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Cysteine Desulfurase-Mediated Sulfur Donation Pathways in Plants and Phototrophic Bacteria

  • Lolla Padmavathi
  • Hong Ye
  • Elizabeth A. H. Pilon-Smits
  • Marinus Pilon
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 27)

Cysteine is the sulfur donor for a number of important cofactor biosynthetic pathways including the synthesis of iron-sulfur clusters, thiamine, biotin and molybdenum cofactor. NifS-like cysteine desulfurase enzymes are key components in these pathways, catalyzing the initial release of S from cysteine. NifS-like enzymes do not work alone but are the first component of a sulfur transfer pathway from cysteine to cofactor. In vivo, NifS-like cysteine desulfurases work in concert with assembly factor proteins to which they transfer the released S and which serve to regulate the cysteine desulfurase activity and orchestrate the delivery of S to downstream targets. In plants, the chloroplast localized iron-sulfur assembly machinery resembles at least in part a machinery that in bacteria is responsible for the synthesis of iron-sulfur clusters under oxidative stress and iron limitation. A similar system operates in photosynthetic bacteria. While we are just beginning to unravel the mechanisms of S-dependent cofactor assembly systems it is already evident that these pathways play pivotal roles in cellular metabolism, and particularly are important to the function of plant plastids.

Keywords

Sulfur Cluster Cluster Assembly Molybdenum Cofactor Sulfur Assimilation Cluster Biogenesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abdel-Ghany SE, Ye H, Garifullina GF, Zhang L, Pilon-Smits EAH and Pilon M (2005) Iron–sulfur cluster biogenesis in chloroplasts. Involvement of the scaffold protein CpIscA. Plant Physiol 138: 161–172PubMedGoogle Scholar
  2. Agar JN, Krebs C, Frazzon J, Huynh BH, Dean DR and Johnson MK (2000) IscU as a scaffold for iron–sulfur cluster biosynthesis: sequential assembly of [2Fe–2S] and [4Fe–4S] clusters in IscU. Biochemistry 39: 7856–7862PubMedGoogle Scholar
  3. Amann K, Lezhneva L, Wanner G, Herrmann R and Meurer J. (2004) Accumulation of Photosystem One1, a member of a novel gene family, is required for accumulation of [4Fe–4S] cluster-containing chloroplast complexes and antenna proteins. Plant Cell 16: 3084–3097PubMedGoogle Scholar
  4. Balasubramanian R, Shen G, Bryant DA and Golbeck JH (2006) Regulatory roles for IscA and SufA in iron homeostasis and redox stress responses in the cyanobacterium Synechococcus sp. strain PCC 7002. J Bacteriol 188: 3182–3191PubMedGoogle Scholar
  5. Baldet P, Alban C and Douce R (1997) Biotin synthesis in higher plants: purification and characterization of bioB gene product equivalent from Arabidopsis thaliana overexpressed in Escherichia coli and its subcellular localization in pea leaf cells. FEBS Lett 419: 206–210PubMedGoogle Scholar
  6. Balk J and Lobreaux S (2005) Biogenesis of iron–sulfur proteins in plants. Trends in Plant Sci 10: 324–331Google Scholar
  7. Balk J, Aguilar Netz DJ, Tepper K, Pierik AJ and Lill R (2005) The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron–sulfur protein assembly. Mol Cell Biol 25: 10833–10841PubMedGoogle Scholar
  8. Balk J, Pierik AJ, Netz DJ, Muhlenhoff U, Lill R (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron–sulphur proteins. EMBO J 23: 2105–2115PubMedGoogle Scholar
  9. Beinert H (2000) Iron–sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5: 2–15PubMedGoogle Scholar
  10. Beinert H and Kiley PJ (1999) [Fe–S] proteins in sensing and regulatory functions. Curr Opin Chem Biol 3: 152–157PubMedGoogle Scholar
