Evaluation of Plant Growth Regulatory Activity of Furofuran Lignan

May 8, 2015 - KEYWORDS: lignan, furofuran lignan, 7,9′:7′,9-diepoxylignan, sesamin, sesamolin, plant growth regulatory activity. □ INTRODUCTION...
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Evaluation of Plant Growth Regulatory Activity of Furofuran Lignan Bearing a 7,9′:7′,9-Diepoxy Structure Using Optically Pure (+)- and (−)-Enantiomers Satoshi Yamauchi,*,†,§ Hiroaki Ichikawa,† Hisashi Nishiwaki,† and Yoshihiro Shuto† †

Faculty of Agriculture, Ehime University, 3-5-7 Tarumi, Matsuyama, Ehime 790-8566, Japan South Ehime Fisheries Research Center, 1289-1 Funakoshi, Ainan, Ehime 798-4292, Japan

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ABSTRACT: The plant growth regulatory activity of furofuran lignan (7,9′:7′,9-diepoxylignan) was evaluated by employing optically pure synthesized (+)- and (−)-enantiomers. (+)-Sesamin possessing a 3,4-methylenedioxy group on the aromatic rings and 7-aryl structure showed growth promotion activity against lettuce roots (EC50 = 0.50 mM); on the other hand, growth inhibitory activity was observed against lettuce shoots (EC50 = 0.38 mM). Against ryegrass shoots, (−)-sesamolin, which has 3,4methylenedioxy groups on the aromatic rings and a 7-acetal structure, was effective in showing growth inhibitory activity (EC50 = 0.23 mM). Different activity levels were observed between (+)- and (−)-enantiomers. It was assumed that the 3,4methylenedioxy group on the aromatic ring was more potent for the plant growth regulatory activity. KEYWORDS: lignan, furofuran lignan, 7,9′:7′,9-diepoxylignan, sesamin, sesamolin, plant growth regulatory activity

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4.6 mm i.d., 5 μm, CHIRALCEL AD-H and OD-H (DAICEL Chemical Industries, Ltd., Tokyo, Japan). Furofuran lignans, 1−14, were synthesized by employing a previously described method14−16 with modification. (+)-Pinoresinol, 1: NMR data agreed with those in the literature;17 [α]D25 +67 (c 0.2, CHCl3), [α]D22 +63 (c 1.2, CHCl3) in the literature;18 tR 51.3 min (OD-H, hexane/isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 276 nm); >99% ee. (−)-Pinoresinol, 2: NMR data agreed with those in the literature;17 [α]D25 −68 (c 0.1, CHCl3), [α]D25 −34.7 (CHCl3) in the litearure;19 tR 17.7 min (OD-H, hexane/isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 276 nm); >99% ee. (+)-Medioresinol, 3: NMR data agreed with those in the literature;20 [α]D25 +68 (c 0.2, CHCl3), [α]D22 +54 (c 1.0, CHCl3) in the literature;18 tR 23.1 min (AD-H, hexane/isopropyl alcohol = 1:4, v/v, 1 mL/min, detected at 280 nm); >99% ee. (−)-Medioresinol, 4: NMR data agreed with those in the literature;20 [α]D25 −69 (c 0.3, CHCl3), [α]D25 −17.0 (c 0.14, CHCl3) in the literature;21 tR 19.8 min (AD-H, hexane/isopropyl alcohol = 1:4, v/v, 1 mL/min, detected at 280 nm); >99% ee. (+)-Syringaresinol, 5: NMR data agreed with those in the literature;20 [α]D25 +38 (c 0.4, CHCl3), [α]D22 +23 (c 0.7, CHCl3) in the literature;18 tR 27.4 min (OD-H, hexane/isopropyl alcohol = 1:4, v/v, 1 mL/min, detected at 273 nm); >99% ee. (−)-Syringaresinol, 6: NMR data agreed with those in the literature;20 [α]D25 −37 (c 0.4, CHCl3), [α]D −28 in the literature;22 tR 41.8 min (OD-H, hexane/isopropyl alcohol = 1:4, v/v, 1 mL/min, detected at 273 nm); >99% ee. (+)-Sesamin, 7: NMR data agreed with those in the literature;23 [α]D25 +64 (c 0.4, CHCl3), [α]D +64.8 (CHCl3) in the literature;24 tR 14.6 min (AD-H, hexane/isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 287 nm); >99% ee. (−)-Sesamin, 8: NMR data agreed with those in the literature;23 [α]D25 −65 (c 0.4, CHCl3), [α]D19 −68.6 (c 0.53, CHCl3) in the

