Diterpenoids with herbicidal and antifungal activities from hulls of rice (Oryza sativa)

Fitoterapia 136 (2019) 104183

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Diterpenoids with herbicidal and antifungal activities from hulls of rice (Oryza sativa)

T

Cheng-Zhen Gua, Xiao-Mei Xiaa, Jing Lva, Jian-Wen Tanc, Scott R. Baersond, Zhi-qiang Pand, ⁎ ⁎ Yuan-Yuan Songb, , Ren-Sen Zengb, a

College of Life Science, Fujian Agriculture and Forestry University, Fuzhou 350002, People's Republic of China College of Crop Science, Fujian Agriculture and Forestry University, Fuzhou 350002, People's Republic of China c South China Botanic Garden, Guangzhou 510642, People's Republic of China d United States Department of Agriculture-Agricultural Research Service, Natural Products Utilization Research Unit, University, Mississippi 38677, USA b

ARTICLE INFO

ABSTRACT

Keywords: Oryza sativa L. Diterpenoids Momilactones Allelopathy Phytoalexin

Diterpenoids are the main secondary metabolites of plants and with a range of biological activities. In the present study, 7 compounds were isolated from the hulls of rice (Oryza sativa L.). Among them, 3 diterpenoids are new namely, 3,20-epoxy-3α-hydroxy- 8,11,13-abietatrie-7-one (1), 4,6-epoxy-3β-hydroxy-9β-pimara-7,15-diene (2) and 2-((E)-3- (4-hydroxy-3-methoxyphenyl) allylidene) momilactone A (3). While, 4 terpenoids are known, namely momilactone A (4), momilactone B (5), ent-7-oxo-kaur-15-en-18-oic acid (6) and orizaterpenoid (7). The structures of these diterpenoids were elucidated using 1D and 2D NMR in combination with ESI-MS and HR-EIMS. Furthermore, all isolated compounds displayed antifungal activities against four crop pathogenic fungi Magnaporthe grisea, Rhizoctonia solani, Blumeria graminearum and Fusarium oxysporum, and phytotoxicity against paddy weed Echinochloa crusgalli. The results suggested that rice could produce plenty of secondary metabolites to defense against weeds and pathogens.

1. Introduction Plants are consistently exposed to various competitors and microbial pathogens. Weeds and crop diseases cause significant yield loss in global crop production. Fortunately, plants have evolved an intricate defense system against weeds and pathogens, including the production of an array of secondary metabolites with allelopathic and antimicrobial activities. Accumulation of antimicrobial is one of the most important defense responses of plants to microbial infection. Phytoalexins are a heterogeneous group of compounds (e.g. flavonoids, alkaloids, terpenoids and polyacetylenes) with antimicrobial activity towards a variety of pathogens [1–3]. These compounds play a vital role in the biochemical defense of plants against pathogens attack and are considered as molecular markers of disease resistance. Increasing understanding of phytoalexin function, biosynthesis and regulation, as well as emerging molecular engineering make it possible to modulate inducible phytoalexins for improving crop protection. Rice (Oryza sativa L.) is one of the staple food crops in the world. Rice plant infected by fungi such as Magnaporthe grisea and Rhizoctonia solani, causing rice blast and sheath blight diseases, which are most serious and common diseases of rice. In response to the fungal infection ⁎

by these two pathogens, rice plants produce two groups of phytoalexins. So far 1 flavanone sakuranetin and 14 diterpenes have been identified as rice phytoalexins. These diterpene phytoalexins include oryzalexin AF [4–6], momilactone A and B [7–8], oryzalexin S [9], and phytocassanes A-E [10,11]. Weeds in paddy field cause substantial damage to rice yield. Use of commercial chemical herbicides is effective, but it is costly and causes environmental problems in the paddy ecosystem [12–14]. Alleopathy is the process whereby plant releases toxic compounds into environment, resulting in a detrimental effect on neighbouring plants or its own sharing the same habitat [15]. Crops with allelopathic potential can suppress weeds in the field, the process of which can replace conventional herbicides, fungicides, or insecticides, resulting in reducing the environmental deterioration [15]. Consequently, rice allelopathy is the best way to control weeds in rice production [14,16]. Although, rice has been extensively studied with respect to its allelopathic potential and its production of allelochemicals [17–19], for instance, the diterpenoids (momilactones A and B) isolated from rice hulls [8,20–21] are reported to inhibit growth and germination of Echinochloa crusgalli [22]. However, there are few reports in the literature on the chemical constituents of rice hulls, therefore identification of further bioactive constituents is

