A New Chromene Derivative and a New Polyalcohol Isolated From the Fungus Xylaria sp. 111A Associated With Garcinia polyantha Leaves

Abstract

From the crude extract of the plant-associated fungus Xylaria sp. collected in Cameroon, a new 2H-chromene derivative, hexacycloxylariolone (1), and a new polyalcohol, xylatriol (2), were isolated, in addition to 3 known compounds, 2,3-furandiol (3), 1,8-dimethoxynaphthalene (4), and 1-palmitoyl-rac-glycerol (5). Their chemical structures were established on the basis of the interpretation of spectroscopic data. Hexacycloxylariolone (1), 1,8-dimethoxynaphthalene (4), and 1-palmitoyl-rac-glycerol (5) showed antiproliferative activity by inhibiting the growth of Raw 264.7 and THP-1 cancer cell lines.

Keywords

antiproliferative activity

Endophytic fungi are promising sources of various bioactive natural products due to their complex interactions with their host plants.¹ In recent years, more attention has been paid to secondary metabolites of endophytic fungi from medicinal plants. Garcinia polyantha, a traditionally edible and medicinal plant in Cameroon, contains various xanthones and benzophenones with cytotoxic activities.² Fungi in the genus Xylaria have been extensively investigated and different classes of bioactive compounds have been isolated, such as antimalarial,³ cytotoxic,^4,5 antimicrobial,⁶ anti-HIV,⁷ antioxidant,⁸ phytotoxic,^9
-11 and immunosuppressive metabolites.¹²

In our continuous search for secondary metabolites with biological importance from natural sources,^13
-15 we have carried out studies on a fungal strain Xylaria sp. originally isolated from the leaves of G. polyantha collected in Cameroon. Thus, the present study undertook the chemical investigation of this fungus cultivated on a sterile steamed unpolished rice medium to afford 5 compounds (1-5), including 2 new ones (Figure 1). Herein, details of the isolation, structural elucidation, and antiproliferative activity against Raw 264.7 and THP-1 cancer cell lines of 1‐5 are presented (Table 1).

Figure 1

Chemical structures of compounds 1-5.

Table 1

Antiproliferative Activity of Extract and Compounds 1-5.

Extract and compounds	IC₅₀ (µg/mL)		IC₅₀ (µM)
Extract and compounds	THP-1	Raw 264.7	THP-1	Raw 264.7
Extract	12.7	30.1	/	/
(1)	82.3	74.6	428.7	388.6
(2)	-	-	/	/
(3)	-	-	/	/
(4)	-	57.2	/	304.0
(5)	94.4	90.5	637.4	611.3
Paclitaxel	3.2	4.5	3.8	5.3

Abbreviation: IC₅₀, half-maximal inhibitory concentration.

“-” Indicates >100 µg/mL and “/” indicates not determined.

Results and Discussion

The Xylaria sp. was isolated from the leaves of G. polyantha and cultivated on an unpolished rice solid medium. The ethyl acetate (EtOAc) extracts of the rice cultures were puriﬁed by combined column chromatographies (CCs) using silica gel, and semipreparative high-performance liquid chromatography (HPLC) to yield compounds 1‐5 (Figure 1).

