Published March 31, 2022 | Version v1
Journal article Restricted

Oxylipin biosynthesis in spikemoss Selaginella moellendorffii: Identification of allene oxide synthase (CYP74L2) and hydroperoxide lyase (CYP74L1)

Description

Toporkova, Yana Y., Askarova, Elena K., Gorina, Svetlana S., Mukhtarova, Lucia S., Grechkin, Alexander N. (2022): Oxylipin biosynthesis in spikemoss Selaginella moellendorffii: Identification of allene oxide synthase (CYP74L2) and hydroperoxide lyase (CYP74L1). Phytochemistry (113051) 195: 1-12, DOI: 10.1016/j.phytochem.2021.113051, URL: http://dx.doi.org/10.1016/j.phytochem.2021.113051

Files

Restricted

The record is publicly accessible, but files are restricted to users with access.

Linked records

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:8C11FFB77A4CD25AFFC2323E5F3BDF4F
URL
http://publication.plazi.org/id/8C11FFB77A4CD25AFFC2323E5F3BDF4F

References

  • Alber, A.V., Renault, H., Basilio-Lopes, A., Bassard, J.E., Liu, Z., Ullmann, P., Lesot, A., Bihel, F., Schmitt, M., Werck-Reichhart, D., Ehlting, J., 2019. Evolution of coumaroyl conjugate 3-hydroxylases in land plants: lignin biosynthesis and defense. Plant J. 99, 924-936. https://doi.org/10.1111/tpj.14373.
  • Anderberg, H.I., Kjellbom, P., Johanson, U., 2012. Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Front. Plant Sci. 3, 33. https://doi.org/10.3389/fpls.2012.00033.
  • 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., Riatno-Pach ´on, 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., Loqu´e, D., Otillar, R., Salamov, A., Schmutz, J., Shapiro, H., Lindquist, E., Lucas, S., Rokhsar, D., Grigoriev, I.V., 2011. The Selaginella genome identifies changes in gene content associated with the evolution of vascular plants. Science 332, 960-963. https://doi.org/10.1126/science.1203810.
  • Bosch, M., Berger, S., Schaller, A., Stintzi, A., 2014a. Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol. 14, 257. https:// doi.org/10.1186/s12870-014-0257-8.
  • Bosch, M., Wright, L.P., Gershenzon, J., Wasternack, C., Hause, B., Schaller, A., Stintzi, A., 2014b. Jasmonic acid and its precursor 12-oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato. Plant Physiol. 166, 396-410. https://doi.org/10.1104/pp.114.237388.
  • Bowman, J.L., Kohchi, T., Yamato, K.T., Jenkins, J., Shu, S., Ishizaki, K., Yamaoka, S., Nishihama, R., Nakamura, Y., Berger, F., Adam, C., Aki, S.S., Althoff, F., Araki, T., Arteaga-Vazquez, M.A., Balasubrmanian, S., Barry, K., Bauer, D., Boehm, C.R., Briginshaw, L., Caballero-Perez, J., Catarino, B., Chen, F., Chiyoda, S., Chovatia, M., Davies, K.M., Delmans, M., Demura, T., Dierschke, T., Dolan, L., Dorantes-Acosta, A. E., Eklund, D.M., Florent, S.N., Flores-Sandoval, E., Fujiyama, A., Fukuzawa, H., Galik, B., Grimanelli, D., Grimwood, J., Grossniklaus, U., Hamada, T., Haseloff, J., Hetherington, A.J., Higo, A., Hirakawa, Y., Hundley, H.N., Ikeda, Y., Inoue, K., Inoue, S.-I., Ishida, S., Jia, Q., Kakita, M., Kanazawa, T., Kawai, Y., Kawashima, T., Kennedy, M., Kinose, K., Kinoshita, T., Kohara, Y., Koide, E., Komatsu, K., Kopischke, S., Kubo, M., Kyozuka, J., Lagercrantz, U., Lin, S.-S., Lindquist, E., Lipzen, A.M., Lu, C.-W., De Luna, E., Martienssen, R.A., Minamino, N., Mizutani, M., Mizutani, M., Mochizuki, N., Monte, I., Mosher, R., Nagasaki, H., Nakagami, H., Naramoto, S., Nishitani, K., Ohtani, M., Okamoto, T., Okumura, M., Phillips, J., Pollak, B., Reinders, A., R¨ovekamp, M., Sano, R., Sawa, S., Schmid, M.W., Shirakawa, M., Solano, R., Spunde, A., Suetsugu, N., Sugano, S., Sugiyama, A., Sun, R., Suzuki, Y., Takenaka, M., Takezawa, D., Tomogane, H., Tsuzuki, M., Ueda, T., Umeda, M., Ward, J.M., Watanabe, Y., Yazaki, K., Yokoyama, R., Yoshitake, Y., Yotsui, I., Zachgo, S., Schmut, J., 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171, 287-304. https://doi.org/10.1016/j.cell.2017.09.030.
