2013, Number 2
<< Back
TIP Rev Esp Cienc Quim Biol 2013; 16 (2)
Hongos endófitos: fuente potencial de metabolitos secundarios bioactivos con utilidad en agricultura y medicina
Sánchez-Fernández RE, Sánchez-Ortiz BL, Sandoval-Espinosa YKM, Ulloa-Benítez Á, Armendáriz-Guillén B, García-Méndez MC, Macías-Rubalcava ML
Language: Spanish
References: 99
Page: 132-146
PDF size: 710.07 Kb.
ABSTRACT
Endophytic fungi are microorganisms that live inside plant tissues without causing disease symptoms. In
most cases, their relationship with the host plant is considered beneficial because the endophyte is able
to produce bioactive metabolites that the host can use as defense mechanisms, and this allows survival
of both organisms. Recent studies have demonstrated that the endophytic fungus confers protection to
the host plant against attack by pathogens and herbivores. Since they have the ability to benefit the host
plant, it is reasonable to think that the diverse bioactive compounds produced by the endophyte might
exhibit potential applications in agriculture and medicine, and also serve as a source of inspiration for the
discovery of new and more active molecules. In this paper, some aspects regarding endophytic fungi are
described: definition, discovery, classification, interactions with their host plants, ecological role, selected
examples of bioactive metabolites, host selection strategy, and methodological strategies for their isolation.
Finally, we show some recent results of our research, which demonstrate that endophytic fungi are promising
sources of new bioactive secondary metabolites.
REFERENCES
Wilson, D. Endophyte the evolution of a term and clarification of its use and definition. Oikos 73, 274-276 (1995).
Rodríguez, R., White, J., Arnold, A.E. & Redman, R. Fungal endophytes: Diversity and ecological roles. New. Phytol. 182, 314-330 (2009).
Schulz, B. & Boyle, C. The endophytic continuum. Mycol. Res. 109, 661-686 (2005).
Strobel, G., Daisy, B., Castillo, U. & Harper, J. Natural products from endophytic microrganisms. J. Nat. Prod. 67, 257-268 (2004).
Tan, R.X. & Zou, W.X. Endophytes: A rich source of functional metabolites. Nat. Prod. Rep. 18, 448-459 (2001).
Kusari, S., Hertweck, C. & Spiteller, M. Chemical ecology of endophytic fungi: Origins of secondary metabolites. Chem. & Biol. 19, 792-798 (2012).
Mittermeier, R.A., Meyers, N. Robles-Gil, P. & Mittermeier, C.G. in Hotspots: Earth’s biologically richest and most endangered ecoregions (ed. CEMEX, México, 1999).
Arnold, E. Understanding the diversity of foliar endophytic fungi: Progress, challenges, and frontiers. Fungal Biol. Rev. 21, 51-66 (2007).
de Bary, A. in Morphologie und physiologie der pilze, flechten, und myxomyceten. Hofmeister’s handbook of physiological botany (Leipzig, Germany, Engelmann, 1866).
Guerin, M.P. Structure particuliere du fruit de quelques graminees. Bot. 12, 365-374 (1898).
Funk, C.R., Halisky, P.M., Ahmad, S. & Hurley, R.H. in How endophytes modify turfgrass performance and response to insect pests in turfgrass breeding and evaluation trials (ed. Lemaire, E.) 137-145 (Avignon, France 1985).
Clay, K. Fungal endophytes of grasses: A defensive mutualism between plants and fungi. Ecology 69, 10-16 (1988).
Rosa, L.H. et al. in Drug Development. A case study based insight into modern strategies (ed. Rundfeldt, C.) 1-18 (Intech, Croatia, 2011).
Herre, E.A. et al. Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88, 550-558 (2007).
Arnold, A.E. et al. Fungal endophytes limit pathogen damage in a tropical tree. PNAS 100, 15649-15654 (2003).
Dreyfuss, M.M. & Chapela, I.H. in The discovery of natural products with therapeutic potential (ed. Gullo, V.P.) 49-80 (Butterworth-Heinemann, London, UK, 1994).
Gao, F.K., Dai, C.C. & Liu, X.Z. Mechanisms of fungal endophytes in plant protection against pathogens. Afr. J. Microbiol. Res. 4(13), 1346-1351 (2010).
