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Specialized diterpenoid metabolism in monocot crops: Biosynthesis and chemical diversity

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  • 1. ∗ & Department of Plant Biology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA

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Murphy, Katherine M., Zerbe, Philipp (2020): Specialized diterpenoid metabolism in monocot crops: Biosynthesis and chemical diversity. Phytochemistry (112289) 172: 1-11, DOI: 10.1016/j.phytochem.2020.112289, URL: http://dx.doi.org/10.1016/j.phytochem.2020.112289

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urn:lsid:plazi.org:pub:2C13C9063405F741FFB1FF86FFDDFFAE

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Publication: 10.3389/fpls.2019.01166 (DOI)
Has part
Figure: 10.5281/zenodo.8294192 (DOI)
Figure: 10.5281/zenodo.8294194 (DOI)
Figure: 10.5281/zenodo.8294196 (DOI)
Figure: 10.5281/zenodo.8294198 (DOI)
Figure: 10.5281/zenodo.8294200 (DOI)

References

  • Alamgir, K.M., Hojo, Y., Christeller, J.T., Fukumoto, K., Isshiki, R., Shinya, T., Baldwin, I.T., Galis, I., 2016. Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory. Plant Cell Environ. 39, 453-466.
  • Atawong, A., Hasegawa, M., Kodama, O., 2002. Biosynthesis of rice phytoalexin: enzymatic conversion of 3beta-hydroxy-9beta-pimara-7,15-dien-19,6beta-olide to momilactone A. Biosci. Biotechnol. Biochem. 66, 566-570.
  • Banerjee, A., Hamberger, B., 2018. P450s controlling metabolic bifurcations in plant terpene specialized metabolism. Phytochemistry Rev. 17, 81-111.
  • Bathe, U., Tissier, A., 2019. Cytochrome P450 enzymes: a driving force of plant diterpene diversity. Phytochemistry 161, 149-162.
  • Bensen, R.J., Johal, G.S., Crane, V.C., Tossberg, J.T., Schnable, P.S., Meeley, R.B., Briggs, S.P., 1995. Cloning and characterization of the maize An1 gene. Plant Cell 7, 75-84.
  • Block, A.K., Vaughan, M.M., Schmelz, E.A., Christensen, S.A., 2019. Biosynthesis and function of terpenoid defense compounds in maize (Zea mays). Planta 249, 21-30.
  • Boutanaev, A.M., Moses, T., Zi, J., Nelson, D.R., Mugford, S.T., Peters, R.J., Osbourn, A., 2015. Investigation of terpene diversification across multiple sequenced plant genomes. Proc. Natl. Acad. Sci. U.S.A. 112, E81-E88.
  • Celedon, J.M., Bohlmann, J., 2019. Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. New Phytol. 224, 1444-1463.
  • Chakraborty, S., Newton, A.C., 2011. Climate change, plant diseases and food security: an overview. Plant Pathol. 60, 2-14.
  • 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.
  • Christensen, S.A., Huffaker, A., Kaplan, F., Sims, J., Ziemann, S., Doehlemann, G., Ji, L., Schmitz, R.J., Kolomiets, M.V., Alborn, H.T., Mori, N., Jander, G., Ni, X., Sartor, R.C., Byers, S., Abdo, Z., Schmelz, E.A., 2015. Maize death acids, 9-lipoxygenase-derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators. Proc. Natl. Acad. Sci. U.S.A. 112, 11407-11412.
  • Christensen, S.A., Sims, J., Vaughan, M.M., Hunter, C., Block, A., Willett, D., Alborn, H.T., Huffaker, A., Schmelz, E.A., 2018. Commercial hybrids and mutant genotypes reveal complex protective roles for inducible terpenoid defenses in maize. J. Exp. Bot. 69, 1693-1705.
  • Crop Protection Network, 2017. Corn disease loss estimates for the United States and Ontario, Canada - 2017. https://crop-protection-network.s3.amazonaws.com/ publications/cpn-2007-17-corn-disease-loss-estimates-2017.pdf, Accessed date: 22 October 2019.
