Crystal structure of 7β-hy­droxy­royleanone isolated from Taxodium ascendens (B.)

Xu, S.; Ma, X.; Ke, R.; Deng, S.; Yang, X.; Song, P.

doi:10.1107/S2056989017011987

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ISSN: 2056-9890

Volume 73| Part 10| October 2017| Pages 1414-1416

https://doi.org/10.1107/S2056989017011987

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Crystal structure of 7β-hydroxyroyleanone isolated from Taxodium ascendens (B.)

Shicheng Xu,^a Xinhua Ma,^a Ruifang Ke,^a Shihao Deng,^a Xinzhou Yang ^a ^* and Ping Song ^b ^*

^aSchool of Pharmaceutical Sciences, South-Central University for Nationalities, Wuhan 430074, People's Republic of China, and ^bCollege of Chemistry and Life Science, Qinghai University for Nationalities, Xining 810007, People's Republic of China
^*Correspondence e-mail: xzyang@mail.scuec.edu.cn, mxhmxh02@163.com

Edited by H. Stoeckli-Evans, University of Neuchâtel, Switzerland (Received 7 July 2017; accepted 18 August 2017; online 5 September 2017)

The title compound, C₂₀H₂₈O₄ [systematic name: (4bS,8aS,10S)-3,10-dihydroxy-2-isopropyl-4b,8,8-trimethyl-4b,5,6,7,8,8a,9,10-octahydrophenanthrene-1,4-dione], is an abietane-type diterpene, which was isolated from Taxodium ascendens (B.). The compound crystallizes in the chiral space group P2₁, but it was not possible to determine the absolute structure of the molecule in the crystal by resonant scattering. The molecular structure is stabilized by two intramolecular O—H⋯O hydrogen bonds, enclosing S(5) and S(6) ring motifs. In the crystal, molecules are linked by O—H⋯O and C—H⋯O hydrogen bonds, forming chains along the [010] direction. The crystal structure of the 10R stereoisomer of the title compound, isolated from the roots of Premna obtusifolia (Verbenaceae), has been reported. It crystallized in the chiral space group P2₁2₁2₁, and the absolute structure was determined as (4bS,8aS,10R), by resonant scattering using Cu Kα radiation [Razak et al. (2010 ). Acta Cryst. E66, o1566–o1567].

Keywords: crystal structure; 7β-hydroxyroyleanone; Taxodium ascendens; hydrogen bonding.

CCDC reference: 1551129

1. Chemical context

Taxodium ascendens Brongn belongs to the Taxodiaceae species, which is native to the south-east of North America and has spread widely over southern China (Si et al., 2001 ). Previous chemical studies of Taxodium ascendens (B.) have described many diterpenes, such as 6,7-dehydroroyleanone, salvinolone and xanthoperol (Kusumoto et al., 2009 ; Gonzalez, 2015 ), and the diterpenoids have attracted much attention in recent years because of their diverse biological properties (Burmistrova et al., 2013 ; Tanaka, 2001 ), such as antibacterial (Yang et al., 2001 ), antioxidant (Kolak et al., 2009 ), antifungal (Topçu & Gören, 2007 ) and anticholinesterase activities (Topçu et al., 2013 ). A detailed phytochemical investigation of a petroleum ether extract of the pollen of Taxodium ascendens Brongn has been carried out and a series of diterpenoids have been isolated, including the title compound, 7β-hydroxyroyleanone. Herein, we present the crystal structure of 7β-hydroxyroyleanone carried out in order to establish unambiguously the stereochemical features of this natural product.

2. Structural commentary

The molecular structure of the title compound is shown in Fig. 1. The structure contains two hydroxy groups, located at atoms C11 and C15, two ketone groups at C14 and C17, and two double bonds, C12=C13 and C15=C16. There are two intramolecular hydrogen bonds, viz. O2—H2⋯O1 and O4—H4⋯O3, which stabilize the molecular conformation. Ring A (atoms C1–C6) has a chair conformation [puckering parameters: amplitude (Q) = 0.552 (2) Å, θ = 4.9 (2)° and φ = 292 (3)°], while ring B (C1/C2/C10–C13) has an envelope conformation, with atom C2 as the flap [puckering parameters: Q = 0.558 (2) Å, θ = 125.1 (2)° and φ = 256.2 (3)°]. Benzoquinone ring C (C12–C17) has a screw-boat conformation [puckering parameters: Q = 0.097 (2) Å, θ = 66.3 (12)° and φ = 29.7 (14)°]. The mean planes of the various rings are inclined to one another in the following manner: A/B = 22.97 (10)°, A/C = 34.52 (10)° and B/C = 12.84 (9)°.