Herre, E.A. et al. In Biotic interactions in the tropics: Their role in the maintenance of species diversity. (ed. Burslem, D.F.R.P., Pinard, M.A. & Hartey, S.E.) 226-227 (Cambridge University Press, Cambridge, UK, 2005).
Zhao, J. et al. in Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology 567-576 (ed. Méndez-Vilas, A., 2010).
González, M.C. et al. Muscodor yucatanensis, a new endophytic ascomycete from Mexican chakah, Bursera simaruba. Mycotaxon 110 (1), 363-372 (2009).
Macías-Rubalcava, M.L. et al. Allelochemical effects of volatile compounds and organic extracts from Muscodor yucatanensis, a tropical endophytic fungus from Bursera simaruba. J. Chem. Ecol. 36, 1122-1131 (2010).
Waller, F. et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS 102, 13386-13391 (2005).
Kageyama, S.A., Mandyam, K.G. & Jumpponen, A. in mycorrhiza: State of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. (ed. Varma, A.) 29-57 (Springer-Verlag, Berlin Heidelberg, 2008).
Bolwerk, A., Lagopodi, A.L., Lugtenberg, B.J.J. & Bloemberg, G.V. Visualization of interactions between a pathogenic and a beneficial Fusarium strain during biocontrol of tomato foot and root rot. Mol. Plant-Microbe Interact. 18, 710-721 (2005).
Macías-Rubalcava, M.L. et al. Naftoquinone spiroketal with allelochemical activity from the newly discovered endophytic fungus Edenia gomezpompae. Phytochem. 69, 1185-1196 (2008).
Body, L. Interspecific combative interactions between wooddecaying basidiomycetes. FEMS Microb. Ecol. 31(3), 185- 194 (2000).
Tuininga, A.R. in: The Fungal Community: It´s organization and role in the ecosystem (ed. Dighton, J., White, J. & Oudemans, J.) 265-283 (CRC Press, E.U., 2005).
Widden, P. in The Mycota IV: Environmental and microbial relationships. (ed. Wicklow, D. T. & Sönderström, B.) 135- 147 (Springer-Verlang, Alemania, 1997).
Rotheray, T.D., Chancellor, M., Jones, T.H. & Boddy, L. Grazing by collembola affects the outcome of interspecific mycelial interactions of cord-forming basidiomycetes. Fungal Ecol. 4(1), 42-55 (2011).
Hynes, J., Müller, C.T., Jones, T.H. & Boddy, L. Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J. Chem. Ecol. 33, 43-57 (2007).
Yuen, T.K., Hyde, K.D. & Hodgkiss, I.J. Interspecific interactions among tropical and subtropical freshwater fungi. Microb. Ecol. 37, 257-262 (1999).
Shearer, C.A. Fungal competition. Can. J. of Bot. 73 (S1), 1259- 1264 (1995).
Wani, M., Taylor, H., Wall, M., Coggon, P. & McPhail, A. Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J. Am. Chem. Soc. 93(9), 2325-2327 (1971).
Gunatilaka, A.A.L. Natural Products from Plant-Associated Microorganisms: Distribution, Structural Diversity, Bioactivity, and Implications of Their Occurrence. J. Nat. Prod. 69, 509-526 (2006).
Nicolaou, K.C. Total synthesis of taxol. Nature 367, 630-634 (1994).
Stierle, A., Strobel, G.A. & Stierle, D. Taxol and taxane production by Taxomyces andreanae. Science 260, 214-216 (1993).
Strobel, G.A., Stierñe, A., Stierle, D. & Hess, W.M. Taxomyces andreanae, a proposed new taxon for a bulbillifeour hyphomycete associated with pacific yew. Mycotaxon 47, 71-78(1993).
Stribel, G. et al. Taxolfrom Pestalotiopsis microspore, an endophytic fungus of Taxus wallachiana. Microbiol. 142, 435-440(1996).
Li, J.Y. et al. Endophytic taxol producing fungi from bald cypress Taxodium distichum. Microbiology 142, 2223-2226 (1996).
Kim, S.U., Strobel, G.A. & Ford, E. Screening of taxol-producing endophytic fungi from Ginkgo biloba and Taxus cuspidata in Korea. Agr. Chem. Biotechnol. 42, 97-99 (1999).
