Advertisement

World Journal of Microbiology and Biotechnology

, Volume 23, Issue 9, pp 1253–1263 | Cite as

Endophytic fungi from Nerium oleander L (Apocynaceae): main constituents and antioxidant activity

  • Wu-Yang HuangEmail author
  • Yi-Zhong Cai
  • Kevin D. Hyde
  • Harold Corke
  • Mei Sun
Original Paper

Abstract

Diverse endophytic fungi exist within plant aerial tissues, with a global estimate of up to a million undescribed species. These endophytes constitute a rich bio-resource for exploration to discover new natural products. Here we investigate fungal endophytes associated with a medicinal plant, Nerium oleander L. (Apocynaceae). A total of 42 endophytic fungal strains were isolated from the host plant. Total antioxidant capacity, xanthine oxidase inhibitory activity, antimicrobial activity, and total phenolic content (TPC) were evaluated for 16 representative fungal cultures grown in improved Czapek’s broth and for the host plant. The total antioxidant capacities and phenolic contents of the fungal cultures ranged from 9.59 to 150.79 μmol trolox/100 mL culture, and from 0.52 to 13.95 mg gallic acid/100 mL culture, respectively. The fungal culture of an endophytic strain Chaetomium sp. showed the strongest antioxidant capacity, contained the highest level of phenolics, and to some extent inhibited xanthine oxidase activity with an IC50 value of 109.8 μg/mL. A significant positive correlation was found between antioxidant capacity and TPC in the tested samples. Most of the endophytic fungal cultures tested have a wide range of antimicrobial activities, which were not very strong, but much better than those of the host plant. The major bioactive constituents of the fungal cultures were investigated using LC-ESI-MS and GC-MS, and preliminary identification detected phenolics (e.g. phenolic acids and their derivatives, flavonoids) and volatile and aliphatic compounds. This study shows that the endophytic fungi isolated from N. oleander can be a potential antioxidant resource.

Keywords

Antimicrobial activity Antioxidant activity Apocynaceae Endophytic fungi Nerium oleander Total phenolic content Xanthine oxidase inhibition 

Notes

Acknowledgments

This research was supported by grants from the University of Hong Kong (Seed Funding for Basic Research). We thank staff of Kadoorie Farm and Botanic Garden for assisting in plant sample collection, Dr L. Cai of the University of Hong Kong for assistance in identifying endophytic fungi, and Dr. Jie Xing of Republic Polytechnic, Singapore, for helping with LC-ESI-MS and GC-MS analyses.

