New Diterpenes from a Godavari Mangrove, Ceriops decandra

• Introduction
• Materials and Methods
• General experimental procedures
• Plant material
• Extraction and isolation
• Isolates
• Supporting Information
• Results and Discussion
• Acknowledgments
• References

Abstract

Eleven new diterpenes, named decandrins A−K (1–11), including nine abietanes (1–9) and two podocarpanes (10–11), were isolated from the barks of an Indian mangrove, Ceriops decandra, collected in the mangrove swamp of Godavari estuary, Andhra Pradesh, together with four known abietanes. The structures of these compounds were established on the basis of spectroscopic data (new compounds) or comparison with data in the literature (known compounds). This is the first report of abietane and podocarpane diterpenoids from C. decandra.

Introduction

Plants of the genus Ceriops (Rhizophoraceae) are mangroves consisting of five species, namely C. tagal (Perr.) C. B. Robinson, C. decandra (Griff.) Ding Hou, C. australis (White) Ballment, Smith & Stoddart, C. zippeliana Blume, and C. pseudodecandra Sheue, Liu, Tsai & Yang. C. tagal and C. decandra are widely distributed along the sea coasts of Africa, Madagascar, South Asia, and South Pacific islands, C. australis is endemic to the littoral zone of Australasia (i.e., Australia, New Zealand, and Papua New Guinea), C. zippeliana occurs in areas of southeastern Asia, and C. pseudodecandra occurs in Australia, New Guinea, and Seram [1], [2], [3], [4]. The barks of C. decandra have been utilized as a folk medicine for the treatment of diarrhea, amoebiasis, hemorrhage, and malignant ulcers in India [5]. A previous chemical investigation of this plant yielded 28 compounds, including five kaurenes, four beyaranes, three pimaranes, and sixteen lupanes [6]. In the current paper, we present the isolation and characterization of eleven new diterpenes (1–11) from the barks of an Indian mangrove, C. decandra, collected in the mangrove swamp of Godavari estuary, Andhra Pradesh, together with four known abietanes.

Materials and Methods

General experimental procedures

Optical rotations were recorded on a Polaptronic HNQW5 automatic high-resolution polarimeter (Schmidt & Haensch Co. Ltd.). UV spectra were obtained on a Beckman DU-640 UV spectrophotometer. NMR spectra were recorded on a Bruker Avance 400 NMR spectrometer in CDCl₃. High-resolution ESI-MS were performed on Bruker APEX II, Bruker maXis UHR-TOF, and Synapt G2 UPLC-Q-TOF mass spectrometers in the positive ion mode. For column chromatography, silica gel (200–300 mesh) (Qingdao Mar. Chem. Ind. Co. Ltd.) and RP C₁₈ gel (YMC) were used. High-pressure liquid chromatography (HPLC) was performed on a Shimadzu LC-6AD controller with an SPD-20A UV-Vis detector equipped with a YMC-Pack ODS-A column (250 × 10 mm i. d., 5 µm) and a YMC-Pack ODS-A column (250 × 4.6 mm i. d., 5 µm).

Plant material

Barks of C. decandra were collected in September 2009 at the mangrove swamp of Godavari estuary, Andhra Pradesh, India. The identification of the plant was performed by one of the authors (T. S.). A voucher sample (No. CD-001) is maintained in Marine Drugs Research Center, College of Pharmacy, Jinan University.