Sun, D.F., Ran, X.Q. & Wang, J.F. Isolation and identification of Taxol producing endophytic fungus from Podocarpus. Acta Microbiol. 48, 589-595(2008).
Liu, L., Liu, S., Chen, X., Guo, L. & Che, Y. Pestalofones A-E, bioactive cyclohexanone derivatives from the plant endophytic fungus Pestalotiopsis fici. Bioorg. Med. Chem. 17(2), 606-613 (2009).
Schwarz, M. et al. 3-Hydroxypropionic acid as a nematicidal principle endophytic fungi. Phytochem. 65, 2239-2245 (2004).
Medeiros, L.S. et al. Evaluation of herbicidal potential of depsides from Cladosporium uredinicola, an endophytic fungus found in Guava fruit. J. Braz. Chem. Soc. 23(8), 1551-1557 (2012).
González, M.C. et al. A new endophytic ascomycete from El Eden Ecological Reserve, Quintana Roo, Mexico. Mycotaxon. 101, 251-260 (2007).
Meléndez González, C. Potencial aleloquímico del endófito Edenia gomezpompae sobre diferentes comunidades de hongos endófitos de plantas tropicales. Tesis de Licenciatura (Universidad Nacional Autónoma de México, México, D.F. 2008) 113 págs.
Siegel, D.A. et al. M eridional v ariations o f s pringtime phytoplankton community in the Sargasso Sea. J. Mar. Res. 48, 379-412 (1990).
Yates, S.G., Fenster, J.C. & Bartelt, R.J. Assay Of tall Fescue seed extracts, fractions and alkaloids using the large milkweed bug. J. Agric. Food Chem. 37, 354-357 (1989).
Patterson, C.G., Potter, D.A. & Fannin, F.F. Feeding deterrency of alkaloids from endophyte- infected grasses to Japanese beetle grubs. Entomol. Exp. Appl. 61, 285-289 (1991).
Riedell, W.E., Kieckhefer, R.E., Petroski, R.J. & Powell, R.G. Naturally occurring and synthetic loline alkaloid derivatives: Insect feeding behavior modification and toxicity. J. Entomol. Sci. 26(1), 122-129 (1991).
Hovey, M.T., Eklund, E.J., Pike, R.D., Mainkar, A.A. & Scheerer, J.R. Synthesis of (+)-acetylnorloline via stereoselective tethered aminohydroxylation. Org. Lett. 13(5), 1246-1249 (2011).
Zhao, J. et al. Antimicrobial metabolites from the endophytic fungus Gliomastix murorum Ppf8 associated with the medicinal plant Paris polyphylla var. yunnanensis. Journal of Medicinal Plants Research 6(11), 2100-2104 (2012).
Rukachaisirikul, V., Sommart, U., Phongpaichit, S., Sakayaroj, J. & Kirtikara, K. Metabolites from the endophytic fungus Phomopsis sp. PSU-D15. Phytochem. 69(3), 783-787 (2008).
Cole, R.J. et al. Mycotoxins produced by Aspergillus fumigatus species isolated from molded silage. J. Agric. Food Chem. 25, 826-830 (1977).
Pinheiro, E.A. et al. Antibacterial activity of alkaloids produced by endophytic fungus Aspergillus sp. EJC08 isolated from medical plant Bauhinia guianensis. Nat. Prod. Res. (2012). In press DOI: 10.1080/14786419.2012.750316.
Debbab, A. et al. Bioactive secondary metabolites from the endophytic fungus Chaetomium sp. Isolated from Salvia officinalis growing in Morocco. Biotechnol. Agron. Soc. Environ. 13(2), 229-234 (2009).
Imlach, W.L., Finch, S.C., Dunlop, J. & Dalziel, J.E. Structural determinants of lolitrems for inhibition of BK large conductance Ca2+-activated K+ channels. Eur. J. Pharmacol. 605(1-3), 36-45 (2009).
Xu, S. et al. Cytotoxic Cytochalasin Metabolites of Endophytic Endothia gyrosa. Chem. Biodivers. 6(5), 739-745 (2009).
