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Formation of Two Methylenedioxy Bridges by a Sesamum CYP81Q Protein Yielding a Furofuran Lignan, (+)-Sesamin

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Formation of Two Methylenedioxy Bridges by a Sesamum CYP81Q Protein Yielding a Furofuran Lignan, (+)-Sesamin Formation of two methylenedioxy bridges by a Sesamum CYP81Q protein yielding a furofuran lignan, (؉)-sesamin Eiichiro Ono*†, Masaaki Nakai‡, Yuko Fukui‡, Namino Tomimori‡, Masako Fukuchi-Mizutani*, Masayuki Saito*, Honoo Satake§, Takaharu Tanaka*§, Masumi Katsuta¶, Toshiaki Umezawaʈ, and Yoshikazu Tanaka* Institutes for *Advanced Technology, ‡Healthcare Science, and §Bioorganic Research, Suntory, 1-1-1 Wakayamadai, Shimamoto-cho, Mishima, Osaka 618-8503, Japan; ¶Department of Field Crop Research, National Institute of Crop Science, 2-1-18 Kan-non dai, Tsukuba, Ibaragi 305-8518, Japan; and ʈResearch Institute for Sustainable Humanosphere, Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan Communicated by Takayoshi Higuchi, Kyoto University, Kyoto, Japan, May 11, 2006 (received for review March 10, 2006) ؉)-Sesamin, a furofuran class lignan, is widespread in vascular of achiral E-coniferyl alcohol (Fig. 1A) (19–21). (ϩ)-Piperitol is) plants and represented by Sesamum spp. (؉)-Sesamin has been of synthesized from it by formation of a methylenedioxy bridge rapidly growing interest because of its beneficial biological effects (22), and (ϩ)-sesamin also is synthesized from (ϩ)-piperitol by in mammals, but its biosynthesis and physiological roles in plants formation of such a bridge (23). These two stepwise methyl- remain to be clarified. It is speculated to be synthesized from enedioxy bridge formations were postulated to be catalyzed by (؉)-pinoresinol by means of (؉)-piperitol by formation of two two consecutively acting S. indicum cytochrome P450 (SiP450) methylenedioxy bridges mediated by two distinct Sesamum indi- enzymes, piperitol synthase (PS) and sesamin synthase (SS), cum cytochrome P450 (SiP450) proteins. Here, we report an SiP450, because only PS activity was observed in sesame seed micro- CYP81Q1, that alone catalyzes (؉)-sesamin biosynthesis from (؉)- somes, and the methylenedioxy bridge formation was inhibited .(pinoresinol by means of (؉)-piperitol by forming two methyl- by various cytochrome P450 enzyme inhibitors (22) (Fig. 1A enedioxy bridges. The CYP81Q1 gene expression profile was tem- In alkaloid biosynthesis, methylenedioxy bridge formations porally consistent with the accumulation pattern of (؉)-sesamin have for the first time been known to be cytochrome P450- during seed development. The CYP81Q1-GFP chimera protein was dependent (24, 25). Eventually, CYP719A1 was identified from colocalized with an endoplasmic reticulum (ER)-targeting chimera Coptis japonica as the first methylenedioxy bridge-forming P450 protein, indicating that (؉)-sesamin biosynthesis occurs on the ER involved in isoquinoline alkaloid biosynthesis (26). This finding cytoplasmic surface. Moreover, we isolated two CYP81Q1 ho- suggested that SiP450s, which belong to the CYP719A subfamily, mologs from other Sesamum spp. Sesamum radiatum CYP81Q2 are involved in (ϩ)-sesamin biosynthetic methylenedioxy bridge showed dual (؉)-piperitol͞(؉)-sesamin synthetic activity. formations. Since then, SiP450 genes have been identified by CYP81Q2, as well as CYP81Q1, therefore, corresponds to a (؉)- comparative EST analysis of sesame seeds, but their functions .(piperitol͞(؉)-sesamin synthase in lignan biosynthesis. In contrast, have yet to be examined (27 Sesamum alatum CYP81Q3 showed no activity, in accord with To clarify the underlying mechanism of (ϩ)-sesamin biosyn- ؉)-sesamin being deficient in S. alatum. Our findings not only thesis, we comprehensively investigated the SiP450 genes that) provide insight into lignan biosynthesis but also unravel a unique are responsible for SS. Interestingly, we identified a previously mode of cytochrome P450 action. uncharacterized SiP450, CYP81Q1, which serves both (ϩ)- sesamin and (ϩ)-piperitol by formation of methylenedioxy P450 ͉ Sesamum indicum ͉ pinoresinol ͉ piperitol bridges on (ϩ)-piperitol and (ϩ)-pinoresinol, respectively. Namely, CYP81Q1 corresponds to a (ϩ)-piperitol͞(ϩ)-sesamin esame (Pedaliaceae, Sesamum indicum L.), a major oil seed synthase (PSS). Unexpectedly, CYP81Q1 has only 24% amino crop of high nutritional value, is widely cultivated throughout acid sequence identity to CYP719A1. We also identified a S functional homolog of CYP81Q1 in Sesamum radiatum,evi- the world. Sesame oil, Ϸ50% of seed weight, contains large dence that this methylenedioxy bridge-forming enzyme is struc- amounts of natural antioxidants (1, 2). The potent antioxidant turally and functionally conserved in the Sesamum genus. Our properties of sesame seed extract mainly are attributable to the findings provide the biochemical and genetic tools to produce a presence of lignans (3). Lignans