Corresponding authors. E-mail addresses: [email protected] (Y.-Y. Song), [email protected] (R.-S. Zeng).

https://doi.org/10.1016/j.fitote.2019.104183 Received 5 April 2019; Received in revised form 22 May 2019; Accepted 27 May 2019 Available online 28 May 2019 0367-326X/ © 2019 Elsevier B.V. All rights reserved.

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still required. The objectives of this study are to isolate and identify new compounds with highly antifungal activity and phytotoxicity from the rice hulls. In this study, we describe the isolation and structure elucidation of three new diterpenoids along with four known terpenoids from the rice hulls. Furthermore, antifungal and phytotoxic activities of the isolated compounds were evaluated in four crop pathogenic fungi M. grisea, R. solani, Blumeria graminearum and Fusarium oxysporum, and paddy weed Echinochloa crusgalli.

302.2240). 2-((E)-3-(4-hydroxy-3-methoxyphenyl) allylidene) momilactone A (3). Yellow solid (CHCl3); [a]20 D − 144 (c 0.1, CHCl3); mp: 238–240 °C; UV (CHCl3) λmax (log ε) 377 nm (4.08); EI-MS m/z 474 [M]+, HR-EI-MS m/z 474.2398 [M]+ (calculated for C30H34O5, 474.2401). 2.5. Biological activities 2.5.1. Phytotoxicity Seeds of E. crusgalli were surface sterilized using 10% H2O2 for 5 min and then washed 5 times with sterile distilled water and followed by germination on a sheet of moist filter paper at 25 °C in the darkness for 2 days. Compounds 1–7 were dissolved in acetone to a final concentration of 2 mg/mL, then were added to sterile distilled water to get 3 concentrations (5, 10, 20 μg/mL). Fifteen E. crusgalli seedlings with similar root and shoot lengths were then arranged randomly on the filter paper in each well in the 6-well plates (contained the above concentrations) and incubated with a 12 h photoperiod in the chamber. To eliminate the effect of acetone on the growth of E. crusgalli, the concentration (20 μg/mL) of acetone was used as blank control. Three replicates were done for each concentration. The lengths of seedling roots and shoots were measured after 3 days. The percentage of growth inhibition of root and shoot lengths was calculated from the following equation: I(%) = [1-T/C]*100%, where T is the average length of treatment (cm) and C is the average length of control (cm).

2. Experimental 2.1. General experiment procedures Melting points were measured on an XT-4 hot-stage microscope and were uncorrected. Optical rotations were determined on a Perkin-Elmer 341 polarimeter at the wavelength of 589 nm and 20 °C in CHCl3. The UV absorptions were measured on a Perkin-Elmer Lambda 650 UV–vis spectrophotometer at the wavelengths of 200–400 nm. All of NMR (1H, 13C, DEPT, HMBC, HSQC, NOESY) spectra were recorded on a Bruker AV600 at 600 MHz using CDCl3 as the solvent. Chemical shifts were referenced to solvent peaks: δH 7.240 and δC 77.230 for CDCl3. TLC was carried out on pre-coated silica (Si) gel G 60 F254 plates. Spots were first detected under UV light (254 and 360 nm), and then heating after dipping in a chamber with 1% vanillin sulfuric acid (ethanol solution) or 6% H2SO4 solution. ESI-MS and HR-EI-MS were recorded on a Micromass Autospec Spectrometer. All solvents used were analytical grade.