  • Dafoe, N.J., Huffaker, A., Vaughan, M.M., Duehl, A.J., Teal, P.E., Schmelz, E.A., 2011. Rapidly induced chemical defenses in maize stems and their effects on short- term growth of Ostrinia nubilalis. J. Chem. Ecol. 37, 984-991.
  • Davis, E.M., Croteau, R., 2000. Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. In: Biosynthesis: Aromatic Polyketides, Isoprenoids, Alkaloids. Springer, pp. 53-95.
  • de Bruijn, W.J.C., Gruppen, H., Vincken, J.P., 2018. Structure and biosynthesis of benzoxazinoids: plant defence metabolites with potential as antimicrobial scaffolds. Phytochemistry 155, 233-243.
  • de Sassi, C., Tylianakis, J.M., 2012. Climate change disproportionately increases herbivore over plant or parasitoid biomass. PLoS One 7, e40557.
  • Ding, Y., Huffaker, A., Kollner, T.G., Weckwerth, P., Robert, C.A.M., Spencer, J.L., Lipka, A.E., Schmelz, E.A., 2017. Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol. 175, 1455-1468.
  • Ding, Y., Murphy, K.M., Poretsky, E., Mafu, S., Yang, B., Char, S.N., Christensen, S.A., Saldivar, E., Wu, M., Wang, Q., Ji, L., Schmitz, R.J., Kremling, K.A., Buckler, E.S., Shen, Z., Briggs, S.P., Bohlmann, J., Sher, A., Castro-Falcon, G., Hughes, C.C., Huffaker, A., Zerbe, P., Schmelz, E.A., 2019. Multiple genes recruited from hormone pathways partition maize diterpenoid defences. Native Plants 5, 1043-1056.
  • Food and Agriculture Organization of the United Nations, 2009. FAO's director-general on how to feed the world in 2050. Popul. Dev. Rev. 35, 837-839.
  • Fu, J., Ren, F., Lu, X., Mao, H., Xu, M., Degenhardt, J., Peters, R.J., Wang, Q., 2016. A tandem array of ent -kaurene synthases in maize with roles in gibberellin and more specialized metabolism. Plant Physiol. 170, 742-751.
  • Gershenzon, J., Dudareva, N., 2007. The function of terpene natural products in the natural world. Nat. Chem. Biol. 3, 408-414.
  • Gomi, K., Satoh, M., Ozawa, R., Shinonaga, Y., Sanada, S., Sasaki, K., Matsumura, M., Ohashi, Y., Kanno, H., Akimitsu, K., Takabayashi, J., 2010. Role of hydroperoxide lyase in white- backed planthopper (Sogatella furcifera Horvath)-induced resistance to bacterial blight in rice, Oryza sativa L. Plant J. 61, 46-57.
  • Hammerbacher, A., Coutinho, T.A., Gershenzon, J., 2019. Roles of plant volatiles in defence against microbial pathogens and microbial exploitation of volatiles. Plant Cell Environ. 42, 2827-2843.
  • Harris, L.J., Saparno, A., Johnston, A., Prisic, S., Xu, M., Allard, S., Kathiresan, A., Ouellet, T., Peters, R.J., 2005. The maize An2 gene is induced by Fusarium attack and encodes an ent -copalyl diphosphate synthase. Plant Mol. Biol. 59, 881-894.
  • Hasegawa, M., Mitsuhara, I., Seo, S., Imai, T., Koga, J., Okada, K., Yamane, H., Ohashi, Y., 2010. Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol. Plant Microbe Interact. 23, 1000-1011.
  • Hemmerlin, A., Hoeffler, J.F., Meyer, O., Tritsch, D., Kagan, I.A., Grosdemange-Billiard, C., Rohmer, M., Bach, T.J., 2003. Cross-talk between the cytosolic mevalonate and the plastidial methyl erythritol phosphate pathways in Tobacco Bright Yellow-2 cells. J. Biol. Chem. 278, 26666-26676.