INTRODUCTION Furofuran lignans (Figure 1) are a representative group of lignans in food plants,1,2 possessing a 7,9′:7′,9-diepoxy3 structure and a wide range of biological activities.2 Although lignans are biosynthesized by plants, the effect of the main structure and stereochemistry on the plant growth regulatory activity had not been clarified. Recently, we demonstrated the plant growth inhibitory activity of 7,9′-epoxylignan4,5 and 7,7′epoxylignan,6,7 giving information on the favored stereochemistry and substituent for the activity. As for dietary furofuran lignan, we can find some reports on the plant growth regulatory activity using isolated compounds.8−10 The activity of isolated oxo-type furofuran lignan was also reported.11 On the other hand, the enantiomeric excess of natural furofuran lignan was estimated as 20−30%,12,13 suggesting that the effect of stereochemistry on the activity should be examined by employing optically pure synthesized compounds. In this research, both enantiomers of common dietary furofuran lignans, (+)- and (−)-pinoresinol, 1 and 2, (+)- and (−)-medioresinol, 3 and 4, (+)- and (−)-syringaresinol, 5 and 6, (+)- and (−)-sesamin, 7 and 8, (+)- and (−)-sesamolin, 9 and 10, (+)- and (−)-sesamolinol, 11 and 12, and (+)- and (−)-samin, 13 and 14, were selected to clarify the plant growth regulatory activity of components of the food plants. With the results of this research, effects of enantiomeric, acetal, and hemiacetal structure on the activity could be compared for the first time. The previously described synthetic methods14−16 were employed with modification to provide the optically pure furofuran lignans.

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MATERIALS AND METHODS Received: Revised: Accepted: Published:

Chemicals. Optical rotation values were measured with a P-2100 instrument (JASCO, Tokyo, Japan). HPLC analysis for compounds was performed with LC-6AD and SPD-6AV instruments (Shimadzu, Kyoto, Japan). The column used for HPLC analyses was a 250 mm × © 2015 American Chemical Society

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March 1, 2015 April 30, 2015 May 8, 2015 May 8, 2015 DOI: 10.1021/acs.jafc.5b01099 J. Agric. Food Chem. 2015, 63, 5224−5228

Article

Journal of Agricultural and Food Chemistry

Figure 1. (+)- and (−)-furofuran lignans (7,9′:7′,9-diepoxylignan). literature;25 tR 12.7 min (AD-H, hexane/isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 287 nm); >99% ee. (+)-Sesamolin, 9: NMR data agreed with those in the literature;26 [α]D25 +198 (c 1.2, CHCl3), [α]D +212 (CHCl3) in the literature;27 tR 13.0 min (AD-H, hexane/isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 287 nm); >99% ee. (−)-Sesamolin, 10: NMR data agreed with those in the literature;26 [α]D25 −195 (c 1.1, CHCl3), [α]D23 −216.44 (c 0.61, CHCl3) in the literature of synthetic research;28 tR 11.3 min (AD-H, hexane/ isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 287 nm); >99% ee. (+)-Sesamolinol, 11: NMR data agreed with those in the literature;29 [α]D25 +179 (c 0.8, CHCl3), [α]D +184 (c 1.0, CHCl3) in literature;29 tR 11.5 min (AD-H, hexane/isopropyl alcohol = 1:1, v/ v, 1 mL/min, detected at 287 nm); >99% ee. (−)-Sesamolinol, 12: NMR data agreed with those of (+)-form in the literature;29 [α]D25 −178 (c 1.4, CHCl3); tR 12.8 min (AD-H, hexane/isopropyl alcohol = 1:1, v/v, 1 mL/min, detected at 287 nm); >99% ee. (+)-Samin, 13: diastereomeric mixture of 7R and 7S; NMR data agreed with those in the literature;30 [α]D25 +92 (c 1.2, CHCl3), [α]D +81.4 (c 0.5, CHCl3) in the literature.31 (−)-Samin, 14: diastereomeric mixture of 7R and 7S; NMR data agreed with those in the literature;30 [α]D25 −90 (c 2.5, CHCl3), [α]D24 −88.18 (c 1.1, CHCl3) in the literature of synthetic research.28 Evaluation of Plant Growth Regulatory Activity. The plant growth regulatory activity of all stereoisomers of lariciresinol was evaluated using lettuce (Lactuca sativa L. Green-wave (Takii Seed Co. Ltd., Kyoto, Japan)) and Italian ryegrass (Lolium multiflorum Lam. Wase-fudo (Takii Seed Co. Ltd.)). A sheet of filter paper (90 mm diameter) was placed in a 90 mm Petri dish and wetted with 500 μL of test sample solution dissolved in acetone at concentrations from 6.0 × 10−3 to 6.0 × 10−8 M. After the filter paper had dried, 3 mL of water was poured into the dish to adjust the final concentration from 1.0 × 10−3 to 1.0 × 10−8 M. Thirty seeds of each plant were placed on the filter paper, and the Petri dishes were sealed with Parafilm. The Petri dishes were then incubated in the dark at 20 °C. The lengths of roots and shoots were measured after 3 days for lettuce and after 5 days for ryegrass by using an ordinary ruler. The roots and shoots lengths of the control were ca. 3 and 1 cm for lettuce and 4 and 3 cm for ryegrass, respectively. Data are presented as percentage differences from the control; positive and negative values represent stimulation and inhibition of plant growth, respectively. Experiments were performed in triplicate or more for each sample (n = 3−7). Statistical analyses

