Structural Basis of Substrate Specificity of Plant 12-Oxophytodienoate Reductases

Journal of Molecular Biology

Volumn 392, Issue 5, 2009, Pages 1266-1277

  Breithaupt, Constanze ^a   Kurzbauer, Robert ^b   Schaller, Florian ^c   Stintzi, Annick ^d   Schaller, Andreas ^d   Huber, Robert ^e,f,g   Macheroux, Peter ^h   Clausen, Tim ^b  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d UNIVERSITY OF HOHENHEIM   (Germany)

^e MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^f CARDIFF UNIVERSITY   (United Kingdom)

^g UNIVERSITY OF DUISBURG ESSEN   (Germany)

^h GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

enantioselectivity; jasmonic acid; old yellow enzyme; OPR; oxyphytodienoate reductase

Indexed keywords

12 OXOPHYTODIENOATE REDUCTASE 1; 12 OXOPHYTODIENOATE REDUCTASE 3; 4 HYDROXYBENZALDEHYDE; AMINO ACID; CYCLOPENTENONE DERIVATIVE; HISTIDINE; ISOENZYME; MUTANT PROTEIN; OXIDOREDUCTASE; PHENYLALANINE; PROTEIN OPR1; PROTEIN OPR3; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL ANALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; ENANTIOSELECTIVITY; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME STRUCTURE; LIGAND BINDING; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; LYCOPERSICON ESCULENTUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 70149104457     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.087     Document Type: Article

References (44)