Figure 1
The molecular structure of the title compound, with the atom labelling and 50% probability displacement ellipsoids. Intramolecular O—H⋯O hydrogen bonds are shown as blue dashed lines (see Table 1

The crystal structure of the 10R stereoisomer of the title compound, isolated from the roots of Premna obtusifolia (Verbenaceae), has been reported twice (see §4, Database survey). It crystallized in the chiral space group P2₁2₁2₁, and the absolute structure was determined as (4bS,8aS,10R) by resonant scattering using Cu Kα radiation (Razak et al., 2010). Comparing the two compounds indicates that the configuration of the three stereocentres in the title compound are (4bS,8aS,10S).

3. Supramolecular features

In the crystal, two strong O—H⋯O hydrogen bonds, namely O2—H2A⋯O3ⁱ and O4—H4⋯O1ⁱⁱ, both approximately running along the b axis, are formed via the hydroxy group and the carbonyl groups (Fig. 2 and Table 1). Furthermore, a weak C11—H11⋯O1ⁱⁱ hydrogen bond occurs from a ring C atom to a carbonyl group, also running along the b-axis direction. These interactions result in the formation of chains propagating along the b-axis direction (Fig. 2 and Table 1).

Table 1
Hydrogen-bond geometry (Å, °)

D—H⋯A	D—H	H⋯A	D⋯A	D—H⋯A
O2—H2A⋯O1	0.82	2.10	2.579 (2)	117
O4—H4⋯O3	0.82	2.37	2.814 (2)	115
O2—H2A⋯O3ⁱ	0.82	2.39	3.153 (2)	155
O4—H4⋯O1ⁱⁱ	0.82	2.33	2.901 (2)	127
C11—H11⋯O1ⁱⁱ	0.98	2.47	3.120 (2)	124
Symmetry codes: (i) x, y-1, z; (ii) x, y+1, z.

Figure 2
A view along the c axis of the crystal packing of the title compound, with hydrogen bonds shown as dashed lines. Only H atoms involved in these interactions have been included.

4. Database survey

A search of the Cambridge Structural Database (CSD, Version 5.27, last update February 2017; Groom et al., 2016 ) for the octahydrophenanthrene-1,4-dione skeleton revealed 14 entries. These include two reports of a compound similar to the title compound, but with no hydroxy group in position 10, i.e. CSD refcodes HACGUN (Eugster et al., 1993 ) and HACGUN01 (Fun et al., 2011 ), and two reports of the stereoisomer of the title compound, with the hydroxy group in position 10 having an R configuration, i.e. QICLIX (Chen et al., 2000 ) and QICLIX01 (Razak et al., 2010).

5. Isolation and crystallization

The title compound was isolated from the pollen of Taxodium ascendens, collected in Wuhan, China, in April 2013 (SC0123). The air-dried pollen (1.8 kg) was extracted with 95% ethanol and then partitioned successively with petroleum ether (PE), ethyl acetate (EtOAc) and n-butyl alcohol (n-BuOH) to give a PE extract (80 g), an EtOAc extract (120 g) and a n-BuOH extract (100 g). The PE extract (80 g) was subjected to normal-phase silica-gel column chromatography (300–400 mesh) with a gradient solvent system of petroleum ether–acetone (1.0–0.1 v/v, containing 0.1% formic acid) to give eight major fractions, denoted F1–F8. Fraction F4 (6 g) was sequentially subjected to normal-phase silica-gel column chromatography (300–400 mesh) with an isocratic elution (petroleum ether–acetone, 2:1 v/v, containing 0.1% formic acid) to give three major fractions, denoted F4.1, F4.2 and F4.3. Fraction F4.3 was purified by semipreparative HPLC (CNCH₃/H₂O, 10:90→100:0, 40 min, containing 0.1% formic acid in both phase), to give an orange solid, which was recrystallized from the mixed solvents of CH₂Cl₂–MeOH (5:2 v/v), affording orange block-like crystals suitable for X-ray diffraction analysis. The ¹H and ¹³C NMR data of 7β-hydroxyroyleanone have been reported elsewhere (Chang & Zhu, 2001 ).

