The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective

Frontiers in Microbiology

Volumn 4, Issue , 2013, Pages

  Mousa, Walaa Kamel ^a,b   Raizada, Manish N ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MANSOURA UNIVERSITY   (Egypt)

Author keywords

Anti microbial; Antifungal; Mycology; Natural products; Pathogen

Indexed keywords

EID: 85126712585     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00065     Document Type: Review

References (123)

1. Aly, A., Debbab, A., Kjer, J., and Proksch, P. (2010). Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers. 41, 1–16.
2. Aly, A. H., Edrada-Ebel, R., Wray, V., Müller, W. E. G., Kozytska, S., Hentschel, U., et al. (2008). Bioac-tive metabolites from the endo-phytic fungus Ampelomyces sp. isolated from the medicinal plant Uros-permum picroides. Phytochemestry 69, 1716–1725.
3. Beagle-Ristaino, J. E., and Papavizas, G. C. (1985). Biological control of Rhizoctonia stem canker and black scurf of potato. Phytopathology 75, 560–564.
4. Betina, V. (1992). Biological effects of the antibiotic brefeldin A (decumbin, cyanein, ascotoxin, synergisidin): a retrospective. Folia Microbiol (Praha). 37, 3–11.
5. Binder, M., and Tamm, C. (1973). The cytochalasans: a new class of biologically active microbial metabo-lites. Angew. Chem. Int. Ed. Engl. 12, 370–380.
6. Blankenship, J. D., Spiering, M. J., Wilkinson, H. H., Fannin, F. F., Bush, L. P., and Schardl, C. L. (2001). Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media. Phytochemistry 58, 395–401.
7. Bok, J. W., Balajee, S. A., Marr, K. A., Andes, D., Nielsen, K. F., Frisvad, J. C., et al. (2005). LaeA, a regulator of morphogenetic fungal virulence fac-tors. Eukaryotic Cell 4, 1574–1582.
8. Boutsika, K., Phillips, M. S., MacFar-lane, S. A., Brown, D. J. F., Holeva, R. C., and Blok, V. C. (2004). Molecular diagnostics of some tri-chodorid nematodes and associated tobacco rattle virus. Plant Pathol. 53, 110–116.
9. Brady, S. F., and Clardy, J. (2000). CR377, a new pentaketide antifungal agent isolated from an endophytic fungus. J. Nat. Prod. 63, 1447–1448.
10. Calhoun, L. A., Findlay, J. A., David Miller, J., and Whitney, N. J. (1992). Metabolites toxic to spruce bud-worm from balsam fir needle endo-phytes. Mycol. Res. 96, 281–286.
11. Canel, C., Moraes, R. M., Dayan, F. E., and Ferreira, D. (2000). Podophyllo-toxin. Phytochemistry 54, 115–120.
12. Capasso, R., Iacobellis, N. S., Bottal-ico, A., and Randazzo, G. (1984). Structure-toxicity relationships of the eremophilane phomenone and PR-toxin. Phytochemistry 23, 2781–2784.
13. Carter, C. J., Cannon, M., and Smith, K. E. (1976). Inhibition of protein synthesis in reticulocyte lysates by trichodermin. Biochem. J. 154, 171–178.
14. Chang, W.-Y., Lantz, V. A., Hennigar, C. R., and Maclean, D. A. (2012). Benefit-cost analysis of spruce bud-worm (Choristoneura fumiferana Clem.) control: incorporating market and non-market values. J. Envi-ron. Manage. 93, 104–112.
15. Chapman, S. W., Sullivan, D. C., and Cleary, J. D. (2008). In search of the Holy Grail of antifungal therapy. Trans. Am. Clin. Climatol. Assoc. 119, 197–216.
16. Che, Y., Gloer, J. B., and Wicklow, D. T. (2002). Phomadecalins A-D and phomapentenone A: new bioac-tive metabolites from Phoma sp. NRRL 25697, a fungal colonist of Hypoxylon stromata. J. Nat. Prod. 65, 399–402.
17. Chen, L., Chen, J., Zheng, X., Zhang, J., and Yu, X. (2007). Identification and antifungal activity of the metabolite of endophytic fungi isolated from llex cornuta. Nongyaoxue Xuebao 9, 143–150.
18. Chu, F. S. (1977). Mode of action of mycotoxins and related compounds. Adv. Appl. Microbiol. 22, 83–143.
