Cell biology of molybdenum in plants

Plant Cell Reports

Volumn 30, Issue 10, 2011, Pages 1787-1797

  Mendel, Ralf R ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Aldehyde oxidase; Molybdenum cofactor; Molybdenum cofactor deficiency; Nitrate reductase; Sulfite oxidase; Xanthine dehydrogenase

Indexed keywords

ALDEHYDE OXIDASE; METALLOPROTEIN; MITOCHONDRIAL PROTEIN; MOLYBDENUM; MOLYBDENUM COFACTOR; NITRATE REDUCTASE; PTERIDINE DERIVATIVE; SULFITE OXIDASE; XANTHINE DEHYDROGENASE;

COENZYME; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; PLANT; REVIEW;

ALDEHYDE OXIDASE; COENZYMES; METALLOPROTEINS; MITOCHONDRIAL PROTEINS; MOLYBDENUM; NITRATE REDUCTASE; PLANTS; PTERIDINES; SULFITE OXIDASE; XANTHINE DEHYDROGENASE;

BACTERIA (MICROORGANISMS);

EID: 80052724734     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-011-1100-4     Document Type: Review

References (81)

1. 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 (Tokyo) 126: 395-401.
2. Arnon DI, Stout PR (1939) Molybdenum as an essential element for higher plants. Plant Physiol 14: 599-602.
3. 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.
4. Bernard DG, Cheng Y, Zhao Y, Balk J (2009) An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol 151: 590-602.
5. Bittner F, Mendel RR (2010) Cell biology of molybdenum. Plant Cell Monogr 17: 119-146.
6. 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.
7. Bortels H (1930) Molybdän als Katalysator bei der biologischen Stickstoffbindung. Arch Mikrobiol 1: 333-342.
8. 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.
9. Carter C, Pan S, Zouhar J, Avila EL, Girke T, Raikhel NV (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16: 3285-3303.
10. 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.
11. Cove DJ, Pateman JA (1963) Independently segregating genetic loci concerned with nitrate reductase activity in Aspergillus nidulans. Nature 198: 262-263.
12. 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.
13. 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.
14. Fido RJ, Gundry CS, Hewitt EJ, Notton BA (1977) Ultrastructural features of molybdenum deficiency and whiptail in cauliflower leaves: effects of nitrogen source and tungsten substitution for molybdenum. Aust J Plant Physiol 4: 675-689.
15. 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.
16. Fitzpatrick KL, Tyerman SD, Kaiser BN (2008) Molybdate transport through the plant sulfate transporter SHST1. FEBS Lett 582: 1508-1513.
17. 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.
18. Gasber A, Klaumann A, Trentmann O, Trampczynska A, Clemens S, Schneider S, Sauer N, Feifer I, Bittner F, Mendel RR, Neuhaus HE (2011) Identification of an Arabidopsis solute carrier critical for intracellular transport and interorgan allocation of molybdate. Plant Biol (in press).
19. 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.
20. 2: combination of enzyme catalysis with a subsequent non-enzymatic reaction step. J Biol Chem 281: 6884-6888.
21. Hänsch R, Lang C, Rennenberg H, Mendel RR (2007) Significance of plant sulfite oxidase. Plant Biol 9: 589-595.
22. 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.
23. 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.
24. 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.
25. Hille R (2002) Molybdenum enzymes containing the pyranopterin cofactor: an overview. Met Ions Biol Syst 39: 187-226.
26. Hille R (2005) Molybdenum-containing hydroxylases. Arch Biochem Biophys 433: 107-116.
27. Hille R, Nishino T, Bittner F (2011) Molybdenum enzymes in higher organisms. Coord Chem Rev 255: 1179-1205.
28. Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52: 1981-1989.
29. Kaiser BN, Gridley KL, Brady JN, Phillips T, Tyerman SD (2005) The role of molybdenum in agricultural plant production. Ann Bot 96: 745-754.
30. 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.
31. Kisker C, Schindelin H, Rees DC (1997b) Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 66: 233-267.
32. Kruse T, Gehl C, Geisler M, Lehrke M, Ringel P, Hallier S, Hansch R, Mendel RR (2010) Identification and biochemical characterization of molybdenum cofactor-binding proteins from Arabidopsis thaliana. J Biol Chem 285: 6623-6635.
33. Kuper J, Llamas A, Hecht HJ, Mendel RR, Schwarz G (2004) Structure of molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430: 803-806.
34. Lang C, Popko J, Wirtz M, Hell R, Herschbach C, Kreuzwieser J, Rennenberg H, Mendel RR, Hansch R (2007) Sulphite oxidase as key enzyme for protecting plants against sulphur dioxide. Plant Cell Environ 30: 447-455.
35. Leimkuhler S, Wuebbens MM, Rajagopalan KV (2011) The history of the discovery of the molybdenum cofactor and novel aspects of its biosynthesis in bacteria. Coord Chem Rev 255: 1129-1144.
36. Leon-Klooserziel 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 tow new loci. Plant J 10: 655-661.
37. Magalon A, Fedor JG, Walburger A, Weiner JH (2011) Molybdenum enzymes in bacteria and their maturation. Coord Chem Rev 255: 1159-1178.