Compound 1 was isolated as a white amorphous powder and was assigned the molecular formula C₁₂H₁₂O ₃ based on the high-resolution electrospray ionization mass spectrometry (HR-ESI-MS) peak at m/z 193.0868 ([M + H]⁺; C₁₂H₁₃O ₃ ⁺, calcd. 193.0865) (Supplemental Figure S1), indicating 6 degrees of unsaturation. Its ultraviolet (UV) spectrum in methanol exhibited maxima at 266 and 322 nm, and the infrared (IR) spectrum showed absorptions at 3849, 3741, and 3100 cm⁻¹ for hydroxyl groups. The proton resonances assigned to the relevant carbon atoms by the heteronuclear single quantum coherence spectrum (Supplemental Figures S1, S2 and S4) showed the presence of 12 carbons, which can be sorted into 1 methyl δ (17.3; 1.16, 3 H, d, J = 6.0 Hz), 2 methines (δ 76.6; 4.02, 1 H, dd, J = 7.2, 4.8 Hz and δ 70.5, 3.74, 1 H, qd, J = 6.0, 4.8 Hz), 5 sp ² methines [δ (132.1, 7.26, 1 H, obs), (132.0; 7.24, 1 H, d, J = 10.8), (130.3; 6.03, 1 H, dd, J = 10,8, 7.2 Hz), (118.4; 6.98, 1 H, dd, J = 7.8, 1.2 Hz), and (115.6; 6.77, 1 H, d, J = 7.8, 1.2 Hz)], 1 olefinic quaternary carbon (δ _C 115.5) and 2 oxygenated sp ² carbons (δ _C 160.4 and 140.1). The above nuclear magnetic resonance (NMR) data (Table 2) suggested that compound 1 has a 1,2,3-trisubstituted benzene ring [δ _H 7.26 (1H, obs), 6.98 (1H, dd, J = 7.8, 1.2), and 6.77 (1H, dd, J = 7.8, 1.2)]. The benzene ring occupying 4 degrees of unsaturation suggested that compound 1 possessed an additional ring including 1 double bond. In the heteronuclear multiple bond correlation (HMBC) spectrum (Supplemental Figure S5), long-range correlations were observed between H-2 (δ _H 4.02) and C-8a (δ _C 140.1); H-3 (δ _H 6.03) and C-2 (δ _C 76.6); and H-4 (δ _H 7.24) and C-2. The aromatic proton H-7 (δ _H 7.26) showed long-range correlations with the carbon signals C-8a and C-5 (160.4); H-8 (δ _H 6.98) showed cross-peaks with the carbon signals C-8a and C-4a (115.5). In the correlation spectroscopy (COSY) (Supplemental Figure S6), cross-peaks were observed between H-6/H-7and H-7/H-8 of the aromatic protons. From the above evidence, the presence of a 5-monosubstituted chromene ring was postulated. The location of the hydroxyl side chain was confirmed to be at C-2 by the HMBC peaks from H-9 (δ _H 3.74) to C-2 and C-10 (δ _C 17.3); H-10 (δ _H 1.16) to C-2 and C-3 (δ _C 130.3); and from H-3 and H-4 to C-2. On that basis, the structure of 1 was established as 2-(1-hydroxyethyl)-2H-chromen-5-ol, a new secondary metabolite to which the name hexacycloxylariolone is given.

Table 2

¹H NMR and¹³C NMR Spectroscopic Data of Compounds 1 and 2 in DMSO-d ₆ (δ in Ppm, J in Hz).

Pos.	1		Pos.	2
	¹³C (150 MHz) δ (C)	¹H (600 MHz) δ (H)		¹³C (150 MHz) δ (C)	¹H (600 MHz) δ (H)
	¹³C (150 MHz) δ (C)	¹H (600 MHz) δ (H)		¹³C (150 MHz) δ (C)	¹H (600 MHz) δ (H)	1	1	26.0	1.89 (d, J = 6.2)
2	76.6 (d)	4.02 (dd, J = 7.2, 4.8)	2	64.3	4.64 m
3	130.3 (d)	6.03 (dd, J = 10.8, 7.2)	3	43.4	2.33 m
4	132.0 (d)	7.24 (d, J = 10.8)	4	71.8	4.25 (dtd, J = 8.4, 5.8, 2.4)
4a	115.5 (s)		5	76.8	3.92 (dtd, J = 9.0, 5.8, 3.3)
5	160.4 (s)		6	26.7	2.07 (m)
6	115.6 (d)	6.77 (dd, J = 7.8; 1.2)	7	11.6	1.68 (t, J = 7.4)
7	132.1 (d)	7.26 (obs)	2-OH		5.13 (d, J = 4.9)
8	118.4 (d)	6.98 (dd, J = 7.8, 1.2)	4-OH		5.02 (d, J = 6.0)
8a	140.1 (s)		5-OH		5.08 (d, J = 5.7)
9	70.5 (d)	3.74 (qd, J = 6.0, 4.8)
10	17.3 (q)	1.16 (d, J = 6.0)

Abbreviations: NMR, nuclear magnetic resonance; obs, obscured by overlapping resonances.

