Skip to main content
SpringerLink
Log in

Cell Biology of Molybdenum

  • Chapter
  • First Online:
Book cover Cell Biology of Metals and Nutrients

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 17))

Abstract

The transition element molybdenum (Mo) is essential for (nearly) all biological systems as it is required by enzymes catalyzing diverse key reactions in the global carbon, sulfur,and nitrogen metabolism. The metal itself is biologically inactive unless it is complexed by a special cofactor. With the exception of bacterial nitrogenase, where Mo is a constituent of the FeMo-cofactor, Mo is bound to a pterin, thus forming the molybdenum cofactor (Moco), which is the active compound at the catalytic site of all other Mo-enzymes. In eukaryotes, the most prominent Mo-enzymes are nitrate reductase, sulfite oxidase, xanthine dehydrogenase, aldehyde oxidase, and the mitochondrial amidoxime reductase. The biosynthesis of Moco involves the complex interaction of six proteins and is a process of four steps, which also includes iron and copper in an indispensable way. Moco, as released after synthesis, is likely to be distributed to the apoproteins of Mo-enzymes by putative Moco-binding proteins. Xanthine dehydrogenase and aldehyde oxidase, but not sulfite oxidase and nitrate reductase, require the postranslational sulfuration of their Mo-site to become active.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ABA:

Abscisic acid

AO:

Aldehyde oxidase

Cnx1-E:

N-terminal domain of Cnx1

Cnx1-G:

C-terminal domain of Cnx1

cPMP:

Cyclic pyranopterin monophosphate

Cu:

Copper

IAA:

Indole-3-acetic acid

Fe:

Iron

FAD:

Flavin adenine dinucleotide

mARC:

Mitochondrial amidoxime reducing component

Mo:

Molybdenum

MoBP:

Molybdenum cofactor binding protein

Moco:

Molybdenum cofactor

MPT:

Molybdopterin

NR:

Nitrate reductase

NO:

Nitric oxide

ROS:

Reactive oxygen species

SO:

Sulfite oxidase

XDH:

Xanthine dehydrogenase

XO:

Xanthine oxidase

References

  • Aguilar M, Cardenas J, Fernandez E (1992) Quantitation of molybdopterin oxidation product in wild-type and molybdenum cofactor deficient mutants of Chlamydomonas reinhardtii. Biochim Biophys Acta 1160:269–274

    CAS  PubMed  Google Scholar 

  • Akaba S, Seo M, Dohmae N, Takio K, Sekimoto H, Kamiya Y, Furuya N, Komano T, Koshiba T (1999) Production of homo- and hetero-dimeric isozymes from two aldehyde oxidase genes of Arabidopsis thaliana. J Biochem 126:395–401

    CAS  PubMed  Google Scholar 

  • Amaya Y, Yamazaki K, Sato M, Noda K, Nishino T, Nishino T (1990) Proteolytic conversion of xanthine dehydrogenase from the NAD-dependent type to the O2-dependent type. Amino acid sequence of rat liver xanthine dehydrogenase and identification of the cleavage sites of the enzyme protein during irreversible conversion by trypsin. J Biol Chem 265:14170–14175

    CAS  PubMed  Google Scholar 

  • Ataya FS, Witte CP, Galvan A, Igeno MI, Fernandez E (2003) Mcp1 encodes the molybdenum cofactor carrier protein in Chlamydomonas reinhardtii and participates in protection, binding, and storage functions of the cofactor. J Biol Chem 278:10885–10890

    Article  CAS  PubMed  Google Scholar 

  • Badwey JA, Robinson JM, Karnovsky MJ, Karnovsky ML (1981) Superoxide production by an unusual aldehyde oxidase in guinea pig granulocytes. Characterization and cytochemical localization. J Biol Chem 256:3479–3486

    CAS  PubMed  Google Scholar 

  • Balk J, Lill R (2004) The cell’s cookbook for iron-sulfur clusters: recipes for fool’s gold? Chembiochem 5:1044–1049

    Article  CAS  PubMed  Google Scholar 

  • Baxter I, Muthukumar B, Park HC, Buchner P, Lahner B, Danku J, Zhao K, Lee J, Hawkesford MJ, Guerinot ML, Salt DE (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet 4:e1000004

    Article  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    Article  CAS  PubMed  Google Scholar 

  • Bittner F, Oreb M, Mendel RR (2001) ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana. J Biol Chem 276:40381–40384