were conducted by one-way ANOVA followed by Tukey’s multiplecomparison test using PRISM software (Graphpad Software, San Diego, CA, USA), and the values of p < 0.01 and 0.05 were considered to be statistically significant.

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RESULTS AND DISCUSSION Optically pure natural furofuran lignans, 1−14, were synthesized by employing a previously described method with modification.14−16 Although some isolated furofuran lignans, (−)-pinoresinol,19 (−)-medioresinol,21 and (−)-syringaresinol,22 from plants showed lower specific optical rotation in the previous studies, we obtained optically pure samples by organic syntheses for this research. These synthetic results enabled us to evaluate the biological activity of the (−)-form for the first time. In the case of hemiacetal type lignans, (+)- and (−)-samin (13 and 14), diastereomeric mixtures of the (7R/S)form were employed. All synthesized furofuran lignans, 1−14, were applied to plant growth regulatory activity test at 1 mM (Figure 2) as a first stage. Against lettuce roots, (+)- and (−)-syringaresinol (5 and 6) and (+)- and (−)-sesamin (7 and 8) promoted the growth (from 40 to 60% from control) with significant difference, whereas (+)- and (−)-medioresinols (3 and 4) had lower activity, suggesting that the 3,5-dimethoxy-4hydroxyphenyl group or 3,4-methylendioxyphenyl group at both the 7 and 7′ positions is favorable for the growth promotion of lettuce roots. A comparable activity level was shown between the corresponding enantiomers. Even if two 3,4-methylenedioxyphenyl groups are present in the structure, the acetal type compound, (+)- and (−)-sesamolin (9 and 10) was inactive, indicating that the 7-aryl structure is more important than the 7-aryloxy group for the growth promotion activity against lettuce roots. No or very weak activities of both enantiomers of pinoresinol (1 and 2) medioresinol (3 and 4), sesamolinol (11 and 12), and samin (13 and 14) would be due to the presence of 3-methoxy-4-hydroxy groups and the acetal/ hemiacetal structure. On the other hand, growth promotion was not observed, but growth inhibitory activity was exhibited against lettuce shoots for (+)- and (−)-sesamin (7 and 8), (+)and (−)-sesamolin (9 and 10), and (+)- and (−)-samin (13 5225

DOI: 10.1021/acs.jafc.5b01099 J. Agric. Food Chem. 2015, 63, 5224−5228

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Journal of Agricultural and Food Chemistry