  11. Beinert H, Holm RH, and Munck E (1997) Iron–sulfur clusters: nature’s modular, multipurpose structures. Science 277: 653–659PubMedGoogle Scholar
  12. Belanger FC, Leustek T, Chu B and Kriz AL (1995) Evidence for the thiamine biosynthetic pathway in higher-plant plastids and its developmental regulation. Plant Mol Biol 29: 809–821PubMedGoogle Scholar
  13. Bui BT, Escalettes F, Chottard G, Florentin D and 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: 2688–2694PubMedGoogle Scholar
  14. Che P, Weaver LM, Wurtele ES and Nikolau BJ (2003) The role of biotin in regulating 3-methylcrotonyl-coenzyme a carboxylase expression in Arabidopsis. Plant Physiol 131: 1479–1486PubMedGoogle Scholar
  15. Cicchillo RM, Lee KH, Baleanu-Gogonea C, Nesbitt NM, Krebs C and Booker SJ (2004) Escherichia coli lipoyl synthase binds two distinct [4Fe–4S] clusters per polypeptide. Biochemistry 43: 11770–11781PubMedGoogle Scholar
  16. Clausen T, Kaiser JT, Steegborn C, Huber R and Kessler D (2000) Crystal structure of the cystine C-S lyase from Synechocystis: stabilization of cysteine persulfide for FeS cluster biosynthesis. Proc Natl Acad Sci USA 97: 3856–3861PubMedGoogle Scholar
  17. Cornah JE, Terry MJ and Smith AG. (2003) Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 8:224–230PubMedGoogle Scholar
  18. Ding B, Smith ES and Ding H (2005) Mobilization of the iron centre in IscA for the iron–sulphur cluster assembly in IscU. Biochem J 389: 797–802PubMedGoogle Scholar
  19. Ding H and Clark RJ (2004a) Characterization of iron binding in IscA, an ancient iron–sulphur cluster assembly protein. Biochem J 15: 433–440Google Scholar
  20. Ding H, Clark RJ and Ding B (2004b) IscA mediates iron delivery for assembly of iron–sulfur clusters in IscU under the limited accessible free iron conditions. J Biol Chem 279: 37499–37504PubMedGoogle Scholar
  21. Dorrestein PC, Zhai H, McLafferty FW and Begley TP (2004) The biosynthesis of the thiazole phosphate moiety of thiamin: the sulfur transfer mediated by the sulfur carrier protein ThiS. Chem Biol 11: 1373–1381PubMedGoogle Scholar
  22. Frazzon J, Fick JR and Dean DR (2002) Biosynthesis of iron–sulphur clusters is a complex and highly conserved process. Biochem Soc Trans 30: 680–685PubMedGoogle Scholar
  23. Hausmann A, Aguilar Netz DDJ, Balk J, Pierik AJ, Muhlenhoff U and Lill R (2005) The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron–sulfur protein assembly machinery. Proc Natl Acad Sci USA 102: 3266–3271PubMedGoogle Scholar
  24. Hawkesford MJ (2007) Uptake, allocation and subcellular transport of sulfate (this book)Google Scholar
  25. Heidenreich T, Wollers S, Mendel RR and Bittner F (2005) Characterization of the NifS-like domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism ofmolybdenum cofactor sulfuration. J. Biol. Chem. 280: 4213–4218PubMedGoogle Scholar
  26. Hell and Wirtz (2007) Metabolism of cysteine in plants and phototrophic bacteria (this book)Google Scholar
  27. Hjorth E, Hadfi K, Zauner S and Maier UG. (2005) Unique genetic compartmentalization of the SUF system in cryptophytes and characterization of a SufD mutant in Arabidopsis thaliana. FEBS Lett. 579: 1129–1135PubMedGoogle Scholar
  28. Jameson GN, Cosper MM, Hernandez HL, Johnson MK and Huynh BH (2004) Role of the [2Fe–2S] cluster in recombinant Escherichia coli biotin synthase. Biochemistry 43: 2022–2031PubMedGoogle Scholar
  29. Johnson D, Dean, D Smith AD and Johnson MK (2005) Structure, function and formation of biological iron–sulfur clusters. Annu Rev Biochem 74: 247–81PubMedGoogle Scholar