    Article  CAS  PubMed  Google Scholar 

  • Boland MJ, Schubert KR (1982) Purine biosynthesis and catabolism in soybean root nodules: incorporation of 14C from 14CO2 into xanthine. Arch Biochem Biophys 213:486–491

    Article  CAS  PubMed  Google Scholar 

  • Bordas J, Bray RC, Garner CD, Gutteridge S, Hasnain SS (1980) X-ray absorption spectroscopy of xanthine oxidase. The molybdenum centres of the functional and the desulpho forms. Biochem J 191:499–508

    CAS  PubMed  Google Scholar 

  • Bortels H (1930) Molybdän als Katalysator bei der biologischen Stickstoffbindung. Arch Mikrobiol 1:333–342

    Article  CAS  Google Scholar 

  • Braaksma FJ, Feenstra WJ (1982) Isolation and characterization of nitrate reductase-deficient mutants of Arabidopsis thaliana. Theor Appl Genet 64:83–90

    Article  CAS  Google Scholar 

  • Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J 50:696–709

    Article  CAS  PubMed  Google Scholar 

  • Campbell WH, Kinghorn KR (1990) Functional domains of assimilatory nitrate reductases and nitrite reductases. Trends Biochem Sci 15:315–319

    Article  CAS  PubMed  Google Scholar 

  • Campbell WH (2001) Structure and function of eukaryotic NAD(P)H:nitrate reductase. Cell Mol Life Sci 58:194–204

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Palma JM, Sandalio LM, Valderrama R, Barroso JB, Del Rio LA (2008) Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves. J Plant Physiol 165:1319–1330

    Article  CAS  PubMed  Google Scholar 

  • Crawford NM (1992) Study of chlorate resistant mutants of Arabidopsis: insights into nitrate assimilation and ion metabolism of plants. In: Setlow JK (ed) Genetic engineering, principles and methods, vol 14. Plenum Press, New York, pp 89–98

    Google Scholar 

  • Da Cruz S, Xenarios I, Langridge J, Vilbois F, Parone P, Martinou J (2003) Proteomic analysis of the mouse liver mitochondrial inner membrane. J Biol Chem 278:41566–41571

    Article  PubMed  CAS  Google Scholar 

  • Datta DB, Triplett EW, Newcomb EH (1991) Localization of xanthine dehydrogenase in cowpea root nodules: implications for the interaction between cellular compartments during ureide biogenesis. Proc Natl Acad Sci USA 88:4700–4702

    Article  CAS  PubMed  Google Scholar 

  • Del Rio LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jimenez A, Lopez-Huertas E, Hernandez JA (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200

    Article  PubMed  Google Scholar 

  • Dos Santos PC, Dean DR, Hu Y, Ribbe MW (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem Rev 104:1159–1173

    Article  PubMed  CAS  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Fernandez E, Matagne RF (1986) In vivo complementation analysis of nitrate reductase-deficient mutants in Chlamydomonas reinhardtii. Curr Genet 10:397–403

    Article  CAS  PubMed  Google Scholar 

  • Fischer K, Barbier GG, Hecht HJ, Mendel RR, Campbell WH, Schwarz G (2005) Structural basis of eukaryotic nitrate reduction: crystal structures of the nitrate reductase active site. Plant Cell 17:1167–1179

    Article  CAS  PubMed  Google Scholar 

  • Fischer K, Llamas A, Tejada-Jimenez M, Schrader N, Kuper J, Ataya FS, Galvan A, Mendel RR, Fernandez E, Schwarz G (2006) Function and structure of the molybdenum cofactor carrier protein from Chlamydomonas reinhardtii. J Biol Chem 281:30186–30194

    Article  CAS  PubMed  Google Scholar 

  • Gabard J, Pelsy F, Marion-Poll A, Caboche M, Saalbach I, Grafe R, Müller AJ (1988) Genetic analysis of nitrate reductase deficient mutants of Nicotiana plumbaginifolia: evidence for six complementation groups among 70 classified molybdenum cofactor deficient mutants. Mol Gen Genet 213:275–281

    Article  Google Scholar 

  • Garattini E, Mendel RR, Romao MJ, Wright R, Terao M (2003) Mammalian molybdo-flavoenzymes, an expanding family of proteins: structure, genetics, regulation, function and pathophysiology. Biochem J 372:15–32

