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Planta Med 2018; 84(14): 1055-1063
DOI: 10.1055/a-0593-6030
Natural Product Chemistry and Analytical Studies
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Botryane Sesquiterpenoids, Cyclopentadepsipeptides, Xanthones, and Trichothecenes from Trichoderma oligosporum

Baosong Chen   *
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
2   Savaid Medicine School, University of Chinese Academy of Sciences, Beijing, P. R. China
,
Erwei Li   *
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
,
Li Liu
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
2   Savaid Medicine School, University of Chinese Academy of Sciences, Beijing, P. R. China
,
Mingfang Liao
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
2   Savaid Medicine School, University of Chinese Academy of Sciences, Beijing, P. R. China
,
Zhaoxiang Zhu
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
,
Wenying Zhuang
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
,
Li Bao
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
,
Hongwei Liu
1   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, P. R. China
2   Savaid Medicine School, University of Chinese Academy of Sciences, Beijing, P. R. China
› Author Affiliations
Further Information

Publication History

received 02 October 2017
revised 28 February 2018

accepted 14 March 2018

Publication Date:
22 March 2018 (online)

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Abstract

Five new botryane sesquiterpenes (1–5), one new cyclopentadepsipeptide (9), and two new xanthones (11 – 12), together with 11 known compounds, were isolated from Trichoderma oligosporum. The structures of the new compounds were identified by comprehensive spectroscopic methods including nuclear magnetic resonance and mass spectrometry. The cytotoxicity of 1–19 was evaluated against K562, A549, and ASPC cell lines. Compounds 5, 8, 11, 17, and 18 showed cytotoxicity against the K562 cell line with more than 50% inhibition at 12.5 µM. As to A549 cell line, compound

8 showed the strongest cytotoxicity with approximately 50% inhibition at 25.0 µM. No compounds showed cytotoxicity against the ASPC cell line.

Key words

Trichoderma oligosporum - Hypocreaceae - botryane sesquiterpenoids - cyclopentadepsipeptides - xanthones - trichothecenes

* These authors contributed equally to this work.


Supporting Information

    The 1H, 13C, and 2D NMR spectra of the new compounds, RP-HPLC-MS chromatogram of the CH2Cl2 extract and compounds 2, 4, and 12, and the CD spectrum of compound 12 are available in the Supporting Information.

