Catalytic strategies of the non-heme iron dependent oxygenases and their roles in plant biology

Current Opinion in Chemical Biology

Volumn 31, Issue , 2016, Pages 126-135

  White, Mark D ^a   Flashman, Emily ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYETHYLPHOSPHONATE DIOXYGENASE; 2 OXOGLUTARATE DEPENDENT OXYGENASE; ACIDOREDUCTONE DIOXYGENASE; CAROTENOID CLEAVAGE DIOXYGENASE; CATECHOL DIOXYGENASE; CYSTEINE DIOXYGENASE; HERBICIDE; IRON; LACTONE DERIVATIVE; MORPHINE; O DEMETHYLASE; OXYGEN; OXYGENASE; RIESKE DIOXYGENASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; HEME;

ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; GENETIC MANIPULATION; NONHUMAN; PLANT BIOTECHNOLOGY; REVIEW; SECONDARY METABOLISM; SIGNAL TRANSDUCTION; STRESS; CATALYSIS; METABOLISM; METHYLATION; PLANT PHYSIOLOGY;

CATALYSIS; HEME; METHYLATION; OXYGENASES; PLANT PHYSIOLOGICAL PHENOMENA;

EID: 84962621689     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2016.02.017     Document Type: Review

References (67)

1. Koehntop K.D., Emerson J.P., Que L. The 2-His-1-carboxylate facial triad: a versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymes. J Biol Inorg Chem 2005, 10:87-93.
2. Krebs C., Galonic Fujimori D., Walsh C.T., Bollinger J.M. Non-heme Fe(IV)-oxo intermediates. Acc Chem Res 2007, 40:484-492.
3. Eser B.E., Barr E.W., Frantom P.A., Saleh L., Bollinger J.M., Krebs C., Fitzpatrick P.F. Direct spectroscopic evidence for a high-spin Fe(IV) intermediate in tyrosine hydroxylase. J Am Chem Soc 2007, 129:11334-11335.
4. Panay A.J., Lee M., Krebs C., Bollinger J.M., Fitzpatrick P.F. Evidence for a high-spin Fe(IV) species in the catalytic cycle of a bacterial phenylalanine hydroxylase. Biochemistry 2011, 50:1928-1933.
5. Bugg T.D., Ramaswamy S. Non-heme iron-dependent dioxygenases: unravelling catalytic mechanisms for complex enzymatic oxidations. Curr Opin Chem Biol 2008, 12:134-140.
6. Fielding A.J., Lipscomb J.D., Que L. A two-electron-shell game: intermediates of the extradiol-cleaving catechol dioxygenases. J Biol Inorg Chem 2014, 19:491-504.
7. 2+ dioxygenase superoxo, alkylperoxo, and bound product intermediates. Science 2007, 316:453-457.
8. Jeoung J.H., Bommer M., Lin T.Y., Dobbek H. Visualizing the substrate-, superoxo-, alkylperoxo-, and product-bound states at the nonheme Fe(II) site of homogentisate dioxygenase. Proc Natl Acad Sci U S A 2013, 110:12625-12630.
9. Knoot C.J., Purpero V.M., Lipscomb J.D. Crystal structures of alkylperoxo and anhydride intermediates in an intradiol ring-cleaving dioxygenase. Proc Natl Acad Sci U S A 2015, 112:388-393.
10. Barry S.M., Challis G.L. Mechanism and catalytic diversity of rieske non-heme iron-dependent oxygenases. ACS Catal 2013, 3.
11. Karlsson A., Parales J.V., Parales R.E., Gibson D.T., Eklund H., Ramaswamy S. Crystal structure of naphthalene dioxygenase: side-on binding of dioxygen to iron. Science 2003, 299:1039-1042.
12. Rivard B.S., Rogers M.S., Marell D.J., Neibergall M.B., Chakrabarty S., Cramer C.J., Lipscomb J.D. Rate-determining attack on substrate precedes rieske cluster oxidation during cis-dihydroxylation by benzoate dioxygenase. Biochemistry 2015, 54:4652-4664.
13. Joseph C.A., Maroney M.J. Cysteine dioxygenase: structure and mechanism. Chem Commun 2007, 3338-3349.