    Article  CAS  PubMed  Google Scholar 

  • González-Guzmán M, Abia D, Salinas J, Serrano R, Rodrigez PL (2004) Two new alleles of the abscisic aldehyde oxidase 3 gene reveal its role in abscisic acid biosynthesis in seeds. Plant Physiol 135:325–333

    Article  PubMed  Google Scholar 

  • Gruenewald S, Wahl B, Bittner F, Hungeling H, Kanzow S, Kotthaus J, Schwering U, Mendel RR, Clement B (2008) The fourth molybdenum containing enzyme mARC: cloning and involvement in the activation of N-hydroxylated prodrugs. J Med Chem 51:8173–8177

    Article  CAS  PubMed  Google Scholar 

  • Gutzke G, Fischer B, Mendel RR, Schwarz G (2001) Thiocarboxylation of molybdopterin synthase provides evidence for the mechanism of dithiolene formation in metal-binding pterins. J Biol Chem 276:36268–36274

    Article  CAS  PubMed  Google Scholar 

  • Hänsch R, Lang C, Riebeseel E, Lindigkeit R, Gessler A, Rennenberg H, Mendel RR (2006) Plant sulfite oxidase as novel producer of H2O2: combination of enzyme catalysis with a subsequent nonenzymatic reaction step. J Biol Chem 281:6884–6888

    Article  PubMed  CAS  Google Scholar 

  • Hanzelmann P, Hernandez HL, Menzel C, Garcia-Serres R, Huynh BH, Johnson MK, Mendel RR, Schindelin H (2004) Characterization of MOCS1A, an oxygen-sensitive iron-sulfur protein involved in human molybdenum cofactor biosynthesis. J Biol Chem 279:34721–34732

    Article  PubMed  CAS  Google Scholar 

  • Hanzelmann P, Schindelin H (2004) Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci USA 101:12870–12875

    Article  PubMed  Google Scholar 

  • Havemeyer A, Bittner F, Wollers S, Mendel R, Kunze T, Clement B (2006) Identification of the missing component in the mitochondrial benzamidoxime prodrug-converting system as a novel molybdenum enzyme. J Biol Chem 281:34796–34802

    Article  CAS  PubMed  Google Scholar 

  • Heidenreich T, Wollers S, Mendel RR, Bittner F (2005) Characterization of the NifS-like domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism of molybdenum cofactor sulfuration. J Biol Chem 280:4213–4218

    Article  CAS  PubMed  Google Scholar 

  • Hesberg C, Hansch R, Mendel RR, Bittner F (2004) Tandem orientation of duplicated xanthine dehydrogenase genes from Arabidopsis thaliana: differential gene expression and enzyme activities. J Biol Chem 279:13547–13554

    Article  CAS  PubMed  Google Scholar 

  • Hille R, Nishino T (1995) Flavoprotein structure and mechanism. 4. Xanthine oxidase and xanthine dehydrogenase. Faseb J 9:995–1003

    CAS  PubMed  Google Scholar 

  • Hille R (1996) The mononuclear molybdenum enzymes. Chem Rev 96:2757–2816

    Article  CAS  PubMed  Google Scholar 

  • Hille R (2002) Molybdenum enzymes containing the pyranopterin cofactor: an overview. Met Ions Biol Syst 39:187–226

    CAS  PubMed  Google Scholar 

  • Hille R (2005) Molybdenum-containing hydroxylases. Arch Biochem Biophys 433:107–116

    Article  CAS  PubMed  Google Scholar 

  • Hoff T, Schnorr KM, Meyer C, Caboche M (1995) Isolation of two Arabidopsis cDNAs involved in early steps of molybdenum cofactor biosynthesis by functional complementation of Escherichia coli mutants. J Biol Chem 270:6100–6107

    Article  CAS  PubMed  Google Scholar 

  • Ibdah M, Chen YT, Wilkerson CG, Pichersky E (2009) An aldehyde oxidase in developing seeds of Arabidopsis converts benzaldehyde to benzoic Acid. Plant Physiol 150:416–423

    Article  CAS  PubMed  Google Scholar 

  • Ivanov NV, Hubalek F, Trani M, Edmondson DE (2003) Factors involved in the assembly of a functional molybdopyranopterin center in recombinant Comamonas acidovorans xanthine dehydrogenase. Eur J Biochem 270:4744–4754

    Article  CAS  PubMed  Google Scholar 

  • Johnson JL, Hainline BE, Rajagopalan KV (1980) Characterization of the molybdenum cofactor of sulfite oxidase, xanthine, oxidase, and nitrate reductase. Identification of a pteridine as a structural component. J Biol Chem 255:1783–1786

