Trichodermaerin: a diterpene lactone from Trichoderma asperellum

Chantrapromma, S.; Jeerapong, C.; Phupong, W.; Quah, C.K.; Fun, H.-K.

doi:10.1107/S1600536814004632

organic compounds

CRYSTALLOGRAPHIC
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ISSN: 2056-9890

Volume 70| Part 4| April 2014| Pages o408-o409

doi:10.1107/S1600536814004632

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Trichodermaerin: a diterpene lactone from Trichoderma asperellum

Suchada Chantrapromma,^a ^*‡ Chotika Jeerapong,^b Worrapong Phupong,^b Ching Kheng Quah ^c and Hoong-Kun Fun ^c §

^aDepartment of Chemistry, Faculty of Science, Prince of Songkla University, Hat-Yai, Songkhla 90112, Thailand, ^bSchool of Science, Walailak University, Thasala, Nakhon Si Thammarat 80160, Thailand, and ^cX-ray Crystallography Unit, School of Physics, Universiti Sains Malaysia, 11800 USM, Penang, Malaysia
^*Correspondence e-mail: suchada.c@psu.ac.th

(Received 1 January 2014; accepted 28 February 2014; online 8 March 2014)

The title compound, C₂₀H₂₈O₃, known as `trichodermaerin' [systematic name: (4E)-4,9,15,16,16-pentamethyl-6-oxatetracyclo[10.3.1.0^1,10.0^5,9]hexadec-4-ene-7,13-dione], is a diterpene lactone which was isolated from Trichoderma asperellum. The structure has a tetracycic 6–5–7–5 ring system, with the cyclohexanone ring adopting a twisted half-chair conformation and the cyclopentane ring adopting a half-chair conformation, whereas the cycloheptene and tetrahydrofurananone rings are in chair and envelope (with the methyl-substituted C atom as the flap) conformations, respectively. The three-dimensional architecture is stabilized by C—H⋯O interactions.

CCDC reference: 989255

Related literature

For standard bond-length data, see: Allen et al. (1987 ). For ring conformations, see: Cremer & Pople (1975 ). For background to Trichoderma and diterpene lactones, see, for example: De los Santos-Villalobos et al. (2011 ); Evidente et al. (2006 ); Hajieghrari et al. (2008 ); Kumar et al. (2012 ); Vinale (2009 ); Xie et al. (2013 ). For the stability of the temperature controller used in the data collection, see: Cosier & Glazer (1986 ).

Experimental

Crystal data

C₂₀H₂₈O₃
M_r = 316.42
Monoclinic, P 2₁
a = 9.1703 (4) Å
b = 10.2234 (5) Å
c = 9.2681 (4) Å
β = 108.539 (1)°
V = 823.81 (6) Å³
Z = 2
Mo Kα radiation
μ = 0.08 mm⁻¹
T = 100 K
0.47 × 0.28 × 0.17 mm

Data collection

Bruker APEX DUO CCD area-detector diffractometer
Absorption correction: multi-scan (SADABS; Bruker, 2009 ) T_min = 0.962, T_max = 0.986
17364 measured reflections
2517 independent reflections
2492 reflections with I > 2σ(I)
R_int = 0.022

Refinement

R[F² > 2σ(F²)] = 0.026
wR(F²) = 0.069
S = 1.06
2517 reflections
213 parameters
1 restraint
H-atom parameters constrained
Δρ_max = 0.29 e Å⁻³
Δρ_min = −0.16 e Å⁻³

Table 1
Hydrogen-bond geometry (Å, °)

D—H⋯A	D—H	H⋯A	D⋯A	D—H⋯A
C3—H3B⋯O3ⁱ	0.99	2.60	3.5649 (14)	165
C16—H16B⋯O2ⁱⁱ	0.98	2.41	3.2810 (16)	148
C20—H20C⋯O3ⁱⁱⁱ	0.98	2.56	3.5292 (15)	173
Symmetry codes: (i) $[-x+1, y-{\script{1\over 2}}, -z]$ ; (ii) $[-x+1, y+{\script{1\over 2}}, -z+1]$ ; (iii) x, y-1, z.

Data collection: APEX2 (Bruker, 2009); cell refinement: SAINT (Bruker, 2009); data reduction: SAINT; program(s) used to solve structure: SHELXTL (Sheldrick, 2008 ); program(s) used to refine structure: SHELXTL; molecular graphics: SHELXTL; software used to prepare material for publication: SHELXTL, PLATON (Spek, 2009 ), Mercury (Macrae et al., 2006 ) and publCIF (Westrip, 2010 ).