2.5.2. Antifungal activities The antifungal activities of compounds 1–7 were performed using the microdilution techniques described by Drummond and Waigh [23]. In order to determine the minimum inhibitory concentration (MIC) conveniently, 96-well plates and resazurin (indicator) were used for this test. Indicator solution (resazurin) concentrations (100 μg/mL and 143 μg/mL) were first prepared. Then, 100 μL of indicator solution (100 μg/mL) was placed into the control wells (11th column) on the 96 well plates. Thereafter, 7 mL indicator solution (143 μg/mL) was mixed with 3 mL test fungus (108 cfu/mL) and then transferred into growth control wells (12th column) and the test wells (1st-10th column). Once 10 μL sample solution (2 mg/mL) and 90 μL indicator solution (100 μg/ mL) were added into the 1st column wells followed by mixing by pipette, half of the solutions (100 μL) from 1st column wells was then transferred into the 2nd column of wells and each subsequent well was treated similarly (doubling dilution) until the 10th column, followed by throwing away the last 100 μL solution. In a plate, six samples could be applied leaving two for negative and positive controls. Finally, the plates were incubated at 28 °C for around 12–16 h, until the growth of control wells transformed from blue colour to pink colour. The blue colour solution means growth inhibition in test wells, while pink colour solution indicates growth or absence of inhibition. The highest dilution showing growth inhibition was taken as the minimal inhibitory concentration (MIC).

2.2. Plant material Hulls of O. sativa (Yue fengzhan 8763) were collected from Institute of rice, Academy of Agricultural Sciences, Guangdong Provincial, China, in March 2011. 2.3. Extraction and isolation Dried and powdered hulls of O. sativa (150 kg) were totally soaked in 550 L ethanol (95%) and refluxed for 6 h at 45 °C. The filtrate was evaporated to dry and got ethanol extract. The ethanol extract was reextracted with chloroform, ethyl acetate and n-butanol successively. The extract of chloroform (2.7 kg) was subjected to the silica-gel column and eluted with petrol-acetone (9:1–0:1) to give six fractions AF. Fraction C (90.9 g) were subjected to silica-gel column (CHCl3:MeOH, 400:1–0:1) to afford five fractions C1-C5. Fraction C2 (9.39 g) was subjected to silica-gel (petroleum ether: acetone, 40:1) and then purified by semi-preparative reversed-phase MPLC (MeOH:H2O, 70:30) to yield compound 2 (20 mg). Fraction C3 was applied to silicagel column (25.6 g) (petroleum ether: acetone, 20:1) and further separated by sephadex LH-20 column chromatography to yield compounds 3 (3 mg), 4 (500 mg), 5 (70 mg) and 6 (5 mg). Fraction C4 (15.2 g) were subjected to silica-gel column (petroleum ether: acetone, 10:1) and then purified by sephadex LH-20 column chromatography (CHCl3:MeOH, 1:4) to give compounds 1 (23 mg) and 7 (40 mg).

3. Results and discussion 3.1. Results and discussion

2.4. Spectroscopic data

The ethanol (EtOH) extract of rice hulls was extracted successively with chloroform, ethyl acetate and n-butanol. The CHCl3 extract was separated and purified by silica gel column chromatography, sephadex column and preparation liquid chromatography. We found three new diterpenoids (1–3) and four known compounds (4–7). The known compounds were identified as momilactone A (4) [13], momilactone B (5) [13], ent-7-oxo-kaur-15-en-18-oic acid (6) [24] and orizaterpenoid (7) [25] based on their spectroscopic data in comparison with the literature. Compound 6 was isolated from rice for the first time (Fig. 2). Compound 1 was isolated from the CHCl3 extract as a white powder

3,20-epoxy-3α-hydroxy-8, 11, 13-abietatrien-7-one (1). Amorphous powder; [a]20 D − 35 (c 0.4, CHCl3); mp: 186–188 °C; UV (CHCl3) λmax (log ε) 252 nm (4.08), 298 nm (3.38); EI-MS m/z 314 [M]+, positive HR-EI-MS m/z 314.1878 [M]+ (calculated for C20H26O3, 314.1876). 4,6-epoxy-3β-hydroxy-9β-pimara-7,15-diene (2). Colorless needles; [a]20 D − 225 (c 0.2, CHCl3); mp: 92–94 °C; UV (CHCl3) λmax (log ε) 237 nm (3.13), 278 nm (3.09); EI-MS m/z 302 [M]+, Positive HR-EI-MS m/z 302.2240 [M]+ (calculated for C20H30O2, 2

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Table 1 13 C and 1H NMR data of compounds 1–3 in CDCl3 (δ in ppm). No.