  • Horie, K., Inoue, Y., Sakai, M., Yao, Q., Tanimoto, Y., Koga, J., Toshima, H., Hasegawa, M., 2015. Identification of UV-induced diterpenes including a new diterpene phytoalexin, phytocassane F, from rice leaves by complementary GC/MS and LC/MS approaches. J. Agric. Food Chem. 63, 4050-4059.
  • Huffaker, A., Kaplan, F., Vaughan, M.M., Dafoe, N.J., Ni, X., Rocca, J.R., Alborn, H.T., Teal, P.E., Schmelz, E.A., 2011. Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol. 156, 2082-2097.
  • Jia, M., Potter, K.C., Peters, R.J., 2016. Extreme promiscuity of a bacterial and a plant diterpene synthase enables combinatorial biosynthesis. Metab. Eng. 37, 24-34.
  • Kanno, Y., Otomo, K., Kenmoku, H., Mitsuhashi, W., Yamane, H., Oikawa, H., Toshima, H., Matsuoka, M., Sassa, T., Toyomasu, T., 2006. Characterization of a rice gene family encoding type-A diterpene cyclases. Biosci. Biotechnol. Biochem. 70, 1702-1710.
  • Kanno, H., Hasegawa, M., Kodama, O., 2012. Accumulation of salicylic acid, jasmonic acid and phytoalexins in rice, Oryza sativa, infested by the white- backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Appl. Entomol. Zool. 47, 27-34.
  • Karunanithi, P.S., Zerbe, P., 2019. Terpene synthases as metabolic gatekeepers in the evolution of plant terpenoid chemical diversity. Front. Plant Sci. https://doi.org/10. 3389/fpls.2019.01166.
  • Kato-Noguchi, H., Ino, T., 2003. Rice seedlings release momilactone B into the environment. Phytochemistry 63, 551-554.
  • Kato-Noguchi, H., Peters, R.J., 2013. The role of momilactones in rice allelopathy. J. Chem. Ecol. 39, 175-185.
  • Kato-Noguchi, H., Kujime, H., Ino, T., 2007. UV-induced momilactone B accumulation in rice rhizosphere. J. Plant Physiol. 164, 1548-1551.
  • Kato-Noguchi, H., Hasegawa, M., Ino, T., Ota, K., Kujime, H., 2010. Contribution of momilactone A and B to rice allelopathy. J. Plant Physiol. 167, 787-791.
  • Kitaoka, N., Wu, Y., Zi, J., Peters, R.J., 2016. Investigating inducible short-chain alcohol dehydrogenases/reductases clarifies rice oryzalexin biosynthesis. Plant J. 88, 271-279.
  • Ko, K.W., Lin, F., Katsumata, T., Sugai, Y., Miyazaki, S., Kawaide, H., Okada, K., Nojiri, H., Yamane, H., 2008. Functional identification of a rice ent -kaurene oxidase, OsKO2, using the Pichia pastoris expression system. Biosci. Biotechnol. Biochem. 72, 3285-3288.
  • Koga, J., Shimura, M., Oshima, K., Ogawa, N., Yamauchi, T., Ogasawara, N., 1995. Phytocassanes A, B, C, and D, novel diterpene phytoalexins from rice, Oryza sativa L. Tetrahedron 51, 7907-7918.
  • Koga, J., Ogawa, N., Yamauchi, T., Kikuchi, M., Ogasawara, N., Shimura, M., 1997. Functional moiety for the antifungal activity of phytocassane E, a diterpene phytoalexin from rice. Phytochemistry 44, 249-253.
  • Kollner, T.G., Schnee, C., Gershenzon, J., Degenhardt, J., 2004. The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16, 1115-1131.
  • Kollner, T.G., Held, M., Lenk, C., Hiltpold, I., Turlings, T.C., Gershenzon, J., Degenhardt, J., 2008a. A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20, 482-494.