Compound 2 was isolated as a white powder. Its molecular formula, C₇H₁₆O₃, was established from an HR-ESI-MS peak at m/z 171.0990 ([M + Na]⁺; C₇H₁₆O₃Na⁺, calcd. 171.0997) (Supplemental Figure S7), indicating no unsaturation. The IR spectrum showed characteristic vibration bands at ν _max 3876 and 3741 cm⁻¹ (OH). The ¹H NMR and ¹³C NMR spectra (Supplemental Figures S8 an S9) showed the presence of 7 carbons, which can be sorted into 2 methyls [δ (26.0; 1.89, 3H, d, J = 6.2 Hz) and (11.6; 1.68, 3H, t, J = 7.4 Hz)], 2 methylenes [δ (43.4; 2.33, 2H, m) and (26.7, 2.33, m)], and 3 oxygenated methines [δ (76.8; 3.92, 1H, dtd, J = 9.0, 5.8, 3.3 Hz); (71.8; 4.25, 1H, dtd, J = 8.4, 5.8, 2.4 Hz), and (64.3; 2.33, 1H, m)]. The heteronuclear multiple quantum coherence (HMQC) spectrum (Supplemental Figure S10) in conjunction with the COSY correlation peaks observed from H-1 to H-7 (Supplemental Figure S12) allowed the assignment of 1 spin system in 2. The HMBC peaks from H-1 (δ _H 3.74) to C-2 (δ _C 64.3) and C-3 (δ _C 43.4); H-3 (δ _H 2.33) to C-2 and C-4 (δ _C 71.8); H-4 (δ _H 4.25) to C-2; H-5 (δ _H 3.92) to C-4; H-6 (δ _H 2.07) to C-5 (δ _C 76.8) and C-7 (11.6), and from H-7 (δ _H 1.68) to C-5 and C-6 unambiguously established that the hydroxyl groups were linked at C-2, C-4, and C-5, respectively (Figure 2). This finding was further confirmed by the HMBC peaks (Supplemental Figure S11) from 4-OH to C-4, C-3, and C-5 and 5-OH to C-5, C-4, and C-6. On the basis of these data, the planar structure of 2 was elucidated as heptane-2,4,5-triol.

Figure 2

Important heteronuclear multiple bond correlation (HMBC), correlation spectroscopy (COSY), and nuclear Overhauser effect spectroscopy (NOESY) correlations for compounds 1 and 2.

The relative configuration of 2 was established from the nuclear Overhauser effect spectroscopy (NOESY) spectrum where clear NOE correlations between H-2 and H-4 (Supplemental Figure S12) indicate that they are on the same face of the molecule. Besides, no correlation was observed between H-2 and H-5, indicating the α-orientation of H-5. The structure of 2 was found to be (2S*, 4S*, 5R*)-heptane-2,4,5-triol, to which the trivial name xylatriol is given.

The known compounds, 2,3-furandiol (3),¹⁶ 1,8-dimethoxynaphthalene (4),^17,18 and 1-palmitoyl-rac-glycerol (5),¹⁹ were identified by comparison of their NMR data with those reported in the literature.

