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Journal of Chemical Ecology

, Volume 36, Issue 10, pp 1122–1131 | Cite as

Allelochemical Effects of Volatile Compounds and Organic Extracts from Muscodor yucatanensis, a Tropical Endophytic Fungus from Bursera simaruba

  • Martha L. Macías-Rubalcava
  • Blanca E. Hernández-Bautista
  • Fabiola Oropeza
  • Georgina Duarte
  • María C. González
  • Anthony E. Glenn
  • Richard T. Hanlin
  • Ana Luisa Anaya
Article

Abstract

Muscodor yucatanensis, an endophytic fungus, was isolated from the leaves of Bursera simaruba (Burseraceae) in a dry, semideciduous tropical forest in the Ecological Reserve El Eden, Quintana Roo, Mexico. We tested the mixture of volatile organic compounds (VOCs) produced by M. yucatanensis for allelochemical effects against other endophytic fungi, phytopathogenic fungi and fungoids, and plants. VOCs were lethal to Guignardia mangifera, Colletotrichum sp., Phomopsis sp., Alternaria solani, Rhizoctonia sp., Phytophthora capsici, and P. parasitica, but had no effect on Fusarium oxysporum, Xylaria sp., the endophytic isolate 120, or M. yucatanensis. VOCs inhibited root elongation in amaranth, tomato, and barnyard grass, particularly those produced during the first 15 days of fungal growth. VOCs were identified by gas chromatography/mass spectrometry and included compounds not previously reported from other Muscodor species and the previously reported compounds octane, 2-methyl butyl acetate, 2-pentyl furan, caryophyllene, and aromadendrene. We also evaluated organic extracts from the culture medium and mycelium of M. yucatanensis on the same endophytes, phytopathogens, and plants. In general, extracts inhibited plants more than endophytic or phytopathogens fungi. G. mangifera was the only organism that was significantly stimulated by both extracts regardless of concentration. Compounds in both organic extracts were identified by gas chromatography/mass spectrometry. We discuss the possible allelopathic role that metabolites of M. yucatanensis play in its ecological interactions with its host plant and other organisms.

Key Words

Allelopathy Bursera simaruba Endophytic fungi Muscodor yucatanensis Phytopathogenic fungi Phytopathogenic fungoids 

Notes

Acknowledgements

This work was supported by grants IN230107 DGAPA-UNAM and CONACyT 81017. We thank Dr. Arturo Gómez-Pompa for support to work in El Eden Ecological Reserve, and to Biol. Juan Castillo for help in the field work. We also thank to Dra. Olga Gómez from Instituto de Fitosanidad, Colegio de Postgraduados, Montecillo, Estado de México for the donation of plant-pathogenic microorganisms used in the bioassays; and Biol. Carmen Loyola for valuable help with photos of results on phytoinhibitory activity of VOCs from Muscodor yucatanensis, and María Teresa Caudillo from Instituto de Ecología, UNAM for support with the bioassays.

