Published September 6, 2018 | Version v1
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Detection of the first higher plant epoxyalcohol synthase: Molecular cloning and characterisation of the CYP74M2 enzyme of spikemoss Selaginella moellendorffii

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Toporkova, Yana Y., Smirnova, Elena O., Gorina, Svetlana S., Mukhtarova, Lucia S., Grechkin, Alexander N. (2018): Detection of the first higher plant epoxyalcohol synthase: Molecular cloning and characterisation of the CYP74M2 enzyme of spikemoss Selaginella moellendorffii. Phytochemistry 156: 73-82, DOI: 10.1016/j.phytochem.2018.08.010, URL: http://dx.doi.org/10.5281/zenodo.8250065

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urn:lsid:plazi.org:pub:FFE2C004E735FF9AFF96FF81FFE3ED0C

References

  • Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.L., Gribskov, M., dePamphilis, C., Albert, V.A., Aono, N., Aoyama, T., Ambrose, B.A., Ashton, N.W., Axtell, M.J., Barker, E., Barker, M.S., Bennetzen, J.L., Bonawitz, N.D., Chapple, C., Cheng, C., Correa, L.G.G., Dacre, M., DeBarry, J., Dreyer, I., Elias, M., Engstrom, E.M., Estelle, M., Feng, L., Finet, C., Floyd, S.K., Frommer, W.B., Fujita, T., Gramzow, L., Gutensohn, M., Harholt, J., Hattori, M., Heyl, A., Hirai, T., Hiwatashi, Y., Ishikawa, M., Iwata, M., Karol, K.G., Koehler, B., Kolukisaoglu, U., Kubo, M., Kurata, T., Lalonde, S., Li, K., Li, Y., Litt, A., Lyons, E., Manning, G., Maruyama, T., Michael, T.P., Mikami, K., Miyazaki, S., Morinaga, S.I., Murata, T., Mueller-Roeber, B., Nelson, D.R., Obara, M., Oguri, Y., Olmstead, R.G., Onodera, N., Petersen, B.L., Pils, B., Prigge, M., Rensing, S.A., Riano-Pachon, D.M., Roberts, A.W., Sato, Y., Scheller, H.V., Schulz, B., Schulz, C., Shakirov, E.V., Shibagaki, N., Shinohara, N., Shippen, D.E., Sorensen, I., Sotooka, R., Sugimoto, N., Sugita, M., Sumikawa, N., Tanurdzic, M., Theissen, G., Ulvskov, P., Wakazuki, S., Weng, J.-K., Willats, W.W.G.T., Wipf, D., Wolf, P.G., Yang, L., Zimmer, A.D., Zhu, Q., Mitros, T., Hellsten, U., Loque, D., Otillar, R., Salamov, A., Schmutz, J., Shapiro, H., Lindquist, E., Lucas, S., Rokhsar, D., Grigoriev, I.V., 2011. The compact Selaginella genome identifies changes in gene content associated with the evolution of vascular plants. Science 332, 960-963.
  • Bernart, M.W., Whatley, G.G., Gerwick, W.H., 1993. Unprecedented oxylipins from the marine green alga Acrosiphonia coalita. J. Nat. Prod. 56, 245-259.
  • Blee, E., Flenet, M., Boachon, B., Fauconnier, M.L., 2012. A non-canonical caleosin from Arabidopsis efficiently epoxidizes physiological unsaturated fatty acids with complete stereoselectivity. FEBS J. 279, 3981-3995.
  • Blee, E., Schuber, F., 1990. Stereochemistry of the epoxidation of fatty acids catalyzed by soybean peroxygenase. Biochem. Biophys. Res. Commun. 173, 1354-1360.
  • Brash, A.R., 2009. Mechanistic aspects of CYP74 allene oxide synthases and related cytochrome P450 enzymes. Phytochemistry 70, 1522-1531.
  • Chang, M.S., Boeglin, W.E., Guengerich, F.P., Brash, A.R., 1996. Cytochrome P450-dependent transformations of 15R - and 15S -hydroperoxyeicosatetraenoic acids: stereoselective formation of epoxy alcohol products. Biochemistry 35, 464-471.
  • Chechetkin, I.R., Osipova, E.V., Tarasova, N.B., Mukhitova, F.K., Hamberg, M., Gogolev, Y.V., Grechkin, A.N., 2009. Specificity of oxidation of linoleic acid homologs by plant lipoxygenases. Biochemistry (Mosc.) 74, 855-861.
  • Dix, T.A., Marnett, L.J., 1985. Conversion of linoleic acid hydroperoxide to hydroxy, keto, epoxyhydroxy, and trihydroxy fatty acids by hematin. J. Biol. Chem. 260, 5351-5357.
  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
  • Gardner, H.W., 1975. Decomposition of linoleic acid hydroperoxides. Enzymic reactions compared with nonenzymic. J. Agric. Food Chem. 23, 129-136.
  • Gardner, H.W., 1989. Oxygen radical chemistry of polyunsaturated fatty acids. Free Radic. Biol. Med. 7, 65-86.