6. Refinement

Crystal data, data collection and structure refinement details are summarized in Table 2. The H atoms were positioned with idealized geometry and refined using a riding model, with O—H = 0.82 Å and C—H = 0.94–0.98 Å, and with U_iso(H) = 1.5U_eq(O,C) for hydroxy and methyl groups, and 1.2U_eq(C) for other H atoms.

Table 2
Experimental details

Crystal data
Chemical formula	C₂₀H₂₈O₄
M_r	332.42
Crystal system, space group	Monoclinic, P2₁
Temperature (K)	296
a, b, c (Å)	10.2570 (18), 7.6151 (13), 11.503 (2)
β (°)	101.110 (3)
V (Å³)	881.6 (3)
Z	2
Radiation type	Mo Kα
μ (mm⁻¹)	0.09
Crystal size (mm)	0.15 × 0.12 × 0.10

Data collection
Diffractometer	Bruker APEXII CCD
No. of measured, independent and observed [I > 2σ(I)] reflections	6669, 3463, 3163
R_int	0.024
(sin θ/λ)_max (Å⁻¹)	0.617

Refinement
R[F² > 2σ(F²)], wR(F²), S	0.030, 0.083, 1.03
No. of reflections	3319
No. of parameters	225
No. of restraints	1
H-atom treatment	H-atom parameters constrained
Δρ_max, Δρ_min (e Å⁻³)	0.18, −0.11
Absolute structure	Flack x determined using 1341 quotients [(I⁺) − (I⁻)]/[(I⁺) + (I⁻)] (Parsons et al., 2013 )
Absolute structure parameter	0.2 (3)
Computer programs: APEX2 (Bruker, 2007 ), SAINT (Bruker, 2007), SHELXS97 (Sheldrick, 2008 ), SHELXTL (Sheldrick, 2008), SHELXL2014 (Sheldrick, 2015 ) and PLATON (Spek, 2009 ).

Supporting information

CCDC reference: 1551129

Crystal structure: contains datablocks I, Global. DOI: https://doi.org/10.1107/S2056989017011987/su5382sup1.cif

Structure factors: contains datablock I. DOI: https://doi.org/10.1107/S2056989017011987/su5382Isup2.hkl

Supporting information file. DOI: https://doi.org/10.1107/S2056989017011987/su5382Isup3.cdx

Supporting information file. DOI: https://doi.org/10.1107/S2056989017011987/su5382Isup4.cml

checkCIF report

Computing details top

Data collection: APEX2 (Bruker, 2007); cell refinement: SAINT (Bruker, 2007); data reduction: SAINT (Bruker, 2007); program(s) used to solve structure: SHELXS97 (Sheldrick, 2008); program(s) used to refine structure: SHELXL2014 (Sheldrick, 2015); molecular graphics: SHELXTL (Sheldrick, 2008); software used to prepare material for publication: SHELXL2014 (Sheldrick, 2015) and PLATON (Spek, 2009).

(4bS,8aS,10S)-3,10-Dihydroxy-2-isopropyl-4b,8,8-trimethyl-4b,5,6,7,8,8a,9,10-octahydrophenanthrene-1,4-dione top

Crystal data top

C₂₀H₂₈O₄	F(000) = 360
M_r = 332.42	D_x = 1.252 Mg m⁻³
Monoclinic, P2₁	Mo Kα radiation, λ = 0.71073 Å
a = 10.2570 (18) Å	Cell parameters from 5396 reflections
b = 7.6151 (13) Å	θ = 2.4–31.8°
c = 11.503 (2) Å	µ = 0.09 mm⁻¹
β = 101.110 (3)°	T = 296 K
V = 881.6 (3) Å³	Block, orange
Z = 2	0.15 × 0.12 × 0.10 mm

Data collection top

Bruker APEXII CCD diffractometer	R_int = 0.024
φ and ω scans	θ_max = 26.0°, θ_min = 1.8°
6669 measured reflections	h = −12→12
3463 independent reflections	k = −9→8
3163 reflections with I > 2σ(I)	l = −14→14