The antiproliferative effect of the crude extract and isolated compounds was investigated against cancer cell lines, RAW 264.7 and THP-1. The results presented in Table 1 indicate that the tested samples showed various extents of antiproliferative activity. The crude extract had the most potent cytotoxic activity against THP-1 cells (half-maximal inhibitory concentration [IC₅₀] 12.7 µg/mL) compared with compounds (1) and (5), which showed their inhibitory effects on the growth of THP-1 cells with IC₅₀ values of 82.3 µg/mL and 94.4 µg/mL, respectively. The lowest activity was observed for compounds 2, 3, and 4, which showed less than 50% of cell viability at the concentration of 100 µg/mL; therefore, their IC₅₀ values could not be determined ( >100 µg/mL). The IC₅₀ values against RAW 264.7 cells ranged between 30.1 µg/mL and 90.5 µg/mL. Our finding is consistent with the literature since other secondary metabolites such as cytochalasins isolated from Xylaria species were previously pointed out to be promising compounds for applications in medicine as drug candidates for the treatment of cancer.^20,21 Therefore, the results of this study indicate that the Xylaria sp. is a potential source of compounds that may serve as leads for anticancer drugs.

Experimental

General Experimental Procedures

Optical rotation values were measured with a Horiba SEPA-300 polarimeter. IR and UV spectra were, respectively, recorded with JASCO A-302 IR and Jasco J-20A, Shimadzu UV mini-1240 spectrophotometers. ¹H, ¹³C, and 2D NMR spectra were recorded on Bruker AMX-500 and Jeol ECZ-600 spectrometers. Proton and carbon chemical shifts are reported in δ (ppm) with reference to trimethylsilane (TMS). Coupling constants (J) are given in Hz. Homonuclear ¹H-¹H connectivity was determined by the COSY 45 experiment and 1-bond ¹H-¹³C connectivity by HMQC. ¹H-¹³C connectivity over 2 or 3 bonds was detected by HMBC. The ESI-MS were recorded on a Double-Focusing Mass Spectrometer (Varian MAT 311A). HR-EI-MS were recorded on JEOL HX 110 and Synapt G2 Mass Spectrometers. Column chromatography was carried out on silica gel 60 (70-230 and 240‐300 mesh sizes, E. Merck), and semipreparative HPLC with a Shimadzu pump and UV LC-10A detector (set at 210 nm) on a Mightysil ODS column (250 × 6.0 mm i.d.) at a flow rate of 1.5 mL/min. Precoated silica gel thin-layer chromatography plates supported on aluminum sheets (E. Merck, F₂₅₄) were used to check the purity of compounds, which were detected either by spraying with 10% vanillin in sulfuric acid followed by heating or by UV irradiation. The vanillin/sulfuric acid spray reagent was prepared by dissolving 1.0 g of vanillin in 100 mL of concentrated sulfuric acid.

Fungal Material

The fungal strain Xylaria sp. 111A was isolated from a healthy leaf of G. polyantha collected in Yaoundé (Cameroon). The plant material was authenticated by Mr NANA Victor of the National Herbarium of Cameroon in Yaoundé, where a voucher specimen (21337/SRF/Cam/Mt Kala) is deposited. The healthy leaf was aseptically cleaned successively with 70% ethanol (EtOH) for 1 minute, 5% sodium hypochlorite for 5 minutes, 70% EtOH for 1 minute, and then rinsed in sterile water 2 times. The aseptically clean samples were dried on sterilized paper and cut into 1-cm pieces. The pieces were placed on plates of potato dextrose agar (PDA) containing chloramphenicol (100 mg/L). After incubation at 25 °C for 7 days, the hyphal tips of the fungi on the plates were removed from the agar plates and transferred to new PDA plates (slant). The strain 111A was isolated and grown on slants of PDA as silver to black colored culture. This strain was identiﬁed as Xylaria sp. by BEX Co. LTD., Japan, using DNA analysis of the 18S rDNA regions and deposited at the laboratory in the Faculty of Agriculture of Yamagata University, Japan.