  30. Julliard J-H and Douce R (1991) Biosynthesis of the thiazole moiety of thiamin (vitamin B1) in higher plant chloroplasts. Proc Natl Acad Sci USA 88: 2042–2045PubMedGoogle Scholar
  31. Kato S, Mihara H, Kurihara T, Yoshimura T and Esaki N (2000) Gene cloning, purification, and characterization of two cyanobacterial NifS homologs driving iron–sulfur cluster formation. Biosci Biotechnol Biochem 64: 2412–2419PubMedGoogle Scholar
  32. Katoh A, Uenohara K, Akita M and Hashimoto T (2006) Early steps in the biosynthesis of NAD in Arabidopsis thaliana start with aspartate and occur in the plastid. Plant Physiol 141: 851–857PubMedGoogle Scholar
  33. Kessler D (2004) Slr0077 of Synechocystis has cysteine desulfurase as well as cystine lyase activity. Biochem Biophys Res Commun 320: 571–577PubMedGoogle Scholar
  34. Kispal G, Csere P, Prohl C and Lill R (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18: 3981–3989PubMedGoogle Scholar
  35. Krebs C, Agar JN, Smith AD, Frazzon J, Dean DR, Huynh BH and Johnson MK (2001) IscA, an alternate scaffold for Fe–S cluster biosynthesis. Biochemistry 40:14069–14080PubMedGoogle Scholar
  36. Kuper J, Llamas A, Hecht HJ, Mendel RR and Schwarz G. (2004) Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430: 803–806PubMedGoogle Scholar
  37. Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R and Van Montagu M (2001) A Mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13: 89–100PubMedGoogle Scholar
  38. Lange H, Mühlenhoff U, Denzel M, Kispal G and Lill R (2004) The heme synthesis defect of mutants impaired in mitochondrial iron-sulfur protein biogenesis is caused by reversible inhibition of ferrochelatase. J Biol Chem 279: 29101–29108PubMedGoogle Scholar
  39. Lauhon CT and Kambampati R (2000) The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamin, and NAD. J Biol Chem 275: 20096–20103PubMedGoogle Scholar
  40. Layer G, Heinz DW, Jahn D and Schubert WD. (2004) Structure and function of radical SAM enzymes. Curr Opin Chem Biol 8:468–476PubMedGoogle Scholar
  41. Layer G, Kervio E, Morlock G, Heinz DW, Jahn D, Retey J and Schubert WD (2005) Structural and functional comparison of HemN to other radical SAM enzymes. Biol Chem 386: 971–980PubMedGoogle Scholar
  42. Leon S, Touraine B, Briat J-F and Lobreaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochem J 366:557–564PubMedGoogle Scholar
  43. Leon S, Touraine B, Ribot C, Briat JF and Loberaux S (2003) Iron–sulphur cluster assembly in plants: distinct NFU proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J 371: 823–830PubMedGoogle Scholar
  44. Leon S, Touraine B, Briat JF and Lobreaux S. (2005) Mitochondrial localization of Arabidopsis thaliana Isu Fe–S scaffold proteins. FEBS Lett. 579:1930–1934PubMedGoogle Scholar
  45. Leonardi R and Roach PL (2004) Thiamine biosynthesis in Escherichia coli: in vitro reconstitution of the thiazole synthase activity. J Biol Chem 279: 17054–17062PubMedGoogle Scholar
  46. Leonardi R, Fairhurst SA, Kriek M, Lowe DJ and Roach PL (2003) Thiamine biosynthesis in Escherichia coli: isolation and initial characterisation of the ThiGH complex. FEBS Lett 539: 95–99PubMedGoogle Scholar
  47. Lezhneva L, Amann K and Meurer J (2004) The universally conserved HCF101 protein is involved in assembly of [4Fe–4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J 37: 174–85PubMedGoogle Scholar
  48. Li H-M, Theg SM, Bauerle CM and Keegstra K (1990) Metal-ion-center assembly of ferredoxin and plastocyanin in isolated chloroplasts. Proc Natl Acad Sci USA 87: 6748–6752PubMedGoogle Scholar