1

2

3

δC

δH (J in Hz)

δC

δH (J in Hz)

δC

δH (J in Hz)

1

33.8

1.68, 2.54 m

33.0

36.1

2.56 s

2 3 4 5 6 7 8 9 10 11

29.5 99.1 40.5 46.5 36.7 198.9 132.2 142.1 36.2 126.9

2.27, 1.98 m

29.0 76.9 46.4 49.6 75.6 117.9 144.9 53.4 33.3 22.9

1.41–1.34 m 1.28–1.25 m 1.88–1.77 m 3.75 dd (7.0, 11.1)

12 13 14

132.7 148.1 124.9

7.39 d (8.2) 7.82 s

37.6 40.2 47.5

15

33.8

2.90 m

149.9

16

23.9

1.21 d (6.8)

109.8

17 18 19

23.9 18.4 27.1

1.21 d (6.8) 1.06 s 1.11 s

22.2 29.6 75.4

20

70.8

4.23 d (9.2) 4.03 d (9.2)

24.4

21 22 23 24 25 26 27 28 29 OCH3

2.17 m 2.64, 2.72 m

7.29 d (8.2)

1.45 d (4.0) 4.49 m 5.55 d (5.0) 1.56–1.52 m 1.23–1.21 m 1.60–1.56 m 1.49–1.46 m 1.92 d (12.0) 2.10 d (12.0) 5.81 dd (17.5,10.7) 4.92 dd (17.5,1.0) 4.87 dd (10.7,1.0) 0.81 s 1.31 s 3.54 d (8.5) 4.11 d (8.5) 1.20 s

129.8 194.1 52.4 46.1 72.8 114.5 147.7 50.2 32.3 24.6 37.6 40.3 47.8 149.2 110.4 22.2 22.6 175.0

2.35 d (5.0) 4.85 d (5.0) 5.71 d (5.0) 1.84 m 1.37, 1.86 m 1.60 m 2.06 d (12.2) 2.21 d (12.2) 5.85 dd (17.5,10.7) 4.94 d (17.5) 4.99 d (10.7) 0.90 s 1.55 s

23.0

0.95 s

140.5 120.9 143.3 129.3 121.5 115.1 147.4 146.9 109.9 56.3

7.51 t (11.4) 6.77 dd (15.1, 11.4) 6.94 d (15.1) 7.09 dd (8.0, 1.5) 6.89 d (8.0) 6.93 d (1.5) 3.93 s

302.2240 [M]+). The 1H NMR spectrum displayed three singlet methyls (δH 0.81, 1.31 and 1.20). Signals at δH 5.55 (d, J = 5.0 Hz, H-7), 5.81 (dd, J = 17.5, 10.7 Hz, H-15), 4.92 (dd, J = 17.5, 1.0 Hz, H-16a) and 4.87 (dd, J = 10.7, 1.0 Hz, H-16b) were assigned to the olefinic protons. The 13C NMR spectrum (Table 1) showed 20 carbons including 3 methyls, 7 methylenes with 1 terminal olefinic carbon (δC 109.8), 6 methines with 2 oxygen-bearing (δC 76.9, 75.6) and 2 olefinic (δC 117.9, 149.9) methines, and 4 quaternary carbons with 1 olefinic carbon (δC 144.9). The NMR data of compound 2 were similar to those of momilactone A, except for the appearance of 1 oxymethine group (δC 76.9), instead of one carbonyl group in momilactone A. In the HMBC spectrum, the correlation of δH 1.31 (H-18) with δC 76.9 (C-3) indicated that the oxymethine group (δC 76.9) was assigned to C-3. The NOESY correlation of δH 3.75 (H-3) with δH 1.45 (H-5) showed that the configuration of hydroxy in C-3 was β. Thus, the structure of compound 2 was identified as 4,6-epoxy-3β-hydroxy-9βpimara-7,15-diene. Compound 3 was isolated as yellow crystals which presented a molecular formula of C30H34O5 (m/z 474.2398) as determined by the HR-EI-MS. The 1H NMR spectrum (Table 1) indicated the presence of three methyl groups at δH 0.90 (s, H-17), 1.55 (s, H-18), 0.95 (s, H-20), seven olefinic protons at δH 5.71 (d, J = 5.0 Hz, H-7), δH 5.85 (dd, J = 17.5, 10.7 Hz, H-15), 4.94 (d, J = 17.5 Hz, H-16a), 4.99 (d, J = 10.7 Hz, H-16b), 7.51 (d, J = 11.4 Hz, H-21), 6.77 (dd, J = 15.1, 11.4 Hz, H-22), 6.94 (d, J = 15.1 Hz, H-23), and three aromatic protons at δH 7.09 (dd, J = 8.0, 1.5 Hz, H-25), 6.89 (d, J = 8.0 Hz, H-26) and 6.93 (d, J = 1.5 Hz, H-29). The 13C NMR spectrum (Table 1) showed