  • Brash, A.R., 2009. Mechanistic aspects of CYP74 allene oxide synthases and related cytochrome P450 enzymes. Phytochemistry 70, 1522-1531. https://doi.org/ 10.1016/j.phytochem.2009.08.005.
  • 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. https://doi. org/10.1134/s0006297909080069.
  • Chen, F., Tholl, D., Bohlmann, J., Pichersky, E., 2011. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J. 66, 212-229. https://doi.org/10.1111/ j.1365-313X.2011.04520.x.
  • Cheon, J., Fujioka, S., Dilkes, B.P., Choe, S., 2013. Brassinosteroids regulate plant growth through distinct signaling pathways in Selaginella and Arabidopsis. PLoS One 8, e81938. https://doi.org/10.1371/journal.pone.0081938.
  • Cowley, T., Walters, D., 2005. Local and systemic effects of oxylipins on powdery mildew infection in barley. Pest Manag. Sci. 61, 572-576. https://doi.org/10.1002/ps.1026.
  • Deboever, E., Deleu, M., Mongrand, S., Lins, L., Fauconnier, M.L., 2020. Plant-pathogen interactions: underestimated roles of phyto-oxylipins. Trends Plant Sci. 25, 22-34. https://doi.org/10.1016/j.tplants.2019.09.009.
  • Fammartino, A., Cardinale, F., G¨obel, C., Mene-Saffrane, L., Fournier, J., Feussner, I., Esquerre-Tugaye, M.T., 2007. Characterization of a divinyl ether biosynthetic pathway specifically associated with pathogenesis in tobacco. Plant Physiol. 143, 378-388. https://doi.org/10.1104/pp.106.087304.
  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x.
  • Ferrari, C., Shivhare, D., Hansen, B.O., Pasha, A., Esteban, E., Provart, N.J., Kragler, F., Fernie, A., Tohge, T., Mutwil, M., 2020. Expression atlas of Selaginella moellendorffii provides insights into the evolution of vasculature, secondary metabolism, and roots. Plant Cell 32 (4), 853-870. https://doi.org/10.1105/tpc.19.00780.
  • Gorina, S.S., Toporkova, Y.Y., Mukhtarova, L.S., Grechkin, A.N., 2019a. The CYP443C1 (CYP74 clan) cytochrome of sea anemone Nematostella vectensis - the first metazoan enzyme possessing hydroperoxide lyase/epoxyalcohol synthase activity. Dokl. Biochem. Biophys. 486, 192-196. https://doi.org/10.1134/S1607672919030086.
  • Gorina, S.S., Mukhitova, F.K., Ilyina, T.M., Toporkova, Y.Y., Grechkin, A.N., 2019b. Detection of unprecedented allene oxide synthase member of CYP74B subfamily: CYP74B33 of carrot (Daucus carota). Biochim. Biophys. Acta 1864, 1580-1590. https://doi.org/10.1016/j.bbalip.2019.07.004.
  • 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. https://doi.org/10.1016/j.bbalip.2016.01.001.
  • Gobel ¨, C., Feussner, I., Schmidt, A., Scheel, D., Sanchez-Serrano, J., Hamberg, M., Rosahl, S., 2001. Oxylipin profiling reveals the preferential stimulation of the 9- lipoxygenase pathway in elicitor-treated potato cells. J. Biol. Chem. 276, 6267-6273. https://doi.org/10.1074/jbc.M008606200.
  • Gran´er, G., Hamberg, M., Meijer, J., 2003. Screening of oxylipins for control of oilseed rape (Brassica napus) fungal pathogens. Phytochemistry 63, 89-95. https://doi.org/ 10.1016/s0031-9422(02)00724-0.
  • Grechkin, A.N., 1998. Recent developments in biochemistry of the plant lipoxygenase pathway. Prog. Lipid Res. 37, 317-352. https://doi.org/10.1016/s0163-7827(98) 00014-9.
  • Grechkin, A.N., 2002. Hydroperoxide lyase and divinyl ether synthase. Prostag. Other Lipid Mediat. 68-69, 457-470. https://doi.org/10.1016/s0090-6980(02)00048-5.