Refinement top

Refinement on F²	Hydrogen site location: inferred from neighbouring sites
Least-squares matrix: full	H-atom parameters constrained
R[F² > 2σ(F²)] = 0.030	w = 1/[σ²(F_o²) + (0.0415P)² + 0.1205P] where P = (F_o² + 2F_c²)/3
wR(F²) = 0.083	(Δ/σ)_max = 0.018
S = 1.03	Δρ_max = 0.18 e Å⁻³
3319 reflections	Δρ_min = −0.11 e Å⁻³
225 parameters	Extinction correction: (SHELXL2014; Sheldrick, 2015), Fc^*=kFc[1+0.001xFc²λ³/sin(2θ)]^-1/4
1 restraint	Extinction coefficient: 0.042 (5)
Primary atom site location: structure-invariant direct methods	Absolute structure: Flack x determined using 1341 quotients [(I+)-(I-)]/[(I+)+(I-)] (Parsons et al., 2013)
Secondary atom site location: difference Fourier map	Absolute structure parameter: 0.2 (3)

Special details top

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.

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

	x	y	z	U_iso*/U_eq
C1	0.18336 (18)	0.9032 (3)	0.38131 (16)	0.0325 (4)
C2	0.12043 (19)	1.0797 (3)	0.33060 (16)	0.0330 (4)
H2	0.0708	1.1210	0.3901	0.040*
C3	0.0151 (2)	1.0710 (3)	0.21358 (18)	0.0436 (5)
C4	−0.0879 (2)	0.9310 (4)	0.2287 (2)	0.0558 (6)
H4A	−0.1416	0.9755	0.2830	0.067*
H4B	−0.1464	0.9124	0.1527	0.067*
C5	−0.0293 (2)	0.7561 (3)	0.2744 (2)	0.0552 (6)
H5A	0.0162	0.7042	0.2163	0.066*
H5B	−0.1003	0.6773	0.2852	0.066*
C6	0.0680 (2)	0.7766 (3)	0.3915 (2)	0.0449 (5)
H6A	0.1043	0.6625	0.4175	0.054*
H6B	0.0210	0.8209	0.4509	0.054*
C7	0.2771 (2)	0.8148 (3)	0.30881 (19)	0.0468 (5)
H7A	0.3432	0.8976	0.2954	0.070*
H7B	0.2267	0.7760	0.2341	0.070*
H7C	0.3198	0.7158	0.3519	0.070*
C8	0.0733 (3)	1.0359 (5)	0.1025 (2)	0.0652 (7)
H8A	0.1034	0.9164	0.1032	0.098*
H8B	0.1467	1.1137	0.1015	0.098*
H8C	0.0061	1.0555	0.0331	0.098*
C9	−0.0575 (3)	1.2484 (4)	0.1956 (3)	0.0632 (7)
H9A	0.0009	1.3358	0.1739	0.095*
H9B	−0.0841	1.2826	0.2679	0.095*
H9C	−0.1347	1.2376	0.1338	0.095*
C10	0.2287 (2)	1.2171 (3)	0.33153 (17)	0.0393 (4)
H10A	0.2976	1.1703	0.2932	0.047*
H10B	0.1914	1.3204	0.2881	0.047*
C11	0.28762 (18)	1.2668 (2)	0.45820 (17)	0.0329 (4)
H11	0.2280	1.3501	0.4866	0.040*
C12	0.30669 (18)	1.1084 (2)	0.53977 (16)	0.0304 (4)
C13	0.26614 (18)	0.9456 (2)	0.50399 (16)	0.0304 (4)
C14	0.3121 (2)	0.8004 (3)	0.58809 (17)	0.0346 (4)
C15	0.38257 (19)	0.8399 (3)	0.71053 (17)	0.0354 (4)
C16	0.40798 (19)	1.0040 (3)	0.75146 (17)	0.0347 (4)
C17	0.36998 (17)	1.1471 (3)	0.66582 (17)	0.0319 (4)
C18	0.4710 (2)	1.0503 (3)	0.87781 (17)	0.0434 (5)
H18	0.4779	1.1785	0.8825	0.052*
C19	0.3826 (3)	0.9924 (4)	0.9633 (2)	0.0596 (7)
H19A	0.2956	1.0422	0.9390	0.089*
H19B	0.4203	1.0321	1.0418	0.089*
H19C	0.3761	0.8667	0.9629	0.089*
C20	0.6116 (2)	0.9766 (4)	0.9132 (2)	0.0596 (7)
H20A	0.6080	0.8506	0.9140	0.089*
H20B	0.6511	1.0186	0.9907	0.089*
H20C	0.6640	1.0143	0.8571	0.089*
O1	0.29606 (19)	0.6460 (2)	0.56208 (14)	0.0538 (4)
O2	0.41656 (17)	0.6964 (2)	0.77776 (13)	0.0485 (4)
H2A	0.3912	0.6082	0.7391	0.073*
O3	0.38668 (15)	1.30061 (19)	0.69666 (13)	0.0441 (4)
O4	0.41202 (14)	1.3502 (2)	0.45960 (14)	0.0458 (4)
H4	0.4286	1.4170	0.5165	0.069*