  • Supporting Information
 

  • References

  • 1 Reino JL, Guerrero RF, Hernández-Galán R, Collado IG. Secondary metabolites from species of the biocontrol agent Trichoderma . Phytochem Rev 2008; 7: 89-123
    PubMedSearch in Google Scholar
  • 2 Garo E, Starks CM, Jensen PR, Fenical W, Lobkovsky E, Clardy J. Trichodermamides A and B, cytotoxic modified dipeptides from the marine-derived fungus Trichoderma virens . J Nat Prod 2003; 66: 423-426
    CrossrefPubMedSearch in Google Scholar
  • 3 Harris GH, Jones ETT, Meinz MS, Nallin-Omstead M, Helms GL, Bills GF. Isolation and structure elucidation of viridiofungins A, B and C. Tetrahedron Lett 2016; 34: 5235-5238
    PubMedSearch in Google Scholar
  • 4 Cutler HG, Jacyno JM, Phillips RS, Vontersch RL, Cole PD, Montemurro N. Cyclonerodiol from a novel source, Trichoderma koningii – plant-growth regulatory activity. Agric Biol Chem 1991; 55: 243-244
    PubMedSearch in Google Scholar
  • 5 Sauviat MP, Laurent D, Kohler F, Pellegrin F. Fumonisin, a toxin from the fungus Fusarium moniliforme sheld, blocks both the calcium current and the mechanical activity in frog atrial muscle. Toxicon 1991; 29: 1025-1031
    CrossrefPubMedSearch in Google Scholar
  • 6 Endo A, Hasumi K, Yamada A, Shimoda R, Takeshima H. The synthesis of compactin (Ml-236b) and monacolin K in fungi. J Antibiot 1986; 39: 1609-1610
    CrossrefPubMedSearch in Google Scholar
  • 7 Endo A. Compactin (Ml-236b) and related-compounds as potential cholesterol-lowering agents that inhibit HMG-CoA reductase. J Med Chem 1985; 28: 401-405
    CrossrefPubMedSearch in Google Scholar
  • 8 Bamburg JR, Strong FM. Mycotoxins of the trichothecane family produced by Fusarium tricinctum and Trichoderma lignorum . Phytochemistry 1969; 8: 2405-2410
    CrossrefPubMedSearch in Google Scholar
  • 9 Mckean C, Tang L, Billam M, Meng T, Theodorakis CW, Kendall RJ, Wang JS. Comparative acute and combinative toxicity of aflatoxin B1 and T-2 toxin in animals and immortalized human cell lines. J Appl Toxicol 2006; 26: 139
    CrossrefPubMedSearch in Google Scholar
  • 10 Wang QX, Yang JL, Qi QY, Bao L, Yang XL, Liu MM, Huang P, Zhang LX, Chen JL, Cai L, Liu HW. 3-Anhydro-6-hydroxy-ophiobolin A, a new sesterterpene inhibiting the growth of methicillin-resistant Staphylococcus aureus and inducing the cell death by apoptosis on K562, from the phytopathogenic fungus Bipolaris oryzae . Bioorg Med Chem Lett 2013; 23: 3547-3550
    CrossrefPubMedSearch in Google Scholar
  • 11 Zhu ZX, Zhuang WY. Three new species of Trichoderma with hyaline ascospores from China. Mycologia 2015; 107: 328-345
    CrossrefPubMedSearch in Google Scholar
  • 12 Duránpatrón R, Hernándezgalán R, Collado IG. Secobotrytriendiol and related sesquiterpenoids: new phytotoxic metabolites from Botrytis cinerea . J Nat Prod 2000; 63: 182-184
    CrossrefPubMedSearch in Google Scholar
  • 13 Ren FX, Zhu SM, Wang B, Li L, Liu XZ, Su RB, Che YS. Hypocriols A–F, heterodimeric botryane ethers from Hypocrea sp., an insect-associated fungus. J Nat Prod 2016; 79: 1848-1856
    CrossrefPubMedSearch in Google Scholar
  • 14 Sumarah MW, Puniani E, Blackwell BA, Miller JD. Characterization of polyketide metabolites from foliar endophytes of Picea glauca . J Nat Prod 2008; 71: 1393-1398
    CrossrefPubMedSearch in Google Scholar
  • 15 Zhang F, Li L, Niu SB, Si YK, Guo LD, Jiang XJ, Che YS. A thiopyranchromenone and other chromone derivatives from an endolichenic fungus, Preussia africana . J Nat Prod 2012; 75: 230-237
    CrossrefPubMedSearch in Google Scholar
  • 16 Shimada A, Takeuchi S, Kusano M, Fujioka S, Kimura Y. Roridin A and verrucarin A, inhibitors of pollen development in Arabidopsis thaliana, produced by Cylindrocarpon sp. Plant Sci 2004; 166: 1307-1312
    CrossrefPubMedSearch in Google Scholar
  • 17 Eppley RM, Mazzola EP, Highet RJ, Bailey WJ. Structure of satratoxin H, a metabolite of Stachybotrys atra. Application of proton and carbon-13 nuclear magnetic resonance. J Org Chem 1977; 42: 240-243
    CrossrefPubMedSearch in Google Scholar
  • 18 Saikawa Y, Okamoto H, Inui T, Makabe M, Okuno T, Suda T, Hashimoto K, Nakata M. Toxic principles of a poisonous mushroom Podostroma cornudamae . Tetrahedron 2001; 57: 8277-8281
    CrossrefPubMedSearch in Google Scholar
  • 19 Jarvis BB, Stahly GP, Pavanasasivam G, Midiwo JO, DeSilva T, Holmlund CE, Mazzola EP, Geoghegan jr. RF. Isolation and characterization of the trichoverroids and new roridins and verrucarins. J Org Chem 1982; 47: 1117-1124
    CrossrefPubMedSearch in Google Scholar