Ortega, H.E. et al. Mycoleptodiscins A and B, Cytotoxic Alkaloids from the Endophytic Fungus Mycoleptodiscus sp. F0194. J. Nat. Prod. (2013). In press DOI: 10.1021/np300792t.
Ferreira Koolen, H.H. et al. An antimicrobial alkaloid and other metabolites produced by Penicillium sp. an endophytic fungus isolated from Mauritia flexuosa L.f. Quím. Nova. 35(4), 771-774 (2012).
Shen, L. et al. Structure and Total Synthesis of Aspernigerin: A Novel Cytotoxic Endophyte Metabolite. Chem. Eur. J. 12(16), 4393-4396 (2006).
Zhang, H., Ma, Y., Liu, R. & Zhou, F. Endophytic fungus Aspergillus tamarii from Ficus carica L., a new source of indolyl diketopiperazines. Biochem. Sys. Ecol. 45, 31-33 (2012).
Isaka, M., Berkaew, P., Intereya, K., Komwijit, S. & Sathitkunanon, T. Antiplasmodial and antiviral cyclohexadepsipeptides from the endophytic fungus Pullularia sp. Tetrahedron 63(29), 6855-6860 (2007).
Shiono, Y. et al. A dimeric pyrrocidine from Neonectria ramulariae is a n inhibitor of prolyl oligopeptidase. Phytochem. Lett. 5(1), 91-95(2012).
Song, Y.C., Huang, W.Y., Sun, C., Wang, F.W. & Tan, R.X. 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(3), 506-509 (2005).
Bultman, T.L. & Leuchtmann, A. Biology of the Epichloë- Botanophila interaction: An intriguing association between fungi and insects. Fungal Biol. Rev. 22 (3-4), 131-138 (2008).
Hughes, C.C., Kennedy-Smith, J.J. & Trauner, D. Synthetic Studies toward the Guanacastepenes. Org. Lett. 5(22), 4113-4115 (2003).
Qin, J.C. et al. Bioactive metabolites produced by Chaetomium globosum, an endophytic fungus isolated from Ginkgo biloba. Bioorg. Med. Chem. Lett. 19(6), 1572-1574 (2009).
Sumarah, M.W. et al. Secondary metabolites from anti-insect extracts of endophytic fungi isolated from Picea rubens. Phytochemistry 71, 760–765 (2010).
Liu, L. et al. Chloropupukeananin, the First Chlorinated Pupukeanane Derivative, and Its Precursors from Pestalotiopsis fici. Org. Lett. 10 (7), 1397–1400 (2008).
Basilio, A. et al. The discovery of moriniafungin, a novel sordarin derivative produced by Morinia pestalozzioides. Bioorg. Med. Chem. 14(2), 560-566 (2006).
Elsaesser, B. et al. X-ray structure determination, absolute conguration and biological activity of phomoxanthone A. Eur. J. Org. Chem. 21, 4563-4570 (2005).
Strobel, G. & Daisy, B. Bioprospecting for Microbial Endophytes and Their Natural Products. Microbiol. Mol. Biol. Rev. 67(4), 491-502 (2003).
Yu, H. et al. Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microb. Res. 165, 437-449(2010).
Gamboa, M.A., Laureano, S. & Bayman, P. Measuring diversity of endophytic fungi in leaf fragments: Does size matter? Mycopathol. 156, 41–45 (2002).
Rodríguez, K.F. The foliar fungal endophytes of the Amazonian palm Euterpe Oleracea. Mycol. 86,376-385(1994).
Ko Ko, T.W., Stephenson, S.L., Bahkali, A.H. & Hyde, K.D. From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers. 50, 113-120 (2011).
Montesinos, E. et al. Plant-microbe interactions and the new biotechnological methods of plant disease control. Int. Microbiol. 5, 169-175 (2010).
Mejía, L.C. et al. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biolog. Cont. 46, 4-14 (2008).
Waqas, M. et al. Endophytic Fungi Produce Gibberellins and Indoleacetic Acid and Promotes Host-Plant Growth during Stress. Molecules 17, 10754-10773 (2012).
Rubini, M.R. et al. Diversity of endophytic fungal community of cacao (Theobroma cacao L .) a nd b iological c ontrol of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. Int. J. Biol. Sci. 1, 24-33 (2005).