with a molecular formula of C20H26O3 (m/z 314.1878) as determined by HR-EI-MS. The 1H NMR spectrum (Table 1) showed two singlet methyls at δH 1.06 (s, H-18) and 1.11 (s, H-19); two methyls as doublets at δH 1.21 (d, J = 6.8 Hz, H-16, 17); three olefinic protons at δH 7.29 (d, J = 8.2 Hz, H-11), 7.39 (d, J = 8.2 Hz, H-12) and δH 7.82 (s, H-14); and two oxygenated methylene signals at δH 4.03 (d, J = 9.2 Hz, H-20β) and 4.23 (d, J = 9.2 Hz, H-20α). The 13C NMR spectrum (Table 1) of compound 1 displayed 20 carbons which were further classified by DEPT experiments as four methyls, four methylenes, five methines and seven quaternary carbons. Six signals between δC 124.88 and 148.14 were assigned to the aromatic carbons. The observed carbon signals at δC 198.89, 70.78 and 99.06 indicated the presence of ketone, oxygenated methylene and carbinol carbon, respectively. The above NMR data were similar to taxamairin C, abietane diterpenes [26], except for the C ring. Compared to taxamairin C, compound 1 had one fewer methoxyl and two quaternary carbons, but had two more methines in C ring, which showed that the substitute groups of hydroxy and methoxy in taxamairin C were replaced by hydrogen. In the HMBC spectrum, the correlations of H-18 with C-3, 4, 5, 19; H-20α with C-1, 3, 5, 10; H-6α with C-4, 5, 7, 8, 10; and H-14 with C-7, 9, 12, 15 were observed, which confirmed the structure of compound 1 (Fig. 3). In the NOESY spectrum, the observed correlations of H-5/H-19, H-18/H-20β, H-2α/H-19, H-1α/H-5, H-1α/H-5 and H-6β/H-20 determined the configuration of 1. Consequently, compound 1 was determined as 3,20-epoxy-3α-hydroxy8,11,13-abietatrien-7-one. Compound 2 was obtained as a colorless needle and its molecular formula was identified as C20H30O2 by the positive HREIMS (m/z 3

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Fig. 1. Effects of seven compounds isolated from rice hulls on seedling growth of Echinochloa crusgalli. The concentrations of 7 tested compounds were 5, 10 and 20 μg/mL. Distilled water was used for control. Phytotoxicity of momilactone A and B was determined in a separate experiment (C, D). Values are mean ± standard error (n = 3). Letters above bars indicate significant difference among treatments (P < 0.05 according to Tukey's multiple range test).

Fig. 2. Structures of compounds 1–7.

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Fig. 3. Key HMBC correlations of compounds 1–3.

showed the highest inhibitory effect, it inhibited the root growth of E. crusgalli by 82.7% at 5 μg/mL.

