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J. Biol. Chem., Vol. 282, Issue 47, 34013-34018, November 23, 2007

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Identification of a Biosynthetic Gene Cluster in Rice for Momilactones^*

Kazuhiro Shimura, Atsushi Okada, Kazunori Okada, Yusuke Jikumaru, Kwang-Wook Ko, Tomonobu Toyomasu, Takeshi Sassa, Morifumi Hasegawa^¶, Osamu Kodama^¶, Naoto Shibuya^||, Jinichiro Koga^**, Hideaki Nojiri, and Hisakazu Yamane¹

From the Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan, the Department of Bioresource Engineering, Yamagata University, Tsuruoka, Yamagata 997-8555, Japan, the ^¶College of Agriculture, Ibaraki University, 3-21-1 Chuo, Ami, Ibaraki 300-0393, Japan, the ^||Department of Life Science, Meiji University, Kawasaki, Kanagawa, 214-8571 Japan, and the ^**Food and Health Research and Development Laboratories, Meiji Seika Kaisha, Ltd., Sakado, Saitama 350-0289, Japan

Rice diterpenoid phytoalexins such as momilactones and phytocassanes are produced in suspension-cultured rice cells treated with a chitin oligosaccharide elicitor and in rice leaves irradiated with UV light. The common substrate geranylgeranyl diphosphate is converted into diterpene hydrocarbon precursors via a two-step sequential cyclization and then into the bioactive phytoalexins via several oxidation steps. It has been suggested that microsomal cytochrome P-450 monooxygenases (P-450s) are involved in the downstream oxidation of the diterpene hydrocarbons leading to the phytoalexins and that a dehydrogenase is involved in momilactone biosynthesis. However, none of the enzymes involved in the downstream oxidation of the diterpene hydrocarbons have been identified. In this study, we found that a putative dehydrogenase gene (AK103462) and two functionally unknown P-450 genes (CYP99A2 and CYP99A3) form a chitin oligosaccharide elicitor- and UV-inducible gene cluster, together with OsKS4 and OsCyc1, the diterpene cyclase genes involved in momilactone biosynthesis. Functional analysis by heterologous expression in Escherichia coli followed by enzyme assays demonstrated that the AK103462 protein catalyzes the conversion of 3-hydroxy-9H-pimara-7,15-dien-19,6-olide into momilactone A. The double knockdown of CYP99A2 and CYP99A3 specifically suppressed the elicitor-inducible production of momilactones, strongly suggesting that CYP99A2, CYP99A3, or both are involved in momilactone biosynthesis. These results provide strong evidence for the presence on chromosome 4 of a gene cluster involved in momilactone biosynthesis.

Received for publication, April 23, 2007 , and in revised form, September 14, 2007.

^* This work was supported in part by Grants-in-Aid for Scientific Research 16208012 and 18580102 from the Japanese Society for the Promotion of Science and by the Program for Promotion of Basic Research Activities for Innovative Biosciences. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed. Fax: 81-3-5841-8030; E-mail: ayamane{at}mail.ecc.u-tokyo.ac.jp.

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