  • 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. https://doi.org/10.1016/j.bbalip.2006.09.002.
  • Grechkin, A.N., Korolev, O.S., Kuramshin, R.A., Efremov, Y.J., Musin, R.S., Latypov, S.K., Ilyasov, A.V., Tarchevsky, I.A., 1987. New physiologically active product of linoleic acid oxidation in pea leaves-12-hydroxy-(9Z)-dodecenoic acid. Dokl. Akad. Nauk SSSR 297, 1257-1260.
  • Grechkin, A.N., Kuramshin, R.A., Latypov, S.K., Safonova, Y.Y., Gafarova, T.E., Ilyasov, A.V., 1991. Hydroperoxides of alpha-ketols. Novel products of the plant lipoxygenase pathway. Eur. J. Biochem. 199, 451-457. https://doi.org/10.1111/ j.1432-1033.1991.tb16143.x.
  • Grechkin, A.N., Mukhtarova, L.S., Latypova, L.R., Gogolev, Y.V., Toporkova, Y.Y., Hamberg, M., 2008. Tomato CYP74C3 is a multifunctional enzyme not only synthesizing allene oxide but also catalyzing its hydrolysis and cyclization. Chembiochem 9, 2498-2505. https://doi.org/10.1002/cbic.200800331.
  • Griffiths, G., 2015. Biosynthesis and analysis of plant oxylipins. Free Radic. Res. 49, 565-582. https://doi.org/10.3109/10715762.2014.1000318.
  • Grover, S., Versani, S., Kolomietx, M.V., Louis, J., 2020. Maize defense elicitor, 12-oxophytodienoic acid, prolongs aphid salivation. Commun. Integr. Biol. 13, 63-66. https://doi.org/10.1080/19420889.2020.1763562.
  • Guo, H.M., Li, H.C., Zhou, S.R., Xue, H.W., Miao, X.X., 2014. Cis -12-oxo-phytodienoic acid stimulates rice defense response to a piercing-sucking insect. Mol. Plant 7, 1683-1692. https://doi.org/10.1093/mp/ssu098.
  • 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. https://doi. org/10.1016/0005-2760(87)90313-4.
  • Hamberg, M., 1991. Transformations of alpha-linolenic acid in leaves of corn (Zea mays L.). Adv. Prostaglandin Thromboxane Leukotriene Res. 21A, 117-124.
  • 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. https://doi.org/10.1002/cbic.200800633.
  • Kato, T., Yamaguchi, Y., Abe, N., et al., 1985. Structure and synthesis of unsaturated trihydroxy C18 fatty: acids in rice plants suffering from rice blast disease. Tetrahedron Lett. 26, 2357-2360. https://doi.org/10.1021/acs.jafc.8b05857.
  • 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. https://doi.org/10.1007/s00425-015-2355-8.
  • Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874. https://doi. org/10.1093/molbev/msw054.
  • 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. https:// doi.org/10.1038/nature07307.
  • Mukhtarova, L.S., Bruhlmann, F., Hamberg, M., Khairutdinov, B.I., Grechkin, A.N., 2018. Plant hydroperoxide-cleaving enzymes (CYP74 family) function as hemiacetal synthases: structural proof of hemiacetals by NMR spectroscopy. Biochim. Biophys. Acta 1863, 1316-1322. https://doi.org/10.1016/j.bbalip.2018.08.011.
  • Mukhtarova, L.S., Lantsova, N.V., Khairutdinov, B.I., Grechkin, A.N., 2020. Lipoxygenase pathway in model bryophytes: 12-oxo-9(13),15-phytodienoic acid is a predominant oxylipin in Physcomitrella patens. Phytochemistry 180. https://doi.org/10.1016/j. phytochem.2020.112533, 112533.
  • Mukhtarova, L.S., Mukhitova, F.K., Gogolev, Y.V., Grechkin, A.N., 2011. Hydroperoxide lyase cascade in pea seedlings: non-volatile oxylipins and their age and stress dependent alterations. Phytochemistry 72, 356-364. https://doi.org/10.1016/j. phytochem.2011.01.013.
  • Nei, M., Kumar, S., 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York. https://doi.org/10.1016/S1055-7903(02)00247-6.
  • Nelson, D.R., 2011. Progress in tracing the evolutionary paths of cytochrome P450. Biochim. Biophys. Acta 1814, 14-18. https://doi.org/10.1016/j. bbapap.2010.08.008.