Supporting information

CCDC reference: 989255

Crystal structure: contains datablocks global, I. DOI: 10.1107/S1600536814004632/hb7180sup1.cif

Structure factors: contains datablock I. DOI: 10.1107/S1600536814004632/hb7180Isup2.hkl

Supporting information file. DOI: 10.1107/S1600536814004632/hb7180Isup3.cml

checkCIF report

Comment top

Trichoderma genus is accepted as a superior biocontrol agent of plant pathogens (Hajieghrari et al., 2008; Kumar et al., 2012). Secondary metabolites from Trichoderma fungi have been reported to inhibit the phytopathogenic growth against Colletotrichum gloeosporioides (De los Santos-Villalobos et al., 2011), Pythium irregular, Sclerotinia sclerotiorum, Rhizoctonia solani (Vinale, 2009) and Sclerotium rolfsii (Evidente et al., 2006). Our study on the chemical constituents and bioactive compounds from Trichoderma asperellum stain F009, collected from soils in Suphan Buri province (Thailand), has led us to the isolation of the title diterpene lactone (I) which is known as "Trichodermaerin". The title compound was briefly reported together with Trichoderma erinaceum (Xie et al., 2013). Our antifungal assay revealed that at 200 ppm of the extract had 76.5% growth inhibition against Colletotrichum gloeosporioides. Herein we report the crystal structure of (I).

The molecule of the title compound has a tetracyclic 6-5-7-5 ring system (Fig. 1). The cyclohexanone ring adopts a twisted half-chair conformation with the puckered C8 and C12 atoms having the maximum deviation of -0.003 (1) and 0.440 (1) Å, respectively from the best plane of the remaining four atoms (C6/C7/C9/C10) and with the puckering parameters Q = 0.6548 (12) Å, θ = 143.53 (10)° and ϕ = 107.15 (18)°. The cyclopentane ring is in a half-chair conformation with the puckered C6 and C12 atoms having the maximum deviation of 0.309 (1) and -0.301 (1) Å, respectively from the mean plane of C5/C10/C11 atoms and with the puckering parameters Q = 0.5030 (12) Å and ϕ = 52.10 (13)°. The cycloheptene ring adopts a standard chair conformation with the puckering parameter Q = 0.6792 (12) Å whereas the tetrahydrofuranone ring is in an envelope conformation with the puckered C4 atom having a deviation of 0.149 (1) Å and the puckering parameters Q = 0.2519 (12) Å and θ = 267.5 (2)° (Cremer & Pople 1975). The bond distances are of normal values (Allen et al., 1987).

In the crystal structure (Fig. 2), the molecules are linked into screw chains through weak C16—H16B···O2 and C20—H20C···O3 interactions (Table 1) and the adjacent chains are further interconnected by weak C3—H3B···O3 interactions (Fig. 3 and Table 1). The crystal of (I) is consolidated by these intermolecular C—H···O weak interactions.

Related literature top

For standard bond-length data, see: Allen et al. (1987). For ring conformations, see: Cremer & Pople (1975). For background to Trichoderma and diterpene lactones, see, for example: De los Santos-Villalobos et al. (2011); Evidente et al. (2006); Hajieghrari et al. (2008); Kumar et al. (2012); Vinale (20093); Xie et al. (2013). For the stability of the temperature controller used in the data collection, see: Cosier & Glazer, (1986).

Experimental top

Trichoderma asperellum stain F009 was inoculated in potato dextrose broth (PDB) for 27 days at room temperature. The broth culture (18 L) was extracted with ethyl acetate to obtain a crude ethyl acetate extract (1.956 g) as a brown viscous liquid. The crude extract was submitted to purification by column chromatography on silica gel with solvent mixtures of increasing polarity (hexane to CH₃OH) to give fourteen fractions (F1-F14). Further separation of the subfraction F4 (122.4 mg) on silica gel column chromatography eluted with 20% ethyl acetate–hexane afforded compound (I) (5.6 mg). Colorless block-shaped single crystals of (I) suitable for X-ray structure determination were recrystallized from ethyl acetate by the slow evaporation of the solvent at room temperature after several days, Mp. 484.05–484.95 K.