  • Gardner, H.W., Jursinic, P.A., 1981. Degradation of linoleic acid hydroperoxides by a cysteine FeCl3 catalyst as a model for similar biochemical reactions: I. Study of oxygen requirement, catalyst and effect of pH. Biochim. Biophys. Acta 665, 100-112.
  • Gardner, H.W., Kleiman, R., 1981. Degradation of linoleic acid hydroperoxides by a cysteine FeCl3 catalyst as a model for similar biochemical reactions: II. Specificity in formation of fatty acid epoxides. Biochim. Biophys. Acta 665, 113-125.
  • Gardner, H.W., Kleiman, R., Weisleder, D., 1974. Homolytic decomposition of linoleic acid hydroperoxide: identification of fatty acid products. Lipids 9, 696-706.
  • Gardner, H.W., Nelson, E.C., Tjarks, L.W., England, R.E., 1984a. Acid-catalyzed transformation of 13(S)-hydroperoxylinoleic acid into epoxyhydroxyoctadecenoic and trihydroxyoctadecenoic acids. Chem. Phys. Lipids 35, 87-101.
  • Gardner, H.W., Weisleder, D., Nelson, E.C., 1984b. Acid catalysis of a linoleic acid hydroperoxide: formation of epoxides by an intramolecular cyclization of the hydroperoxide group. J. Org. Chem. 49, 508-515.
  • Garscha, U., Oliw, E.H., 2009. Leucine/valine residues direct oxygenation of linoleic acid by (10R)- and (8R)-dioxygenases: expression and site-directed mutagenesis of (10R)- dioxygenase with epoxyalcohol synthase activity. J. Biol. Chem. 284, 13755-13765.
  • Gogolev, Y.V., Gorina, S.S., Gogoleva, N.E., Toporkova, Y.Y., Chechetkin, I.R., Grechkin, A.N., 2012. Green leaf divinyl ether synthase: gene detection, molecular cloning and identification of a unique CYP74B subfamily member. Biochim. Biophys. Acta 1821, 287-294.
  • Gorina, S.S., Toporkova, Y.Y., Mukhtarova, L.S., Chechetkin, I.R., Khairutdinov, B.I., Gogolev, Y.V., Grechkin, A.N., 2014. Detection and molecular cloning of CYP74Q1 gene: identification of Ranunculus acris leaf divinyl ether synthase. Biochim. Biophys. Acta 1841, 1227-1233.
  • Gorina, S.S., Toporkova, Y.Y., Mukhtarova, L.S., Smirnova, E.O., Chechetkin, I.R., Khairutdinov, B.I., Gogolev, Y.V., Grechkin, A.N., 2016. Oxylipin biosynthesis in spikemoss Selaginella moellendorffii: molecular cloning and identification of divinyl ether synthases CYP74M1 and CYP74M3. Biochim. Biophys. Acta 1861, 301-309.
  • Gotoh, O., 1992. Substrate recognition sites in cytochrome P450 family 2 (CYPB) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. J. Biol. Chem. 267, 83-90.
  • Grechkin, A.N., 1998. Recent developments in biochemistry of the plant lipoxygenase pathway. Prog. Lipid Res. 37, 317-352.
  • Grechkin, A.N., 2002. Hydroperoxide lyase and divinyl ether synthase. Prostag. Other Lipid Mediat. 68-69, 457-470.
  • Grechkin, A.N., Bruhlmann, F., Mukhtarova, L.S., Gogolev, Y.V., Hamberg, M., 2006. Hydroperoxide lyases (CYP74C and CYP74B) catalyze the homolytic isomerization of fatty acid hydroperoxides into hemiacetals. Biochim. Biophys. Acta 1761, 1419-1428.
  • Grechkin, A.N., Fazliev, F.N., Ilyasov, A.V., 1995. Potato lipoxygenase-catalyzed formation of novel 9,10-epoxy-11-hydroxy compounds. Bioorg. Khim. 21, 399-400.
  • Grechkin, A.N., Ilyasov, A.V., Hamberg, M., 1997. On the mechanism of biosynthesis of divinyl ether oxylipins by enzyme from garlic bulbs. Eur. J. Biochem. 245, 137-142.
  • Hamberg, M., 1987. Mechanism of corn hydroperoxide isomerase: detection of 12,13(S)- oxido-9(Z),11-octadecadienoic acid. Biochim. Biophys. Acta 920, 76-84.
  • Hamberg, M., Gotthammar, B., 1973. A new reaction of unsaturated fatty acid hydroperoxides: formation of 11-hydroxy-12,13-epoxy-9-octadecenoic acid from 13- hydroperoxy-9,11-octadecadienoic acid. Lipids 8, 737-744.
  • Hamberg, M., Hamberg, G., 1996. Peroxygenase-catalyzed fatty acid epoxidation in cereal seeds. Sequential oxidation of linoleic acid into 9(S),12(S),13(S)-trihydroxy- 10(E)-octadecenoic acid. Plant Physiol. 110, 807-815.
