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Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization.

Breithaupt C, Kurzbauer R, Lilie H, Schaller A, Strassner J, Huber R, Macheroux P, Clausen T
Proc Natl Acad Sci U S A 103 14337-42 (2006)
Related entries: 2hs6, 2hs8

Cited: 55 times
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Abstract

12-Oxophytodienoate reductase (OPR) 3, a homologue of old yellow enzyme (OYE), catalyzes the reduction of 9S,13S-12-oxophytodienoate to the corresponding cyclopentanone, which is subsequently converted to the plant hormone jasmonic acid (JA). JA and JA derivatives, as well as 12-oxophytodienoate and related cyclopentenones, are known to regulate gene expression in plant development and defense. Together with other oxygenated fatty acid derivatives, they form the oxylipin signature in plants, which resembles the pool of prostaglandins in animals. Here, we report the crystal structure of OPR3 from tomato and of two OPR3 mutants. Although the catalytic residues of OPR3 and related OYEs are highly conserved, several characteristic differences can be discerned in the substrate-binding regions, explaining the remarkable substrate stereoselectivity of OPR isozymes. Interestingly, OPR3 crystallized as an extraordinary self-inhibited dimer. Mutagenesis studies and biochemical analysis confirmed a weak dimerization of OPR3 in vitro, which correlated with a loss of enzymatic activity. Based on structural data of OPR3, a putative mechanism for a strong and reversible dimerization of OPR3 in vivo that involves phosphorylation of OPR3 is suggested. This mechanism could contribute to the shaping of the oxylipin signature, which is critical for fine-tuning gene expression in plants.

Articles - 2hsa mentioned but not cited (4)

  1. Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization. Breithaupt C, Kurzbauer R, Lilie H, Schaller A, Strassner J, Huber R, Macheroux P, Clausen T. Proc Natl Acad Sci U S A 103 14337-14342 (2006)
  2. VASCo: computation and visualization of annotated protein surface contacts. Steinkellner G, Rader R, Thallinger GG, Kratky C, Gruber K. BMC Bioinformatics 10 32 (2009)
  3. A Liquid Chromatography-High Resolution Mass Spectrometry (LC-HRMS) Method for the Determination of Free Hydroxy Fatty Acids in Cow and Goat Milk. Kokotou MG, Mantzourani C, Bourboula A, Mountanea OG, Kokotos G. Molecules 25 E3947 (2020)
  4. The crystal structure of XdpB, the bacterial old yellow enzyme, in an FMN-free form. Zahradník J, Kolenko P, Palyzová A, Černý J, Kolářová L, Kyslíková E, Marešová H, Grulich M, Nunvar J, Šulc M, Kyslík P, Schneider B. PLoS One 13 e0195299 (2018)


Reviews citing this publication (9)

  1. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Wasternack C, Hause B. Ann Bot 111 1021-1058 (2013)
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  5. The wound hormone jasmonate. Koo AJ, Howe GA. Phytochemistry 70 1571-1580 (2009)
  6. The Oxylipin Pathways: Biochemistry and Function. Wasternack C, Feussner I. Annu Rev Plant Biol 69 363-386 (2018)
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  8. Old yellow enzymes: structures and structure-guided engineering for stereocomplementary bioreduction. Shi Q, Wang H, Liu J, Li S, Guo J, Li H, Jia X, Huo H, Zheng Z, You S, Qin B. Appl Microbiol Biotechnol 104 8155-8170 (2020)
  9. Post-translational modifications: emerging regulators manipulating jasmonate biosynthesis and signaling. Yi R, Shan X. Plant Cell Rep 42 215-222 (2023)

Articles citing this publication (42)