  49. Lill R and Kispal G (2000) Maturation of cellular Fe–S proteins: an essential function of mitochondria. Trends Biochem Sci 25: 352–356PubMedGoogle Scholar
  50. Lill R and Muhlenhoff U (2005) Iron–sulfur protein biogenesis in eukaryotes. Trends Biochem Sci 30: 133–141PubMedGoogle Scholar
  51. Loiseau L, Ollagnier-de-Choudens S, Nachin L, Fontecave M and Barras F (2003) Biogenesis of Fe–S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase. J Biol Chem 278: 38352–38359PubMedGoogle Scholar
  52. Loiseau L, Ollagnier-de Choudens S, Lascoux D, Forest E, Fontecave M and Barras F (2005) Analysis of the heteromeric CsdA-CsdE cysteine desulfurase, assisting [Fe–S] cluster biogenesis in Escherichia coli. J Biol Chem 280: 26760–26769PubMedGoogle Scholar
  53. Mendel RR (2005) Molybdenum: biological activity and metabolism. Dalton Trans 21: 3404–3409PubMedGoogle Scholar
  54. Mendel RR and Hansch R. (2002) Molybdoenzymes and molybdenum cofactor in plants. J Exp Bot 53:1689–1698PubMedGoogle Scholar
  55. Mihara H and Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60: 12–23PubMedGoogle Scholar
  56. Mihara H, Kurihara T, Yoshimura T, Soda K and Esaki N (1997) Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. Gene cloning, purification, and characterization of a novel pyridoxal enzyme. J Biol Chem 272: 22417–22424PubMedGoogle Scholar
  57. Mihara H, Kurihara T, Yoshimura T and Esaki N (2000) Kinetic and mutational studies of three NifS homologs from Escherichia coli: mechanistic difference between L-cysteine desulfurase and L-selenocysteine lyase reactions. J Biochem 127: 559–567PubMedGoogle Scholar
  58. Moller GM, Kunkel T and Chua N-H (2001) A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev 15: 90–103PubMedGoogle Scholar
  59. Muhlenhoff U, Gerber J, Richhardt N and Lill R (2003) Components involved in assembly and dislocation of iron–sulfur clusters on the scaffold protein Isu1p. EMBO J 22: 4815–4825PubMedGoogle Scholar
  60. Nachin L, Loiseau L, Expert D and Barras F (2003) SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe–S] biogenesis under oxidative stress. EMBO J 22: 427–437PubMedGoogle Scholar
  61. Nakai Y, Umeda N, Suzuki T, Nakai M, Hayashi H, Watanabe K and Kagamiyama H. (2004) Yeast Nfs1p is involved in thio-modification of both mitochondrial and cytoplasmic tRNAs. J Biol Chem 279:12363–12368PubMedGoogle Scholar
  62. Nishio K and Nakai M (2000) Transfer of iron–sulfur cluster from NifU to apoferredoxin. J Biol Chem 275: 22615–22618PubMedGoogle Scholar
  63. Oda Y, Samanta SK, Rey FE, Wu L, Liu X, Yan T, Zhou J and Harwood CS (2005) Functional genomic analysis of three nitrogenase isozymes in the photosynthetic bacterium Rhodopseudomonas palustris. J Bacteriol 187: 7784–7794PubMedGoogle Scholar
  64. Ollagnier-de Choudens S, Nachin L, Sanakis Y, Loiseau L, Barras F and Fontecave M (2003) SufA from Erwinia chrysanthemi. Characterization of a scaffold protein required for iron–sulfur cluster assembly. J Biol Chem 278:17993–18001PubMedGoogle Scholar
  65. Ollagnier-de-Choudens S, Sanakis Y and Fontecave M (2004) SufA/IscA: reactivity studies of a class of scaffold proteins involved in [Fe–S] cluster assembly. J Biol Inorg Chem 9: 828–838PubMedGoogle Scholar
  66. Ollagnier de Choudens S, Loiseau L, Sanakis Y, Barras F and Fontecave M (2005) Quinolinate synthetase, an iron–sulfur enzyme in NAD biosynthesis. FEBS Lett 579: 3737–3743Google Scholar
  67. Outten FW, Wood MJ, Munoz FM and Storz G (2003) The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe–S cluster assembly in Escherichia coli. J Biol Chem 278: 45713–45719PubMedGoogle Scholar