Atomic displacement parameters (Å²) top

	U¹¹	U²²	U³³	U¹²	U¹³	U²³
C1	0.0336 (9)	0.0310 (10)	0.0314 (9)	0.0013 (7)	0.0025 (7)	−0.0020 (7)
C2	0.0350 (9)	0.0332 (10)	0.0304 (8)	0.0038 (8)	0.0052 (7)	0.0013 (7)
C3	0.0406 (11)	0.0488 (13)	0.0373 (10)	0.0060 (9)	−0.0025 (8)	0.0032 (9)
C4	0.0404 (11)	0.0618 (17)	0.0577 (14)	−0.0007 (11)	−0.0090 (10)	0.0018 (12)
C5	0.0486 (13)	0.0476 (15)	0.0628 (14)	−0.0103 (10)	−0.0057 (11)	−0.0022 (11)
C6	0.0455 (11)	0.0353 (12)	0.0499 (12)	−0.0063 (9)	−0.0008 (9)	0.0018 (9)
C7	0.0472 (12)	0.0483 (14)	0.0435 (11)	0.0137 (10)	0.0048 (9)	−0.0089 (10)
C8	0.0711 (16)	0.087 (2)	0.0342 (11)	0.0040 (15)	0.0019 (10)	−0.0009 (13)
C9	0.0588 (15)	0.0589 (18)	0.0639 (15)	0.0147 (12)	−0.0083 (12)	0.0115 (13)
C10	0.0454 (11)	0.0375 (11)	0.0343 (9)	−0.0008 (9)	0.0059 (8)	0.0086 (9)
C11	0.0348 (9)	0.0251 (10)	0.0386 (9)	0.0002 (7)	0.0062 (7)	0.0025 (7)
C12	0.0296 (8)	0.0283 (10)	0.0331 (9)	0.0036 (7)	0.0057 (7)	0.0015 (7)
C13	0.0319 (9)	0.0274 (10)	0.0312 (9)	0.0035 (7)	0.0042 (7)	−0.0006 (7)
C14	0.0409 (10)	0.0244 (10)	0.0370 (9)	0.0001 (8)	0.0038 (7)	0.0002 (8)
C15	0.0421 (10)	0.0280 (10)	0.0343 (9)	0.0038 (8)	0.0030 (8)	0.0053 (7)
C16	0.0376 (9)	0.0330 (11)	0.0315 (9)	−0.0003 (8)	0.0017 (7)	0.0000 (8)
C17	0.0303 (8)	0.0276 (10)	0.0374 (9)	0.0008 (7)	0.0058 (7)	−0.0008 (8)
C18	0.0539 (12)	0.0355 (11)	0.0351 (10)	−0.0038 (9)	−0.0058 (8)	−0.0008 (9)
C19	0.0685 (16)	0.0722 (19)	0.0364 (11)	−0.0044 (13)	0.0059 (10)	−0.0088 (11)
C20	0.0518 (13)	0.0643 (17)	0.0538 (13)	−0.0058 (12)	−0.0119 (11)	0.0043 (12)
O1	0.0789 (11)	0.0247 (8)	0.0491 (9)	0.0005 (8)	−0.0098 (8)	−0.0004 (7)
O2	0.0687 (10)	0.0291 (8)	0.0405 (8)	0.0007 (7)	−0.0074 (7)	0.0059 (6)
O3	0.0557 (9)	0.0269 (8)	0.0456 (8)	−0.0017 (6)	−0.0004 (7)	−0.0048 (6)
O4	0.0443 (8)	0.0421 (9)	0.0517 (8)	−0.0115 (7)	0.0111 (6)	0.0015 (7)