Computing details top

Data collection: APEX2 (Bruker, 2009); cell refinement: SAINT (Bruker, 2009); data reduction: SAINT (Bruker, 2009); program(s) used to solve structure: SHELXTL (Sheldrick, 2008); program(s) used to refine structure: SHELXTL (Sheldrick, 2008); molecular graphics: SHELXTL (Sheldrick, 2008); software used to prepare material for publication: SHELXTL (Sheldrick, 2008), PLATON (Spek, 2009), Mercury (Macrae et al., 2006) and publCIF (Westrip, 2010).

Figures top

	Fig. 1. The molecular structure of the title compound, showing 40% probability displacement ellipsoids.
	Fig. 2. The crystal packing of the title compound viewed along the a axis, showing screw chains. Only H atoms involved in hydrogen bonds were shown for clarity. Hydrogen bonds are shown as dashed lines.
	Fig. 3. Showing the connection of the adjacent screw chains by C—H···O weak interactions. Only H atoms involved in hydrogen bonds were shown for clarity. Hydrogen bonds are shown as dashed lines.

(4E)-4,9,15,16,16-Pentamethyl-6-oxatetracyclo[10.3.1.0^1,10.0^5,9]hexadec-4-ene-7,13-dione top

Crystal data top

C₂₀H₂₈O₃	F(000) = 344
M_r = 316.42	D_x = 1.276 Mg m⁻³
Monoclinic, P2₁	Melting point = 484.05–484.95 K
Hall symbol: P 2yb	Mo Kα radiation, λ = 0.71073 Å
a = 9.1703 (4) Å	Cell parameters from 2517 reflections
b = 10.2234 (5) Å	θ = 2.3–30.0°
c = 9.2681 (4) Å	µ = 0.08 mm⁻¹
β = 108.539 (1)°	T = 100 K
V = 823.81 (6) Å³	Block, colorless
Z = 2	0.47 × 0.28 × 0.17 mm

Data collection top

Bruker APEX DUO CCD area-detector diffractometer	2517 independent reflections
Radiation source: sealed tube	2492 reflections with I > 2σ(I)
Graphite monochromator	R_int = 0.022
ϕ and ω scans	θ_max = 30.0°, θ_min = 2.3°
Absorption correction: multi-scan (SADABS; Bruker, 2009)	h = −12→12
T_min = 0.962, T_max = 0.986	k = −14→14
17364 measured reflections	l = −13→12

Refinement top

Refinement on F²	Primary atom site location: structure-invariant direct methods
Least-squares matrix: full	Secondary atom site location: difference Fourier map
R[F² > 2σ(F²)] = 0.026	Hydrogen site location: inferred from neighbouring sites
wR(F²) = 0.069	H-atom parameters constrained
S = 1.06	w = 1/[σ²(F_o²) + (0.0476P)² + 0.0833P] where P = (F_o² + 2F_c²)/3
2517 reflections	(Δ/σ)_max = 0.001
213 parameters	Δρ_max = 0.29 e Å⁻³
1 restraint	Δρ_min = −0.16 e Å⁻³

Crystal data top

C₂₀H₂₈O₃	V = 823.81 (6) Å³
M_r = 316.42	Z = 2
Monoclinic, P2₁	Mo Kα radiation
a = 9.1703 (4) Å	µ = 0.08 mm⁻¹
b = 10.2234 (5) Å	T = 100 K
c = 9.2681 (4) Å	0.47 × 0.28 × 0.17 mm
β = 108.539 (1)°

Data collection top

Bruker APEX DUO CCD area-detector diffractometer	2517 independent reflections
Absorption correction: multi-scan (SADABS; Bruker, 2009)	2492 reflections with I > 2σ(I)
T_min = 0.962, T_max = 0.986	R_int = 0.022
17364 measured reflections

Refinement top

R[F² > 2σ(F²)] = 0.026	1 restraint
wR(F²) = 0.069	H-atom parameters constrained
S = 1.06	Δρ_max = 0.29 e Å⁻³
2517 reflections	Δρ_min = −0.16 e Å⁻³
213 parameters

Special details top

Experimental. The crystal was placed in the cold stream of an Oxford Cryosystems Cobra open-flow nitrogen cryostat (Cosier & Glazer, 1986) operating at 100.0 (1) K.

Geometry. All esds (except the esd in the dihedral angle between two l.s. planes) are estimated using the full covariance matrix. The cell esds are taken into account individually in the estimation of esds in distances, angles and torsion angles; correlations between esds in cell parameters are only used when they are defined by crystal symmetry. An approximate (isotropic) treatment of cell esds is used for estimating esds involving l.s. planes.