potent against lettuce shoots. These facts suggest that the substituent on the aromatic ring is a more important factor than the structure of the 7 position and the enantiomeric structure against growth inhibition of lettuce shoots at 1 mM. In our previous study on lignans bearing a 7,9′-epoxy structure4,5 and a 7,7′-epoxy structure,6,7 only growth inhibitory activity against lettuce was observed. We found growth promotion activity of furofuran lignan bearing a 7,9′:7′,9-diepoxy structure against lettuce roots in this study. (+)- and (−)-Sesamin showed both growth promotion activity against lettuce roots and growth inhibitory activity against lettuce shoots at 1 mM. Against ryegrass at 1 mM (Figure 2C,D), we observed only growth inhibitory activity on both roots and shoots elongation. (+)-Pinoresinol (1) (−65%) was 1.5-fold more potent than (−)-pinoresinol (2) (−40%) against ryegrass roots with significant difference. The activities of other compounds against ryegrass roots were lower (< −25%). (−)-Sesamolin (10) exhibited the highest activity of the growth inhibitory activity against ryegrass shoots (−55%) with significant difference at 1 mM; on the other hand, its enantiomer, (+)-sesamolin (9), was 2-fold less potent. The activities of other compounds containing pinoresinol, which had the highest activity against ryegrass roots, were < −35%. The higher growth inhibitory activities of shoots against both lettuce and ryegrass at 1 mM were observed in only (−)-sesamolin (10), bearing a 3,4methylenedioxyphenyl group and acetal structure. However, the activity of 10 against roots of lettuce and ryegrass was not observed. In the ryegrass growth experiment, different activity levels between corresponding enantiomers were observed. As a next step, dilution experiments (from 10−4 to 10−8 M) of the active compounds at 1 mM were performed (Figure 3). Although significant difference was not observed, (+)-sesamin (7) was effective to some extent, exhibiting promotion activity (+40%) against lettuce roots at 10−4 M (Figure 3A,B). In the experiment on growth of lettuce shoots, (+)- and (−)-sesamin (7 and 8) and (+)- and (−)-sesamolin (9 and 10) were proved to show from −40 to −30% inhibitory activity with significant difference at 10−4 M. The growth promotion activity of (+)and (−)-syringaresinol (5 and 6) and (−)-sesamin (8) against lettuce roots and the growth inhibitory activity of (+)- and (−)-samin (13 and 14) against lettuce shoots at 1 mM dramatically disappeared by 10-fold dilution as in our previous experiment employing 7,9′- and 7,7′-epoxylignan possessing a 3-methoxy-4-hydroxyphenyl group.4,6 Considering these results, 7-(3,4-methylenedioxyphenyl)/(3,4-methylenedioxyphenoxy) and 7′-(3,4-methylenedioxyphenyl) compounds are more advantageous for lettuce growth regulation at diluted concentration. The enantiospecific activity of sesamin was clarified by this dilution experiment; only (+)-sesamin (7) showed growth promotion activity (+40%) against lettuce roots at 10−4 M. In the dilution experiment on ryegrass (Figure 3C,D), (−)-sesamolin (10) showed growth inhibitory activity (−45%) against shoots at 10−4 M with significant difference; on the other hand, the higher activities of (+)- and (−)-pinoresinol (1 and 2) against roots at 1 mM dramatically disappeared at 10−4 M. It could be assumed that the (−)-form, 7-(3,4methylenedioxyphenoxy) acetal structure, and 7′-(3,4-methylenedioxyphenyl) structure are favorable for the highest ryegrass shoot inhibitory activity at diluted condition. The lower activity of hemiacetal type (−)-samin (14), which is converted from 10 by hydrolysis, means that the acetal type (−)-sesamolin (10) is an active compound in the plant body.

Figure 2. Plant growth regulatory activity of (+)- and (−)-furofuran lignans, 1−14, at 1 mM against (A) lettuce roots, (B) lettuce shoots, (C) ryegrass roots, and (D) ryegrass shoots. (∗∗) p < 0.01; (∗) p < 0.05. (−)-Verrucosin showed −95 and −60% growth inhibition activity against lettuce roots and shoots, respectively. (+)-Verrucosin showed −98 and −63% growth inhibition activity against ryegrass roots and shoots, respectively.6

and 14), showing growth inhibitory activity with significant difference (from −40 to −50% from control). Because the activity level of the 7-aryl structure, 7 and 8, was similar to that of the 7-acetal structure, 9 and 10, it could be assumed that the 3,4-methylenedioxy groups on both 7 and 7′ aromatic rings are important for growth inhibitory activity against lettuce shoots. The activity of the 7-hemiacetal structure is also similar to those of the 7-aryl and 7-acetal structures. The enantiomeric structures did not affect the activity. The activities of both enantiomers of pinoresinol (1 and 2), medioresinol (3 and 4), syringaresinol (5 and 6), and sesamolinol (11 and 12) were less 5226