Geometric parameters (Å, º) top

C1—C13	1.535 (2)	C10—C11	1.514 (3)
C1—C7	1.543 (3)	C10—H10A	0.9700
C1—C6	1.547 (3)	C10—H10B	0.9700
C1—C2	1.555 (3)	C11—O4	1.423 (2)
C2—C10	1.525 (3)	C11—C12	1.517 (3)
C2—C3	1.556 (3)	C11—H11	0.9800
C2—H2	0.9800	C12—C13	1.347 (3)
C3—C4	1.534 (4)	C12—C17	1.499 (3)
C3—C8	1.534 (3)	C13—C14	1.485 (3)
C3—C9	1.538 (4)	C14—O1	1.217 (3)
C4—C5	1.514 (4)	C14—C15	1.485 (3)
C4—H4A	0.9700	C15—C16	1.343 (3)
C4—H4B	0.9700	C15—O2	1.345 (2)
C5—C6	1.522 (3)	C16—C17	1.470 (3)
C5—H5A	0.9700	C16—C18	1.514 (3)
C5—H5B	0.9700	C17—O3	1.224 (2)
C6—H6A	0.9700	C18—C19	1.526 (3)
C6—H6B	0.9700	C18—C20	1.527 (3)
C7—H7A	0.9600	C18—H18	0.9800
C7—H7B	0.9600	C19—H19A	0.9600
C7—H7C	0.9600	C19—H19B	0.9600
C8—H8A	0.9600	C19—H19C	0.9600
C8—H8B	0.9600	C20—H20A	0.9600
C8—H8C	0.9600	C20—H20B	0.9600
C9—H9A	0.9600	C20—H20C	0.9600
C9—H9B	0.9600	O2—H2A	0.8200
C9—H9C	0.9600	O4—H4	0.8200

C13—C1—C7	107.26 (15)	H9A—C9—H9C	109.5
C13—C1—C6	110.93 (16)	H9B—C9—H9C	109.5
C7—C1—C6	109.52 (18)	C11—C10—C2	109.46 (15)
C13—C1—C2	106.21 (15)	C11—C10—H10A	109.8
C7—C1—C2	115.53 (17)	C2—C10—H10A	109.8
C6—C1—C2	107.36 (15)	C11—C10—H10B	109.8
C10—C2—C1	109.97 (15)	C2—C10—H10B	109.8
C10—C2—C3	114.73 (16)	H10A—C10—H10B	108.2
C1—C2—C3	117.15 (16)	O4—C11—C10	108.25 (15)
C10—C2—H2	104.5	O4—C11—C12	109.85 (15)
C1—C2—H2	104.5	C10—C11—C12	112.14 (16)
C3—C2—H2	104.5	O4—C11—H11	108.9
C4—C3—C8	111.1 (2)	C10—C11—H11	108.9
C4—C3—C9	107.4 (2)	C12—C11—H11	108.8
C8—C3—C9	107.3 (2)	C13—C12—C17	121.81 (17)
C4—C3—C2	108.08 (18)	C13—C12—C11	123.18 (16)
C8—C3—C2	114.31 (18)	C17—C12—C11	114.97 (16)
C9—C3—C2	108.44 (19)	C12—C13—C14	116.48 (16)
C5—C4—C3	114.45 (19)	C12—C13—C1	123.93 (17)
C5—C4—H4A	108.6	C14—C13—C1	119.50 (16)
C3—C4—H4A	108.6	O1—C14—C13	123.26 (19)
C5—C4—H4B	108.6	O1—C14—C15	116.57 (18)
C3—C4—H4B	108.6	C13—C14—C15	120.16 (17)
H4A—C4—H4B	107.6	C16—C15—O2	122.88 (17)
C4—C5—C6	111.5 (2)	C16—C15—C14	123.19 (18)
C4—C5—H5A	109.3	O2—C15—C14	113.92 (17)
C6—C5—H5A	109.3	C15—C16—C17	116.50 (17)
C4—C5—H5B	109.3	C15—C16—C18	124.83 (19)
C6—C5—H5B	109.3	C17—C16—C18	118.67 (18)
H5A—C5—H5B	108.0	O3—C17—C16	120.63 (18)
C5—C6—C1	112.19 (18)	O3—C17—C12	118.58 (17)
C5—C6—H6A	109.2	C16—C17—C12	120.78 (17)
C1—C6—H6A	109.2	C16—C18—C19	110.77 (18)
C5—C6—H6B	109.2	C16—C18—C20	112.1 (2)
C1—C6—H6B	109.2	C19—C18—C20	111.7 (2)
H6A—C6—H6B	107.9	C16—C18—H18	107.3
C1—C7—H7A	109.5	C19—C18—H18	107.3
C1—C7—H7B	109.5	C20—C18—H18	107.3
H7A—C7—H7B	109.5	C18—C19—H19A	109.5
C1—C7—H7C	109.5	C18—C19—H19B	109.5
H7A—C7—H7C	109.5	H19A—C19—H19B	109.5
H7B—C7—H7C	109.5	C18—C19—H19C	109.5
C3—C8—H8A	109.5	H19A—C19—H19C	109.5
C3—C8—H8B	109.5	H19B—C19—H19C	109.5
H8A—C8—H8B	109.5	C18—C20—H20A	109.5
C3—C8—H8C	109.5	C18—C20—H20B	109.5
H8A—C8—H8C	109.5	H20A—C20—H20B	109.5
H8B—C8—H8C	109.5	C18—C20—H20C	109.5
C3—C9—H9A	109.5	H20A—C20—H20C	109.5
C3—C9—H9B	109.5	H20B—C20—H20C	109.5
H9A—C9—H9B	109.5	C15—O2—H2A	109.5
C3—C9—H9C	109.5	C11—O4—H4	109.5