  • 20 Jegorov A, Havlíček V, Hušák M, Kratochvíl Β, Císařová I, Satkev J, Žabka M. Crystal structure of cyclo (2-hydroxy-i-valeryl-isoleucyl-2-hydroxy-i-valeryl-alanyl-threonyl) dihydrate, C23H39N3O8·2H2O. Z Kristallogr 2005; 220: 113-115
    PubMedSearch in Google Scholar
  • 21 Gerards M, Snatzke G. Circular dichroism, XCIII determination of the absolute configuration of alcohols, olefins, epoxides, and ethers from the CD of their “in situ” complexes with [Rh2(O2CCF3)4]. Tetrahedron Asymmetr 1990; 1: 221-236
    CrossrefPubMedSearch in Google Scholar
  • 22 Frelek J, Szczepek WJ. [Rh2(O2CCF3)4] as an auxiliary chromophore in chiroptical studies on steroidal alcohols. Tetrahedron Asymmetr 1999; 10: 1507-1520
    CrossrefPubMedSearch in Google Scholar
  • 23 Daoubi M, Duran-Patron R, Hernandez-Galan R, Benharref A, Hanson JR, Collado IG. The role of botrydienediol in the biodegradation of the sesquiterpenoid phytotoxin botrydial by Botrytis cinerea . Tetrahedron 2006; 62: 8256-8261
    CrossrefPubMedSearch in Google Scholar
  • 24 Flack HD. On enantiomorph-polarity estimation. Acta Crystallogr A 1983; 39: 876-881
    CrossrefPubMedSearch in Google Scholar
  • 25 Beutler JA, McCall KL, Herbert K, Herald DL, Pettit GR, Johnson T, Shoemaker RH, Boyd MR. Novel cytotoxic diterpenes from Casearia arborea . J Nat Prod 2000; 63: 657-661
    CrossrefPubMedSearch in Google Scholar
  • 26 Assante G, Camarda L, Merlini L, Nasini G. Mycochromone and mycoxanthone: two new metabolites from Mycosphaerella rosigena . Phytochemistry 1979; 18: 311-313
    CrossrefPubMedSearch in Google Scholar
  • 27 Barraclough D, Locksley HD, Scheinmann F, Magalhães MT, Gottlieb OR. Applications of proton magnetic resonance spectroscopy in the structural investigation of xanthones. J Chem Soc B 1970; 603-612
    PubMedSearch in Google Scholar
  • 28 Krohn K, Kouam SF, Kuigoua GM, Hussain H, Cludius-Brandt S, Flörke U, Kurtán T, Pescitelli G, Di BL, Draeger S. Xanthones and oxepino[2,3-b]chromones from three endophytic fungi. Chem Eur J 2009; 15: 12121-12132
    CrossrefPubMedSearch in Google Scholar
  • 29 Wang YC, Zheng ZH, Liu SC, Zhang H, Li EW, Guo LD, Che YS. Oxepinochromenones, furochromenone, and their putative precursors from the endolichenic pungus Coniochaeta sp. J Nat Prod 2010; 73: 920-924
    CrossrefPubMedSearch in Google Scholar
  • 30 Rebordinos L, Cantoral JM, Prieto MV, Hanson JR, Collado IG. The phytotoxic activity of some metabolites of Botrytis cinerea . Phytochemistry 1996; 42: 383-387
    CrossrefPubMedSearch in Google Scholar
  • 31 Khamthong N, Rukachaisirikul V, Phongpaichit S, Preedanon S, Sakayaroj J. An antibacterial cytochalasin derivative from the marine-derived fungus Diaporthaceae sp. PSU-SP2/4. Phytochem Letters 2014; 10: 5-9
    PubMedSearch in Google Scholar
  • 32 Silva GH, Oliveira CMD, Teles HL, Pauletti PM, Castro-Gamboa I, Silva DHS, Bolzani VS, Young MCM, Costa-Neto CM, Pfenning LH. Sesquiterpenes from Xylaria sp., an endophytic fungus associated with Piper aduncum (Piperaceae). Phytochem Letters 2010; 3: 164-167
    PubMedSearch in Google Scholar
  • 33 Kimura Y, Fujioka H, Nakajima H, Hamasaki T, Isogai A. Isolation and structures of O-Methyldihydrobotrydial and deacetyl-O-methyldihydrobotrydialone produced by Botrytis squamosa . Agric Biol Chem 1988; 52: 1845-1847
    PubMedSearch in Google Scholar
  • 34 Shao HJ, Qin XD, Dong ZJ, Zhang HB, Liu JK. Induced daldinin A, B, C with a new skeleton from cultures of the ascomycete Daldinia concentrica . Cheminform 2008; 61: 115-119
    PubMedSearch in Google Scholar
  • 35 Krohn K, Dai JU, Aust HJ, Drager S, Schulz B. Botryane metabolites from the fungus Geniculosporium sp. isolated from the marine red alga Polysiphonia . J Nat Prod 2005; 68: 400
    CrossrefPubMedSearch in Google Scholar
  • 36 Xie LW, Jiang SM, Zhu HH, Sun W, Ouyang YC, Dai SK, Li X. Potential inhibitors against Sclerotinia sclerotiorum, produced by the fungus Myrothecium sp associated with the marine sponge Axinella sp. Eur J Plant Pathol 2008; 122: 571-578
    CrossrefPubMedSearch in Google Scholar
  • 37 Wang YQ, Bao L, Yang XL, Li L, Li SF, Gao H, Yao XS, Wen HA, Lie HW. Bioactive sesquiterpenoids from the solid culture of the edible mushroom Flammulina velutipes growing on cooked rice. Food Chem 2012; 132: 1346-1353
    CrossrefPubMedSearch in Google Scholar
  • 38 Zhang F, Liu SC, Lu XH, Guo LD, Zhang H, Che YS. Allenyl and alkynyl phenyl ethers from the endolichenic fungus Neurospora terricola . J Nat Prod 2009; 72: 1782-1785
    CrossrefPubMedSearch in Google Scholar