DOI: 10.1021/acs.jafc.5b01099 J. Agric. Food Chem. 2015, 63, 5224−5228

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We evaluated EC50 values of furofuran lignans of higher activity (7,9′:7′,9-diepoxylignan) in this experiment (Table 1). The highest active compounds were (+)-sesamin (7) against lettuce shoots (growth inhibition, EC50 = 0.38 mM) and (−)-sesamolin (10) against ryegrass shoots (growth inhibition, EC50 = 0.23 mM). The activity of compounds bearing a 3methoxy-4-hydroxyphenyl group, which is a common phenyl group in the natural lignans, was weak. The highest activity of 7,9′:7′,9-diepoxylignan bearing a 3-methoxy-4-hydroxyphenyl group was shown against ryegrass roots by (+)-pinoresinol (1) (growth inhibition, EC50 = 0.95 mM). In this experiment, growth promotion activity of lignan was also discovered. The growth promotion activity of (+)-sesamin (7) against lettuce roots (EC50 = 0.50 mM) was 2-fold higher than that of (+)-syringaresinol (EC50 = 1.00 mM). To confirm the growth promotion/inhibitory activities of these compounds, the effects of these compounds on germination were examined, showing 83−101% germination from control. These compounds did not affect much the germination. This research clarified the plant growth regulatory activity of popular furofuran lignan bearing a 7,9′:7′,9-diepoxy structure using enantiomerically pure synthesized (+)- and (−)-enantiomers for the first time. Compared the activity, the potency of a methylenedioxy group on the aromatic rings and some difference of activity level between enantiomers were more shown. It is evaluated that (+)-sesamin and (−)-sesamolin were more potent in this research. It is noteworthy that (+)-sesamin promotes the growth of lettuce roots and inhibits lettuce shoots. It could be assumed that a 7,9′:7′,9-diepoxy structure is less potent than the 7,9′- and 7,7′-epoxy structures at 1 mM. However, a 7,9′:7′,9-diepoxy structure bearing a 3,4-methylenedioxy group is more potent at lower concentration. Because both enantiomers showed activity, enantiomers seem to have no specific target. Lignans have been focused on their antioxidant activities and medicinal effect.32 This research showed the plant growth regulatory activity of (+)- and (−)-furofuran lignans. The biosynthetic research of furofuran lignan is now continuing.33,34 By the combination of structure− activity relationships with the biosynthetic research, new food plants producing higher amounts of growth regulatory lignans could be developed.

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AUTHOR INFORMATION

Corresponding Author

*(S.Y.) Phone: +81-89-946-9846. Fax: +81-89-977-4364. Email: [email protected]. Funding

We are grateful to Marutomo Co. for financial support.

Figure 3. Plant growth regulatory activity of (+)- and (−)-furofuran lignans under diluted conditions against (A) lettuce roots, (B) lettuce shoots, (C) ryegrass roots, and (D) ryegrass shoots. (∗∗) p < 0.01; (∗) p < 0.05.

Notes

The authors declare no competing financial interest.

Table 1. EC50 Valuesa of (+)-Pinoresinol, (+)-Syringaresinol, (+)-Sesamin, and (−)-Sesamolin lettuce (EC50, mM)

a

ryegrass (EC50, mM)

compound

roots

shoots

roots

shoots

(+)-pinoresinol (1) (+)-syringaresinol (5) (+)-sesamin (7) (−)-sesamolin (10)

>1.00 1.00 ± 0.35 (promotion) 0.50 ± 0.26 (promotion) >1.00

>1.00 >1.00 0.38 ± 0.19 (inhibition) >1.00

0.95 ± 0.31 (inhibition) >1.00 >1.00 >1.00

>1.00 >1.00 >1.00 0.23 ± 0.04 (inhibition)

EC50 values of 1 and 5 were determined by dilution experiment from 1 to 0.2 mM. 5227