References

  1. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654CrossRefGoogle Scholar
  2. Barnett HL, Hunter BB (1998) Illustrated genera of imperfect fungi. APS Press: St. Paul, Minnesota. ISBN: 0-89054-192-2Google Scholar
  3. Cai YZ, Luo Q, Sun M, Corke H (2004) Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci 74:2157–2184CrossRefGoogle Scholar
  4. Cameron DC, Cooney CL (1986) A novel fermentation: the production of R(-)-1,2-propanediol and acetol by Clostridium thermosaccharolyticum. Bio-Technology 4:651–654Google Scholar
  5. Carmichael JW, Brycekendrick W, Conners IL, Lynne S (1980) Genera of hyphomycetes. The University of Alberta Press: Edmonton, Alberta, Canada. ISBN: 0888640382Google Scholar
  6. Christensen LP, Brandt K (2006) Bioactive polyacetylenes in food plants of the Apiaceae family: occurrence, bioactivity and analysis. J Pharm Biomed Anal 41:683–693CrossRefGoogle Scholar
  7. dos Santos MD, Martins PR, dos Santos PA, Bortocan R, Iamamoto Y, Lopes NP (2005) Oxidative metabolism of 5-O-caffeoylquinic acid (chlorogenic acid), a bioactive natural product, by metalloporphyrin and rat liver mitochondria. Eur J Pharm Sci 26:62–70CrossRefGoogle Scholar
  8. EI-Shazly MM, EI-Zayat EM, Hermersdorfer H (2000) Insecticidal activity, mammalian cytotoxity and mutagenicity of an ethanolic extract from Nerium oleander (Apocynaceae). Ann Appl Biol 136:153–157CrossRefGoogle Scholar
  9. Ezra D, Hess WM, Strobel GA (2004) New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology-SGM 150:4023–4031CrossRefGoogle Scholar
  10. Faeth SH, Hammon KE (1997) Fungal endophytes in oak trees: long-term patterns of abundance and association with leafminers. Ecology 78:810–819CrossRefGoogle Scholar
  11. Fu L, Zhang S, Li N, Wang J, Zhao M, Sakai J, Hasegawa T, Mitsui T, Kataoka T, Oka S, Kiuchi M, Hirose K, Ando M (2005) Three new triterpenes from Nerium oleander and biological activity of the isolated compounds. J Nat Prod 68:198–206CrossRefGoogle Scholar
  12. Ganley RJ, Brunsfeld SJ, Newcombe G (2004) A community of unknown, endophytic fungi in western white pine. Proc Nat Acad Sci USA 101:10107–10112CrossRefGoogle Scholar
  13. Harper JK, Arif AM, Ford EJ, Strobel GA, Porco JA, Tomer DP, Oneill KL, Heider EM, Grant DM (2003) Pestacin: a 1,3-dihydro isobenzofuran from Pestalotiopsis microspora possessing antioxidant and antimycotic activities. Tetrahedron 59:2471–2476CrossRefGoogle Scholar
  14. Huang WY, Cai YZ, Xing J, Corke H, Sun M 2007 A potential antioxidant resource: endophytic fungi isolated from traditional Chinese medicinal plants. Econ Bot (in press)Google Scholar
  15. Ji YB (1999) Pharmacological action and application of anticancer traditional Chinese medicine. Heilongjiang Science Press: Heilongjiang, China. ISBN: 7538832793Google Scholar
  16. Kong LD, Cai Y, Huang WW, Cheng HK, Tan RX (2000) Inhibition of xanthine oxidase by some Chinese medicinal plants used to treat gout. J Ethnopharmacol 73:199–207CrossRefGoogle Scholar
  17. Kweon M, Hwang H, Sung H (2001) Identification and antioxidant activity of novel chlorogenic acid derivatives from Bamboo (Phyllostachys edulis). J Agric Food Chem 49:4646–4655CrossRefGoogle Scholar
  18. Li H, Meng JC, Cheng CHK, Higa T, Tanaka J, Tan RX (1999) New guaianolides and xanthine oxidase inhibitory flavonols from Ajania fruticulosa. J Nat Prod 62:1053–1055CrossRefGoogle Scholar
  19. Mosaddik MA, Banbury L, Forster P, Booth R, Markham J, Leach D, Waterman PG (2004) Screening of some Australian Flacourtiaceae species for in vitro antioxidant, cytotoxic and antimicrobial activity. Phytomedicine 11:461–466CrossRefGoogle Scholar
  20. Nagao A, Seki M, Kobayashi H 1999 Inhibition of xanthine oxidase by flavonoids. Biosci Biotechnol Biochem 63:1767–1790Google Scholar
  21. Nogueira MA, de Oliveira JS, Ferraz S (1996) Nematicidal hydrocarbons from Mucuna aterrima. Phytochemistry 42:997–998CrossRefGoogle Scholar
  22. Noro T, Oda Y, Toxhio M, Ueno A, Fukushima S (1983) Inhibition of xanthine oxidase from the flowers and buds of Daphne genkwa. Chemical and Pharm Bull 31:3984–3987Google Scholar
  23. Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophytic fungi of wild banana (Musa acuminata) at Doi Suthep Pui National Park, Thailand. Mycol Res 105:1508–1513Google Scholar