    CAS  PubMed  Google Scholar 

  • Johnson JL, Hainline BE, Rajagopalan KV, Arison BH (1984) The pterin component of the molybdenum cofactor. Structural characterization of two fluorescent derivatives. J Biol Chem 259:5414–5422

    CAS  PubMed  Google Scholar 

  • Johnson JL, Duran M (2001) Molybdenum cofactor deficiency and isolated sulfite oxidase deficiency. In: Scriver C, Beaudet A, Sly W, Valle D (eds) The metabolic and molecular bases of inherited disease. McGraw-Hill, New York, pp 3163–3177

    Google Scholar 

  • Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52:1981–1989

    Article  CAS  PubMed  Google Scholar 

  • Kisker C, Schindelin H, Pacheco A, Wehbi WA, Garrett RM, Rajagopalan KV, Enemark JH, Rees DC (1997a) Molecular basis of sulfite oxidase deficiency from the structure of sulfite oxidase. Cell 91:973–983

    Article  CAS  PubMed  Google Scholar 

  • Kisker C, Schindelin H, Rees DC (1997b) Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 66:233–267

    Article  CAS  PubMed  Google Scholar 

  • Kispal G, Csere P, Prohl C, Lill R (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. Embo J 18:3981–3989

    Article  CAS  PubMed  Google Scholar 

  • Kleinhofs A, Warner RL, Lawrence JM, Jeter JM, Kudrna DA (1989) Molecular genetics of nitrate reductase in barley. In: Wray JL, Kinghorn JR (eds) Molecular and genetic aspects of nitrate assimilation. Oxford University Press, Oxford, pp 197–211

    Google Scholar 

  • Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T (2004) Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiol 134:1697–1707

    Article  CAS  PubMed  Google Scholar 

  • Kozmin SG, Leroy P, Pavlov YI, Schaaper RM (2008) YcbX and yiiM, two novel determinants for resistance of Escherichia coli to N-hydroxylated base analogues. Mol Microbiol 68:51–65

    Article  CAS  PubMed  Google Scholar 

  • Kruse T, Geisler M, Lehrke M, Ringel P, Mendel RR (2009) Identification and biochemical characterization of molybdenum cofactor-binding proteins from Arabidopsis thaliana. J Biol Chem (unpublished)

    Google Scholar 

  • Kuper J, Palmer T, Mendel RR, Schwarz G (2000) Mutations in the molybdenum cofactor biosynthetic protein Cnx1G from Arabidopsis thaliana define functions for molybdopterin binding. Mo-insertion and molybdenum cofactor stabilization. Proc Natl Acad Sci USA 97:6475–6480

    Article  CAS  PubMed  Google Scholar 

  • Kuper J, Llamas A, Hecht HJ, Mendel RR, Schwarz G (2004) Structure of molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430:806–806

    Article  CAS  Google Scholar 

  • Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100

    Article  CAS  PubMed  Google Scholar 

  • Lang C, Popko J, Wirtz M, Hell R, Herschbach C, Kreuzwieser J, Rennenberg H, Mendel RR, Hänsch R (2007) Sulfite oxidase as key enzyme for protecting plants against sulfur dioxide. Plant Cell Environ 30:447–455

    Article  CAS  PubMed  Google Scholar 

  • Leimkühler S, Klipp W (1999) Role of XDHC in Molybdenum cofactor insertion into xanthine dehydrogenase of Rhodobacter capsulatus. J Bacteriol 181:2745–2751

    PubMed  Google Scholar 

  • Leimkühler S, Wuebbens MM, Rajagopalan KV (2001) Characterization of Escherichia coli MoeB and its involvement in the activation of molybdopterin synthase for the biosynthesis of the molybdenum cofactor. J Biol Chem 276:34695–34701

    Article  PubMed  Google Scholar 

  • Leon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JAD, Koorneef M (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661

    Article  CAS  PubMed  Google Scholar 

  • Lewis NJ, Hurt P, Sealy-Lewis HM, Scazzocchio C (1978) The genetic control of the molybdoflavoproteins in Aspergillus nidulans. IV. A comparison between purine hydroxylase I and II. Eur J Biochem 91:311–316

    Article  CAS  PubMed  Google Scholar 

  • Lill R, Muhlenhoff U (2006) Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu Rev Cell Dev Biol 22:457–486