DOI: 10.1021/acs.jafc.5b01099 J. Agric. Food Chem. 2015, 63, 5224−5228

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(19) Lin-gen, Z.; Seligmann, O.; Jurcic, K.; Wagner, H. Inhaltsstoffe von Daphne tangutica. Planta Med. 1982, 45, 172−176. (20) Nakasone, Y.; Takara, K.; Wada, K.; Tanaka, J.; Yogi, S.; Nakatani, N. Antioxidant compounds isolated from kokuto, noncentrifugal cane sugar. Biosci., Biotechnol., Biochem. 1996, 60, 1714− 1716. (21) Badawi, M. M.; Handa, S. S.; Kinghorn, A. D.; Cordell, G. A.; Farnsworth, N. R. Plant anticancer agents. XXVII: antileukemic and cytotoxic constituents of Dirca occidentalis. J. Pharm. Sci. 1983, 72, 1285−1287. (22) Anjaneyulu, A. S. R.; Murty, S. Chemical examination of heartwood of Guazuma tomentosa Kunth. Indian J. Chem. 1981, 20B, 85−87. (23) Kim, J.-C.; Kim, K.-H.; Jung, J.-C.; Park, O.-S. An efficient asymmetric synthesis of furofuran lignans: (+)-sesamin and (−)-sesamin. Tetrahedron: Asymmetry 2006, 17, 3−6. (24) Rao, E. V.; Sasthry, K. V.; Palanivelu, T. J. Lignan from the stem bark of Zanthoxylum acanthapodium DC. Curr. Sci. 1975, 44, 228−230. (25) Abe, F.; Yahara, S.; Kubo, K.; Nonaka, G.; Okabe, H.; Nishioka, I. Studies on Xanthoxylim spp. II. Constituents of the bark of Xanthoxylum piperitum DC. Chem. Pharm. Bull. 1974, 22, 2650−2655. (26) Kang, S. S.; Kim, J. S.; Jung, J. H.; Kim, Y. H. NMR assignments of two furofuran lignans from sesame seeds. Arch. Pharmacal Res. 1995, 18, 361−363. (27) Haslam, E.; Haworth, R. D. The constituents of natural phenolic resins. Part XXIII. The constitution of sesamolin. J. Chem. Soc. 1955, 827−833. (28) Takano, S.; Ohkawa, T.; Tamori, S.; Satoh, S.; Ogasawara, K. Enantio-controlled route to the furofuran lignans: the total synthesis of (−)-sesamolin, (−)-sesamin, and (−)-acuminatolide. J. Chem. Soc., Chem. Commun. 1988, 189−191. (29) Osawa, T.; Nagata, M.; Namiki, M.; Fukuda, Y. Sesamolinol, a novel antioxidant isolated from sesame seeds. Agric. Biol. Chem. 1985, 49, 3351−3352. (30) Maiti, G.; Adhikari, S.; Roy, S. G. Stereoselective total synthesis of (±)-samin and the dimethoxy analogue, the general furofuran lignan precursors. Tetrahedron 1995, 51, 8389−8396. (31) Fukuda, Y.; Isobe, M.; Nagata, M.; Osawa, T.; Namiki, M. Acidic transformation of sesamolin, the sesame-oil constituent, into an antioxidant bisepoxylignan, sesaminol. Heterocycles 1986, 24, 923−926. (32) Saleem, M.; Kim, H. J.; Ali, M. S.; Lee, Y. S. An update on bioactive lignans. Nat. Prod. Rep. 2005, 22, 696−816. (33) Satake, H.; Ono, E.; Murata, J. Recent advances in the metabolic engineering of lignan biosynthesis pathway for the production of transgenic plant-based food and supplements. J. Agric. Food Chem. 2013, 61, 11721−11729. (34) Renouard, S.; Tribalatc, M.-A.; Lamblin, F.; Mongelard, G.; Fliniaux, O.; Corbin, C.; Marosevic, D.; Pilard, S.; Demailly, H.; Gutierrez, L.; Hano, C.; Mesnard, F.; Lainé, E. RNAi-mediared pinoresinol larisiresinol reductase silencing in flaz (Linum usitatissimum L.) seed coat: consequences on lignans and neolignans accumulation. J. Plant Physiol. 2014, 171, 1372−1377.

ACKNOWLEDGMENTS Part of this study was performed at INCS (Johoku station) of Ehime University.