Extraction and isolation

Air-dried barks (7.4 kg) of C. decandra were extracted with 95 % EtOH at room temperature (5 × 40 L, 48 h each). The EtOH extract was concentrated under reduced pressure, followed by suspension in water and extraction with ethyl acetate. The ethyl acetate extract was suspended again in water and extracted with chloroform. The resulting extract (65.2 g) was subjected to silica gel column chromatography (780 × 90 mm i. d., 200–300 mesh, 2000 g) and eluted with petroleum ether-acetone [100 : 0 (10 L), 100 : 1 (10 L), 50 : 1 (10 L), 30 : 1 (10 L), 20 : 1 (10 L), 10 : 1 (10 L), 5 : 1 (10 L), 3 : 1 (10 L), 2 : 1 (10 L), 1 : 1 (10 L), 1 : 2 (10 L)] to yield 285 fractions. Fractions 78–113 (F1) were combined and further purified using RP C₁₈ column chromatography (530 × 63 mm i. d., 50 µm, 800 g) and eluted with acetone-H₂O (gradient 30, 45, 60, 75, 90, 100 %, each 3 L) to afford 190 subfractions. Then subfractions F1.49–66 were combined and subjected to preparative HPLC (YMC-Pack 250 × 10 mm i. d., 5 µm, 55 % MeCN in H₂O, flow rate 3 mL/min) to afford 3 (4.7 mg), 5,8,11,13-abietatetraen-3,7-dione (2.9 mg), and 3β,7α-dihydroxy-abieta-8,11,13-triene (3.8 mg). Subfractions F1.76–96 were combined and subjected to preparative HPLC (YMC-Pack 250 × 10 mm i. d., 5 µm, 65 % MeCN in H₂O, flow rate 3 mL/min) to afford seven subfractions. Subfraction F1.76–96–1 was subjected to preparative HPLC (YMC-Pack 250 × 4.6 mm i. d., 5 µm, 65 % MeCN in H₂O, flow rate 1 mL/min) to afford 1 (7.2 mg) and 4 (5.7 mg). Subfraction F1.76–96–5 was subjected to preparative HPLC (YMC-Pack 250 × 4.6 mm i. d., 5 µm, 75 % MeOH in H₂O, flow rate 1 mL/min) to afford 5 (4.6 mg). Fractions 131–146 (F2) were combined and further purified using RP C₁₈ column chromatography (410 × 45 mm i. d., 50 µm, 320 g) and eluted with acetone-H₂O (gradient 30, 45, 60, 75, 90, 100 %, each 1.5 L) to afford 67 subfractions. Subfractions F2.18–19 were combined and subjected to preparative HPLC (YMC-Pack 250 × 4.6 mm i. d., 5 µm, 55 % MeCN in H₂O, flow rate 1 mL/min) to afford 6 (3.8 mg) and 8 (8.0 mg). Fractions 173–204 (F3) were combined and further purified using RP C₁₈ column chromatography (350 × 63 mm i. d., 50 µm, 520 g) eluted with acetone-H₂O (gradient 30, 45, 60, 75, 90, 100 %, each 1.5 L) to afford 57 subfractions. Subfractions F3.5–7 were combined and subjected to preparative HPLC (YMC-Pack 250 × 10 mm i. d., 5 µm, 48 % MeOH in H₂O, flow rate 3 mL/min) to afford 7 (5.6 mg) and 11 (7.2 mg). Subfractions F3.8–13 were combined and subjected to preparative HPLC (YMC-Pack 250 × 10 mm i. d., 5 µm, 34 % MeCN in H₂O, flow rate 3 mL/min) to afford 2 (4.4 mg), 3 (11.2 mg), 9 (4.7 mg), and 10 (6.4 mg). Subfractions F3.15–17 were combined and subjected to preparative HPLC (YMC-Pack 250 × 10 mm i. d., 5 µm, 38 % MeCN in H₂O, flow rate 3 mL/min) to afford 14,18-dihydroxyabieta-8,11,13-trien-7-one (1.2 mg) and 15,18-dihydroxyabieta-8,11,13-triene (3.0 mg).

Isolates

Decandrin A (1) (3β-hydroxy-5,8,11,13-abietatetraen-7-one): Colorless solid; [α]_D ²⁵ − 18.9 (c 0.61, Me₂CO); UV_max (191.5, 213.2, 260.3 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 1]; HR-ESI-MS: m/z = 299.1983 [M + H]⁺ (calcd. for C₂₀H₂₇O₂: 299.2006).

Decandrin B (2) (3β,13β-dihydroxy-8(14)-abietaen-7-one): Colorless solid; [α]_D ²⁵ 0 (c 0.40, Me₂CO); UV_max (247.1 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 1]; HR-ESI-MS: m/z = 343.2244 [M + Na]⁺ (calcd. for C₂₀H₃₂NaO₃: 343.2244).

Decandrin C (3) (15-hydroxy-8,11,13-abietatrien-3,7-dione): Colorless solid; [α]_D ²⁵ + 13.0 (c 0.54, Me₂CO); UV_max (205.5, 279.9, 319.1 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 1]; HR-ESI-MS: m/z = 315.1941 [M + H]⁺ (calcd. for C₂₀H₂₇O₃: 315.1955).