  • 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. 368, 20120474. https://doi.org/10.1098/rstb.2012.0474.
  • 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. https://doi.org/10.1016/j. phytochem.2015.08.003.
  • Ponce de Le´on, I., Hamberg, M., Castresana, C., 2015. Oxylipins in moss development and defense. Front. Plant Sci. 6, 483. https://doi.org/10.3389/fpls.2015.00483.
  • Pratiwi, P., Tanaka, G., Takahashi, T., Xie, X., Yoneyama, K., Matsuura, H., Takahashi, K., 2017. Identification of jasmonic acid and jasmonoyl-isoleucine, and characterization of AOS, AOC, OPR and JAR1 in the model lycophyte Selaginella moellendorffii. Plant Cell Physiol. 58, 789-801. https://doi.org/10.1093/pcp/ pcx031.
  • Pietryczuk, A., Czerpak, R., 2011. Effect of traumatic acid on antioxidant activity in Chlorella vulgaris (Chlorophyceae). Plant Growth Regul. 65, 279-286. https://doi. org/10.1007/s10725-011-9599-5.
  • Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M.J., Kift, N., Carbonne, F., Griffiths, G., Esquerre-Tugaye, M.-T., Rosahl, S., Castresana, C., Hamberg, M., Fournier, J., 2005. Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139, 1902-1913. https://doi.org/10.1104/pp.105.066274.
  • Rzhetsky, A., Nei, M., 1992. A simple method for estimating and testing minimum evolution trees. Mol. Biol. Evol. 9, 945-967. https://doi.org/10.1093/ oxfordjournals.molbev.a040771.
  • Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425. https://doi.org/10.1093/ oxfordjournals.molbev.a040454.
  • Scalschi, L., Sanmartin, M., Camanes t, G., Troncho, P., Sanchez-Serrano ´, J.J., Garcia-Agustin, P., Vicedo, B., 2015. Silencing of OPR3 in tomato reveals the role of OPDA in callose deposition during the activation of defense responses against Botrytis cinerea. Plant J. 81, 304-315. https://doi.org/10.1111/tpj.12728.
  • Schenkman, J.B., Jansson, I., 2006. Spectral analyses of cytochromes P450. Methods Mol. Biol. 320, 11-18. https://doi.org/10.1385/1-59259-998-2:11.
  • Schluttenhofer, C., 2020. Origin and evolution of jasmonate signaling. Plant Sci. 298 https://doi.org/10.1016/j.plantsci.2020.110542, 110542.
  • Scholz, J., Brodhun, F., Hornung, E., Herrfurth, C., Stumpe, M., Beike, A.K., Faltin, B., Frank, W., Reski, R., Feussner, I., 2012. Biosynthesis of allene oxides in Physcomitrella patens. BMC Plant Biol. 12, 228. https://doi.org/10.1186/1471-2229- 12-228.
  • Stumpe, M., Kandzia, R., G¨obel, C., Rosahl, S., Feussner, I., 2001. A pathogen-inducible divinyl ether synthase (CYP74D) from elicitor-treated potato suspension cells. FEBS Lett. 507, 371-376. https://doi.org/10.1016/s0014-5793(01)03019-8.
  • Stumpe, M., Bode, J., Gobel ¨, C., Wichard, T., Schaaf, A., Frank, W., Frank, M., Reski, R., Pohnert, G., Feussner, I., 2006. Biosynthesis of C9-aldehydes in the moss Physcomitrella patens. Biochim. Biophys. Acta 1761, 301-312. https://doi.org/ 10.1016/j.bbalip.2006.03.008.
  • Tijet, N., Brash, A.R., 2002. Allene oxide synthases and allene oxides. Prostag. Other Lipid Mediat. 68-69, 423-431. https://doi.org/10.1016/S0090-6980(02)00046-1.
  • 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. https://doi.org/10.1016/j.febslet.2008.09.005.
  • 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. https://doi.org/10.1016/j. febslet.2013.06.030.
  • 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. https://doi.org/10.1016/j.bbalip.2016.11.007.
  • 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, 1099-1109. https://doi.org/ 10.1016/j.bbalip.2017.07.015.