Refinement. Refinement of F² against ALL reflections. The weighted R-factor wR and goodness of fit S are based on F², conventional R-factors R are based on F, with F set to zero for negative F². The threshold expression of F² > 2sigma(F²) is used only for calculating R-factors(gt) etc. and is not relevant to the choice of reflections for refinement. R-factors based on F² are statistically about twice as large as those based on F, and R- factors based on ALL data will be even larger.

Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å²) top

	x	y	z	U_iso*/U_eq
O1	0.56994 (9)	0.42031 (8)	0.42963 (9)	0.01666 (16)
O2	0.36991 (11)	0.48960 (10)	0.49811 (11)	0.0247 (2)
O3	0.76108 (11)	1.06399 (9)	0.03459 (10)	0.02325 (19)
C1	0.67439 (12)	0.47448 (10)	0.36106 (11)	0.01291 (18)
C2	0.46151 (13)	0.51131 (11)	0.43292 (12)	0.01624 (19)
C3	0.47893 (11)	0.63000 (11)	0.34415 (12)	0.01470 (19)
H3A	0.4634	0.7112	0.3955	0.018*
H3B	0.4043	0.6281	0.2400	0.018*
C4	0.64611 (11)	0.62098 (10)	0.33997 (11)	0.01189 (17)
C5	0.64570 (11)	0.66703 (10)	0.18078 (11)	0.01136 (17)
H5A	0.5761	0.6033	0.1095	0.014*
C6	0.79247 (11)	0.66867 (11)	0.13020 (11)	0.01212 (17)
C7	0.92305 (11)	0.75723 (11)	0.23495 (11)	0.01437 (19)
H7A	0.9311	0.7310	0.3412	0.017*
C8	0.88414 (13)	0.90599 (12)	0.22599 (13)	0.0189 (2)
H8A	0.8515	0.9288	0.3149	0.023*
H8B	0.9798	0.9552	0.2359	0.023*
C9	0.76116 (13)	0.95343 (12)	0.08374 (12)	0.0166 (2)
C10	0.63987 (12)	0.85336 (11)	0.01091 (11)	0.01396 (19)
H10A	0.5598	0.8898	−0.0805	0.017*
C11	0.56749 (12)	0.80094 (11)	0.12984 (12)	0.01427 (19)
H11A	0.5880	0.8615	0.2174	0.017*
H11B	0.4549	0.7904	0.0837	0.017*
C12	0.72306 (12)	0.73384 (11)	−0.03161 (11)	0.01303 (18)
C13	0.84953 (12)	0.52859 (11)	0.12202 (12)	0.0158 (2)
H13A	0.9357	0.5320	0.0793	0.019*
H13B	0.7653	0.4781	0.0501	0.019*
C14	0.90411 (12)	0.45392 (12)	0.27425 (13)	0.0176 (2)
H14A	0.9707	0.3809	0.2633	0.021*
H14B	0.9686	0.5138	0.3528	0.021*
C15	0.77981 (11)	0.39824 (11)	0.33248 (11)	0.01390 (19)
C16	0.75106 (12)	0.69002 (12)	0.48303 (12)	0.0160 (2)
H16A	0.7178	0.6679	0.5706	0.024*
H16B	0.7446	0.7849	0.4672	0.024*
H16C	0.8575	0.6612	0.5023	0.024*
C17	1.08590 (12)	0.73508 (14)	0.22352 (14)	0.0221 (2)
H17A	1.1588	0.7943	0.2938	0.033*
H17B	1.0848	0.7526	0.1192	0.033*
H17C	1.1173	0.6443	0.2503	0.033*
C18	0.84033 (13)	0.77677 (12)	−0.10901 (12)	0.0170 (2)
H18A	0.7866	0.8195	−0.2060	0.026*
H18B	0.8958	0.7000	−0.1277	0.026*
H18C	0.9136	0.8382	−0.0428	0.026*
C19	0.60412 (13)	0.64867 (12)	−0.14867 (12)	0.0176 (2)
H19A	0.5600	0.6985	−0.2429	0.026*
H19B	0.5221	0.6234	−0.1074	0.026*
H19C	0.6546	0.5699	−0.1702	0.026*
C20	0.78631 (13)	0.25306 (11)	0.36025 (13)	0.0175 (2)
H20A	0.7042	0.2277	0.4012	0.026*
H20B	0.8863	0.2300	0.4334	0.026*
H20C	0.7727	0.2069	0.2642	0.026*

