Skip to main content

Advertisement

Log in

Antiproliferative, Antifungal, and Antibacterial Activities of Endophytic Alternaria Species from Cupressaceae

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Recent research has shown the bioprospecting of endophytic fungi from Cupressaceae. Here, we further uncover that the healthy cypress plants such as Cupressus arizonica, Cupressus sempervirens var. cereiformis, and Thuja orientalis host highly bioactive endophytic Alternaria fungal species. Indeed, endophytic Alternaria alternata, Alternaria pellucida, and Alternaria tangelonis were recovered from healthy Cupressaceous trees. Biodiversity and bioactivity of recovered endophytic Alternaria species were a matter of biogeography and host identity. We further extracted such Alternaria’s metabolites and highlighted their significant antiproliferative, growth inhibitory, and antibacterial activities against the model target fungus Pyricularia oryzae and the model pathogenic bacteria Bacillus sp., Erwinia amylovora, and Pseudomonas syringae. In vitro assays also indicated that endophytic Alternaria species significantly inhibited the growth of cypress fungal phytopathogens Diplodia seriata, Phaeobotryon cupressi, and Spencermartinsia viticola. In conclusion, since the recovered Alternaria species were originally reported as pathogenic and allergenic fungi, our findings suggest a possible ecological niche for them inside the foliar tissues of Cupressaceous trees. Moreover, in this study, the significant bioactivities of endophytic Alternaria species in association with Cupressaceae plant family are reported.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abdollahzadeh J, Mohammadi Goltapeh E, Javadi A, Shams-Bakhsh M, Zare R, Phillips AJL (2009) Barriopsis iraniana and Phaeobotryon cupressi: two new species of the Botryosphaeriaceae from trees in Iran. Persoonia 23:1–8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16

    Article  Google Scholar 

  3. Anaissie EJ, Bodey GP, Rinaldi MG (1989) Emerging fungal pathogens. Eur J Clin Microbiol Infect Dis 8:323–330

    Article  CAS  PubMed  Google Scholar 

  4. Bacon CW, White JF (2000) Microbial endophytes. Marcel Dekker Inc, New York

    Google Scholar 

  5. Brase S, Encinas A, Keck J, Nising CF (2009) Chemistry and biology of mycotoxins and related fungal metabolites. Chem Rev 109:3903–3990

    Article  CAS  PubMed  Google Scholar 

  6. Cantani A, Ciaschi V (2004) Epidemiology of Alternaria alternata allergy: a prospective study in 6840 Italian asthmatic children. Eur Rev Med Pharmacol Sci 8:289–294

    CAS  PubMed  Google Scholar 

  7. Duke SO, Dayan FE (2011) Modes of action of microbially-produced phytotoxins. Toxins 3:1038–1064

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Ershad J (2009) Fungi of Iran, 3rd edn. Iranian Research Institute of Plant Protection Press, Tehran, p 531

    Google Scholar 

  9. Fralish JS, Franklin SB (2002) Taxonomy and ecology of woody plants in North American forests. Wiley, New York

    Google Scholar 

  10. Gao SS, Li XM, Wang BG (2009) Perylene derivatives produced by Alternaria alternata an endophytic fungus isolated from Laurencia species. Nat Prod Commun 4:1477–1480

    CAS  PubMed  Google Scholar 

  11. Garau J, Diamond RD, Lagrotteria LB, Kabins SA (1977) Alternaria osteomyelitis. Ann Intern Med 86:747–748

    Article  CAS  PubMed  Google Scholar 

  12. Greenwald J, Brendler T, Jaenicke C (2004) PDR for herbal medicines, 3rd edn. Thomson Healthcare, Montvale

    Google Scholar 

  13. Hoffman MT, Arnold AE (2008) Geographic locality and host identity shape fungal endophyte communities in Cupressaceous trees. Mycol Res 112:331–334

    Article  CAS  PubMed  Google Scholar 

  14. Hoffman MT, Arnold AE (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76:4063–4075

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Hosseyni Moghaddam MS (2013) Study on some biological effects of natural products from endophytes of cypress. MSc thesis Bu-Ali Sina University of Hamedan, Iran p 180

  16. Hosseyni Moghaddam MS, Soltani J (2013) An investigation on the effects of photoperiod, aging and culture media on vegetative growth and sporulation of rice blast pathogen Pyricularia oryzae. Prog Biol Sci 3:135–143

    Google Scholar 

  17. Hosseyni Moghaddam MS, Soltani J (2013) Bioactivity of endophytic Trichoderma fungal species from the plant family Cupressaceae. Ann Microbiol. doi:10.1007/s13213-013-0710-1

    Google Scholar 

  18. Hosseyni Moghaddam MS, Soltani J, Babalhavaeji F, Hamzei J, Nazeri S, Mirzaei S (2013) Bioactivities of endophytic Penicillia from Cupressaceae. J Crop Prot 2:421–433

    Google Scholar 

  19. Kobayashi H, Namikoshi M, Yoshimoto T, Yokochi T (1996) A screening method for antimitotic and antifungal substances using conidia of P. oryzae, modification and application to tropical marine fungi. J Antibiot 49:873–879

    Article  CAS  PubMed  Google Scholar 

  20. Kour A, Shawl AS, Rehman S, Sultan PH, Qazi PH, Suden P, Khajuria RK, Verma V (2008) Isolation and identification of an endophytic strain of Fusarium oxysporum producing podophyllotoxin from Juniperus recurva. World J Microbiol Biotechnol 24:1115–1121