Table 2 Minimum inhibitory concentrations (MIC) of 7 compounds isolated from rice hulls against 4 crop pathogenic fungi. Compounds

1 2 3 4 5 6 7

3.3. Antifungal activities

MIC (μg/mL) Magnaporthe grisea

Rhizoctoni solani

Blumeria gramineaum

Fusarium oxysporum

12.5 6.25 25 12.5 12.5 6.25 100

12.5 12.5 25 12.5 12.5 25 25

25 25 12.5 12.5 6.25 50 25

25 25 50 12.5 6.25 25 50

The compounds 1–7 were tested for their antifungal activities against M. grisea, R. solani, B. graminearum and F. oxysporum by microdilution technique [23]. The bioassay data (Table 2) displayed that compounds 1–7 showed antifungal activities. According to the Table [2], compounds 2 and 6 had the lowest MIC value of 6.25 μg/mL for M. grisea. MIC values of compounds 1, 2, 4 and 5 were 12.5 μg/mL for R. solani, while momilactone B (5) had lowest MIC value of 6.25 μg/mL for B. graminearum and F. oxysporum. The MIC value of momilactone A (4) was 12.5 μg/mL for all tested 4 fungi. In conclusion, 7 diterpenes including three new ones (1–3) were isolated from the hulls of rice, and compound 6 was isolated from rice for the first time. Compounds 2–5 are pimarane diterpene, compounds 1 and 6 are abietane diterpene and kaurane diterpene, respectively. All the compounds could inhibit the growth of E. crusgalli, and showed the antifungal activities against M. grisea, R. solani, B. graminearum and F. oxysporum. The results suggested that rice could produce plenty of secondary metabolites to defense against weeds and pathogens. In addition, the results provided the lead compounds for the synthesis of new herbicide and bactericide, and supplied the basis for the prevention of crop disease and weed.

Minimum inhibitory concentration (MIC), the lowest concentration of a compound that completely inhibited the visible growth against tested fungal species.

resonances for all 30 carbons which included 4 methyls, 5 methylenes, 11 methines and 10 quaternary carbons. Signals at δC 194.08 and 175.04 showed the presence of a ketone and lactone group, respectively. Olefinic carbons were assigned to δC 114.49, 147.72, 149.2, 110.43, 129.78, 140.52, 120.91, and 143.26. Additionally, 6 signals at δC 129.31, 121.54, 115.08, 147.39, 146.97, and 109.95 for aromatic carbons were observed. The NMR data (Table 1) of compound 3 were similar to those of momilactone A (4), a diterpenoid [8,13]. Compared with momilactone A, compound 3 had one more hydroxyl, 11 more carbons signals including 1 trisubstituted phenyl, 2 double bonds and 1 methoxyl, but had fewer 1 methylene. In the HMBC spectrum, correlations of H-1 with C-2 (δC 129.8), C-3 (δC 194.1) and C-21 (δC 140.5); H-21 with C-1 (δC 36.1), C-3 and C-23 (δC 143.3); H-23 with C-21, C-25 (δC 121.5) and C-29 (δC 109.9) showed that 1 double bond was between C-2 and C-21, another double bond between C-22 and C-23 and conjugated with phenyl. In addition, the hydroxyl and methoxyl were located at C-27, C-28, respectively, on basis of the HMBC correlations of hydroxy proton with C-27 (δC 147.4) and methoxy proton with C-28 (δC 146.9) (Fig. 3). Thus, the structure of compound 3 was identified as 2((E)-3-(4-hydroxy-3-methoxyphenyl) allylidene) momilactone A, which was formed by the addition and dehydration reactions of 4-hydroxy-3methoxy cinnamic aldehyde and momilactone A.

Acknowledgments This research was financially supported by the National Natural Science Foundation of China (31800332, 31670414, 31770474), the Young and Middle-aged Teachers Education Scientific Research Project of Fujian Provincial Department of Education (JAT170203). Conflict of interest The authors declared that they have no conflicts of interest to this work. We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted. Appendix A. Supplementary data

3.2. Phytotoxicity

Supplementary data to this article can be found online at https:// doi.org/10.1016/j.fitote.2019.104183.

E. crusgalli is the most serious weed in paddy field and affects both growth and yield of the rice. In this study, the bioactivities of compounds 1–7 against E. crusgalli were evaluated at the concentration from 5 μg/mL to 20 μg/mL. The bioassay data (Fig. 1) showed that all compounds significantly inhibited the E. crusgalli seedlings. Compounds 1–4, 6 and 7 displayed similar inhibitory effects, and they inhibited root growth by 29%–43% at 20 μg/mL. While, momilactone B (5)

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