Atomic displacement parameters (Å²) top

	U¹¹	U²²	U³³	U¹²	U¹³	U²³
O1	0.0190 (3)	0.0147 (4)	0.0198 (4)	0.0004 (3)	0.0111 (3)	0.0019 (3)
O2	0.0280 (4)	0.0209 (4)	0.0337 (5)	−0.0020 (4)	0.0217 (4)	0.0015 (4)
O3	0.0322 (5)	0.0150 (4)	0.0242 (4)	−0.0030 (3)	0.0112 (3)	0.0008 (3)
C1	0.0145 (4)	0.0132 (4)	0.0119 (4)	0.0001 (3)	0.0052 (3)	0.0008 (3)
C2	0.0177 (4)	0.0148 (5)	0.0181 (4)	−0.0008 (4)	0.0084 (4)	−0.0013 (4)
C3	0.0138 (4)	0.0154 (5)	0.0172 (4)	0.0013 (4)	0.0082 (3)	0.0015 (4)
C4	0.0125 (4)	0.0122 (4)	0.0123 (4)	0.0010 (3)	0.0058 (3)	0.0003 (3)
C5	0.0112 (4)	0.0117 (4)	0.0120 (4)	0.0013 (3)	0.0049 (3)	0.0006 (3)
C6	0.0116 (4)	0.0140 (4)	0.0119 (4)	0.0012 (3)	0.0053 (3)	0.0002 (3)
C7	0.0114 (4)	0.0176 (5)	0.0136 (4)	−0.0012 (4)	0.0033 (3)	−0.0001 (4)
C8	0.0185 (5)	0.0187 (5)	0.0180 (5)	−0.0035 (4)	0.0035 (4)	−0.0027 (4)
C9	0.0203 (5)	0.0154 (5)	0.0164 (4)	−0.0006 (4)	0.0088 (4)	−0.0014 (4)
C10	0.0146 (4)	0.0135 (5)	0.0141 (4)	0.0009 (3)	0.0050 (3)	0.0018 (4)
C11	0.0145 (4)	0.0137 (5)	0.0160 (4)	0.0036 (3)	0.0068 (3)	0.0028 (4)
C12	0.0143 (4)	0.0135 (4)	0.0115 (4)	−0.0010 (3)	0.0045 (3)	0.0000 (3)
C13	0.0182 (4)	0.0152 (5)	0.0168 (4)	0.0040 (4)	0.0096 (4)	0.0010 (4)
C14	0.0156 (4)	0.0182 (5)	0.0211 (5)	0.0057 (4)	0.0088 (4)	0.0051 (4)
C15	0.0149 (4)	0.0138 (4)	0.0128 (4)	0.0023 (4)	0.0041 (3)	0.0012 (4)
C16	0.0183 (4)	0.0171 (5)	0.0128 (4)	−0.0020 (4)	0.0053 (3)	−0.0029 (4)
C17	0.0122 (4)	0.0313 (6)	0.0234 (5)	−0.0006 (4)	0.0066 (4)	0.0023 (5)
C18	0.0192 (4)	0.0198 (5)	0.0144 (4)	−0.0029 (4)	0.0085 (3)	0.0001 (4)
C19	0.0197 (4)	0.0190 (5)	0.0131 (4)	−0.0043 (4)	0.0038 (3)	−0.0013 (4)
C20	0.0191 (5)	0.0131 (5)	0.0184 (5)	0.0033 (4)	0.0033 (4)	0.0005 (4)