Decandrin D (4) (18-hydroxy-5,8,11,13-abietatetraen-7-one): Colorless solid; [α]_D ²⁵ − 26.7 (c 0.45, Me₂CO); UV_max (192.0, 213.2, 261.4 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 2]; HR-ESI-MS: m/z = 299.1980 [M + H]⁺ (calcd. for C₂₀H₂₇O₂: 299.2006).

Decandrin E (5) (6,8,11,13-abietatetraen-3β-ol): Colorless solid; [α]_D ²⁵ + 49.8 (c 0.60, Me₂CO); UV_max (213.1, 260.6 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 2]; HR-ESI-MS: m/z = 285.2209 [M + H]⁺ (calcd. for C₂₀H₂₉O: 285.2213).

Decandrin F (6) (18-hydroxy-7,13-abietadien-6-one): Colorless solid; [α]_D ²⁵ + 43.3 (c 0.21, Me₂CO); UV_max (193.7, 295.8 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 2]; HR-ESI-MS: m/z = 303.2311 [M + H]⁺ (calcd. for C₂₀H₃₁O₂: 303.2319).

Decandrin G (7) (3β,15-dihydroxy-8,11,13-abietatrien-7-one): Colorless solid; [α]_D ²⁵ + 23.2 (c 0.56, Me₂CO); UV_max (210.5, 254.2, 301.8 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 3]; HR-ESI-MS: m/z = 317.2116 [M + H]⁺ (calcd. for C₂₀H₂₉O₃: 317.2111).

Decandrin H (8) (3β-hydroxy-8(14),12-abietadien-7-one): Colorless solid; [α]_D ²⁵ + 30.9 (c 0.55, Me₂CO); UV_max (190.6, 219.9, 300.2 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 3]; HR-ESI-MS: m/z = 303.2288 [M + H]⁺ (calcd. for C₂₀H₃₁O₂: 303.2319).

Decandrin I (9) (15,18-dihydroxy-6,8,11,13-abietatetraene): Colorless solid; [α]_D ²⁵ + 27.6 (c 0.46, Me₂CO); UV_max (218.9, 266.2 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 3]; HR-ESI-MS: m/z = 323.1978 [M + Na]⁺ (calcd. for C₂₀H₂₈NaO₂: 323.1982); 623.4064 [2M + Na]⁺ (calcd. for C₄₀H₅₆NaO₄: 623.4071).

Decandrin J (10) (18-hydroxy-6,8(14)-podocarpadien-13-one): Colorless solid; [α]_D ²⁵ + 1.09 (c 0.64, Me₂CO); UV_max (289.7 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 4]; HR-ESI-MS: m/z = 261.1855 [M + H]⁺ (calcd. for C₁₇H₂₅O₂: 261.1849); 283.1672 [M + Na]⁺ (calcd. for C₁₇H₂₄NaO₂: 283.1669); 543.3452 [2M + Na]⁺ (calcd. for C₃₄H₄₈NaO₄: 543.3445).

Decandrin K (11) (3β-hydroxy-6,8(14)-podocarpadien-13-one): Colorless solid; [α]_D ²⁵ + 34.9 (c 0.72, Me₂CO); UV_max (289.7 nm); for ¹H and ¹³C NMR spectroscopic data, see [Table 4]; HR-ESI-MS: m/z = 261.1855 [M + H]⁺ (calcd. for C₁₇H₂₅O₂: 261.1849); 283.1675 [M + Na]⁺ (calcd. for C₁₇H₂₄NaO₂: 283.1669); 543.3463 [2M + Na]⁺ (calcd. for C₃₄H₄₈NaO₄: 543.3445).

Supporting Information

Original spectra for compounds 1–11 are available as Supporting Information.