  • Toporkova, Y.Y., Smirnova, E.O., Gorina, S.S., Mukhtarova, L.S., Grechkin, A.N., 2018a. Detection of the first higher plant epoxyalcohol synthase: molecular cloning and characterisation of the CYP74M2 enzyme of spikemoss Selaginella moellendorffii. Phytochemistry 156, 73-82. https://doi.org/10.1016/j.phytochem.2018.08.010.
  • Toporkova, Y.Y., Gorina, S.S., Bessolitsyna, E.K., Smirnova, E.O., Fatykhova, V.S., Bruhlmann, F., Ilyina, T.M., Mukhtarova, L.S., Grechkin, A.N., 2018b. Double function hydroperoxide lyases/epoxyalcohol synthases (CYP74C) of higher plants: identification and conversion into allene oxide synthases by site-directed mutagenesis. Biochim. Biophys. Acta 1863, 369-378. https://doi.org/10.1016/j. bbalip.2018.01.002.
  • Toporkova, Y.Y., Smirnova, E.O., Mukhtarova, L.S., Gorina, S.S., Grechkin, A.N., 2020a. Catalysis by allene oxide synthases (CYP74A and CYP74C): alterations by the Phe/ Leu mutation at the SRS-1 region. Phytochemistry 169, 112152. https://doi.org/ 10.1016/j.phytochem.2019.112152.
  • Toporkova, Y.Y., Askarova, E.K., Gorina, S.S., Ogorodnikova, A.V., Mukhtarova, L.S., Grechkin, A.N., 2020b. Epoxyalcohol synthase activity of the CYP74B enzymes of higher plants. Biochim. Biophys. Acta 1865, 158743. https://doi.org/10.1016/j. bbalip.2020.158743.
  • Varsani, S., Grover, S., Zhou, S., Koch, K.G., Huang, P.C., Kolomiets, M.V., Williams, W. P., Heng-Moss, T., Sarath, G., Luthe, D.S., Jander, G., Louis, J., 2019. 12-Oxophytodienoic acid acts as a regulator of maize defense against corn leaf aphid. Plant Physiol. 179, 1402-1415. https://doi.org/10.1104/pp.18.01472.
  • Vick, B.A., Zimmerman, D.C., Weisleder, D., 1979. Thermal alteration of a cyclic fatty acid produced by a flaxseed extract. Lipids 14, 734-740. https://doi.org/10.1007/ BF02533899.
  • Weber, H., Chetelat, A., Caldelari, D., Farmer, E.E., 1999. Divinyl ether fatty acid synthesis in late blight-diseased potato leaves. Plant Cell 11, 485-493. https://doi. org/10.1105/tpc.11.3.485.
  • Weng, J.K., Akiyama, T., Ralph, J., Chapple, C., 2011. Independent recruitment of an Omethyltransferase for syringyl lignin biosynthesis in Selaginella moellendorffii. Plant Cell 23, 2708-2724. https://doi.org/10.1105/tpc.110.081547.
  • Weng, J.K., Banks, J.A., Chapple, C., 2008a. Parallels in lignin biosynthesis: a study in Selaginella moellendorffii reveals convergence across 400 million years of evolution. Commun. Integr. Biol. 1, 20-22. https://doi.org/10.4161/cib.1.1.6466.
  • Weng, J.K., Li, X., Stout, J., Chapple, C., 2008b. Independent origins of syringyl lignin in vascular plants. Proc. Natl. Acad. Sci. U.S.A. 105, 7887-7892. https://doi.org/ 10.1073/pnas.0801696105.
  • Wilson, R.A., Gardner, H.W., Keller, N.P., 2001. Cultivar-dependent expression of a maize lipoxygenase responsive to seed infesting fungi. Mol. Plant Microbe Iinteract. 14, 980-987. https://doi.org/10.1094/MPMI.2001.14.8.980.
  • Yokota, T., Ohnishi, T., Shibata, K., Asahina, M., Nomura, T., Fujita, T., Ishizaki, K., Kohchi, T., 2017. Occurrence of brassinosteroids in non-flowering land plants, liverwort, moss, lycophyte and fern. Phytochemistry 136, 46-55. https://doi.org/ 10.1016/j.phytochem.2016.12.020.
  • Yoneyama, K., Mori, N., Sato, T., Yoda, A., Xie, X., Okamoto, M., Iwanaga, M., Ohnishi, T., Nishiwaki, H., Asami, T., Yokota, T., Akiyama, K., Yoneyama, K., Nomura, T., 2018. Conversion of carlactone to carlactonoic acid is a conserved function of MAX1 homologs in strigolactone biosynthesis. New Phytol. 218 (4), 1522-1533. https://doi.org/10.1111/nph.15055.
  • 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.