    Article  CAS  PubMed  Google Scholar 

  • Llamas A, Mendel RR, Schwarz G (2004) Synthesis of adenylated molybdopterin: an essential step for molybdenum insertion. J Biol Chem 279:55241–55246

    Article  CAS  PubMed  Google Scholar 

  • Llamas A, Otte T, Multhaup G, Mendel RR, Schwarz G (2006) The Mechanism of nucleotide-assisted molybdenum insertion into molybdopterin. A novel route toward metal cofactor assembly. J Biol Chem 281:18343–18350

    Article  CAS  PubMed  Google Scholar 

  • Magalon A, Mendel RR. Chapter 3.6.3.13, Biosynthesis and Insertion of the Molybdenum Cofactor. In: Böck A, Curtiss III R, Kaper JB, Karp PD, Neidhardt FC, Nyström T, Slauch JM, Squires CL (eds) EcoSal–Escherichia coli and Salmonella: cellular and molecular biology. http://www.ecosal.org. ASM Press, Washington, D.C.

  • Massey V, Edmondson DE (1970) On the mechansim of inactivation of xanthine oxidase by cyanide. J Biol Chem 245:6595–6598

    CAS  PubMed  Google Scholar 

  • Matthies A, Rajagopalan KV, Mendel RR, Leimkuhler 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

    Article  CAS  PubMed  Google Scholar 

  • Matthies A, Nimtz M, Leimkuhler S (2005) Molybdenum cofactor biosynthesis in humans: identification of a persulfide group in the rhodanese-like domain of MOCS3 by mass spectrometry. Biochemistry 44:7912–7920

    Article  CAS  PubMed  Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414

    Article  CAS  PubMed  Google Scholar 

  • Mendel RR (2009) Cell biology of molybdenum. BioFactors 35:429–434

    Article  CAS  PubMed  Google Scholar 

  • Mendel RR, Müller AJ (1976) A common genetic determinant of xanthine dehydrogenase and nitrate reductase in Nicotiana tabacum. Biochem Physiol Pflanzen 170:538–541

    CAS  Google Scholar 

  • Mendel RR (1992) The plant molybdenum cofactor (MoCo) – its biochemical and molecular genetics. In: Gresshoff PM (ed) Plant biotechnology and development – current topics in plant molecular biology, 1st edn. CRC Press, Boca Raton, pp 11–16

    Google Scholar 

  • Mendel RR, Schwarz G (2002) Biosynthesis and molecular biology of the molybdenum cofactor (Moco). Met Ions Biol Syst 39:317–368

    CAS  PubMed  Google Scholar 

  • Mercer JF (2001) The molecular basis of copper-transport diseases. Trends Mol Med 7:64–69

    Article  CAS  PubMed  Google Scholar 

  • Millar LJ, Heck IS, Sloan J, Kana’n GJ, Kinghorn JR, Unkles SE (2001) Deletion of the cnxE gene encoding the gephyrin-like protein involved in the final stages of molybdenum cofactor biosynthesis in Aspergillus nidulans. Mol Genet Genomics 266:445–453

    Article  CAS  PubMed  Google Scholar 

  • Montalbini P (1992) Inhibition of hypersensitive response by allopurinol applied to the host in the incompatible relationship between Phaseolus vulgaris and Uromyces phaseoli. J Phytopathol 134:218–228

    Article  CAS  Google Scholar 

  • Montalbini P, Della Torre G (1996) Evidence of a two-fold mechanism responsible for the inhibition by allopurinol of the hypersensitive reponse induced in tobacco by tobacco necrosis virus. Phys Mol Plant Pathol 48:273–287

    Article  CAS  Google Scholar 

  • Montalbini P (1998) Purification and some properties of xanthine dehydrogenase from wheat leaves. Plant Sci 134:89–102

    Article  CAS  Google Scholar 

  • Montalbini P (2000) Xanthine dehydrogenase from leaves of leguminous plants: purification, characterization and properties of the enzyme. J Plant Phys 156:3–16

    CAS  Google Scholar 

  • Moorhead GB, Meek SE, Douglas P, Bridges D, Smith CS, Morrice N, MacKintosh C (2003) Purification of a plant nucleotide pyrophosphatase as a protein that interferes with nitrate reductase and glutamine synthetase assays. Eur J Biochem 270:1356–1362

    Article  CAS  PubMed  Google Scholar 

  • Müller AJ, Mendel RR (1989) Biochemical and somatic cell genetics of nitrate reductase in Nicotiana. In: Wray JL, Kinghorn JR (eds) Molecular and genetic aspects of nitrate assimilation. Oxford University Press, Oxford, pp 166–185