Geometric parameters (Å, º) top

O1—C2	1.3691 (14)	C10—H10A	1.0000
O1—C1	1.4195 (12)	C11—H11A	0.9900
O2—C2	1.2012 (14)	C11—H11B	0.9900
O3—C9	1.2186 (15)	C12—C18	1.5343 (14)
C1—C15	1.3323 (14)	C12—C19	1.5403 (15)
C1—C4	1.5220 (15)	C13—C14	1.5410 (15)
C2—C3	1.5027 (16)	C13—H13A	0.9900
C3—C4	1.5486 (14)	C13—H13B	0.9900
C3—H3A	0.9900	C14—C15	1.5185 (15)
C3—H3B	0.9900	C14—H14A	0.9900
C4—C16	1.5398 (14)	C14—H14B	0.9900
C4—C5	1.5476 (14)	C15—C20	1.5043 (16)
C5—C11	1.5480 (14)	C16—H16A	0.9800
C5—C6	1.5597 (13)	C16—H16B	0.9800
C5—H5A	1.0000	C16—H16C	0.9800
C6—C13	1.5349 (15)	C17—H17A	0.9800
C6—C7	1.5674 (14)	C17—H17B	0.9800
C6—C12	1.5783 (14)	C17—H17C	0.9800
C7—C17	1.5470 (15)	C18—H18A	0.9800
C7—C8	1.5582 (17)	C18—H18B	0.9800
C7—H7A	1.0000	C18—H18C	0.9800
C8—C9	1.5165 (16)	C19—H19A	0.9800
C8—H8A	0.9900	C19—H19B	0.9800
C8—H8B	0.9900	C19—H19C	0.9800
C9—C10	1.5040 (15)	C20—H20A	0.9800
C10—C11	1.5517 (14)	C20—H20B	0.9800
C10—C12	1.5561 (15)	C20—H20C	0.9800

C2—O1—C1	110.06 (9)	C5—C11—H11B	110.7
C15—C1—O1	119.76 (10)	C10—C11—H11B	110.7
C15—C1—C4	130.91 (10)	H11A—C11—H11B	108.8
O1—C1—C4	109.25 (9)	C18—C12—C19	106.08 (8)
O2—C2—O1	120.97 (11)	C18—C12—C10	111.51 (9)
O2—C2—C3	129.62 (11)	C19—C12—C10	109.14 (8)
O1—C2—C3	109.40 (9)	C18—C12—C6	115.73 (8)
C2—C3—C4	104.12 (9)	C19—C12—C6	114.33 (9)
C2—C3—H3A	110.9	C10—C12—C6	99.96 (8)
C4—C3—H3A	110.9	C6—C13—C14	115.69 (9)
C2—C3—H3B	110.9	C6—C13—H13A	108.4
C4—C3—H3B	110.9	C14—C13—H13A	108.4
H3A—C3—H3B	109.0	C6—C13—H13B	108.4
C1—C4—C16	107.83 (9)	C14—C13—H13B	108.4
C1—C4—C5	111.74 (8)	H13A—C13—H13B	107.4
C16—C4—C5	119.53 (9)	C15—C14—C13	116.69 (9)
C1—C4—C3	100.66 (8)	C15—C14—H14A	108.1
C16—C4—C3	107.69 (8)	C13—C14—H14A	108.1
C5—C4—C3	107.66 (8)	C15—C14—H14B	108.1
C4—C5—C11	114.85 (8)	C13—C14—H14B	108.1
C4—C5—C6	123.30 (8)	H14A—C14—H14B	107.3
C11—C5—C6	105.02 (8)	C1—C15—C20	122.34 (10)
C4—C5—H5A	103.8	C1—C15—C14	121.70 (10)
C11—C5—H5A	103.8	C20—C15—C14	115.93 (9)
C6—C5—H5A	103.8	C4—C16—H16A	109.5
C13—C6—C5	110.19 (8)	C4—C16—H16B	109.5
C13—C6—C7	111.36 (8)	H16A—C16—H16B	109.5
C5—C6—C7	112.48 (8)	C4—C16—H16C	109.5
C13—C6—C12	112.81 (8)	H16A—C16—H16C	109.5
C5—C6—C12	99.45 (8)	H16B—C16—H16C	109.5
C7—C6—C12	110.03 (8)	C7—C17—H17A	109.5
C17—C7—C8	110.42 (9)	C7—C17—H17B	109.5
C17—C7—C6	115.91 (9)	H17A—C17—H17B	109.5
C8—C7—C6	114.45 (8)	C7—C17—H17C	109.5
C17—C7—H7A	104.9	H17A—C17—H17C	109.5
C8—C7—H7A	104.9	H17B—C17—H17C	109.5
C6—C7—H7A	104.9	C12—C18—H18A	109.5
C9—C8—C7	116.93 (9)	C12—C18—H18B	109.5
C9—C8—H8A	108.1	H18A—C18—H18B	109.5
C7—C8—H8A	108.1	C12—C18—H18C	109.5
C9—C8—H8B	108.1	H18A—C18—H18C	109.5
C7—C8—H8B	108.1	H18B—C18—H18C	109.5
H8A—C8—H8B	107.3	C12—C19—H19A	109.5
O3—C9—C10	123.42 (10)	C12—C19—H19B	109.5
O3—C9—C8	122.25 (11)	H19A—C19—H19B	109.5
C10—C9—C8	114.33 (10)	C12—C19—H19C	109.5
C9—C10—C11	109.78 (9)	H19A—C19—H19C	109.5
C9—C10—C12	107.20 (8)	H19B—C19—H19C	109.5
C11—C10—C12	105.28 (8)	C15—C20—H20A	109.5
C9—C10—H10A	111.4	C15—C20—H20B	109.5
C11—C10—H10A	111.4	H20A—C20—H20B	109.5
C12—C10—H10A	111.4	C15—C20—H20C	109.5
C5—C11—C10	105.11 (8)	H20A—C20—H20C	109.5
C5—C11—H11A	110.7	H20B—C20—H20C	109.5
C10—C11—H11A	110.7