19. Compant, S., Duffy, B., Nowak, J., Clé-ment, C., and Barka, E. A. (2005). Use of plant growth-promoting bac-teria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71, 4951–4959.
20. Cota, B. B., Rosa, L. H., Caligiorne, R. B., Rabello, A. L. T., Almeida Alves, T. M., Rosa, C. A., et al. (2008). Altenusin, a biphenyl isolated from the endophytic fungus Alternaria sp., inhibits trypanoth-ione reductase from Trypanosoma cruzi. FEMS Microbiol. Lett. 285, 177–182.
21. Cutler, H. G., and LeFiles, J. H. (1978). Trichodermin: effects on plants. Plant Cell Physiol. 19, 177–182.
22. Dai, J., Krohn, K., Draeger, S., and Schulz, B. (2009). New naphthalene-chroman coupling products from the endophytic fungus, Nodulispo-rium sp. from Erica arborea. European J. Org. Chem. 2009, 1564–1569.
23. Dai, J., Krohn, K., Flörke, U., Draeger, S., Schulz, B., Kiss-Szikszai, A., et al. (2006). Metabolites from the endophytic fungus Nodulispo-rium sp. from Juniperus cedre. European J. Org. Chem. 2006, 3498–3506.
24. de Boer, A. H., and Leeuwen, I. J. (2012). Fusicoccanes: diterpenes with sur-prising biological functions. Trends Plant Sci. 17, 360–368.
25. Dettrakul, S., Kittakoop, P., Isaka, M., Nopichai, S., Suyarnsestakorn, C., Tanticharoen, M., et al. (2003). Antimycobacterial pimarane diter-penes from the fungus Diaporthe sp. Bioorg. Med. Chem. Lett. 13, 1253–1255.
26. Djoukeng, J., Polli, S., Larignon, P., and Abou-Mansour, E. (2009). Identification of phytotoxins from Botryosphaeria obtusa, a pathogen of black dead arm disease of grapevine. Eur. J. Plant Pathol. 124, 303–308.
27. Eisenreich, W., Menhard, B., Hylands, P. J., Zenk, M. H., and Bacher, A. (1996). Studies on the biosyn-thesis of taxol: the taxane carbon skeleton is not of mevalonoid ori-gin. Proc. Natl. Acad. Sci. U.S.A. 93, 6431–6436.
28. Eyberger, A. L., Dondapati, R., and Porter, J. R. (2006). Endophyte fungal isolates from Podophyllum pelta-tum produce podophyllotoxin. J. Nat. Prod. 69, 1121–1124.
29. Faeth, S. H., Bush, L. P., and Sullivan, T. J. (2002). Peramine alkaloid variation in Neotyphodium-infected Arizona fescue: effects of endophyte and host genotype and environment. J. Chem. Ecol. 28, 1511–1526.
30. Findlay, J. A., Buthelezi, S., Li, G., Seveck, M., and Miller, J. D. (1997). Insect toxins from an endophytic fungus from Wintergreen. J. Nat. Prod. 60, 1214–1215.
31. Gao, R., Gao, C., Tian, X., Yu, X., Di, X., Xiao, H., et al. (2004). Insecti-cidal activity of deoxypodophyllo-toxin, isolated from Juniperus sabina L, and related lignans against larvae of Oieris rapae L. Pest Manag. Sci. 60, 1131–1136.
32. Gao, S. S., Li, X. M., Li, C. S., Proksch, P., and Wang, B. G. (2011). Peni-cisteroids A and B, antifungal and cytotoxic polyoxygenated steroids from the marine alga-derived endo-phytic fungus Penicillium chryso-genum QEN-24S. Biorg. Med. Chem. Lett. 21, 2894–2897.
33. Gelderblom, W. C. A., Kriek, N. P. J., Marasas, W. F. O., and Thiel, P. G. (1991). Toxicity and carcino-genicity of the Fusarium moniliforme metabolite, Fumonisin B1, in rats. Carcinogenesis 12, 1247–1251.
34. Guo, B., Dai, J. R., Ng, S., Huang, Y., Leong, C., Ong, W., et al. (2000). Cytonic acids A and B: novel tridep-side inhibitors of hCMV protease from the endophytic fungus Cyton-aema sp. J. Nat. Prod. 63, 602–604.
35. Haraguchi, H., Abo, T., Hashimoto, K., and Yagi, A. (1992). Action-mode of antimicrobial altersolanol A in Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem. 56, 3498–3506.
36. Harri, E., Loeffler, W., Sigg, H. P., Stae-helin, S., and Tamm, C. (1963). Uber die isolierung der stoffwech-selprodukte aus Penicellium brefel-dianum Dodge. Helv. Chim. Acta 46, 1235–1244.