    Google Scholar 

  • Nishino T, Nishino T (1997) The conversion from the dehydrogenase type to the oxidase type of rat liver xanthine dehydrogenase by modification of cysteine residues with fluorodinitrobenzene. J Biol Chem 272:29859–29864

    Article  CAS  PubMed  Google Scholar 

  • Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 37:113–116

    CAS  Google Scholar 

  • Nowak K, Luniak N, Witt C, Wustefeld Y, Wachter A, Mendel RR, Hansch R (2004) Peroxisomal localization of sulfite oxidase separates it from chloroplast-based sulfur assimilation. Plant Cell Physiol 45:1889–1894

    Article  CAS  PubMed  Google Scholar 

  • Nussaume L, Vincentz M, Meyer C, Boutin JP, Caboche M (1995) Post-transcriptional regulation of nitrate reductase by light is abolished by an N-terminal deletion. Plant Cell 7:611–621

    Article  CAS  PubMed  Google Scholar 

  • Pateman JA, Cove DJ, Rever BM, Roberts DB (1964) A common cofactor for nitrate reductase and xanthine dehydrogenase which also regulates the synthesis of nitrate reductase. Nature 201:58–60

    Article  CAS  PubMed  Google Scholar 

  • Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Met Ions Biol Syst 39:3–74

    Google Scholar 

  • Perez-Vicente R, Alamillo JM, Cardenas J, Pineda M (1992) Purification and substrate inactivation of xanthine dehydrogenase from Chlamydomonas reinhardtii. Biochim Biophys Acta 1117:159–166

    CAS  PubMed  Google Scholar 

  • Raab S, Drechsel G, Zarepour M, Hartung W, Koshiba T, Bittner F, Hoth S (2009) Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J 59:39–51

    Article  CAS  PubMed  Google Scholar 

  • Rajagopalan KV, Johnson JL (1992) The pterin molybdenum cofactors. J Biol Chem 267:10199–10202

    CAS  PubMed  Google Scholar 

  • Rajagopalan KV (1996) Biosynthesis of the molybdenum cofactor. In: Neidhardt FC (ed) Escherichia coli and Salmonella typhimurium. ASM Press, Washington, DC, pp 674–679

    Google Scholar 

  • Rees DC, Akif Tezcan F, Haynes CA, Walton MY, Andrade S, Einsle O, Howard JB (2005) Structural basis of biological nitrogen fixation. Philos Transact A Math Phys Eng Sci 363:971–984 discussion 1035-1040

    Article  CAS  PubMed  Google Scholar 

  • Reiss J, Cohen N, Dorche C, Mandel H, Mendel RR, Stallmeyer B, Zabot MT, Dierks T (1998) Mutations in a polycistronic nuclear gene associated with molybdenum cofactor deficiency. Nat Genet 20:51–53

    Article  CAS  PubMed  Google Scholar 

  • Reiss J, Johnson JL (2003) Mutations in the molybdenum cofactor biosynthetic genes MOCS1, MOCS2, and GEPH. Hum Mutat 21:569–576

    Article  CAS  PubMed  Google Scholar 

  • Rieder C, Eisenreich W, O’Brien J, Richter G, Götze E, Boyle P, Blanchard S, Bacher A, Simon H (1998) Rearrangement reactions in the biosynthesis of molybdopterin – an NMR study with multiply 13C/15N labelled precursors. Eur J Biochem 255:24–36

    Article  CAS  PubMed  Google Scholar 

  • Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Trelles F, Tarrio R, Ayala FJ (2003) Convergent neofunctionalization by positive Darwinian selection after ancient recurrent duplications of the xanthine dehydrogenase gene. Proc Natl Acad Sci USA 100:13413–13417

    Article  CAS  PubMed  Google Scholar 

  • Sagi M, Scazzocchio C, Fluhr R (2002) The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J 31:305–317

    Article  CAS  PubMed  Google Scholar 

  • Sandalio LM, Fernandez VM, Ruperez FL, del Rio LA (1988) Superoxide free radicals are produced in glyoxysomes. Plant Physiol 127:1–4

    Article  Google Scholar 

  • Santamaria-Araujo JA, Fischer B, Otte T, Nimtz M, Mendel RR, Wray V, Schwarz G (2004) The tetrahydropyranopterin structure of the sulfur-free and metal-free molybdenum cofactor precursor. J Biol Chem 279:15994–15999

