an unusual C-terminal extension and is involved in thioredoxin and antioxidant metabolism. J Biol Chem 278:1480–1486
Wood JL (1987) Sulfane sulfur. Methods Enzymol 143:25–29
Wróbel M, Lewandowska I, Bronowicka-Adamska P, Paszewski A (2009) The level of sulfane sulfur in the fungus Aspergillus nidulans wild type and mutant strains. Amino Acids 37:565–571
Yang SH, Berberich T, Miyazaki A, Sano H, Kusano T (2003) Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis. Plant Cell Physiol 44:1037–1044
Zhao Y, Dai X, Blackwell HE, Schreiber SL, Chory J (2003) SIR1, an upstream component in auxin signaling identified by chemical genetics. Science 301:1107–1110
Acknowledgments
We would like to thank Dr. Fabio Forlani, Milan, Italy, for stimulating discussions. The work was financially supported by the Deutsche Forschungsgemeinschaft (PA 764/1-4 and 5, PA 764/7-1) and by the DAAD (Vigoni 0815171).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Papenbrock, J., Guretzki, S. & Henne, M. Latest news about the sulfurtransferase protein family of higher plants. Amino Acids 41, 43–57 (2011). https://doi.org/10.1007/s00726-010-0478-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-010-0478-6
Keywords
- Arabidopsis thaliana
- 3-Mercaptopyruvate
- Oxidative stress
- Thioredoxin
- Thiosulfate