14. Crawford J.A., Li W., Pierce B.S. Single turnover of substrate-bound ferric cysteine dioxygenase with superoxide anion: enzymatic reactivation, product formation, and a transient intermediate. Biochemistry 2011, 50:10241-10253.
15. van der Donk W.A., Krebs C., Bollinger J.M. Substrate activation by iron superoxo intermediates. Curr Opin Struct Biol 2010, 20:673-683.
16. Zhu H., Peck S.C., Bonnot F., van der Donk W.A., Klinman J.P. Oxygen-18 kinetic isotope effects of nonheme iron enzymes HEPD and MPnS support iron(III) superoxide as the hydrogen abstraction species. J Am Chem Soc 2015.
17. Al-Babili S., Bouwmeester H.J. Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 2015, 66:161-186.
18. Alder A., Jamil M., Marzorati M., Bruno M., Vermathen M., Bigler P., Ghisla S., Bouwmeester H., Beyer P., Al-Babili S. The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 2012, 335:1348-1351.
19. Schwartz S.H., Tan B.C., Gage D.A., Zeevaart J.A., McCarty D.R. Specific oxidative cleavage of carotenoids by VP14 of maize. Science 1997, 276:1872-1874.
20. Frusciante S., Diretto G., Bruno M., Ferrante P., Pietrella M., Prado-Cabrero A., Rubio-Moraga A., Beyer P., Gomez-Gomez L., Al-Babili S., et al. Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc Natl Acad Sci U S A 2014, 111:12246-12251.
21. Bruno M., Beyer P., Al-Babili S. The potato carotenoid cleavage dioxygenase 4 catalyzes a single cleavage of beta-ionone ring-containing carotenes and non-epoxidated xanthophylls. Arch Biochem Biophys 2015, 572:126-133.
22. Ilg A., Bruno M., Beyer P., Al-Babili S. Tomato carotenoid cleavage dioxygenases 1A and 1B: Relaxed double bond specificity leads to a plenitude of dialdehydes, mono-apocarotenoids and isoprenoid volatiles. FEBS Open Bio 2014, 4:584-593.
23. Messing S.A., Gabelli S.B., Echeverria I., Vogel J.T., Guan J.C., Tan B.C., Klee H.J., McCarty D.R., Amzel L.M. Structural insights into maize viviparous14, a key enzyme in the biosynthesis of the phytohormone abscisic acid. Plant Cell 2010, 22:2970-2980.
24. Schmidt H., Kurtzer R., Eisenreich W., Schwab W. The carotenase AtCCD1 from Arabidopsis thaliana is a dioxygenase. J Biol Chem 2006, 281:9845-9851.
25. Sui X., Golczak M., Zhang J., Kleinberg K.A., von Lintig J., Palczewski K., Kiser P.D. Utilization of dioxygen by carotenoid cleavage oxygenases. J Biol Chem 2015.
26. Harrison P.J., Bugg T.D. Enzymology of the carotenoid cleavage dioxygenases: reaction mechanisms, inhibition and biochemical roles. Arch Biochem Biophys 2014, 544:105-111.
27. Harrison P.J., Newgas S.A., Descombes F., Shepherd S.A., Thompson A.J., Bugg T.D. Biochemical characterization and selective inhibition of beta-carotene cis-trans isomerase D27 and carotenoid cleavage dioxygenase CCD8 on the strigolactone biosynthetic pathway. FEBS J 2015.
28. Farrow S.C., Facchini P.J. Functional diversity of 2-oxoglutarate/Fe(II)-dependent dioxygenases in plant metabolism. Front Plant Sci 2014, 5:524.
29. Yamaguchi S. Gibberellin metabolism and its regulation. Annu Rev Plant Biol 2008, 59:225-251.
30. Sasaki A., Ashikari M., Ueguchi-Tanaka M., Itoh H., Nishimura A., Swapan D., Ishiyama K., Saito T., Kobayashi M., Khush G.S., et al. Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 2002, 416:701-702.
31. Thomas S.G., Phillips A.L., Hedden P. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci U S A 1999, 96:4698-4703.