C13—C1—C2—C10	54.86 (19)	C11—C12—C13—C1	−6.7 (3)
C7—C1—C2—C10	−63.9 (2)	C7—C1—C13—C12	105.6 (2)
C6—C1—C2—C10	173.59 (16)	C6—C1—C13—C12	−134.8 (2)
C13—C1—C2—C3	−171.78 (16)	C2—C1—C13—C12	−18.5 (2)
C7—C1—C2—C3	69.5 (2)	C7—C1—C13—C14	−70.9 (2)
C6—C1—C2—C3	−53.1 (2)	C6—C1—C13—C14	48.6 (2)
C10—C2—C3—C4	−178.36 (19)	C2—C1—C13—C14	164.98 (16)
C1—C2—C3—C4	50.4 (2)	C12—C13—C14—O1	−171.2 (2)
C10—C2—C3—C8	57.4 (3)	C1—C13—C14—O1	5.6 (3)
C1—C2—C3—C8	−73.8 (3)	C12—C13—C14—C15	8.3 (3)
C10—C2—C3—C9	−62.3 (2)	C1—C13—C14—C15	−174.92 (17)
C1—C2—C3—C9	166.5 (2)	O1—C14—C15—C16	179.6 (2)
C8—C3—C4—C5	76.0 (3)	C13—C14—C15—C16	0.1 (3)
C9—C3—C4—C5	−166.9 (2)	O1—C14—C15—O2	−1.6 (3)
C2—C3—C4—C5	−50.1 (3)	C13—C14—C15—O2	178.92 (17)
C3—C4—C5—C6	56.2 (3)	O2—C15—C16—C17	177.42 (18)
C4—C5—C6—C1	−58.2 (3)	C14—C15—C16—C17	−3.9 (3)
C13—C1—C6—C5	170.39 (19)	O2—C15—C16—C18	−3.1 (3)
C7—C1—C6—C5	−71.4 (2)	C14—C15—C16—C18	175.61 (19)
C2—C1—C6—C5	54.8 (2)	C15—C16—C17—O3	178.2 (2)
C1—C2—C10—C11	−68.9 (2)	C18—C16—C17—O3	−1.4 (3)
C3—C2—C10—C11	156.51 (17)	C15—C16—C17—C12	−0.2 (3)
C2—C10—C11—O4	162.26 (16)	C18—C16—C17—C12	−179.73 (17)
C2—C10—C11—C12	40.9 (2)	C13—C12—C17—O3	−169.35 (19)
O4—C11—C12—C13	−125.08 (19)	C11—C12—C17—O3	8.4 (2)
C10—C11—C12—C13	−4.7 (3)	C13—C12—C17—C16	9.0 (3)
O4—C11—C12—C17	57.2 (2)	C11—C12—C17—C16	−173.16 (16)
C10—C11—C12—C17	177.58 (16)	C15—C16—C18—C19	−63.3 (3)
C17—C12—C13—C14	−12.5 (3)	C17—C16—C18—C19	116.2 (2)
C11—C12—C13—C14	169.93 (16)	C15—C16—C18—C20	62.2 (3)
C17—C12—C13—C1	170.90 (16)	C17—C16—C18—C20	−118.2 (2)