Extraction and Isolation

Xylaria sp. was cultivated in 10 Erlenmeyer flasks (1000 mL each) containing 50 g of sterile steamed unpolished rice. Each flask received about 5 small pieces of mycelium from the PDA plate under sterile conditions. After 4 weeks of growing at 25 °C, the moldy unpolished rice was extracted with EtOAc (2.0 L), and taken to dryness. The resulting extract was further partitioned into n-hexane fraction (0.5 L), EtOAc fraction (0.5 L), and aqueous fraction (0.5 L). The EtOAc fraction (3.50 g) was chromatographed on a silica gel column with stepwise elution with n-hexane-EtOAc 100:0-0:100, v/v, and EtOAc/MeOH 50:50, 0:100, v/v, respectively, to afford fractions A, B, C, and D. Fraction A (0.8 g) was further chromatographed on a silica gel column using stepwise elution (chloroform [CHCl₃]/EtOAc) to afford fractions A-1 to A-6. Fractions A-3 (43 mg) (CHCl₃-EtOAc 50/50, v/v) and A-4 (72 mg) (CHCl₃-EtOAc, 40:60, v/v) were further separated by octadecyl silica gel column chromatography eluting with isocratic acetonitrile-water (60:40) to yield 1 (2.1 mg) and 3 (10.2 mg). Fractions B and C (n-hexane/EtOAc 30/80, 40:60) were combined (1.8 g) and further column chromatography on silica gel using a gradient of CHCl₃/EtOAc 100:0-0:100, v/v afforded 2 (14.6 mg), 4 (10.3 mg), and 5 (11.1 mg).

Hexacycloxylariolone (1)

White powder. $[α]_{D}^{25}$ = +0,55 (c 0.03, MeOH). UV (MeOH): 266 and 322 nm IR (ν_max, KBr): 3849, 3741, 3100, 1673, 1631, 1531, and 1295. HR-ESI-MS: m/z 193.0868 [M + H]⁺, (calcd. for C₁₂H₁₃O ₃ m/z 193.0865). ¹H and ¹³C NMR see Table 2.

Xylatriol (2)

White powder. $[α]_{D}^{25}$ = +6.7 (c 0.3, MeOH). IR (ν_max, KBr): 3876, 3741, 1708 and 1527 cm⁻¹. HR-ESI-MS: m/z 171.0990 [M + Na]⁺, (calcd. for C₇H₁₆O₃Na m/z 171.0997). ¹H and ¹³C NMR see Table 2.

Antiproliferative Activity

The mouse macrophages Raw 264.7 cell line and the THP-1 human monocytic leukemia cell line were cultured, respectively, in Dulbecco’s modified Eagle’s medium and Roswell Park Memorial Institute 1640 culture medium containing 2 mM l-glutamine supplemented with 0.1% 2-mercaptoethanol. All the culture media were supplemented with 10% fetal calf serum and 1% antibiotics comprising 100 IU/mL penicillin and 100 µL/mL streptomycin. Cells were maintained at 37 °C in a humidified atmosphere containing 5% carbon dioxide.

Cell proliferation was evaluated using the cell proliferation reagent WST-1 (2-(4-iodophenyl)−3- (4-nitrophenyl)−5-(2,4-disulfophenyl)−2H-tetrazolium) (Roche Diagnostics, Germany), according to the manufacturer’s instructions. Cells were seeded (10⁴ cells/100 µL per well) in 96-well plates in triplicate and incubated overnight. The next day, the cells were exposed to different concentrations (1 µg/mL, 10 µg/mL, 30 µg/mL, 60 µg/mL, and 100 µg/mL) of either extract or compounds and incubated for 48 hours. Then the medium in each well was aspirated, and WST-1 solution, diluted 1:10 with fresh medium, was added to each well, and the plates incubated at 37 °C for 60 minutes. The absorbance was recorded at 450 nm/690 nm using a Synergy Multi-Mode Microplate Reader (BioTek). Results were expressed as the percentage of viable cells relative to the control without treatment. A concentration-response analysis was performed to determine the compound concentrations required to inhibit the growth of cancer cells by 50% (IC₅₀) using GraphPad Prism software.