  24. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans CA (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237CrossRefGoogle Scholar
  25. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581CrossRefGoogle Scholar
  26. Rodrigues KF, Costa GL, Carvalho MP, Epifanio RDA (2005) Evaluation of extracts produced by some tropical fungi as potential cholinesterase inhibitors. World J Microbiol Biotechnol 21:1617–1621CrossRefGoogle Scholar
  27. Rouveix B (2003) Antibiotic safety assessment. Int J Antimicrobial Agents 21:215–221CrossRefGoogle Scholar
  28. Sakakibara H, Honda Y, Nakagawa S, Ashida H, Kanazawa K (2003) Simultaneous determination of all polyphenols in vegetables, fruits, and teas. J Agric Food Chem 51:571–581CrossRefGoogle Scholar
  29. Schulz B, Boyle C, Draeger S, Römmert AK (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004CrossRefGoogle Scholar
  30. Schulz B, Wanke U, Draeger S, Aust HJ (1993) Endophytes from herbaceous plants and shrubs, effectiveness of surface sterilization methods. Mycol Res 97:1447–1450CrossRefGoogle Scholar
  31. Shan B, Cai YZ, Sun M, Corke H (2005) Antioxidant capacity of 26 spice extracts and characterization of their phenolic constituents. J Agric Food Chem 53:7749–7759CrossRefGoogle Scholar
  32. Shen L, Jiao RH, Ye YH, Wang XT, Xu C, Song YC, Zhu HL, Tan RX. (2006) Absolute configuration of new cytotoxic and other bioactive trichothecene macrolides. Chem A Eur J 12:5596–5602CrossRefGoogle Scholar
  33. Shiono Y (2006) Anthracobic acids A and B, two polyketides, produced by an endophytic fungus Anthracobia sp. Chem Biodivers 3:217–223CrossRefGoogle Scholar
  34. Song YC, Huang WY, Sun C, Wang FW, Tan RX (2005) Characterization of graphislactone a as the antioxidant and free radical-scavenging substance from the culture of Cephalosporium sp IFB-E001, an endophytic fungus in Trachelospermum jasminoides. Biol Pharm Bull 28:506–509CrossRefGoogle Scholar
  35. Song YC, Li H, Ye YH, Shan CY, Yang YM, Tan RX (2004) Endophytic naphthopyrone metabolites are co-inhibitors of xanthine oxidase, SW1116 cell and some microbial growths. FEMS Microbiol Lett 241:67–72CrossRefGoogle Scholar
  36. Surveswaran S, Cai YZ, Corke H, Sun M 2007 Systematic evaluation of natural phenolic antioxidants from 133 Indian medicinal plants. Food Chem 102:938–953CrossRefGoogle Scholar
  37. Takacs S, Gries G, Gries R (2001) Communication ecology of webbing clothes moth: 4. Identification of male- and female-produced pheromones. Chemoecology 11:153–159CrossRefGoogle Scholar
  38. Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459CrossRefGoogle Scholar
  39. Tanaka T, Kawase M, Tani S (2004) α-Hydroxyketones as inhibitors of urease. Bioorg Med Chem 12:501–505CrossRefGoogle Scholar
  40. Wiyakrutta S, Sriubolmas N, Panphut W, Thongon N, Danwiserkanjana K, Ruangrungsi N, Meevootisom V (2004) Endophytic fungi with anti-microbial, anti-cancer, anti-malarial activities isolated from Thai medicinal plants. World J Microbiol Biotechnol 20:265–272CrossRefGoogle Scholar
  41. Yu J, Wang LM, Walzem RL, Miller EG, Pike LM, Patil BS (2005) Antioxidant activity of citrus limonoids, flavonoids, and coumarins. J Agric Food Chem 53:2009–2014CrossRefGoogle Scholar
  42. Zhang HW, Huang WY, Song YC, Chen JR, Tan RX (2005) Four 6H-dibenzo[b,d]pyran-6-one derivatives produced by the endophyte Cephalosporium acremonium IFB-E007. Helv Chim Acta 88:2861–2864CrossRefGoogle Scholar
  43. Zini CA, Zanin KD, Christensen E, Caramão EB, Pawliszyn J (2003) Solid-phase microextraction of volatile compounds from the chopped leaves of three species of Eucalyptus. J Agric Food Chem 51:2679–2686CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Wu-Yang Huang
    • 1
    Email author
  • Yi-Zhong Cai
    • 2
  • Kevin D. Hyde
    • 3
  • Harold Corke
    • 2
  • Mei Sun
    • 1
  1. 1.Department of ZoologyThe University of Hong KongHong KongP. R. China
  2. 2.Department of BotanyThe University of Hong KongHong KongP. R. China
  3. 3.Centre for Research in Fungal Diversity, Department of Ecology and BiodiversityThe University of Hong KongHong KongP. R. China

Personalised recommendations