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  3. The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. Stumpe M, Göbel C, Faltin B, Beike AK, Hause B, Himmelsbach K, Bode J, Kramell R, Wasternack C, Frank W, Reski R, Feussner I. New Phytol 188 740-749 (2010)
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  6. Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Kallenbach M, Alagna F, Baldwin IT, Bonaventure G. Plant Physiol 152 96-106 (2010)
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  8. Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations. Kallenbach M, Bonaventure G, Gilardoni PA, Wissgott A, Baldwin IT. Proc Natl Acad Sci U S A 109 E1548-57 (2012)
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  10. Phylogenetic analysis, structural evolution and functional divergence of the 12-oxo-phytodienoate acid reductase gene family in plants. Li W, Liu B, Yu L, Feng D, Wang H, Wang J. BMC Evol Biol 9 90 (2009)
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  12. 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. Hall M, Stueckler C, Kroutil W, Macheroux P, Faber K. Angew Chem Int Ed Engl 46 3934-3937 (2007)
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  14. AtOPR3 specifically inhibits primary root growth in Arabidopsis under phosphate deficiency. Zheng H, Pan X, Deng Y, Wu H, Liu P, Li X. Sci Rep 6 24778 (2016)
  15. Chemoenzymatic asymmetric synthesis of pregabalin precursors via asymmetric bioreduction of β-cyanoacrylate esters using ene-reductases. Winkler CK, Clay D, Davies S, O'Neill P, McDaid P, Debarge S, Steflik J, Karmilowicz M, Wong JW, Faber K. J Org Chem 78 1525-1533 (2013)
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  17. Nicotinamide-independent asymmetric bioreduction of C=C-bonds via disproportionation of enones catalyzed by enoate reductases. Stueckler C, Reiter TC, Baudendistel N, Faber K. Tetrahedron 66 663-667 (2010)
  18. Bioreduction of alpha-methylcinnamaldehyde derivatives: chemo-enzymatic asymmetric synthesis of Lilial and Helional. Stueckler C, Mueller NJ, Winkler CK, Glueck SM, Gruber K, Steinkellner G, Faber K. Dalton Trans 39 8472-8476 (2010)
  19. Overexpression of Arabidopsis OPR3 in Hexaploid Wheat (Triticum aestivum L.) Alters Plant Development and Freezing Tolerance. Pigolev AV, Miroshnichenko DN, Pushin AS, Terentyev VV, Boutanayev AM, Dolgov SV, Savchenko TV. Int J Mol Sci 19 E3989 (2018)
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  23. Classification of protein functional surfaces using structural characteristics. Tseng YY, Li WH, Li WH. Proc Natl Acad Sci U S A 109 1170-1175 (2012)
  24. Genome-Wide Analysis of OPR Family Genes in Cotton Identified a Role for GhOPR9 in Verticillium dahliae Resistance. Liu S, Sun R, Zhang X, Feng Z, Wei F, Zhao L, Zhang Y, Zhu L, Feng H, Zhu H. Genes (Basel) 11 E1134 (2020)
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  27. Creation of male-sterile lines that can be restored to fertility by exogenous methyl jasmonate for the establishment of a two-line system for the hybrid production of rice (Oryza sativa L.). Pak H, Wang H, Kim Y, Song U, Tu M, Wu D, Jiang L. Plant Biotechnol J 19 365-374 (2021)
  28. Nitrile as Activating Group in the Asymmetric Bioreduction of β-Cyanoacrylic Acids Catalyzed by Ene-Reductases. Winkler CK, Clay D, Turrini NG, Lechner H, Kroutil W, Davies S, Debarge S, O'Neill P, Steflik J, Karmilowicz M, Wong JW, Faber K. Adv Synth Catal 356 1878-1882 (2014)
  29. Regulation of Sixth Seminal Root Formation by Jasmonate in Triticum aestivum L. Pigolev A, Miroshnichenko D, Dolgov S, Savchenko T. Plants (Basel) 10 219 (2021)
  30. STRUCTURAL AND FUNCTIONAL CONSEQUENCES OF CIRCULAR PERMUTATION ON THE ACTIVE SITE OF OLD YELLOW ENZYME. Daugherty AB, Horton JR, Cheng X, Lutz S. ACS Catal 5 892-899 (2015)
  31. Overcoming co-product inhibition in the nicotinamide independent asymmetric bioreduction of activated C=C-bonds using flavin-dependent ene-reductases. Winkler CK, Clay D, van Heerden E, Faber K. Biotechnol Bioeng 110 3085-3092 (2013)
  32. The structure of glycerol trinitrate reductase NerA from Agrobacterium radiobacter reveals the molecular reason for nitro- and ene-reductase activity in OYE homologues. Oberdorfer G, Binter A, Wallner S, Durchschein K, Hall M, Faber K, Macheroux P, Gruber K. Chembiochem 14 836-845 (2013)
  33. Effects of overexpression of jasmonic acid biosynthesis genes on nicotine accumulation in tobacco. Chen H, Wang B, Geng S, Arellano C, Chen S, Qu R. Plant Direct 2 e00036 (2018)
  34. Fungal Jasmonate as a Novel Morphogenetic Signal for Pathogenesis. Liu Y, Pagac M, Yang F, Patkar RN, Naqvi NI. J Fungi (Basel) 7 693 (2021)
  35. Clone and Function Verification of the OPR gene in Brassica napus Related to Linoleic Acid Synthesis. Tan M, Niu J, Peng DZ, Cheng Q, Luan MB, Zhang ZQ. BMC Plant Biol 22 192 (2022)
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  37. Structural insights into stereospecific reduction of α, β-unsaturated carbonyl substrates by old yellow enzyme from Gluconobacter oxydans. Yin B, Deng J, Lim L, Yuan YA, Wei D. Biosci Biotechnol Biochem 79 410-421 (2015)
  38. Structural investigation into the C-terminal extension of the ene-reductase from Ralstonia (Cupriavidus) metallidurans. Opperman DJ. Proteins 85 2252-2257 (2017)
  39. Multifunctional enzymes in oxylipin metabolism. Wasternack C, Feussner I. Chembiochem 9 2373-2375 (2008)
  40. Ene Reductase Enabled Intramolecular β-C-H Functionalization of Substituted Cyclohexanones for Efficient Synthesis of Bridged Bicyclic Nitrogen Scaffolds. Jiang G, Huang C, Harrison W, Li H, Zhou M, Zhao H. Angew Chem Int Ed Engl 62 e202302125 (2023)
  41. Molecular cloning, characterization and expression analysis of two 12-oxophytodienoate reductases (NtOPR1 and NtOPR2) from Nicotiana tabacum. Huang F, Abbas F, Rothenberg DO, Imran M, Fiaz S, Rehman NU, Amanullah S, Younas A, Ding Y, Cai X, Chen X, Yu L, Ye X, Jiang L, Ke Y, He Y. Mol Biol Rep 49 5379-5387 (2022)
  42. Promoter variations in DBR2-like affect artemisinin production in different chemotypes of Artemisia annua. Wang X, Wu L, Xiang L, Gao R, Yin Q, Wang M, Liu Z, Leng L, Su Y, Wan H, Ma T, Chen S, Shi Y. Hortic Res 10 uhad164 (2023)


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