Results and Discussion

Decandrin A (1) was obtained as a colorless solid. The molecular formula C₂₀H₂₆O₂ was established by HR-ESI-MS (m/z 299.1983, calcd. for [M + H]⁺ 299.2006). The NMR spectroscopic data of 1 ([Table 1]) indicated the presence of a benzene ring [δ _H 7.99 (d, 2.0), δ _C 123.5; δ _H 7.43 (br s), δ _C 125.1; δ _H 7.43 (br s), δ _C 131.4; δ _C 129.8, 147.2, 150.8], an olefinic methine group [δ _H 6.57 (br s), δ _C 125.8], an oxygenated methine group [δ _H 3.43 (dd, J = 11.2, 4.4 Hz), δ _C 76.5], five methyl groups [δ _H 1.31 (3H, s), δ _C 22.3; δ _H 1.28 (d, J = 6.9 Hz), δ _C 23.8; δ _H 1.28 (d, J = 6.9 Hz), δ _C 23.8; δ _H 1.37 (3H, s), δ _C 27.4; δ _H 1.54 (3H, s), δ _C 32.2], and a conjugated ketone group (δ _C 186.1). The above NMR spectroscopic data of 1 were similar to those of 5,8,11,13-abietatetraen-3,7-dione [7], except for the replacement of the C-3 ketone group of the latter by a hydroxyl group, which was corroborated by ¹H−¹H COSY correlations between H₂-2 and the oxygenated H-3 [δ _H 3.43 (dd, J = 11.2, 4.4 Hz)], and HMBC correlations from H₃-18 and H₃-19 to the oxygenated C-3 (δ _C 76.5) ([Fig. 2]). The α-orientation of H-3 was suggested by its axial-axial and axial-equatorial coupling constants with H₂-2, viz. J (H_aH_a) = 11.2 Hz and J (H_aH_e) = 4.4 Hz, respectively. Thus, 1 was assigned as 3β-hydroxy-5,8,11,13-abietatetraen-7-one ([Fig. 1]).

Decandrin B (2), appearing as a colorless solid, had the molecular formula C₂₀H₃₂O₃ as established by HR-ESI-MS (m/z 343.2244, calcd. for [M + Na]⁺ 343.2244). The NMR spectroscopic data of 2 ([Table 1]) were similar to those of sabiperone E [8], except for the replacement of the C-3 ketone group of the latter by a hydroxyl group, which was corroborated by ¹H−¹H COSY correlations between H₂-2 and the oxygenated H-3 [δ _H 3.31 (dd, J = 11.5, 4.0 Hz)], and HMBC correlations from H₃-18 and H₃-19 to the oxygenated C-3 (δ _C 78.6) ([Fig. 2]). Furthermore, the α-orientation of H-3 was suggested by its axial-axial and axial-equatorial coupling constants with H₂-2, viz. J (H_aH_a) = 11.5 Hz and J (H_aH_e) = 4.0 Hz, respectively. The β-orientation of 13-OH was indicated by the similar ¹³C NMR data of its C-ring [δ _C 138.1 (C-8), 18.6 (C-11), 29.5 (C-12), 71.8 (C-13), 139.9 (C-14)] to those of sabiperone E [δ _C 137.6 (C-8), 18.9 (C-11), 29.5 (C-12), 72.0 (C-13), 141.0 (C-14)] with a 13β-OH group, but quite different from those of sabiperone D [δ _C 136.0 (C-8), 21.2 (C-11), 32.8 (C-12), 72.6 (C-13), 142.0 (C-14)] with a 13α-OH moiety [8] ([Table 1]). The α-orientation of H-5 and H-9 was established by NOE interactions between H-3/H-5, H₃-18/H-5, and H-9/H-5 ([Fig. 3]). Based on the above results, the structure of 2 was identified as 3β,13β-dihydroxy-8(14)-abietaen-7-one ([Fig. 1]).

Decandrin C (3) was obtained as a colorless solid. The molecular formula C₂₀H₂₆O₃ was established by HR-ESI-MS (m/z 315.1941, calcd. for [M + H]⁺ 315.1955). The NMR spectroscopic data of 3 ([Table 1]) were similar to those of 3β-hydroxy-abieta-8,11,13-trien-7-one [9], except for the replacement of 3-OH of the latter by a ketone group and the presence of 15-OH. HMBC correlations from H₃-19 and H₂-1 to the carbon (δ _C 214.3) of the ketone group suggested its location at C-3 ([Fig. 2]). An oxygenated quaternary carbon (δ _C 72.3), indicated by the ¹³C NMR and DEPT spectroscopic data, was shown to be C-15 by HMBC correlations from H₃-16 and H₃-17 to this carbon ([Fig. 2]). In addition, the attachment of a hydroxyl group to C-15 was confirmed by the molecular formula of 3. Therefore, 3 was elucidated as 15-hydroxy-8,11,13-abietatrien-3,7-dione ([Fig. 1]).