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REFERENCES

(1) Penalvo, J. L.; Adlercreutz, H.; Uehara, M.; Ristimaki, A.; Watanabe, S. Lignan content of selected foods from Japan. J. Agric. Food Chem. 2008, 56, 401−409. (2) Ayres, D. C.; Loike, J. D. Lignans; Cambridge University Press: Cambridge, UK, 1990. (3) Moss, G. P. Nomenclature of lignans and neolignans (IUPAC recommendations 2000). Pure Appl. Chem. 2000, 72, 1493−1523. (4) Nishiwaki, H.; Kumamoto, M.; Shuto, Y.; Yamauchi, S. Stereoselective syntheses of all stereoisomers of lariciresinol and their plant growth inhibitory activities. J. Agric. Food Chem. 2011, 59, 13089−13095. (5) Yamauchi, S.; Kumamoto, M.; Ochi, Y.; Nishiwaki, H.; Shuto, Y. Structure-plant growth inhibitory activity relationship of lariciresinol. J. Agric. Food Chem. 2013, 61, 12297−12306. (6) Nishiwaki, H.; Nakayama, K.; Shuto, Y.; Yamauchi, S. Synthesis of all stereoisomers of 3,3′-dimethoxy-7,7′-epoxylignane-4,4′-diol and their plant growth inhibitory activity. J. Agric. Food Chem. 2014, 62, 651−659. (7) Yamauchi, S.; Nakayama, K.; Nishiwaki, H.; Shuto, Y. Structureplant phytotoxic activity relationship of 7,7′-epoxylignanes, (+)- and (−)-verrucosin: simplification on the aromatic ring substituents. Bioorg. Med. Chem. Lett. 2014, 24, 4798−4803. (8) Cutillo, F.; D’Abrosca, B.; D.Greca, M.; Fiorentino, A.; Zarrelli, A. Lignans and neolignans from Brassica f ruticulosa: effects on seed germination and plant growth. J. Agric. Food Chem. 2003, 51, 6165− 6172. (9) Macías, F. A.; López, A.; Varela, R. M.; Torres, A.; Molinillo, J. M. G. Bioactive lignans from a cultivar of Helianthus annuus. J. Agric. Food Chem. 2004, 52, 6443−6447. (10) DellaGreca, M.; Mancino, A.; Previtera, L.; Zarrelli, A.; Zuppolini, S. Lignans from Phillyrea angustifolia L. Phytochem. Lett. 2011, 4, 118−121. (11) Kato-Noguchi, H.; Kobayashi, A.; Ohno, O.; Kimura, F.; Fujii, Y.; Suenaga, K. Phytotoxic substances with allelopathic activity may be central to the strong invasive potential of Brachiaria brizantha. J. Plant Physiol. 2014, 171, 525−530. (12) Suzuki, S.; Umezawa, T.; Shimada, M. Stereochemical diversity in lignan biosynthesis of Arctium lappa L. Biosci., Biotechnol., Biochem. 2002, 66, 1262−1269. (13) Finefield, J. M.; Sherman, D. H.; Kreitman, M.; Williams, R. M. Enantiomeric natural products; occurrence and biogenesis. Angew. Chem., Int. Ed. 2012, 51, 4802−4936. (14) Yamauchi, S.; Sugahara, T.; Matsugi, J.; Someya, T.; Masuda, T.; Kishida, T.; Akiyama, K.; Maruyama, M. Effect of the benzylic structure of lignan on antioxidant activity. Biosci., Biotechnol., Biochem. 2007, 71, 2283−2290. (15) Yamauchi, S.; Bando, S.; Kinoshita, Y. Synthesis of 1,2oxygenated 6-arylfurofuran lignan: stereoselective synthesis of (1S,2S,5R,6S)-1-hydroxysamin. Biosci., Biotechnol., Biochem. 2002, 66, 1495−1499. (16) Yamauchi, S.; Ina, T.; Kirikihara, T.; Masuda, T. Synthesis and antioxidant activity of oxygenated furofuran lignans. Biosci., Biotechnol., Biochem. 2004, 68, 183−192. (17) Roy, S. C.; Rana, K. K.; Guin, C. (±)-Lariciresinol, (±)-acuminatin, and (±)-lariciresinol monomethyl ether and furofuran lignans (±)-sesamin, (±)-eudesmin, (±)-piperitol methyl ether, (±)-pinoresinol, (±)-piperitol, and (±)-pinoresinol monomethyl ether by radical cyclization of epoxides using a transition-metal radical source. J. Org. Chem. 2002, 67, 3242−3248. (18) Kikuchi, T.; Matsuda, S.; Kadota, S.; Tai, T. Studies on the constituents of medicinal and related plants in Sri Lanka. III. Novel sesquilignans from Hedvotis lawsoniae. Chem. Pharm. Bull. 1985, 33, 1444−1451. 5228

DOI: 10.1021/acs.jafc.5b01099 J. Agric. Food Chem. 2015, 63, 5224−5228