  • Kollner, T.G., Schnee, C., Li, S., Svatos, A., Schneider, B., Gershenzon, J., Degenhardt, J., 2008b. Protonation of a neutral (S)-beta-bisabolene intermediate is involved in (S)- beta-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J. Biol. Chem. 283, 20779-20788.
  • Kono, Y., Kojima, A., Nagai, R., Watanabe, M., Kawashima, T., Onizawa, T., Teraoka, T., Watanab, M., Koshino, H., Uzawa, J., Suzuki, Y., Sakurai, A., 2004. Antibacterial diterpenes and their fatty acid conjugates from rice leaves. Phytochemistry 65, 1291-1298.
  • Laule, O., Furholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., Lange, M., 2003. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 100, 6866-6871.
  • Lenk, C., Kollner, T.G., Erb, M., Degenhardt, J., 2012. Two enzymes responsible for the formation of herbivore-induced volatiles of maize, the methyltransferase AAMT1 and the terpene synthase TPS23, are regulated by a similar signal transduction pathway. Entomol. Exp. Appl. 144, 86-92.
  • Liang, X.Z., Wu, Y., Chambers, R.G., Schmoldt, D.L., Gao, W., Liu, C., Liu, Y.A., Sun, C., Kennedy, J.A., 2017. Determining climate effects on US total agricultural productivity. Proc. Natl. Acad. Sci. U.S.A. 114, E2285-E2292.
  • Liu, M., Lu, S., 2016. Plastoquinone and ubiquinone in plants: biosynthesis, physiological function and metabolic engineering. Front. Plant Sci. 7, 1898.
  • Lu, X., Zhang, J., Brown, B., Li, R., Rodriguez-Romero, J., Berasategui, A., Liu, B., Xu, M., Luo, D., Pan, Z., Baerson, S., Gershenzon, J., Li, Z., Sesma, A., Yang, B., Peters, R.J., 2018. Inferring roles in defense from metabolic allocation of rice diterpenoids. Plant Cell 30, 1119-1131.
  • Mafu, S., Ding, Y., Murphy, K.M., Yaacoobi, O., Addison, J.B., Wang, Q., Shen, Z., Briggs, S.P., Bohlmann, J., Castro-Falcon, G., Hughes, C.C., Betsiashvili, M., Huffaker, A., Schmelz, E.A., Zerbe, P., 2018. Discovery, biosynthesis and stress-related accumulation of dolabradiene-derived defenses in maize. Plant Physiol. 176, 2677-2690.
  • Mao, H., Liu, J., Ren, F., Peters, R.J., Wang, Q., 2016. Characterization of CYP71Z18 indicates a role in maize zealexin biosynthesis. Phytochemistry 121, 4-10.
  • Miyamoto, K., Fujita, M., Shenton, M.R., Akashi, S., Sugawara, C., Sakai, A., Horie, K., Hasegawa, M., Kawaide, H., Mitsuhashi, W., Nojiri, H., Yamane, H., Kurata, N., Okada, K., Toyomasu, T., 2016. Evolutionary trajectory of phytoalexin biosynthetic gene clusters in rice. Plant J. 87, 293-304.
  • Morrone, D., Jin, Y., Xu, M., Choi, S.Y., Coates, R.M., Peters, R.J., 2006. An unexpected diterpene cyclase from rice: functional identification of a stemodene synthase. Arch. Biochem. Biophys. 448, 133-140.
  • Morrone, D., Chen, X., Coates, R.M., Peters, R.J., 2010. Characterization of the kaurene oxidase CYP701A3, a multifunctional cytochrome P450 from gibberellin biosynthesis. Biochem. J. 431, 337-344.
  • Morrone, D., Hillwig, M.L., Mead, M.E., Lowry, L., Fulton, D.B., Peters, R.J., 2011. Evident and latent plasticity across the rice diterpene synthase family with potential implications for the evolution of diterpenoid metabolism in the cereals. Biochem. J. 435, 589-595.