  • Hughes, R.K., De Domenico, S., Santino, A., 2009. Plant cytochrome CYP74 family: biochemical features, endocellular localisation, activation mechanism in plant defence and improvements for industrial applications. Chembiochem 10, 1122-1133.
  • Jin, J., Boeglin, W.E., Cha, J.K., Brash, A.R., 2012. 8R -Lipoxygenase-catalyzed synthesis of a prominent cis -epoxyalcohol from dihomo-γ- linolenic acid: a distinctive transformation compared with S -lipoxygenases. J. Lipid Res. 53, 292-299.
  • Kato, T., Yamaguchi, Y., Ohnuma, S., Uyerhara, T., Namai, T., Kodama, M., Shiobara, Y., 1986. Structural elucidation of 11-hydroxy-12,13-epoxyoctadeca-(9Z,15Z)-dienoic acids from rice plants suffering from rice blast disease. J. Chem. Soc. Chem. Commun. 10, 743-744.
  • Koeduka, T., Ishizaki, K., Mwenda, C.M., Hori, K., Sasaki-Sekimoto, Y., Ohta, H., Kohchi, T., Matsui, K., 2015. Biochemical characterization of allene oxide synthases from the liverwort Marchantia polymorpha and green microalgae Klebsormidium flaccidum provides insight into the evolutionary divergence of the plant CYP74 family. Planta 242, 1175-1186.
  • Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
  • Lee, D.-S., Nioche, P., Hamberg, M., Raman, C.S., 2008. Structural insights into the evolutionary paths of oxylipin biosynthesis enzymes. Nature 455, 363-370.
  • Nelson, D.R., Goldstone, J.V., Stegeman, J.J., 2013. The cytochrome P450 genesis locus: the origin and evolution of animal cytochrome P450s. Philos. Trans. R. Soc. Lond. B Biol. Sci. 201 3 (368), 20120474.
  • Ogorodnikova, A.V., Mukhitova, F.K., Grechkin, A.N., 2015. Oxylipins in the spikemoss Selaginella martensii: detection of divinyl ethers, 12-oxophytodienoic acid and related cyclopentenones. Phytochemistry 118, 42-50.
  • Schenkman, J.B., Jansson, I., 2006. Spectral analyses of cytochromes P450. Meth. Mol.
  • Song, W.-C., Baertschi, S.W., Boeglin, W.E., Harris, T.M., Brash, A.R., 1993. Formation of epoxyalcohols by a purified allene oxide synthase. Implications for the mechanism of allene oxide synthesis. J. Biol. Chem. 268, 6293-6298.
  • Thomas, C.P., Boeglin, W.E., Garcia-Diaz, Y., O'Donnell, V.B., Brash, A.R., 2013. Steric analysis of epoxyalcohol and trihydroxy derivatives of 9-hydroperoxy-linoleic acid from hematin and enzymatic synthesis. Chem. Phys. Lipids 167-168, 21-32.
  • Toporkova, Y.Y., Ermilova, V.S., Gorina, S.S., Mukhtarova, L.S., Osipova, E.V., Gogolev, Y.V., Grechkin, A.N., 2013. Structure-function relationship in the CYP74 family: conversion of divinyl ether synthases into allene oxide synthases by site-directed mutagenesis. FEBS Lett. 587, 2552-2558.
  • Toporkova, Y.Y., Fatykhova, V.S., Gogolev, Y.V., Khairutdinov, B.I., Mukhtarova, L.S., Grechkin, A.N., 2017a. Epoxyalcohol synthase of Ectocarpus siliculosus. First CYP74- related enzyme of oxylipin biosynthesis in brown algae. Biochim. Biophys. Acta 1761, 1419-1428.
  • Toporkova, Y.Y., Gogolev, Y.V., Mukhtarova, L.S., Grechkin, A.N., 2008. Determinants governing the CYP74 catalysis: conversion of allene oxide synthase into hydroperoxide lyase by site-directed mutagenesis. FEBS Lett. 582, 3423-3428.
  • Toporkova, Y.Y., Gorina, S.S., Mukhitova, F.K., Hamberg, M., Ilyina, T.M., Mukhtarova, L.S., Grechkin, A.N., 2017b. Identification of CYP443D1 (CYP74 clan) of Nematostella vectensis as a first cnidarian epoxyalcohol synthase and insights into its catalytic mechanism. Biochim. Biophys. Acta 1862 (10 Pt A), 1099-1109.
  • Wilson, R.A., Gardner, H.W., Keller, N.P., 2001. Cultivar-dependent expression of a maize lipoxygenase responsive to seed infesting fungi. Mol. Plant Microb. Interact. 14, 980-987.
  • Yu, Z., Schneider, C., Boeglin, W.E., Marnett, L.J., Brash, A.R., 2003. The lipoxygenase gene ALOXE3 implicated in skin differentiation encodes a hydroperoxide isomerase. Proc. Natl. Acad. Sci. U.S.A. 100, 9162-9167.
  • Zuckerkandl, E., Pauling, L., 1965. Evolutionary divergence and convergence in proteins. In: Bryson, V., Vogel, H.J. (Eds.), Evolving Genes and Proteins. Academic Press, New York, pp. 97-166.