References

  1. Arnold, A. E., Maynard, Z., and Gilbert, G. S. 2001. Fungal endophytes in dicotyledonous neotropical trees: Patterns of abundance and diversity. Mycol. Res. 105:1502–1507.CrossRefGoogle Scholar
  2. Arnold, A. E., Mejia L. C., Kyllo, D., Rojas, E. I., Maynard, Z., Robbins, N., and Herre, E. A. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc. Nat. Acad. Sci. USA. 100:15649–15654.CrossRefPubMedGoogle Scholar
  3. Atmosukarto, I., Castillo, U., Hess, W. M., Sears, J., and Strobel, G. A. 2005. Isolation and characterization of Muscodor albus I-41.3s, a volatile antibiotic producing fungus. Plant Sci. 169:854–861.CrossRefGoogle Scholar
  4. Daisy, B., Strobel, G, Ezra, D., Castillo, U., Baird, G., and Hess, W. M. 2002a. Muscodor vitigenus sp.nov. an endophyte from Paullinia paullinoides. Mycotaxon 84:39–50.Google Scholar
  5. Daisy, B., Strobel, G., Ezra, D., Castillo, U., Ezra, D., Sears, J., Weaver, D., and Runyon, J. 2002b. Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741.PubMedGoogle Scholar
  6. Espinosa-garcía, F. J., Saldívar-garcía, P., and Langenheim, J. 1993. Dose-dependent effects in vitro of essential oils on the growth of two endophytic fungi in coastal redwood leaves. Biochem. Syst. Ecol. 21:185–194.CrossRefGoogle Scholar
  7. Ezra, D., Hess, W. M., and Strobel, G. A. 2004a. New endophytic isolates of Muscodor albus, a volatile antibiotic producing fungus. Microbiology 150:4023–4031.CrossRefPubMedGoogle Scholar
  8. Ezra, D., Jasper, J., Rogers, T., Knighton, B., Grimsrud, E., and Strobel, G.A. 2004b. Proton transfer reaction-mass spectrometry as a technique to measure volatile emissions of M. albus. Plant Sci. 166:1471–1477.CrossRefGoogle Scholar
  9. Gilbert, G. S., and Strong, D. R. 2007. Fungal symbionts of tropical trees. Ecology 88:539–540.CrossRefGoogle Scholar
  10. González, M. C., Anaya, A. L., Glenn, A. E., Saucedo-garcía, A., Macías-rubalcava, M. L., and Hanlin, R. T. 2007. A new endophytic ascomycete from El Eden Ecological Reserve, Quintana Roo, Mexico. Mycotaxon 101:251–260.Google Scholar
  11. González, M. C., Anaya, A. L., Glenn, A. E., Macías-rubalcava, M. L., Hernández-bautista, B. E., and Hanlin, R. T. 2009. Muscodor yucatanensis, a new endophytic ascomycete from Mexican chakah, Bursera simaruba. Mycotaxon 110:363–372.Google Scholar
  12. Herre, E. A., Mejía, L. C., Kyllo, D. A., Rojas, E., Maynard, Z., Butler, A., and Van Bael. S. A. 2007. Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88:550–558.CrossRefPubMedGoogle Scholar
  13. Macías-rubalcava, M. L., Hernández-bautista, B. E., Jiménez-estrada, M., Hernández-ortega, S., Saucedo-garcía, A., Muria-gonzález, M. J., González-villaseñor, M. C., Glenn, A. E., Hanlin, R. T., and Anaya, A. L. 2008. Naphthoquinone spiroketal with allelochemical activity from the newly discoverd endophytic fungus Edenia gomezpompae. Phytochemistry 69:1185–1196.CrossRefPubMedGoogle Scholar
  14. Mead, R., Curnow, R. N., and Hasted, A. M. (eds.). 2002. Statistical Methods In Agriculture And Experimental Biology. 3rd Ed. Chapman and Hall. CRC Press, Boca Raton, FL.Google Scholar
  15. Mitchell, A. M., Strobel, G. A., Hess, W. M., Vargas, P. N., and Ezra, D. 2008. Muscodor crispans, a novel endophyte from Ananas ananassoides in the Bolivian Amazon. Fungal Divers. 31:37–43.Google Scholar
  16. Rodrigues, K. F., Sieber, T. N., Grünig, C. R., and Holdenrieder, O. 2004. Characterization of Guignardia mangiferae isolated from tropical plants based on morphology, ISSR-PCR amplifications and ITS1-5.8S-ITS2 sequences. Mycol. Res. 108:45–52.CrossRefPubMedGoogle Scholar
  17. Rodríguez, R. J., White, Jr. J. F. Arnold, A. E., and Redman, R. S. 2009. Fungal endophytes: Diversity and functional roles. Tansley Review. New Phytol. 182:314–330.CrossRefGoogle Scholar
  18. Saikkonen, K., Faeth, S. H., Helander, M., and Sullivan, T .J. 1998. Fungal endophytes: A continuum of interactions with host plants. Annu. Rev. Eco. System. 29: 319–343.CrossRefGoogle Scholar
  19. Schulz, B., and Boyle, C. 2005. The endophytic continuum. Rev. Mycol. Res. 109:661–686.CrossRefGoogle Scholar
  20. Schulz, B., Boyle, C., Draeger, S., Römmert, A. K., and Krohn, K. 2002. Endophytic fungi: A source of novel biologically active secondary metabolites. Mycol. Res. 106:996–1004.CrossRefGoogle Scholar
  21. Sopalun, K., Strobel, G. A., Hess, W. M., and Worapong, J. 2003. A record of Muscodor albus, an endophyte from Myristica fragrans in Thailand. Mycotaxon 88:239–248.Google Scholar
  22. STROBEL, G. A. 2006. Muscodor albus and its biological promise. J. Ind. Microbiol. Biotechnol. 33:514–522CrossRefPubMedGoogle Scholar
  23. Strobel, G. A., Dirske, E., Sears, J., and Markworth, C. 2001. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950.PubMedGoogle Scholar
  24. Strobel, G. A., Kluck, K., Hess, W. M., Sears, J., Ezra, D., and Vargas, P. N. 2007. Muscodor albus E-6, an endophyte of Guazuma ulmifolia making volatile antibiotics: Isolation, characterization and experimental establishment in the host plant. Microbiology 153:2613–2620.CrossRefPubMedGoogle Scholar
  25. Tan, R. X., and Zou, W. X. 2001. Endophytes: A rich source of functional metabolites. Nat. Prod. Rep. 18:448–459.CrossRefPubMedGoogle Scholar
  26. Worapong, J., Strobel, G. A., Ford, E., Li, J. Y., and Hess, W. M. 2001. Muscodor albus anam. gen. et sp. nov., an endophyte from Cinnamomum zeylanicum. Mycotaxon 79:67–79.Google Scholar
  27. Worapong, J., Strobel, G. A, Daisy, B., Castillo, U., Baird, G., and Hess, W. M. 2002. Muscodor roseus anna. nov. an endophyte from Grevillea pteridifolia. Mycotaxon 81:463–475.Google Scholar
  28. Yue, Q., Miller, C. J., White, J. F., and Richardson, M. D. 2000. Isolation and characterization of fungal inhibitors from Epicloë festucae. J. Agric. Food Chem. 48:4687–4692.CrossRefPubMedGoogle Scholar
  29. Zar, J. H. 2007. Biostatistical Analysis. 5th ed. Prentice Hall, Upper Saddle River, New Jersey.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Martha L. Macías-Rubalcava
    • 1
  • Blanca E. Hernández-Bautista
    • 1
  • Fabiola Oropeza
    • 1
  • Georgina Duarte
    • 2
  • María C. González
    • 3
  • Anthony E. Glenn
    • 4
  • Richard T. Hanlin
    • 5
  • Ana Luisa Anaya
    • 1
  1. 1.Instituto de Ecología, Departamento de Ecología FuncionalUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  2. 2.Facultad de Química, Unidad de Servicios de Apoyo a la Investigación. Laboratorio de Espectrometría de MasasUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  3. 3.Instituto de Biología. Departamento de Botánica. Laboratorio de MicromicetosUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  4. 4.USDA, ARS, Toxicology & Mycotoxin Research UnitRussell Research CenterAthensUSA
  5. 5.Museum of Natural History AnnexUniversity of GeorgiaBogartUSA

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