  • Mullet, J., Morishige, D., McCormick, R., Truong, S., Hilley, J., McKinley, B., Anderson, R., Olson, S.N., Rooney, W., 2014. Energy sorghum-a genetic model for the design of C4 grass bioenergy crops. J. Exp. Bot. 65, 3479-3489.
  • Murphy, K.M., Ma, L.T., Ding, Y., Schmelz, E.A., Zerbe, P., 2018. Functional characterization of two class II diterpene synthases indicates additional specialized diterpenoid pathways in maize (Zea mays). Front. Plant Sci. 9, 1542.
  • Nelson, D., Werck-Reichhart, D., 2011. A P450-centric view of plant evolution. Plant J. 66, 194-211.
  • Nemoto, T., Cho, E.M., Okada, A., Okada, K., Otomo, K., Kanno, Y., Toyomasu, T., Mitsuhashi, W., Sassa, T., Minami, E., Shibuya, N., Nishiyama, M., Nojiri, H., Yamane, H., 2004. Stemar-13-ene synthase, a diterpene cyclase involved in the biosynthesis of the phytoalexin oryzalexin S in rice. FEBS Lett. 571, 182-186.
  • Oerke, E.C., 2006. Crop losses to pests. J. Agric. Sci. 144, 31-43.
  • Otomo, K., Kenmoku, H., Oikawa, H., Konig, W.A., Toshima, H., Mitsuhashi, W., Yamane, H., Sassa, T., Toyomasu, T., 2004. Biological functions of ent - and syn -copalyl diphosphate synthases in rice: key enzymes for the branch point of gibberellin and phytoalexin biosynthesis. Plant J. 39, 886-893.
  • Park, H.L., Lee, S.W., Jung, K.H., Hahn, T.R., Cho, M.H., 2013. Transcriptomic analysis of UV-treated rice leaves reveals UV-induced phytoalexin biosynthetic pathways and their regulatory networks in rice. Phytochemistry 96, 57-71.
  • Pelot, K.A., Chen, R., Hagelthorn, D.M., Young, C.A., Addison, J.B., Muchlinski, A., Tholl, D., Zerbe, P., 2018. Functional diversity of diterpene synthases in the biofuel crop switchgrass. Plant Physiol. 178, 54-71.
  • Peters, R.J., 2006. Uncovering the complex metabolic network underlying diterpenoid phytoalexin biosynthesis in rice and other cereal crop plants. Phytochemistry 67, 2307-2317.
  • Peters, R.J., 2010. Two rings in them all: the labdane-related diterpenoids. Nat. Prod. Rep. 27, 1521-1530.
  • Prisic, S., Xu, M., Wilderman, P.R., Peters, R.J., 2004. Rice contains two disparate ent - copalyl diphosphate synthases with distinct metabolic functions. Plant Physiol. 136, 4228-4236.
  • Quan, N.V., Tran, H.D., Xuan, T.D., Ahmad, A., Dat, T.D., Khanh, T.D., Teschke, R., 2019. Momilactones A and B are alpha-amylase and alpha-glucosidase inhibitors. Molecules 24, E482.
  • Ray, D.K., Ramankutty, N., Mueller, N.D., West, P.C., Foley, J.A., 2012. Recent patterns of crop yield growth and stagnation. Nat. Commun. 3, 1293.
  • Ray, D.K., Mueller, N.D., West, P.C., Foley, J.A., 2013. Yield trends are insufficient to double global crop production by 2050. PLoS One 8, e66428.
  • Ray, D.K., Gerber, J.S., MacDonald, G.K., West, P.C., 2015. Climate variation explains a third of global crop yield variability. Nat. Commun. 6, 5989.
  • Ren, Y.Y., West, C.A., 1992. Elicitation of diterpene biosynthesis in rice (Oryza sativa L.) by chitin. Plant Physiol. 99, 1169-1178.