  68. Outten FW, Djaman O and Storz G (2004) A suf operon requirement for Fe–S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol 52: 861–872PubMedGoogle Scholar
  69. Park J-H, Dorrestein PC, Zhai H, Kinsland C, McLafferty FW and Begley TP (2003) Biosynthesis of the thiazole moiety of thiamin pyrophosphate (vitamin B1). Biochemistry 42: 12430–12438PubMedGoogle Scholar
  70. Petit J-M, Briat J-F and Lobreaux S (2001) Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem J 359: 575–582PubMedGoogle Scholar
  71. Picciocchi A, Douce R and Alban C (2003) The plant biotin synthase reaction. Identification and characterization of essential mitochondrial accessory protein components. J Biol Chem 278: 24966–24975PubMedGoogle Scholar
  72. Pilon M, America T, van ‘t Hof R, de Kruijff B and Weisbeek P (1995) Protein translocation into chloroplasts. In: Advances in molecular and cell biology (Rothman SS Ed.) Membrane protein transport. JAI Press, Greenwich. Vol 4, pp 229–255Google Scholar
  73. Pilon-Smits EA, Garifullina GF, Abdel-Ghany S, Kato S, Mihara H, Hale KL, Burkhead JL, Esaki N, Kurihara T and Pilon M (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiol 130: 1309–1318PubMedGoogle Scholar
  74. Pondarre C, Antiochos BB, Campagna DR, Clarke SSL, Greer EL, Deck KM, McDonald A, Han AP, Medlock A, Kutok JL, Anderson SA, Eisenstein RS and Fleming MD (2006) The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron–sulfur cluster biogenesis. Hum Mol Genet 15: 953–964PubMedGoogle Scholar
  75. Raven JA, Evans MC and Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynthesis Res 60: 111–149Google Scholar
  76. Ribeiro DT, Farias LP, de Almeida JD, Kashiwabara PM, Ribeiro AF, Silva-Filho MC, Menck CF and Van Sluys MA (2005) Functional characterization of the thi1 promoter region from Arabidopsis thaliana. J Exp Bot 56: 1797–1804PubMedGoogle Scholar
  77. Schneider G and Lindqvist Y (2001) Structural enzymology of biotin biosynthesis. FEBS Lett 495: 7–11PubMedGoogle Scholar
  78. Seidler A, Jaschkowitz K and Wollenberg M (2001) Incorporation of iron–sulphur clusters in membrane-bound proteins. Biochem Soc Trans 29: 418–421PubMedGoogle Scholar
  79. Shikanai T, Müller-Moulé P, Munekage Y, Niyogi K and Pilon M (2003) PAA1, a P-type ATPase of Arabidopsis, Functions in Copper Transport in Chloroplasts. Plant Cell 15: 1333–1346PubMedGoogle Scholar
  80. Shingles R, North M and McCarty RE (2002) Ferrous Ion Transport across Chloroplast Inner Envelope Membranes. Plant Physiol 128: 1022–1030PubMedGoogle Scholar
  81. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF and Miller NE (2001) Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res 29: 1097–1106PubMedGoogle Scholar
  82. Stockel J and Oelmuller R (2004) A novel protein for photosystem I biogenesis. J. Biol. Chem. 279: 10243–10251PubMedGoogle Scholar
  83. Takahashi Y and Tokumoto U (2002) A third bacterial system for the assembly of iron–sulfur clusters with homologs in archaea and plastids. J Biol Chem 277: 28380–28383PubMedGoogle Scholar
  84. Takahashi Y, Mitsui A, Hase T and Matsubara H (1986) Formation of the iron sulfur cluster of ferredoxin in isolated chloroplasts. Proc Natl Acad Sci USA 83: 2434–2437PubMedGoogle Scholar
  85. Takahashi Y, Mitsui A and Matsubara H (1990) Formation of the Fe–S cluster of ferredoxin in lysed spinach chloroplasts. Plant Physiol 95: 97–103Google Scholar
  86. Tong WH and Rouault TA (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron–sulfur cluster biogenesis and iron homeostasis. Cell Metab 3: 199–210PubMedGoogle Scholar