C2—O1—C1—C15	−173.20 (10)	C7—C8—C9—O3	−150.53 (11)
C2—O1—C1—C4	9.64 (11)	C7—C8—C9—C10	30.16 (14)
C1—O1—C2—O2	−173.44 (10)	O3—C9—C10—C11	−124.95 (11)
C1—O1—C2—C3	7.53 (12)	C8—C9—C10—C11	54.36 (12)
O2—C2—C3—C4	160.06 (12)	O3—C9—C10—C12	121.19 (12)
O1—C2—C3—C4	−21.02 (11)	C8—C9—C10—C12	−59.51 (11)
C15—C1—C4—C16	−85.57 (13)	C4—C5—C11—C10	156.08 (8)
O1—C1—C4—C16	91.17 (9)	C6—C5—C11—C10	17.42 (10)
C15—C1—C4—C5	47.72 (15)	C9—C10—C11—C5	−100.89 (10)
O1—C1—C4—C5	−135.54 (8)	C12—C10—C11—C5	14.19 (10)
C15—C1—C4—C3	161.77 (11)	C9—C10—C12—C18	−45.64 (11)
O1—C1—C4—C3	−21.50 (10)	C11—C10—C12—C18	−162.50 (8)
C2—C3—C4—C1	24.59 (10)	C9—C10—C12—C19	−162.51 (9)
C2—C3—C4—C16	−88.18 (10)	C11—C10—C12—C19	80.63 (10)
C2—C3—C4—C5	141.69 (9)	C9—C10—C12—C6	77.25 (9)
C1—C4—C5—C11	161.08 (8)	C11—C10—C12—C6	−39.61 (9)
C16—C4—C5—C11	−71.71 (12)	C13—C6—C12—C18	−74.27 (11)
C3—C4—C5—C11	51.45 (11)	C5—C6—C12—C18	169.02 (9)
C1—C4—C5—C6	−68.68 (12)	C7—C6—C12—C18	50.76 (12)
C16—C4—C5—C6	58.53 (13)	C13—C6—C12—C19	49.47 (11)
C3—C4—C5—C6	−178.31 (9)	C5—C6—C12—C19	−67.25 (10)
C4—C5—C6—C13	65.63 (12)	C7—C6—C12—C19	174.50 (8)
C11—C5—C6—C13	−160.19 (8)	C13—C6—C12—C10	165.87 (8)
C4—C5—C6—C7	−59.28 (13)	C5—C6—C12—C10	49.15 (9)
C11—C5—C6—C7	74.90 (10)	C7—C6—C12—C10	−69.10 (9)
C4—C5—C6—C12	−175.68 (9)	C5—C6—C13—C14	−64.06 (11)
C11—C5—C6—C12	−41.51 (9)	C7—C6—C13—C14	61.49 (11)
C13—C6—C7—C17	39.01 (12)	C12—C6—C13—C14	−174.21 (9)
C5—C6—C7—C17	163.27 (9)	C6—C13—C14—C15	77.90 (13)
C12—C6—C7—C17	−86.84 (11)	O1—C1—C15—C20	4.36 (15)
C13—C6—C7—C8	169.33 (9)	C4—C1—C15—C20	−179.19 (10)
C5—C6—C7—C8	−66.41 (11)	O1—C1—C15—C14	−173.71 (9)
C12—C6—C7—C8	43.47 (11)	C4—C1—C15—C14	2.75 (17)
C17—C7—C8—C9	110.78 (10)	C13—C14—C15—C1	−59.24 (14)
C6—C7—C8—C9	−22.18 (13)	C13—C14—C15—C20	122.58 (11)

Hydrogen-bond geometry (Å, º) top

D—H···A	D—H	H···A	D···A	D—H···A
C3—H3B···O3ⁱ	0.99	2.60	3.5649 (14)	165
C16—H16B···O2ⁱⁱ	0.98	2.41	3.2810 (16)	148
C20—H20C···O3ⁱⁱⁱ	0.98	2.56	3.5292 (15)	173

Symmetry codes: (i) −x+1, y−1/2, −z; (ii) −x+1, y+1/2, −z+1; (iii) x, y−1, z.