    Article  CAS  PubMed  Google Scholar 

  • Sauer P, Frebortova J, Sebela M, Galuszka P, Jacobsen S, Pec P, Frebort I (2002) Xanthine dehydrogenase of pea seedlings: a member of the plant molybdenum oxidoreductase family. Plant Physiol Biochem 40:393–400

    Article  CAS  Google Scholar 

  • Schrader N, Kim EY, Winking J, Paulukat J, Schindelin H, Schwarz G (2004) Biochemical characterization of the high affinity binding between the glycine receptor and gephyrin. J Biol Chem 279:18733–18741

    Article  CAS  PubMed  Google Scholar 

  • Schwarz G, Boxer DH, Mendel RR (1997a) Molybdenum cofactor biosynthesis. The plant protein Cnx1 binds molybdopterin with high affinity. J Biol Chem 272:26811–26814

    Article  CAS  PubMed  Google Scholar 

  • Schwarz G, Boxer DH, Mendel RR (1997b) The plant protein Cnx1 binds molybdopterin and is involved in the last step of molybdenum cofactor biosynthesis. In: Pfleiderer W, Rokos H (eds) Chemistry and biology of pteridines and folates. Blackwell Science, Berlin, pp 697–702

    Google Scholar 

  • Schwarz G, Schulze J, Bittner F, Eilers T, Kuper J, Bollmann G, Nerlich A, Brinkmann H, Mendel RR (2000) The molybdenum cofactor biosynthetic protein Cnx1 complements molybdate-repairable mutants, transfers molybdenum to the metal binding pterin, and is associated with the cytoskeleton. Plant Cell 12:2455–2472

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Koiwai H, Akaba S, Komano T, Oritani T, Kamiya Y, Koshiba T (2000a) Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. Plant J 23:481–488

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Peeters AJ, Koiwai H, Oritani T, Marion-Poll A, Zeevaart JA, Koornneef M, Kamiya Y, Koshiba T (2000b) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Acad Sci USA 97:12908–12913

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Koshiba T (2002) The complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48

    Article  CAS  PubMed  Google Scholar 

  • Sigel A, Sigel H (2002) Molybdenum and tungsten. Their roles in biological processes. Marcel Dekker, New York

    Google Scholar 

  • Skipper L, Campbell WH, Mertens JA, Lowe DJ (2001) Pre-steady-state kinetic analysis of recombinant Arabidopsis NADH:nitrate reductase: rate-limiting processes in catalysis. J Biol Chem 276:26995–27002

    Article  CAS  PubMed  Google Scholar 

  • Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, 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 29:1097–1106

    Article  CAS  PubMed  Google Scholar 

  • Stallmeyer B, Drugeon G, Reiss J, Haenni AL, Mendel RR (1999a) Human molybdopterin synthase gene: identification of a bicistronic transcript with overlapping reading frames. Am J Hum Genet 64:698–705

    Article  CAS  PubMed  Google Scholar 

  • Stallmeyer B, Schwarz G, Schulze J, Nerlich A, Reiss J, Kirsch J, Mendel RR (1999b) The neurotransmitter receptor-anchoring protein gephyrin reconstitutes molybdenum cofactor biosynthesis in bacteria, plants, and mammalian cells. Proc Natl Acad Sci USA 96:1333–1338

    Article  CAS  PubMed  Google Scholar 

  • Stiefel EI (2002) The biogeochemistry of molybdenum and tungsten. Met Ions Biol Syst 39:1–29

    CAS  PubMed  Google Scholar 

  • Tejada-Jimenez M, Llamas A, Sanz-Luque E, Galvan A, Fernandez E (2007) A high-affinity molybdate transporter in eukaryotes. Proc Natl Acad Sci USA 104:20126–20130

    Article  CAS  PubMed  Google Scholar 

  • Terao M, Kurosaki M, Marini M, Vanoni MA, Saltini G, Bonetto V, Bastone A, Federico C, Saccone S, Fanelli R, Salmona M, Garattini E (2001) Purification of the aldehyde oxidase homolog 1 (AOH1) protein and cloning of the AOH1 and aldehyde oxidase homolog 2 (AOH2) genes. Identification of a novel molybdo-flavoprotein gene cluster on mouse chromosome 1. J Biol Chem 276:46347–46363