are phenylpropanoid dimers in beneficial natural product, (ϩ)-sesamin. which phenylpropane units are linked by the central carbons of the side chains, and they constitute an abundant class of phe- Results nylpropanoids (4). They are widely distributed in vascular plants. Sesame Lignans Are Synthesized Specifically in the Later Phase of (ϩ)-Sesamin, first isolated in 1890, is a major furofuran lignan Seed Development. Lignan mixtures extracted from S. indicum in sesame seeds and is distinguished by two characteristic seeds at six developmental stages, germinating seeds, and leaves methylenedioxy bridges (2) (Fig. 1A). It has a growth-retarding were analyzed by HPLC (Fig. 1B). (ϩ)-Sesamin, detected first at effect on some plants, as well as a synergistic effect with stage 4, reached a maximum at stage 5 and then was slightly pyretherum insecticides (5, 6). (ϩ)-Sesamin has been shown to decreased at stage 6 in fully matured seeds (Fig. 1C). On have a wide range of biological effects: protection against germination, (ϩ)-sesamin content markedly was decreased, in- ethanol- and carbon tetrachloride-induced liver damage (7, 8), improvement of fatty acid metabolism (9–11), antiinflammatory effects (12), increased vitamin E activities (13, 14), inhibition of Conflict of interest statement: No conflicts declared. vascular superoxide production (15, 16), and induction of nitric Abbreviations: SiP450, Sesamum indicum cytochrome P450; RT, retention time; PSS, (ϩ)- oxide (17). Therefore, it is an extremely interesting natural piperitol͞(ϩ)-sesamin synthase; PS, piperitol synthase; SS, sesamin synthase. compound from the viewpoint of health care (18). Data deposition: The sequences reported in this paper have been deposited in the DNA The (ϩ)-sesamin biosynthetic pathway has been deduced from Databank of Japan database [accession nos. AB194714 (CYP81Q1), AB194715 (CYP81Q2), results of radioisotope tracer and enzymatic experiments (19). and AB194716 (CYP81Q3)]. (ϩ)-Pinoresinol, the first lignan in the lignan pathway, is syn- †To whom correspondence should be addressed. E-mail: eiichiro࿝[email protected]. thesized by stereoselective phenoxy radical coupling of two units © 2006 by The National Academy of Sciences of the USA 10116–10121 ͉ PNAS ͉ June 27, 2006 ͉ vol. 103 ͉ no. 26 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0603865103 Downloaded by guest on September 25, 2021 Fig. 2. Gene expression analyses by RT-PCR. Temporal CYP81Q1 expression patterns during seed development (A) and in aerial organs (B). C3H is S. indicum p-coumarate 3-hydroxylase (CYP98A20) expressed in phenylpro- panoid biosynthesis (29). ger, germinating seeds treated with H2O for 2 days; l, leaves; p, petals; st, stems; sp, seed pods. in the later phases of seed development (Fig. 1C). Consequently, a cDNA library was constructed from seeds in stages 4–5 and screened with probe mixtures of 13 Arabidopsis cytochrome P450 genes. To obtain various SiP450 genes, these probes were selected from different P450 subfamilies. One hundred ninety- two positive clones were obtained after a second screening and clustered finally in 17 independent molecular species of SiP450. To further screen these candidate SiP450 genes, their expression patterns were examined by RT-PCR. One candidate SiP450, SiP189, had an expression profile consistent with the develop- mental accumulation pattern of (ϩ)-sesamin. Its expression began at stage 3, reached a maximum at stage 4, and then decreased before seed maturation was complete (Figs. 1C and 2A). It also was expressed in leaves but not in germinating seeds, petals, or stems, whereas the S. indicum p-coumarate 3-hydrox- ylase (C3H, CYP98A20) gene, which is involved in phenylpro- panoid pathway, was expressed ubiquitously (Fig. 2B) (29). SiP189 bears an ORF of 1,518 bp for 506 aa (Fig. 3B). It has 52%, 49%, and 24% amino acid sequence identity, respectively, to a functionally unknown Arabidopsis P450, CYP81D2 (NM 119899); Glycyrrhiza CYP81E1, catalyzing a 2Ј hydroxylation of isoflavone (30); and Coptis CYP719A1 (26) (Fig. 3 A and C). The SiP189 gene has a single 171-bp intron 898 bp downstream from the start codon, whereas the CYP81D2 gene has two introns in its genomic structure (Fig. 3B). Southern blot analysis showed Fig. 1. Developmental regulation of lignan biosynthesis. (A) Lignan struc- that the SiP189 gene exists as a single gene in the S. indicum tures in Sesamum spp. (B) Sesame seed development. Numbers correspond to genome (Fig. 3C). SiP189 has been designated CYP81Q1 by the developmental seed stages. (Scale bars: Upper, 1 cm; Lower, 2 mm.) (C) P450 nomenclature committee. It has conserved regions in Developmental accumulation changes in five sesame lignans determined by cytochrome P450 proteins (Fig. 6, which is published as sup- HPLC after treatment with ␤-glucosidase. ND, not detected. porting information on the PNAS web site), a helix K region, an PLANT BIOLOGY
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