38. 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. CRC Press, Boca Raton, pp 11-16.
39. Mendel RR, Müller AJ (1976) A common genetic determinant of xanthine dehydrogenase and nitrate reductase in Nicotiana tabacum. Biochem Physiol Pflanzen 170: 538-541.
40. Mendel RR, Schwarz G (2002) Biosynthesis and molecular biology of the molybdenum cofactor (Moco). Met Ions Biol Syst 39: 317-368.
41. Mendel RR, Schwarz G (2011) Molybdenum cofactor biosynthesis in plants and humans. Coord Chem Rev 255: 1145-1158.
42. Mendel RR, Alikulov ZA, Lvov NP, Müller AJ (1981) Presence of the molybdenum-cofactor in nitrate reductase-deficient mutant cell lines of Nicotiana tabacum. Mol Gen Genet 181: 395-399.
43. Mengel K, Kirkby EA (2001) Principles of plant nutrition. Springer, Berlin.
44. 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.
45. Montalbini P (1992a) 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.
46. Montalbini P (1992b) Ureides and enzymes of ureide synthesis in wheat seeds and leaves and effect of allopurinol on Puccinia recondita f. sp. tritici infection. Plant Sci 87: 225-231.
47. Montalbini P, Della Torre G (1996) Evidence of a two-fold mechanism responsible for the inhibition by allopurinol of the hypersensitive response induced in tobacco by tobacco necrosis virus. Phys Mol Plant Pathol 48: 273-287.
48. 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.
49. 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.
50. Pastori GM, Rio LA (1997) Natural senescence of pea leaves: an activated oxygen-mediated function for peroxisomes. Plant Physiol 113: 412-418.
51. Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Met Ions Biol Syst 39: 39-74.
52. 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.
53. Rajagopalan KV (1996) Biosynthesis of the molybdenum cofactor. In: Neidhardt FC (ed) Escherichia coli and Salmonella typhimurium. ASM Press, Washington, DC, pp 674-679.
54. Reiss J, Johnson JL (2003) Mutations in the molybdenum cofactor biosynthetic genes MOCS1, MOCS2, and GEPH. Hum Mutat 21: 569-576.
55. 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.
56. 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.
57. Sandalio LM, Fernandez VM, Ruperez FL, del Rio LA (1988) Superoxide free radicals are produced in glyoxysomes. Plant Physiol 127: 1-4.
58. Schrader N, Fischer K, Theis K, Mendel RR, Schwarz G, Kisker C (2003) The crystal structure of plant sulfite oxidase provides insights into sulfite oxidation in plants and animals. Structure 11: 1251-1263.
59. Schwarz G, Mendel RR (2006) Molybdenum cofactor biosynthesis and molybdenum enzymes. Annu Rev Plant Biol 57: 623-647.
60. Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460: 839-847.
61. Seo M, Koshiba T (2002) The complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7: 41-48.
62. 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.
63. 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.
64. Silvestri S, Murphy AM, Buonaurio R, Carr JP (2008) Allopurinol, an inhibitor of purine catabolism, enhances susceptibility of tobacco to Tobacco mosaic virus. Virus Res 137: 257-260.
65. 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.
66. 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.
67. 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.
68. Tejada-Jimenez M, Galvan A, Fernandez E (2011) Algae and humans share a molybdate transporter. Proc Natl Acad Sci USA 108: 6420-6425.
69. 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.
70. Teschner J, Lachmann N, Schulze J, Geisler M, Selbach K, Santamaria-Araujo J, Balk J, Mendel RR, Bittner F (2010) A novel role for Arabidopsis mitochondrial ABC transporter ATM3 in molybdenum cofactor biosynthesis. Plant Cell 22: 468-480.
71. 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.
72. Turnlund JR (2002) Molybdenum metabolism and requirements in humans. Met Ions Biol Syst 39: 727-739.
73. 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.
74. Wahl B, Reichmann D, Niks D, Krompholz N, Havemeyer A, Clement B, Meßerschmidt T, Rothkegel M, Biester H, Hille R, Mendel RR, Bittner F (2010) Biochemical and spectroscopic characterization of the human mitochondrial amidoxime reducing components hmARC-1 and hmARC-2 suggests the existence of a new molybdenum-enzyme family in eukaryotes. J Biol Chem 285: 37847-37859.
75. Wang P, Du Y, Song CP (2011) Phosphorylation by MPK6: a conserved transcriptional modification mediates nitrate reductase activation and NO production? Plant Signal Behav (in press).
76. 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.
77. 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.
78. 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.
79. 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.
80. Zarepour M, Kaspari K, Stagge S, Retmeiere R, Mendel RR, Bittner F (2010) Xanthine dehydrogenase AtXDH1 from Arabidopsis thaliana is a potent producer of superoxide anions via its NADH oxidase activity. Plant Mol Biol 72: 301-310.
81. Zhang Y, Gladyshev VN (2008) Molybdoproteomes and evolution of molybdenum utilization. J Mol Biol 379: 881-899.