  87. Touraine B, Boutin J, Marion-Poll A, Briat J, Peltier G and Lobreaux S (2004) Nfu2: a scaffold protein required for [4Fe–4S] and ferredoxin iron–sulfur cluster assembly in Arabidopsis chloroplasts. Plant J 40:101–111PubMedGoogle Scholar
  88. Van Hoewyk D, Abdel-Ghany SE, Cohu C, Herbert S, Kugrens P, Pilon M and Pilon-Smits EAH (2007) Chloroplast iron-sulfur cluster protein maturation requires the essential cysteine desulfurylase CpNifS. Proc Natl Acad Sci USA 104:5686–5691PubMedGoogle Scholar
  89. Walsby CJ, Ortillo D, Yang J, Nnyepi MR, Broderick WE, Hoffman BM and Broderick JB (2005) Spectroscopic approaches to elucidating novel iron–sulfur chemistry in the “radical-SAM” protein superfamily. Inorg Chem 44: 727–741PubMedGoogle Scholar
  90. Wang T, Shen G, Balasubramanian R, McIntosh L, Bryant DA and Golbeck JH (2004) The sufR gene (sll0088 in Synechocystis sp. strain PCC 6803) functions as a repressor of the sufBCDS operon in iron–sulfur cluster biogenesis in cyanobacteria. J Bacteriol 186: 956–967PubMedGoogle Scholar
  91. Xiong L, Ishitani M, Lee H and Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell. 13:2063–83PubMedGoogle Scholar
  92. Xu XM and Moller SG. (2004) AtNAP7 is a plastidic SufC-like ATP-bindingGoogle Scholar
  93. Xu XM and Moller SG (2006) AtSufE is an essential activator of plastidic and mitochondrial desulfurases in Arabidopsis. EMBO J 25: 900–909PubMedGoogle Scholar
  94. Xu XM, Adams S, Chua NH and Moller SG (2005) AtNAP1 represents an atypical SufB protein in Arabidopsis plastids. J Biol Chem 280: 6648–6654PubMedGoogle Scholar
  95. Yabe T and Nakai M (2006) Arabidopsis AtIscA-I is affected by deficiency of Fe–S cluster biosynthetic scaffold AtCnfU-V. Biochem Biophys Res Commun 340: 1047–1052PubMedGoogle Scholar
  96. Yabe T, Morimoto K, Kikuchi S, Nishio K, Terashima I and Nakai M (2004) The Arabidopsis chloroplastic NifU-like protein CnfU, which can act as an iron–sulfur cluster scaffold protein, is required for biogenesis of ferredoxin and photosystem I. Plant Cell 16: 993–1007PubMedGoogle Scholar
  97. Ye H, Garifullina GF, Abdel-Ghany S, Zhang L, Pilon-Smits EAH and Pilon M (2005) AtCpNifS is required for iron–sulfur cluster formation in ferredoxin in vitro. Planta 220:602–608PubMedGoogle Scholar
  98. Ye H, Abdel-Ghany SE, Anderson TD, Pilon-Smits EA and Pilon M (2006a) CpSufE activates the cysteine desulfurase CpNifS for chloroplastic Fe–S cluster formation. J Biol Chem 281: 8958–8969PubMedGoogle Scholar
  99. Ye H, Pilon M and Pilon-Smits EAH (2006b) Iron Sulfur Cluster Biogenesis in Chloroplasts. New Phytologist 171: 285–292PubMedGoogle Scholar
  100. Zeller T, Moskvin OV, Li K, Klug G and Gomelsky M (2005) Transcriptome and physiological responses to hydrogen peroxide of the facultatively phototrophic bacterium Rhodobacter sphaeroides. J Bacteriol 187: 7232–7242PubMedGoogle Scholar
  101. Zheng L, White RH, Cash VL, Jack RF and Dean DR (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci USA 90: 2754–2758PubMedGoogle Scholar
  102. Zheng L, White RH, Cash VL and Dean DR (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33: 4714–4720PubMedGoogle Scholar
  103. Zheng L, Cash VL, Flint DH and Dean DR (1998) Assembly of Iron–Sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273: 13264–13272PubMedGoogle Scholar
  104. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA and Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562–4570PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Lolla Padmavathi
    • 1
  • Hong Ye
    • 1
  • Elizabeth A. H. Pilon-Smits
    • 1
  • Marinus Pilon
    • 1
  1. 1.Department of BiologyColorado State UniversityFort CollinsUSA

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