Decandrin D (4), appearing as a colorless solid, had the molecular formula C₂₀H₂₆O₂ as established by HR-ESI-MS (m/z 299.1980, calcd. for [M + H]⁺ 299.2006). The NMR spectroscopic data of 4 ([Table 2]) were similar to those of 1, except for the presence of a hydroxyl group at C-18 and the absence of one hydroxyl group at C-3 in 1. An oxygenated CH₂ group (δ _C 70.9), indicated by the ¹³C NMR and DEPT spectroscopic data, was suggested to be CH₂-18 by HMBC correlations between H₂-18/C-5 and H₃-19/C-18 ([Fig. 2]). In addition, the attachment of a hydroxyl group to C-18 was confirmed by the molecular formula of 4. Consequently, the structure of 4 was determined to be 18-hydroxy-5,8,11,13-abietatetraen-7-one ([Fig. 1]).

Decandrin E (5) was obtained as a colorless solid. The molecular formula C₂₀H₂₈O was established by HR-ESI-MS (m/z 285.2209, calcd. for [M + H]⁺ 285.2213). The NMR spectroscopic data of 5 ([Table 2]) were similar to those of 1, except for the presence of a Δ^6,7 double bond and the absence of a Δ^5,6 double bond and one C-7 ketone group in 1. The presence of a Δ^6,7 double bond was corroborated by a proton spin system, H-5−H-6−H-7, which was deduced from ¹H−¹H COSY correlations, and further confirmed by HMBC correlations between H-6/C-4, H-6/C-8, H-7/C-14, and H-7/C-9 ([Fig. 2]). In addition, the α-orientation of H-3 was suggested by its axial-axial and axial-equatorial coupling constants with H₂-2, viz. J (H_aH_a) = 11.1 Hz and J (H_aH_e) = 4.5 Hz, respectively. The α-orientation of H-5 was established by NOE interactions between H-3/H-5 and H₃-18/H-5 ([Fig. 3]). Hence, 5 was assigned as 6,8,11,13-abietatetraen-3β-ol ([Fig. 1]).

Decandrin F (6), appearing as a colorless solid, had the molecular formula C₂₀H₃₀O₂ as established by HR-ESI-MS (m/z 303.2311, calcd. for [M + H]⁺ 303.2319). The NMR spectroscopic data of 6 ([Table 2]) were similar to those of 7,13-abietadien-18-ol [10], except for the presence of a ketone group at C-6, which was confirmed by the HMBC correlation from H-5 to C-6 (δ _C 202.7) ([Fig. 2]). Based on the above results, the structure of 6 was identified as 18-hydroxy-7,13-abietadien-6-one ([Fig. 1]).

Decandrin G (7) was obtained as a colorless solid. The molecular formula C₂₀H₂₈O₃ was established by HR-ESI-MS (m/z 317.2116, calcd. for [M + H]⁺ 317.2111). The NMR spectroscopic data of 7 ([Table 3]) were similar to those of 3, except for the replacement of the C-3 ketone group in 3 by a hydroxyl group, which was confirmed by ¹H−¹H COSY correlations between H₂-2 and the oxygenated H-3 [δ _H 3.35 (dd, J = 11.2, 4.8 Hz)], and HMBC correlations from H₃-18 and H₃-19 to the oxygenated C-3 (δ _C 78.1) ([Fig. 2]). The α-orientation of H-3 was suggested by its axial-axial and axial-equatorial coupling constants with H₂-2, viz. J (H_aH_a) = 11.2 Hz and J (H_aH_e) = 4.8 Hz, respectively. The α-orientation of H-5 was established by NOE interactions between H-3/H-5 and H₃-18/H-5 ([Fig. 3]). Therefore, the structure of 7 was established as 3β,15-dihydroxy-8,11,13- abietatrien-7-one ([Fig. 1]).