32. Barboza L., Effgen S., Alonso-Blanco C., Kooke R., Keurentjes J.J., Koornneef M., Alcazar R. Arabidopsis semidwarfs evolved from independent mutations in GA20ox1, ortholog to green revolution dwarf alleles in rice and barley. Proc Natl Acad Sci U S A 2013, 110:15818-15823.
33. Jia Q., Zhang J., Westcott S., Zhang X.Q., Bellgard M., Lance R., Li C. GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley. Funct Integr Genomics 2009, 9:255-262.
34. Rose N.R., McDonough M.A., King O.N., Kawamura A., Schofield C.J. Inhibition of 2-oxoglutarate dependent oxygenases. Chem Soc Rev 2011, 40:4364-4397.
35. Rose N.R., Woon E.C., Tumber A., Walport L.J., Chowdhury R., Li X.S., King O.N., Lejeune C., Ng S.S., Krojer T., et al. Plant growth regulator daminozide is a selective inhibitor of human KDM2/7 histone demethylases. J Med Chem 2012, 55:6639-6643.
36. Zhou R., Yu M., Pharis R.P. 16,17-Dihydro gibberellin A5 competitively inhibits a recombinant Arabidopsis GA 3beta-hydroxylase encoded by the GA4 gene. Plant Physiol 2004, 135:1000-1007.
37. Thinnes C.C., England K.S., Kawamura A., Chowdhury R., Schofield C.J., Hopkinson R.J. Targeting histone lysine demethylases - progress, challenges, and the future. Biochim Biophys Acta 2014, 1839:1416-1432.
38. Cho J.N., Ryu J.Y., Jeong Y.M., Park J., Song J.J., Amasino R.M., Noh B., Noh Y.S. Control of seed germination by light-induced histone arginine demethylation activity. Dev Cell 2012, 22:736-748.
39. Chen Q., Chen X., Wang Q., Zhang F., Lou Z., Zhang Q., Zhou D.X. Structural basis of a histone H3 lysine 4 demethylase required for stem elongation in rice. PLoS Genet 2013, 9:e1003239.
40. Hagel J.M., Facchini P.J. Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat Chem Biol 2010, 6:273-275.
41. Farrow S.C., Facchini P.J. Dioxygenases catalyze O-demethylation and O, O-demethylenation with widespread roles in benzylisoquinoline alkaloid metabolism in opium poppy. J Biol Chem 2013, 288:28997-29012.
42. Berim A., Kim M.J., Gang D.R. Identification of a unique 2-oxoglutarate-dependent flavone 7-O-demethylase completes the elucidation of the lipophilic flavone network in basil. Plant Cell Physiol 2015, 56:126-136.
43. Runguphan W., Glenn W.S., O'Connor S.E. Redesign of a dioxygenase in morphine biosynthesis. Chem Biol 2012, 19:674-678.
44. Zhang Z., Ren J.S., Clifton I.J., Schofield C.J. Crystal structure and mechanistic implications of 1-aminocyclopropane-1-carboxylic acid oxidase - the ethylene-forming enzyme. Chem Biol 2004, 11:1383-1394.
45. 2 activation by the ethylene-forming enzyme 1-aminocyclopropane-1-carboxylic acid oxidase. Proc Natl Acad Sci U S A 2008, 105:1814-1819.
46. Murphy L.J., Robertson K.N., Harroun S.G., Brosseau C.L., Werner-Zwanziger U., Moilanen J., Tuononen H.M., Clyburne J.A. A simple complex on the verge of breakdown: isolation of the elusive cyanoformate ion. Science 2014, 344:75-78.
47. Brisson L., El Bakkali-Taheri N., Giorgi M., Fadel A., Kaizer J., Reglier M., Tron T., Ajandouz el H., Simaan A.J. 1-Aminocyclopropane-1-carboxylic acid oxidase: insight into cofactor binding from experimental and theoretical studies. J Biol Inorg Chem 2012, 17:939-949.
48. Borowski T., Bassan A., Siegbahn P.E. 4-Hydroxyphenylpyruvate dioxygenase: a hybrid density functional study of the catalytic reaction mechanism. Biochemistry 2004, 43:12331-12342.
49. Moran G.R. 4-Hydroxyphenylpyruvate dioxygenase and hydroxymandelate synthase: exemplars of the alpha-keto acid dependent oxygenases. Arch Biochem Biophys 2014, 544:58-68.