Hydrogen-bond geometry (Å, º) top

D—H···A	D—H	H···A	D···A	D—H···A
C3—H3B···O3ⁱ	0.99	2.60	3.5649 (14)	165
C16—H16B···O2ⁱⁱ	0.98	2.41	3.2810 (16)	148
C20—H20C···O3ⁱⁱⁱ	0.98	2.56	3.5292 (15)	173

Symmetry codes: (i) −x+1, y−1/2, −z; (ii) −x+1, y+1/2, −z+1; (iii) x, y−1, z.

Footnotes

‡Thomson Reuters ResearcherID: A-5085-2009.

§Additional correspondence author, e-mail: hkfun@usm.my. Thomson Reuters ResearcherID: A-3561-2009

Acknowledgements

CJ and WP thank the Utilization of Natural Products Research Unit, Walailak University, for a wide range of facility support. The authors extend their appreciation to the Prince of Songkla University and the Universiti Sains Malaysia for the APEX DE2012 grant No. 1002/PFIZIK/910323.

References

Allen, F. H., Kennard, O., Watson, D. G., Brammer, L., Orpen, A. G. & Taylor, R. (1987). J. Chem. Soc. Perkin Trans. 2, pp. S1–19. CrossRef Web of Science Google Scholar
Bruker (2009). APEX2, SAINT and SADABS. Bruker AXS Inc., Madison, Wisconsin, USA. Google Scholar
Cosier, J. & Glazer, A. M. (1986). J. Appl. Cryst. 19, 105–107. CrossRef CAS Web of Science IUCr Journals Google Scholar
Cremer, D. & Pople, J. A. (1975). J. Am. Chem. Soc. 97, 1354–1358. CrossRef CAS Web of Science Google Scholar
De los Santos-Villalobos, S., Guzmán-Ortiz, D. A., De-Folter, S., Gómez-Lim, M. A., Délano-Frier, J. P., De-Folter, S., Sánchez-García, P. & Peña-Cabriales, J. J. (2011). Biol. Control. 2, 221–234. Google Scholar
Evidente, A., Cabras, A., Maddau, L., Marras, L., Andolfi, A., Melck, D. & Motta, A. (2006). J. Agric. Food Chem. 54, 6588–6592. Web of Science CrossRef PubMed CAS Google Scholar
Hajieghrari, B., Torabi-Giglou, M., Mohammadi, M. R. & Davari, M. (2008). Afr. J. Biotechnol. 7, 967–972. Google Scholar
Kumar, P., Misra, A. K., Modi, D. R. & Gupta, V. K. (2012). Arch Phytopathol. Plant Prot. 45, 1237–1245. CrossRef CAS Google Scholar
Macrae, C. F., Edgington, P. R., McCabe, P., Pidcock, E., Shields, G. P., Taylor, R., Towler, M. & van de Streek, J. (2006). J. Appl. Cryst. 39, 453–457. Web of Science CrossRef CAS IUCr Journals Google Scholar
Sheldrick, G. M. (2008). Acta Cryst. A64, 112–122. Web of Science CrossRef CAS IUCr Journals Google Scholar
Spek, A. L. (2009). Acta Cryst. D65, 148–155. Web of Science CrossRef CAS IUCr Journals Google Scholar
Vinale, F., Flematti, G., Sivasithamparam, K., Lorito, M., Marra, R., Skelton, B. W. & Ghisalberti, E. L. (2009). J. Nat. Prod. 72, 2032–2035. Web of Science CSD CrossRef PubMed CAS Google Scholar
Westrip, S. P. (2010). J. Appl. Cryst. 43, 920–925. Web of Science CrossRef CAS IUCr Journals Google Scholar
Xie, Z.-L., Li, H.-J., Wang, L.-Y., Liang, W.-L., Liu, W. & Lan, W.-J. (2013). Nat. Prod. Commun. 8, 67–68. Web of Science CAS PubMed Google Scholar