Decandrin H (8), appearing as a colorless solid, had the molecular formula C₂₀H₃₀O₂ as established by HR-ESI-MS (m/z 303.2288, calcd. for [M + H]⁺ 303.2319). The NMR spectroscopic data of 8 ([Table 3]) were similar to those of 2, except for the presence of a Δ ^12,13 double bond and the absence of 13-OH in 2. The existence of a Δ ^12,13 double bond was corroborated by ¹H−¹H COSY correlations between H₂-11 and H-12, and HMBC correlations between H₂-11/C-10, H₂-11/C-12, H₃-16/C-13, and H₃-17/C-13 ([Fig. 2]). Hence, 8 was identified as 3β-hydroxy-8(14),12-abietadien-7-one ([Fig. 1]).

Decandrin I (9) was obtained as a colorless solid. The molecular formula C₂₀H₂₈O₂ was established by HR-ESI-MS (m/z 323.1978, calcd. for [M + Na]⁺ 323.1982). The NMR spectroscopic data of 9 ([Table 3]) were similar to those of 15,19-dihydroxy- abieta-6,8,11,13-tetraene [11], except for the different orientation of the C-4−linked methyl group. The β-orientation of the C-4−linked methyl group was established by NOE interactions between protons of this methyl group and H₃-20 ([Fig. 3]). Thus, the structure of 9 was identified as 15,18-dihydroxy-6,8,11,13-abietatetraene ([Fig. 1]).

Decandrin J (10), appearing as a colorless solid, had the molecular formula C₁₇H₂₄O₂ as established by HR-ESI-MS (m/z 261.1855, calcd. for [M + H]⁺ 261.1849). The NMR spectroscopic data of 10 ([Table 4]) were similar to those of abiesanordine B [12], except for the presence of a Δ^6,7 double bond, which was corroborated by a proton spin system, H-5−H-6−H-7, and further confirmed by HMBC correlations between H-6/C-5, H-6/C-10, H-7/C-5, H-7/C-8, H-7/C-9, and H-7/C-14 ([Fig. 2]). Consequently, the structure of 10 was concluded to be 18-hydroxy-6,8(14)-podocarpadien-13-one ([Fig. 1]).

Decandrin K (11) was obtained as a colorless solid. The molecular formula C₁₇H₂₄O₂ was established by HR-ESI-MS (m/z 261.1855, calcd. for [M + H]⁺ 261.1849). The NMR spectroscopic data of 11 ([Table 4]) were similar to those of 10, except for the presence of a hydroxyl group at C-3 and the absence of one hydroxyl group at C-18 in 10. An oxygenated CH group (δ _C 78.5), indicated by the ¹³C NMR and DEPT spectroscopic data, was suggested to be CH-3 by ¹H−¹H COSY correlations between H₂-2 and H-3 [δ _H 3.36 (dd, J = 11.6, 4.2 Hz)], and HMBC correlations from H₃-18 and H₃-19 to C-3 (δ _C 78.5) ([Fig. 2]). In addition, the attachment of a hydroxyl group to C-3 was confirmed by the molecular formula of 11. Furthermore, the α-orientation of H-3 was suggested by its axial-axial and axial-equatorial coupling constants with H₂-2, viz. J (H_aH_a) = 11.6 Hz and J (H_aH_e) = 4.2 Hz, respectively. Based on the above results, the structure of 11 was identified as 3β-hydroxy-6,8(14)-podocarpadien-13-one ([Fig. 1]).

By comparison of their physical and spectroscopic data with those of literatures, the structures of four known abietanes were identified as 5,8,11,13-abietatetraen-3,7-dione [7], 3β,7α-dihydroxy-abieta-8,11,13-triene [13], 14,18-dihydroxyabieta-8,11,13-trien-7-one [14], and 15,18-dihydroxyabieta-8,11,13-triene [15], respectively. All the above diterpenes were identified from this mangrove plant for the first time.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (NO. 31100258 to M. Y. L.; NO.s 31170331 and 81125022 to J. W.) and the Guangdong Key Science and Technology Special Project (NO. 2011A080403020 to J. W.).

Conflict of Interest

The authors declare no conflict of interest.