50. He P., Moran G.R. Structural and mechanistic comparisons of the metal-binding members of the vicinal oxygen chelate (VOC) superfamily. J Inorg Biochem 2011, 105:1259-1272.
51. Heap I. The International Survey of Herbicide Resistant Weeds 2015.
52. Siehl D.L., Tao Y., Albert H., Dong Y., Heckert M., Madrigal A., Lincoln-Cabatu B., Lu J., Fenwick T., Bermudez E., et al. Broad 4-hydroxyphenylpyruvate dioxygenase inhibitor herbicide tolerance in soybean with an optimized enzyme and expression cassette. Plant Physiol 2014, 166:1162-1176.
53. Ahrens H., Lange G., Muller T., Rosinger C., Willms L., van Almsick A. 4-Hydroxyphenylpyruvate dioxygenase inhibitors in combination with safeners: solutions for modern and sustainable agriculture. Angew Chem Int Ed Engl 2013, 52:9388-9398.
54. Sauter M., Lorbiecke R., Ouyang B., Pochapsky T.C., Rzewuski G. The immediate-early ethylene response gene OsARD1 encodes an acireductone dioxygenase involved in recycling of the ethylene precursor S-adenosylmethionine. Plant J 2005, 44:718-729.
55. Pochapsky T.C., Pochapsky S.S., Ju T., Mo H., Al-Mjeni F., Maroney M.J. Modeling and experiment yields the structure of acireductone dioxygenase from Klebsiella pneumoniae. Nat Struct Biol 2002, 9:966-972.
56. Maroney M.J., Ciurli S. Nonredox nickel enzymes. Chem Rev 2014, 114:4206-4228.
57. Xu L., Jia J., Lv J., Liang X., Han D., Huang L., Kang Z. Characterization of the expression profile of a wheat aci-reductone-dioxygenase-like gene in response to stripe rust pathogen infection and abiotic stresses. Plant Physiol Biochem 2010, 48:461-468.
58. Weits D.A., Giuntoli B., Kosmacz M., Parlanti S., Hubberten H.M., Riegler H., Hoefgen R., Perata P., van Dongen J.T., Licausi F. Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat Commun 2014, 5:3425.
59. Gibbs D.J., Conde J.V., Berckhan S., Prasad G., Mendiondo G.M., Holdsworth M.J. Group VII ethylene response factors coordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiol 2015, 169:23-31.
60. Tarhonskaya H., Chowdhury R., Leung I.K., Loik N.D., McCullagh J.S., Claridge T.D., Schofield C.J., Flashman E. Investigating the contribution of the active site environment to the slow reaction of hypoxia-inducible factor prolyl hydroxylase domain 2 with oxygen. Biochem J 2014, 463:363-372.
61. Myllyharju J. Prolyl 4-hydroxylases, master regulators of the hypoxia response. Acta Physiol (Oxf) 2013, 208:148-165.
62. Cheng A.X., Han X.J., Wu Y.F., Lou H.X. The function and catalysis of 2-oxoglutarate-dependent oxygenases involved in plant flavonoid biosynthesis. Int J Mol Sci 2014, 15:1080-1095.
63. Vigani G., Morandini P., Murgia I. Searching iron sensors in plants by exploring the link among 2'-OG-dependent dioxygenases, the iron deficiency response and metabolic adjustments occurring under iron deficiency. Front Plant Sci 2013, 4:169.
64. Porta H., Rocha-Sosa M. Plant lipoxygenases. Physiological and molecular features. Plant Physiol 2002, 130:15-21.
65. Zhang K., Halitschke R., Yin C., Liu C.J., Gan S.S. Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc Natl Acad Sci U S A 2013, 110:14807-14812.
66. Zhao Z., Zhang Y., Liu X., Zhang X., Liu S., Yu X., Ren Y., Zheng X., Zhou K., Jiang L., et al. A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev Cell 2013, 27:113-122.
67. Khan M.I., Giridhar P. Plant betalains: chemistry and biochemistry. Phytochemistry 2015, 117:267-295.