  • Sakamoto, T., Miura, K., Itoh, H., Tatsumi, T., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Agrawal, G.K., Takeda, S., Abe, K., Miyao, A., Hirochika, H., Kitano, H., Ashikari, M., Matsuoka, M., 2004. An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134, 1642-1653.
  • Salazar-Cerezo, S., Martinez-Montiel, N., Garcia-Sanchez, J., Perez, Y.T.R., Martinez- Contreras, R.D., 2018. Gibberellin biosynthesis and metabolism: a convergent route for plants, fungi and bacteria. Microbiol. Res. 208, 85-98.
  • Savary, S., Willocquet, L., Pethybridge, S.J., Esker, P., McRoberts, N., Nelson, A., 2019. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430-439.
  • Schmelz, E.A., Kaplan, F., Huffaker, A., Dafoe, N.J., Vaughan, M.M., Ni, X., Rocca, J.R., Alborn, H.T., Teal, P.E., 2011. Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc. Natl. Acad. Sci. U.S.A. 108, 5455-5460.
  • Schmelz, E.A., Huffaker, A., Sims, J.W., Christensen, S.A., Lu, X., Okada, K., Peters, R.J., 2014. Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins. Plant J. 79, 659-678.
  • Schnee, C., Kollner, T.G., Gershenzon, J., Degenhardt, J., 2002. The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-betafarnesene, (E)-nerolidol, and (E,E)-farnesol after herbivore damage. Plant Physiol. 130, 2049-2060.
  • Schnee, C., Ko llner, T.G., Held, M., Turlings, T.C., Gershenzon, J., Degenhardt, J., 2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc. Natl. Acad. Sci. U.S.A. 103, 1129-1134.
  • Sesma, A., Osbourn, A.E., 2004. The rice leaf blast pathogen undergoes developmental processes typical of root- infecting fungi. Nature 431, 582-586.
  • Shen, Q., Pu, Q., Liang, J., Mao, H., Liu, J., Wang, Q., 2019. CYP71Z18 overexpression confers elevated blast resistance in transgenic rice. Plant Mol. Biol. 100, 579-589.
  • Shimura, K., Okada, A., Okada, K., Jikumaru, Y., Ko, K.W., Toyomasu, T., Sassa, T., Hasegawa, M., Kodama, O., Shibuya, N., Koga, J., Nojiri, H., Yamane, H., 2007. Identification of a biosynthetic gene cluster in rice for momilactones. J. Biol. Chem. 282, 34013-34018.
  • Spielmeyer, W., Ellis, M., Robertson, M., Ali, S., Lenton, J.R., Chandler, P.M., 2004. Isolation of gibberellin metabolic pathway genes from barley and comparative mapping in barley, wheat and rice. Theor. Appl. Genet. 109, 847-855.
  • Swaminathan, S., Morrone, D., Wang, Q., Fulton, D.B., Peters, R.J., 2009. CYP76M7 is an ent -cassadiene C11alpha-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice. Plant Cell 21, 3315-3325.
  • Tholl, D., 2015. Biosynthesis and biological functions of terpenoids in plants. Adv. Biochem. Eng. Biotechnol. 148, 63-106.
  • Tilman, D., Balzer, C., Hill, J., Befort, B.L., 2011. Global food demand and the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. U.S.A. 108, 20260-20264.
  • Toyomasu, T., Kagahara, T., Okada, K., Koga, J., Hasegawa, M., Mitsuhashi, W., Sassa, T., Yamane, H., 2008. Diterpene phytoalexins are biosynthesized in and exuded from the roots of rice seedlings. Biosci. Biotechnol. Biochem. 72, 562-567.
  • Toyomasu, T., Usui, M., Sugawara, C., Otomo, K., Hirose, Y., Miyao, A., Hirochika, H., Okada, K., Shimizu, T., Koga, J., Hasegawa, M., Chuba, M., Kawana, Y., Kuroda, M., Minami, E., Mitsuhashi, W., Yamane, H., 2014. Reverse-genetic approach to verify physiological roles of rice phytoalexins: characterization of a knockdown mutant of