    Article  CAS  Google Scholar 

  21. Kumaran RS, Muthumary J, Hur BK (2008) Production of Taxol from Phyllosticta spinarum an endophytic fungus of Cupressus sp. Eng Life Sci 8:438–446

    Article  CAS  Google Scholar 

  22. Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798

    Article  CAS  PubMed  Google Scholar 

  23. Kusari S, Lamshoft M, Spiteller M (2009) Aspergillus fumigatus fresenius an endophytic fungus from Juniperus communis L Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. Appl Microbiol 107:1364–5072

    Article  Google Scholar 

  24. Kusari S, Pandey SP, Spiteller M (2013) Untapped mutualistic paradigms linking host plant and endophytic fungal production of similar bioactive secondary metabolites. Phytochemistry 91:81–87

    Article  CAS  PubMed  Google Scholar 

  25. Lou J, Fu L, Peng Y, Zhou L (2013) Metabolites from Alternaria fungi and their bioactivities. Molecules 18:5891–5935

    Article  PubMed  Google Scholar 

  26. Manning SC, Schaefer SD, Close LG, Vuitch F (1991) Culture-positive allergic fungal sinusitis. Arch Otolaryngol 117:174–178

    Article  CAS  Google Scholar 

  27. Mishra A, Gond SK, Kumar A, Sharma VK, Verma SK, Kharwar RN, Sieber TN (2012) Season and tissue type affect fungal endophyte communities of the Indian medicinal plant Tinospora cordifolia more strongly than geographic location. Microb Ecol 64:388–398

    Article  PubMed  Google Scholar 

  28. Mobius N, Hertweck C (2009) Fungal phytotoxins as mediators of virulence. Curr Opin Plant Biol 12:390–398

    Article  PubMed  Google Scholar 

  29. Morrison VA, Haake RJ, Weisdorf DJ (1993) The spectrum of non-Candida fungal infections following bone marrow transplantation. Medicine (Baltimore) 72:78–89

    Article  CAS  Google Scholar 

  30. Musetti R, Vecchione A, Stringher L, Borselli S, Zulini L, Marzani C, D’Ambrosio M, di Toppi Pertot LS (2006) Inhibition of sporulation and ultrastructural alterations of grapevine downy mildew by the endophytic fungus Alternaria alternata. Phytopathology 96:689–698

    Article  CAS  PubMed  Google Scholar 

  31. Ryan R, Germaine K, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  32. Ryan R, Ryan D, Dowling DN (2007) An acquired efflux system is responsible for copper resistance in Xanthomonas strain IG8. FEMS Microbiol Lett 268:40–46

    Article  CAS  PubMed  Google Scholar 

  33. Schell WA (2000) Unusual fungal pathogens in fungal rhinosinusitis. Otolaryngol Clin N Amer 33:367–373

    Article  CAS  Google Scholar 

  34. Shipunov A, Newcombe G, Raghavendra AK, Anderson CL (2008) Hidden diversity of endophytic fungi in an invasive plant. Am J Bot 95:1096–1108

    Article  PubMed  Google Scholar 

  35. Shweta S, Gurumurthy BR, Ravikanth G, Ramanan US, Shivanna MB (2013) Endophytic fungi from Miquelia dentata Bedd produce the anti-cancer alkaloid camptothecine. Phytomedicine 1520:337–342

    Article  Google Scholar 

  36. Simmons EG (2007) Alternaria: an identification manual. CBS Fungal Biodiversity Centre, Utrecht, p 775

    Google Scholar 

  37. Steel RGD, Torrie JH, Dicky DA (1997) Principles and procedures of statistics: a biometrical approach, 3rd edn. McGraw Hill Book, International Co, Singapore

    Google Scholar 

  38. Strange RN (2007) Phytotoxins produced by plant pathogens. Nat Prod Rep 24:127–144

    Article  CAS  PubMed  Google Scholar 

  39. Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5:535–544

    Article  CAS  PubMed  Google Scholar 

  40. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268

    Article  CAS  PubMed  Google Scholar 

  41. Sun Y, Wang Q, Lu X, Okane I, Kakishima M (2011) Endophytic fungi associated with two Suaeda species growing in alkaline soil in China. Mycosphere 2:239–248

    Google Scholar 

  42. Thomma BPHJ (2003) Alternaria spp: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236

    Article  CAS  PubMed  Google Scholar 

  43. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–66

    Article  CAS  PubMed  Google Scholar 

  44. Vartivarian SE, Anaissie EJ, Bodey GP (1993) Emerging fungal pathogens in immunocompromised patients: classification diagnosis and management. Clin Infect Dis 17:487–491

    Article  Google Scholar 

Download references

Acknowledgments

Dr. Jafar Abdollahzadeh (PhD), Dr. Salar Jamali (PhD), and Abolghasem Ghasemi (MSc) are appreciated for their generous gifting of target fungi and bacteria. We are thankful to our colleagues Dr. Soheila Mirzaei (PhD), Freydoun Babalhavaeji (MSc), and Dr. Javad Hamzei (PhD) at Bu-Ali Sina University of Hamedan, Iran, for their helpful technical discussions. J. S. dedicates this work to the memory of Adrina Ezmiri.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jalal Soltani.

Additional information

Jalal Soltani and Mahdieh S. Hosseyni Moghaddam have contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soltani, J., Hosseyni Moghaddam, M.S. Antiproliferative, Antifungal, and Antibacterial Activities of Endophytic Alternaria Species from Cupressaceae. Curr Microbiol 69, 349–356 (2014). https://doi.org/10.1007/s00284-014-0594-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-014-0594-8

Keywords

Navigation