1. Massey V. The chemical and biological versatility of riboflavin. Biochem. Soc. Trans. 28 (2000) 283-296
2. Williams R.E., and Bruce N.C. 'New uses for an old enzyme'-the old yellow enzyme family of flavoenzymes. Microbiology 148 (2002) 1607-1614
3. Vick B.A., and Zimmerman D.C. Biosynthesis of jasmonic acid by several plant species. Plant Physiol. 75 (1984) 458-461
4. Schaller F., Schaller A., and Stintzi A. Biosynthesis and metabolism of jasmonates. J. Plant Growth Regul. 23 (2004) 179-199
5. Wasternack C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. (Lond) 100 (2007) 681-697
6. Stintzi A., and Browse J. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl Acad. Sci. USA 97 (2000) 10625-10630
7. Stintzi A., Weber H., Reymond P., Browse J., and Farmer E.E. Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl Acad. Sci. USA 98 (2001) 12837-12842
8. Schaller F., Biesgen C., Müssig C., Altmann T., and Weiler E.W. 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210 (2000) 979-984
9. Strassner J., Schaller F., Frick U.B., Howe G.A., Weiler E.W., Amrhein N., et al. Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductases reveals differential roles for octadecanoid biosynthesis in the local versus the systemic wound response. Plant J. 32 (2002) 585-601
10. Tani T., Sobajima H., Okada K., Chujo T., Arimura S., Tsutsumi N., et al. Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227 (2008) 517-526
11. Breithaupt C., Strassner J., Breitinger U., Huber R., Macheroux P., Schaller A., and Clausen T. X-ray structure of 12-oxophytodienoate reductase 1 provides structural insight into substrate binding and specificity within the family of OYE. Structure 9 (2001) 419-429
12. Breithaupt C., Kurzbauer R., Lilie H., Schaller A., Strassner J., Huber R., et al. Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization. Proc. Natl Acad. Sci. USA 103 (2006) 14337-14342
13. Fox B.G., Malone T.E., Johnson K.A., Madson S.E., Aceti D., Bingman C.A., et al. X-ray structure of Arabidopsis At1g77680, 12-oxophytodienoate reductase isoform 1. Proteins 61 (2005) 206-208
14. Malone T.E., Madson S.E., Wrobel R.L., Jeon W.B., Rosenberg N.S., Johnson K.A., et al. X-ray structure of Arabidopsis At2g06050, 12-oxophytodienoate reductase isoform 3. Proteins: Struct., Funct., Bioinf. 58 (2005) 243-245
15. Massey V., and Schopfer L.M. Reactivity of old yellow enzyme with alpha-NADPH and other pyridine-nucleotide derivatives. J. Biol. Chem. 261 (1986) 1215-1222
16. Niino Y.S., Chakraborty S., Brown B.J., and Massey V. A new old yellow enzyme of Saccharomyces cerevisiae. J. Biol. Chem. 270 (1995) 1983-1991
17. Meah Y., and Massey V. Old yellow enzyme: stepwise reduction of nitro-olefins and catalysis of aci-nitro tautomerization. Proc. Natl Acad. Sci. USA 97 (2000) 10733-10738
18. Fox K.M., and Karplus P.A. Old yellow enzyme at 2-angstrom resolution-overall structure, ligand-binding, and comparison with related flavoproteins. Structure 2 (1994) 1089-1105
19. Abramovitz A.S., and Massey V. Interaction of phenols with old yellow enzyme-physical evidence for charge-transfer complexes. J. Biol. Chem. 251 (1976) 5327-5336
20. Strassner J., Fürholz A., Macheroux P., Amrhein N., and Schaller A. A homolog of old yellow enzyme in tomato-spectral properties and substrate specificity of the recombinant protein. J. Biol. Chem. 274 (1999) 35067-35073
21. Hall M., Stueckler C., Ehammer C., Pointner E., Oberdorfer G., Gruber K., et al. Asymmetric bioreduction of C{double bond, short}C bonds using enoate reductases OPR1, OPR3 and YqjM: enzyme-based stereocontrol. Adv. Synth. Catal. 350 (2008) 411-418
22. Sobajima H., Takeda M., Sugimori M., Kobashi N., Kiribuchi K., Cho E.M., et al. Cloning and characterization of a jasmonic acid-responsive gene encoding 12-oxophytodienoic acid reductase in suspension-cultured rice cells. Planta 216 (2003) 692-698
23. Matsui H., Nakamura G., Ishiga Y., Toshima H., Inagaki Y., Toyoda K., et al. Structure and expression of 12-oxophytodienoate reductase (subgroup I) genes in pea, and characterization of the oxidoreductase activities of their recombinant products. Mol. Genet. Genomics 271 (2004) 1-10
24. Zhang J., Simmons C., Yalpani N., Crane V., Wilkinson H., and Kolomiets M. Genomic analysis of the 12-oxo-phytodienoic acid reductase gene family of Zea mays. Plant Mol. Biol. 59 (2005) 323-343
25. Agrawal G.K., Tamogami S., Han O., Iwahashi H., and Rakwal R. Rice octadecanoid pathway. Biochem. Biophys. Res. Commun. 317 (2004) 1-15
26. Rensing S.A., Lang D., Zimmer A.D., Terry A., Salamov A., Shapiro H., et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319 (2008) 64-69
27. Hall M., Stueckler C., Kroutil W., Macheroux P., and Faber K. Asymmetric bioreduction of activated alkenes using cloned 12-oxophytodienoate reductase isoenzymes OPR-1 and OPR-3 from Lycopersicon esculentum (tomato): a striking change of stereoselectivity. Angew. Chem., Int. Ed. Engl. 46 (2007) 3934-3937
28. Stuermer R., Hauer B., Hall M., and Faber K. Asymmetric bioreduction of activated C{double bond, short}C bonds using enoate reductases from the old yellow enzyme family. Curr. Opin. Chem. Biol. 11 (2007) 203-213
29. Strassner J., Fürholz A., Schaller F., Macheroux P., Weiler E.W., Amrhein N., and Schaller A. Overexpression and characterization of 12-oxophytodienoic acid reductase from tomato, a member of the OYE family. In: Ghisla S., Kroneck P., Macheroux P., and Sund H. (Eds). Flavins and Flavoproteins (1999), Agency for Scientific Publ., Berlin 655-658
30. Otwinowsky Z., and Minor W. DENZO: A Film Processing Program for Macromolecular Crystallography (1993), Yale University Press, New Haven, CT
31. Navaza J. Amore-an automated package for molecular replacement. Acta Crystallogr., Sect. A: Found. Crystallogr. 50 (1994) 157-163
32. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
33. Engh R.A., and Huber R. Accurate bond and angle parameters for x-ray protein-structure refinement. Acta Crystallogr., Sect. A: Found. Crystallogr. 47 (1991) 392-400
34. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr., Sect. A: Found. Crystallogr. 47 (1991) 110-119
35. Kleywegt G.J., and Jones T.A. Model building and refinement practice. Methods Enzymol. 277 (1997) 208-230
36. Kraulis P.J. Molscript-a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24 (1991) 946-950
37. Nicholls A., Sharp K.A., and Honig B. Protein folding and association-insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct., Funct., Genet. 11 (1991) 281-296
38. Merritt E.A., and Murphy M.E.P. Raster3d version-2.0-a program for photorealistic molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 869-873
39. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
40. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007) 2947-2948
41. Barton G.J. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 6 (1993) 37-40
42. Zerbe P., Weiler E.W., and Schaller F. Preparative enzymatic solid phase synthesis of cis(+)-12-oxo-phytodienoic acid-physical interaction of AOS and AOC is not necessary. Phytochemistry 68 (2007) 229-236
43. Laudert D., Hennig P., Stelmach B.A., Muller A., Andert L., and Weiler E.W. Analysis of 12-oxo-phytodienoic acid enantiomers in biological samples by capillary gas chromatography mass spectrometry using cyclodextrin stationary phases. Anal. Biochem. 246 (1997) 211-217
44. Schaller F., Hennig P., and Weiler E.W. B12-oxophytodienoate-10,11-reductase: occurrence of two isoenzymes of different specificity against stereoisomers of 12-oxophytodienoic acid. Plant Physiol. 118 (1998) 1345-1351