Hydrogen-bond geometry (Å, º) top

D—H···A	D—H	H···A	D···A	D—H···A
O2—H2A···O1	0.82	2.10	2.579 (2)	117
O4—H4···O3	0.82	2.37	2.814 (2)	115
O2—H2A···O3ⁱ	0.82	2.39	3.153 (2)	155
O4—H4···O1ⁱⁱ	0.82	2.33	2.901 (2)	127
C11—H11···O1ⁱⁱ	0.98	2.47	3.120 (2)	124

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

Funding information

Funding for this research was provided by: Natural Science Foundation of Qinghai Province (grant No. 2016-ZJ-908); National Natural Science Foundation of China grant (grant No. 81573561).

References

Bruker (2007). APEX2 and SAINT. Bruker AXS Inc., Madison, Wisconsin, USA.
Burmistrova, O., Simoes, M. F., Rijo, P., Quintana, J., Bermejo, J. & Estevez, F. (2013). J. Nat. Prod. 76, 1413–1423. Web of Science CrossRef CAS PubMed
Chang, J. & Zhu, N. S. (2001). Nat. Prod. Res. Dev. 13, 27–29. CAS
Chen, X., Liao, R.-A., Weng, L.-H., Xie, Q.-L. & Deng, F.-J. (2000). Chin. J. Struct. Chem. 19, 122–125. CAS
Eugster, C. H., Ruedi, P., Tanudjaja, T., Bieri, J. H., Prewo, R. & Linden, A. (1993). Private communication. CCDC, Cambridge, England.
Fun, H.-K., Chantrapromma, S., Salae, A. W., Razak, I. A. & Karalai, C. (2011). Acta Cryst. E67, o1032–o1033. Web of Science CSD CrossRef IUCr Journals
Gonzalez, M. A. (2015). Nat. Prod. Rep. 32, 684–704. Web of Science CAS PubMed
Groom, C. R., Bruno, I. J., Lightfoot, M. P. & Ward, S. C. (2016). Acta Cryst. B72, 171–179. Web of Science CSD CrossRef IUCr Journals
Kolak, U., Kabouche, A., Öztürk, M., Kabouche, Z., Topçu, G. & Ulubelen, A. (2009). Phytochem. Anal. 20, 320–327. Web of Science CrossRef PubMed CAS
Kusumoto, N., Ashitani, T., Hayasaka, Y., Murayama, T., Ogiyama, K. & Takahashi, K. (2009). J. Chem. Ecol. 35, 635–642. Web of Science CrossRef PubMed CAS
Parsons, S., Flack, H. D. & Wagner, T. (2013). Acta Cryst. B69, 249–259. Web of Science CrossRef CAS IUCr Journals
Razak, I. A., Salae, A. W., Chantrapromma, S., Karalai, C. & Fun, H.-K. (2010). Acta Cryst. E66, o1566–o1567. Web of Science CSD CrossRef IUCr Journals
Sheldrick, G. M. (2008). Acta Cryst. A64, 112–122. Web of Science CrossRef CAS IUCr Journals
Sheldrick, G. M. (2015). Acta Cryst. C71, 3–8. Web of Science CrossRef IUCr Journals
Si, Y., Zhang, C.-K., Yao, X.-H. & Tu, Z.-B. (2001). J. Wuhan Bot. Res. 19, 517–520.
Spek, A. L. (2009). Acta Cryst. D65, 148–155. Web of Science CrossRef CAS IUCr Journals
Tanaka, R. (2001). Bioorg. Med. Chem. 9, 1911–1921. Web of Science CrossRef PubMed
Topçu, G. & Gören, A. C. (2007). Rec. Nat. Prod. 1, 1–16.
Topçu, G., Kolak, U., Ozturk, M., Boga, M., Hatipoglu, S. D., Bahadori, F., Culhaoglu, B. & Dirmenci, T. (2013). Nat. Prod. J, 3, 3–9.
Yang, Z., Kitano, Y., Chiba, K., Shibata, N., Kurokawa, H., Doi, Y., Arakawa, Y. & Tada, M. (2001). Bioorg. Med. Chem. 9, 347–356. Web of Science CrossRef PubMed CAS

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