• References

• 1 Wu J, Xiao Q, Xu J, Li MY, Pan JY, Yang MH. Natural products from true mangrove flora: source, chemistry and bioactivities. Nat Prod Rep 2008; 25: 955-981
  CrossrefPubMedSearch in Google Scholar
• 2 Huang YL, Tan FX, Su GH, Deng SL, He HH, Shi SH. Population genetic structures of three species in the mangrove genus Ceriops (Rhizophoraceae) from Indo West Pacific. Genetica 2008; 133: 47-56
  CrossrefPubMedSearch in Google Scholar
• 3 Sheue CR, Liu HY, Tsai CC, Rashid SMA, Yong JWH, Yang YP. On the morphology and molecular basis of segregation of Ceriops zippeliana and C. decandra (Rhizophoraceae) from Asia. Blumea 2009; 54: 220-227
  CrossrefPubMedSearch in Google Scholar
• 4 Sheue CR, Liu HY, Tsai CC, Yang YP. Comparison of Ceriops pseudodecanda sp. nov. (Rhizophoraceae), a new mangrove species in Australasia, with related species. Bot Stud 2010; 51: 237-248
  PubMedSearch in Google Scholar
• 5 Rastogi RP, Mehrotra BN. Compendium of Indian plants. New Delhi: New Delhi Publications & Information Directorate; 1991
  Search in Google Scholar
• 6 Wang H, Li MY, Wu J. Chemical constituents and some biological activities of plants from the Genus Ceriops . Chem Biodivers 2012; 9: 1-11
  CrossrefPubMedSearch in Google Scholar
• 7 Matsumoto T, Takeda Y, Soh K, Matsumura H, Imai S. A new synthesis of 3-oxosapriparaquinone, a diterpene from Salvia prionitic Hance (Libiatae). Chem Pharm Bull 1996; 44: 1588-1590
  CrossrefPubMedSearch in Google Scholar
• 8 Janar J, Nugroho AE, Wong CP, Hirasawa Y, Kaneda T, Shirota O, Morita H. Sabiperones A–F, new diterpenoids from Juniperus sabina . Chem Pharm Bull 2012; 60: 154-159
  CrossrefPubMedSearch in Google Scholar
• 9 Seca AML, Silva AMS, Bazzocchi IL, Jimenez IA. Diterpene constituents of leaves from Juniperus brevifolia . Phytochemistry 2008; 69: 498-505
  CrossrefPubMedSearch in Google Scholar
• 10 San Feliciano A, Miguel del Corral JM, Gordaliza M, Salinero M. ¹³C NMR data for abieta-7,13-diene diterpenoids. Magn Reson Chem 1993; 31: 841-844
  CrossrefPubMedSearch in Google Scholar
• 11 Yang NJ, Liu L, Tao WW, Duan JA, Tian LJ. Diterpenoids from Pinus massoniana resin and their cytotoxicity against A431 and A549 cells. Phytochemistry 2010; 71: 1528-1533
  CrossrefPubMedSearch in Google Scholar
• 12 Yang XW, Li SM, Feng L, Shen YH, Tian JM, Liu XH, Zeng HW, Zhang C, Zhang WD. Abiesanordines A−N: fourteen new norditerpenes from Abies georgei . Tetrahedron 2008; 64: 4354-4362
  CrossrefPubMedSearch in Google Scholar
• 13 Tanaka CMA, Radke VSCO, Silva CC, Nakamura CV, Oliveira PL, Kato L, Oliveira CMA. Abietatrenes diterpenoids from Sagittaria montevidensis SSP montevidensis . Quim Nova 2010; 33: 30-32
  CrossrefPubMedSearch in Google Scholar
• 14 Chen CY, Lin RJ, Huang JC, Wu YH, Cheng MJ, Hung HC, Lo WL. Chemical constituents from the whole plant of Gaultheria itoana Hayata. Chem Biodivers 2009; 6: 1737-1743
  CrossrefPubMedSearch in Google Scholar
• 15 Miguel de Corral JM, Gordaliza M, Salinero MA, Sanfeliciano A. ¹³C NMR data for abieta-8,11,13-triene diterpenoids. Magn Reson Chem 1994; 32: 774-781
  CrossrefPubMedSearch in Google Scholar