Conclusion

The chemical investigation of Xylaria sp. obtained from G. polyantha led to the isolation of a new 2H-chromene derivative, hexacycloxylariolone (1), and a new polyalcohol, xylatriol (2), along with 3 known compounds, 2,3-furandiol (3), 1,8-dimethoxynaphthalene (4), and 1-palmitoyl-rac-glycerol (5). An antiproliferative in vitro bioassay was used to evaluate the crude extract and isolated compounds against Raw 264.7 and THP-1 cancer cell lines. The crude extract, hexacycloxylariolone (1), 1,8-dimethoxynaphthalene (4), and 1-palmitoyl-rac-glycerol (5) showed moderate antiproliferative activity. None of the isolated compounds has been reported from the host plant. This finding could provide new perspectives in the study of the chemical diversity of endophytes from other parts of this plant.

Supplemental Material

Figure S1 - Supplemental material for A New Chromene Derivative and a New Polyalcohol Isolated From the Fungus Xylaria sp. 111A Associated With Garcinia polyantha Leaves

Supplemental material, Figure S1, for A New Chromene Derivative and a New Polyalcohol Isolated From the Fungus Xylaria sp. 111A Associated With Garcinia polyantha Leaves by Hycienth Fung Tegha, Jean-Bosco Jouda, Jean Paul Dzoyem, Denis Kehdinga Sema, Bosco Peron Leutcha, Eric Allémann, Florence Delie, Yoshihito Shiono, Norbert Sewald and Alain Meli Lannang in Natural Product Communications

Footnotes

Acknowledgments

We thank the Georg Forster Fellowship for Experienced Researchers (ID N° 1137675) at the University of Bielefeld (Germany) to AML.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The authors are thankful to the German Academic Exchange Service (DAAD) for the financial support to the Yaounde-Bielefeld Graduate School of Natural Products with Antiparasite and Antibacterial activities (YaBiNaPA), project N° 57316173.

ORCID iD

Alain Meli Lannang

Supplemental Material

Supplemental material for this article is available online.

References

Long

Tang

Wang

L-Y.

Gao

. Absolute configuration and biological activities of meroterpenoids from an endophytic fungus of Lycium barbarum . J Nat Prod. 2019;82(8):2229-2237.doi:10.1021/acs.jnatprod.9b00288

31397570

Lannang

AM.

Tatsimo

SJN.

Fouotsa

Dzoyem

JP.

Saxena

AK.

Sewald

. Cytotoxic compounds from the leaves of Garcinia polyantha . Chem Biodivers. 2014;11(6):975-981.doi:10.1002/cbdv.201300401

24934683

Sawadsitang

Mongkolthanaruk

Suwannasai

Sodngam

. Antimalarial and cytotoxic constituents of Xylaria cf. cubensis PK108. Nat Prod Res. 2015;29(21):2033-2036.doi:10.1080/14786419.2015.1017724

25738405

Shiono

Motoki

Koseki

Murayama

Tojima

Kimura

. Isopimarane diterpene glycosides, apoptosis inducers, obtained from fruiting bodies of the ascomycete Xylaria polymorpha . Phytochemistry. 2009;70(7):935-939.doi:10.1016/j.phytochem.2009.03.023

19467682

Wang

W-X.

Z-H.

H-L

et al. Cytotoxic 19,20-epoxycytochalasans from endophytic fungus Xylaria cf. curta. Fitoterapia. 2019;137:104253. doi:10.1016/j.fitote.2019.104253

31271786

Tarman

Palm

GJ.

Porzel

et al. Helicascolide C, a new lactone from an Indonesian marine algicolous strain of Daldinia eschscholzii (Xylariaceae, Ascomycota). Phytochem Lett. 2012;5(1):83-86.doi:10.1016/j.phytol.2011.10.006

Singh

SB.

Zink

Polishook

et al. Structure and absolute stereochemistry of HIV-1 integrase inhibitor integric acid. A novel eremophilane sesquiterpenoid produced by a Xylaria sp. Tetrahedron Lett. 1999;40(50):8775-8779.doi:10.1016/S0040-4039(99)01878-X

Liu

Dong

Chen

Jiang

Yan

. Antioxidant activity and phenolics of an endophytic Xylaria sp. from Ginkgo biloba . Food Chem. 2007;105(2):548-554.doi:10.1016/j.foodchem.2007.04.008

Shiono

Murayama

. New eremophilane-type sesquiterpenoids, eremoxylarins A and B from xylariaceous endophytic fungus YUA-026. Z Naturforsch B. 2005;60(8):885-890.doi:10.1515/znb-2005-0812

10.