    Article  CAS  PubMed  Google Scholar 

  • Teschner J, Lachmann N, Geisler M, Selbach K, Balk J, Mendel RR, Bittner F (2009) A novel role for the mitochondrial ABC transporter ATM3 from Arabidopsis in molybdenum cofactor biosynthesis. Plant Cell (under revision)

    Google Scholar 

  • Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci USA 104:18807–18812

    Article  CAS  PubMed  Google Scholar 

  • Turnlund JR (2002) Molybdenum metabolism and requirements in humans. Met Ions Biol Syst 39:727–739

    CAS  PubMed  Google Scholar 

  • Verslues PE, Zhu JK (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379

    Article  CAS  PubMed  Google Scholar 

  • Wahl RC, Rajagopalan KV (1982) Evidence for the inorganic nature of the cyanolyzable sulfur of molybdenum hydroxylases. J Biol Chem 257:1354–1359

    CAS  PubMed  Google Scholar 

  • Warner CK, Finnerty V (1981) Molybdenum hydroxylases in Drosophila. II Molybdenum cofactor in xanthine dehydrogenase, aldehyde oxidase and pyridoxal oxidase. Mol Gen Genet 184:92–96

    Article  CAS  PubMed  Google Scholar 

  • Witte CP, Igeno MI, Mendel RR, Schwarz G, Fernandez E (1998) The Chlamydomonas reinhardtii MoCo carrier protein is multimeric and stabilizes molybdopterin cofactor in a molybdate charged form. FEBS Lett 431:205–209

    Article  CAS  PubMed  Google Scholar 

  • Wollers S, Heidenreich T, Zarepour M, Zachmann D, Kraft C, Zhao Y, Mendel RR, Bittner F (2008) Binding of sulfurated molybdenum cofactor to the C-terminal domain of ABA3 from Arabidopsis thaliana provides insight into the mechanism of molybdenum cofactor sulfuration. J Biol Chem 283:9642–9650

    Article  CAS  PubMed  Google Scholar 

  • Wuebbens MM, Rajagopalan KV (1993) Structural characterization of a molybdopterin precursor. J Biol Chem 268:13493–13498

    CAS  PubMed  Google Scholar 

  • Wuebbens MM, Rajagopalan KV (1995) Investigation of the early steps of molybdopterin biosynthesis in Escherichia coli through the use of in vivo labeling studies. J Biol Chem 270:1082–1087

    Article  CAS  PubMed  Google Scholar 

  • Wuebbens MM, Rajagopalan KV (2003) Mechanistic and mutational studies of Escherichia coli molybdopterin synthase clarify the final step of molybdopterin biosynthesis. J Biol Chem 278:14523–14532

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Ishitani M, Lee H, 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 13:2063–2083

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92

    Article  CAS  PubMed  Google Scholar 

  • Yesbergenova Z, Yang G, Oron E, Soffer D, Fluhr R, Sagi M (2005) The plant Mo-hydroxylases aldehyde oxidase and xanthine dehydrogenase have distinct reactive oxygen species signatures and are induced by drought and abscisic acid. Plant J 42:862–876

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Gladyshev VN (2008) Molybdoproteomes and evolution of molybdenum utilization. J Mol Biol 379:881–899

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the many people who worked with us over the years on molybdenum. In particular we are grateful to Dr. Robert Hänsch for critical discussions. The research was consistenly supported by the Deutsche Forschungsgemeinschaft (R.R.M., F.B.) which is gratefully acknowledged. Financial support came also from the European Union (R.R.M.) and the Fonds der Chemischen Industrie (R.R.M.).

Author information

Authors and Affiliations

  1. Department of Plant Biology, Technical University of Braunschweig, Humboldtstrasse 1, 38106, Braunschweig, Germany

    Florian Bittner & Ralf-Rainer Mendel

Authors
  1. Florian Bittner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ralf-Rainer Mendel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ralf-Rainer Mendel .

Editor information

Editors and Affiliations

  1. Fak. Biowissenschaften, Universität Heidelberg, Im Neuenheimer Feld 360, Heidelberg, 69120, Germany

    Rüdiger Hell

  2. Botanisches Institut, TU Braunschweig, Humboldtstr. 1, Braunschweig, 38106, Germany

    Ralf-Rainer Mendel

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bittner, F., Mendel, RR. (2010). Cell Biology of Molybdenum. In: Hell, R., Mendel, RR. (eds) Cell Biology of Metals and Nutrients. Plant Cell Monographs, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10613-2_6

Download citation

Publish with us

Policies and ethics

Search

Navigation