Correspondence

• References

• 1 Wu J, Xiao Q, Xu J, Li MY, Pan JY, Yang MH. Natural products from true mangrove flora: source, chemistry and bioactivities. Nat Prod Rep 2008; 25: 955-981
  CrossrefPubMedSearch in Google Scholar
• 2 Huang YL, Tan FX, Su GH, Deng SL, He HH, Shi SH. Population genetic structures of three species in the mangrove genus Ceriops (Rhizophoraceae) from Indo West Pacific. Genetica 2008; 133: 47-56
  CrossrefPubMedSearch in Google Scholar
• 3 Sheue CR, Liu HY, Tsai CC, Rashid SMA, Yong JWH, Yang YP. On the morphology and molecular basis of segregation of Ceriops zippeliana and C. decandra (Rhizophoraceae) from Asia. Blumea 2009; 54: 220-227
  CrossrefPubMedSearch in Google Scholar
• 4 Sheue CR, Liu HY, Tsai CC, Yang YP. Comparison of Ceriops pseudodecanda sp. nov. (Rhizophoraceae), a new mangrove species in Australasia, with related species. Bot Stud 2010; 51: 237-248
  PubMedSearch in Google Scholar
• 5 Rastogi RP, Mehrotra BN. Compendium of Indian plants. New Delhi: New Delhi Publications & Information Directorate; 1991
  Search in Google Scholar
• 6 Wang H, Li MY, Wu J. Chemical constituents and some biological activities of plants from the Genus Ceriops . Chem Biodivers 2012; 9: 1-11
  CrossrefPubMedSearch in Google Scholar
• 7 Matsumoto T, Takeda Y, Soh K, Matsumura H, Imai S. A new synthesis of 3-oxosapriparaquinone, a diterpene from Salvia prionitic Hance (Libiatae). Chem Pharm Bull 1996; 44: 1588-1590
  CrossrefPubMedSearch in Google Scholar
• 8 Janar J, Nugroho AE, Wong CP, Hirasawa Y, Kaneda T, Shirota O, Morita H. Sabiperones A–F, new diterpenoids from Juniperus sabina . Chem Pharm Bull 2012; 60: 154-159
  CrossrefPubMedSearch in Google Scholar
• 9 Seca AML, Silva AMS, Bazzocchi IL, Jimenez IA. Diterpene constituents of leaves from Juniperus brevifolia . Phytochemistry 2008; 69: 498-505
  CrossrefPubMedSearch in Google Scholar
• 10 San Feliciano A, Miguel del Corral JM, Gordaliza M, Salinero M. ¹³C NMR data for abieta-7,13-diene diterpenoids. Magn Reson Chem 1993; 31: 841-844
  CrossrefPubMedSearch in Google Scholar
• 11 Yang NJ, Liu L, Tao WW, Duan JA, Tian LJ. Diterpenoids from Pinus massoniana resin and their cytotoxicity against A431 and A549 cells. Phytochemistry 2010; 71: 1528-1533
  CrossrefPubMedSearch in Google Scholar
• 12 Yang XW, Li SM, Feng L, Shen YH, Tian JM, Liu XH, Zeng HW, Zhang C, Zhang WD. Abiesanordines A−N: fourteen new norditerpenes from Abies georgei . Tetrahedron 2008; 64: 4354-4362
  CrossrefPubMedSearch in Google Scholar
• 13 Tanaka CMA, Radke VSCO, Silva CC, Nakamura CV, Oliveira PL, Kato L, Oliveira CMA. Abietatrenes diterpenoids from Sagittaria montevidensis SSP montevidensis . Quim Nova 2010; 33: 30-32
  CrossrefPubMedSearch in Google Scholar
• 14 Chen CY, Lin RJ, Huang JC, Wu YH, Cheng MJ, Hung HC, Lo WL. Chemical constituents from the whole plant of Gaultheria itoana Hayata. Chem Biodivers 2009; 6: 1737-1743
  CrossrefPubMedSearch in Google Scholar
• 15 Miguel de Corral JM, Gordaliza M, Salinero MA, Sanfeliciano A. ¹³C NMR data for abieta-8,11,13-triene diterpenoids. Magn Reson Chem 1994; 32: 774-781
  CrossrefPubMedSearch in Google Scholar

• Supplementary Material