Zhang

Xiao

Sun

Q-Q.

Qin

J-C.

Pescitelli

Gao

J-M

. Characterization of cytochalasins from the endophytic Xylaria sp. and their biological functions. J Agric Food Chem. 2014;62(45):10962-10969.doi:10.1021/jf503846z

25350301

11.

García-Méndez

MC.

Macías-Ruvalcaba

NA.

Lappe-Oliveras

Hernández-Ortega

Macías-Rubalcava

. Phytotoxic potential of secondary metabolites and semisynthetic compounds from endophytic fungus Xylaria feejeensis strain SM3e-1b isolated from Sapium macrocarpum . J Agric Food Chem. 2016;64(21):4255-4263.doi:10.1021/acs.jafc.6b01111

27159617

12.

Chen

H-P.

Zhao

Z-Z.

Cheng

G-G

et al. Immunosuppressive nor-isopimarane diterpenes from cultures of the fungicolous fungus Xylaria longipes HFG1018. J Nat Prod. 2020;83(2):401-412.doi:10.1021/acs.jnatprod.9b00889

31961677

13.

Jouda

J-B.

Mfotie Njoya

Mbazoa

et al. Lambertellin from Pycnoporus sanguineus MUCL 51321 and its anti-inflammatory effect via modulation of MAPK and NF-κB signaling pathways. Bioorg Chem. 2018;80:216-222.doi:10.1016/j.bioorg.2018.06.021

29957490

14.

Jouda

J-B.

Njoya

EM.

Fobofou

SAT

et al. Natural polyketides isolated from the endophytic fungus Phomopsis sp. CAM212 with a semisynthetic derivative downregulating the ERK/IκBα signaling pathways. Planta Med. 2020;86(13-14):1032-1042.doi:10.1055/a-1212-2930

32757200

15.

Lannang

AM.

Sema

DK.

Tatsimo

SJN

et al. A new depsidone derivative from the leaves of Garcinia polyantha . Nat Prod Res. 2018;32(9):1033-1038.doi:10.1080/14786419.2017.1378201

28931317

16.

Calvinho

KUD.

Laursen

AB.

Yap

KMK

et al. Selective CO₂ reduction to C₃ and C₄ oxyhydrocarbons on nickel phosphides at overpotentials as low as 10 mV. Energy Environ Sci. 2018;11(9):2550-2559.doi:10.1039/C8EE00936H

17.

Dai

Krohn

Draeger

Schulz

. New naphthalenechroman coupling products from the endophytic fungus, Nodulisporium sp. from Erica arborea . Eur J Org Chem. 2009;10:1564-1569.doi:10.1002/ejoc.200801106

18.

Anke

Stadler

Mayer

Sterner

. Secondary metabolites with nematicidal and antimicrobial activity from nematophagous fungi and ascomycetes. Can J Bot. 1995;73(S1):932-939.doi:10.1139/b95-341

19.

Lainer

Dawid

Dunkel

Gläser

Wittl

Hofmann

. Characterization of bitter-tasting oxylipins in Poppy seeds (Papaver somniferum L.. J Agric Food Chem. 2020;68(38):10361-10373.doi:10.1021/acs.jafc.9b06655

31841329

20.

Macías-Rubalcava

ML.

Sánchez-Fernández

. Secondary metabolites of endophytic Xylaria species with potential applications in medicine and agriculture. World J Microbiol Biotechnol. 2017;33(1):15.doi:10.1007/s11274-016-2174-5

27896581

21.

Wei

YM.

Espinosa-Artiles

et al. Sesquiterpenes and other constituents of Xylaria sp. NC1214, a fungal endophyte of the moss Hypnum sp. Phytochemistry. 2015;118:102-108.doi:10.1016/j.phytochem.2015.08.010

26324074

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