Bhagobaty, R.K. & Joshi, S.R. Promotion of seed germination of Green gram and Chick pea by Penicillium verruculosum RS7PF, a root endophytic fungus of Potentilla fulgens L. Adv. Biotech. 8(12), 7-15 (2009).
Neilan, B.A., Pomatia, F., Nettinga, A.G. & Calamarib, D. Effects of erythromycin, tetracycline and ibuprofen on the growth of Synechocystis sp. and Lemna minor. Aquat. Toxicol. 67(4), 387-396 (2004).
Mann, R.S & Kaufman, P.E. Natural Product Pesticides: Their Development, Delivery and use against Insect Vectors. Rev. in Org. Chem. 9, 185-202 (2012).
Homan, A.M. et al. Purication, identication and activity of phomodione, a furandione from an endophytic Phoma species. Phytochem. 69, 1049-1056 (2008).
Rhoden, S.A., García, A., Bongiorno, V.A., Azevedo, J.L. & Pamphile, J.A. Antimicrobial Activity of Crude Extracts of Endophytic Fungi Isolated from Medicinal Plant Trichilia elegans a. Juss. JAPS 2(8), 57-59 (2012).
Rosa, L.H. et al. Antifungal activity of extracts from endophytic fungi associated with Smallanthus maintained in vitro as autotrophic cultures and as pot plants in the greenhouse. Can. J. Microbiol. 58, 1202–1211 (2012).
Zhu, J.W. et al. Elucidation of Strict Structural Requirements of Brefeldin A as an inducer of differentiations and apoptosis. Biorg. Med. Chem. 8, 455-463 (2000).
Weber, D. et al. Phomol, a new a ntiinflammatory metabolite from an endophyte of the medicinal plant Erythrina cristagalli. J. Antibiot. 57(9), 559-563 (2004).
Dompeipen, E.J., Srikandace, Y., Suharso, W.P., Cahyana, H. & Simanjuntak, P. Potential endophytic microbes selection for antidiabetic bioactive compounds production. Asian J. of Biochem. 6, 465-471 (2011).
Mata, R. et al. Antidiabetic properties of selected Mexican copalchis of the Rubiaceae family. Phytochem. 68(15), 2087-2095 (2007).
Schmeda-Hirschmann, G., Hormozabal, E., Astudillo, L., Rodríguez, J. & Theoduloz, C. Secondary metabolites from endophytic fungi isolated from the Chilean gymnosperm Prumnopitys andina (Lleuque). World J. Microbiol. Biotech. 21(1), 27-32 (2005).
Mayorga, P., Pérez, K. R., Cruz, S.M. & Cáceres, A. Comparison of bioassays using the anostracan crustaceans Artemia salina and Thamnocephalus platyurus f or p lant e xtract t oxicity screening. Braz. of Pharmacog. 20, 897-903 (2010).
Morettia, A., Muléa, G., Ritienib, A. & Logriecoa, A. Further data on the production of beauvericin, enniatins and fusaproliferin and toxicity to Artemia salina by Fusarium species of Gibberella fujikuroi species complex. Int. J. of Food Microbiol. 118(2), 158-163 (2007).
Guimaraes, D.O. et al. Biological activities from extracts of endophytic fungi isolated from Viguiera arenaria and Tithonia diversifolia. Immunol. Med. Microbiol. 52, 134- 144 (2008).
DiMasi, J.A., Hansen, R.W. & Grabowski, H.G. The price of innovation: new estimates of drug development costs. J. of Health Econ. 22, 151-185 (2003).
Baskin-Bey, E.S. et al. Clinical trial of the pan-caspase inhibitor, IDN-6556, in human liver preservation injury. Am. J. of Trans. 7, 218-225 (2007).
Sánchez Fernández, R.E. Determinación del potencial alelopático de los extractos del medio de cultivo y del micelio de un hongo endófito aislado de Lonchocarpus castilloi (Fabaceae). Tesis de Licenciatura (Universidad Nacional Autónoma de México, México, D.F., 2010) 87 págs.
Armendáriz Guillén, B. Hongos endófitos productores de metabolitos secundarios con potencial fitotóxico y antifúngico. Tesis de Licenciatura (Universidad Nacional Autónoma de México, México, D.F., 2013) 106 págs.
Full text