37. Hatakeyama, T., Koseki, T., Murayama, T., and Shiono, Y. (2010). Eremophi-lane sesquiterpenes from the endo-phyte Microdiplodia sp. KS 75-1 and revision of the stereochemistries of phomadecalins C and D. Phytochem. Lett. 3, 148–151.
38. Heinstein, P. F., Lee, S. I., and Floss, H. G. (1971). Isolation of dimethylallylpy-rophosphate: tryptophan dimethy-lallyl transferase from the ergot fungus (Claviceps sp.). Biochem. Bio-phys. Res. Comm. 44, 1244–1251.
39. Hezari, M., Lewis, N. G., and Croteau, R. (1995). Purification and char-acterization of taxa-4(5),11(12)-diene synthase from Pacific yew (Taxus brevifolia) that catalyzes the first committed step of taxol biosynthesis. Arch. Biochem. Bio-phys. 322, 437–444.
40. Hiroyuki, K., Teruhiko, Y., Michi, O., Sadao, S., Akitoshi, T., and Tadayuki, S. (1992). Gamahonolides A, B, and gamahorin, novel antifungal compounds from stromata of Epichloe typhina on Phleum pratense. Biosci. Biotechnol. Biochem. 56, 1096–1099.
41. Horn, W. S., Simmonds, M. S. J., Schwartz, R. E., and Blaney, W. M. (1995). Phomopsichalasin, a novel antimicrobial agent from an endo-phytic Phomopsis sp. Tetrahedron 51, 3969–3978.
42. Horwitz, S. B. (1994). Taxol (paclitaxel): mechanisms of action. Ann. Oncol. 5(Suppl 6), S3–S6.
43. Hussain, H., Akhtar, N., Draeger, S., Schulz, B., Pescitelli, G., Sal-vadori, P., et al. (2009). New bioac-tive 2,3-epoxycyclohexenes and iso-coumarins from the endophytic fungus Phomopsis sp. from Laurus azor-ica. European J. Org. Chem. 2009, 749–756.
44. Isaka, M., Chinthanom, P., Boonruang-prapa, T., Rungjindamai, N., and Pinruan, U. (2010). Eremophilane-type sesquiterpenes from the fungus Xylaria sp. BCC 21097. J. Nat. Prod. 73, 683–687.
45. Johann, S., Rosa, L. H., Rosa, C. A., Perez, P., Cisalpino, P. S., Zani, C. L., et al. (2012). Antifungal activity of altenusin isolated from the endophytic fungus Alternaria sp. Against the pathogenic fungus Paracoccidioides brasiliensis. Rev. Iberoam. Micol. 29, 205–209.
46. Johnston-Monje, D., and Raizada, M. N. (2011a). “Integration of biotech-nologies – plant and endophyte rela-tionships: nutrient management,” in Comprehensive Biotechnology, 2nd Edn, Vol. 4, ed. M. Moo-Young (Toronto: Elsevier), 713–726.
47. Johnston-Monje, D., and Raizada, M. N. (2011b). Conservation and diversity of seed associated endophytes in across boundaries of evolution, ethnography and ecology. PLoS ONE 6:e20396. doi:10.1371/journal.pone.0020396
48. Ju, Y., Sacalis, J. N., and Still, C. C. (1998). Bioactive flavonoids from endophyte-infected blue grass (Poa ampla). J. Agric. Food Chem. 46, 3785–3788.
49. Justice, M. C., Hsu, M. J., Tse, B., Ku, T., Balkovec, J., Schmatz, D., et al. (1998). Elongation factor 2 as a novel target for selective inhibition of fungal protein synthesis. J. Biol. Chem. 273, 3148–3151.
50. Kim, S., Shin, D. S., Lee, T., and Oh, K. B. (2004). Periconicins, two new fusic-occane diterpenes produced by an endophytic fungus Periconia sp. with antibacterial activity. J. Nat. Prod. 67, 448–450.
51. Kjer, J., Wray, V., Edrada-Ebel, R., Ebel, R., Pretsch, A., Lin, W., et al. (2009). Xanalteric acids I and II and related phenolic compounds from an endo-phytic Alternaria sp. Isolated from the mangrove plant Sonneratia alba. J. Nat. Prod. 72, 2053–2057.
52. Koshino, H., Terada, S. I., Yoshihara, T., Sakamura, S., Shimanuki, T., Sato, T., et al. (1988). Three phenolic acid derivatives from stromata of Epichloe typhina on Phleum pratense. Phytochemistry 27, 1333–1338.
53. Kour, A., Shawl, A., Rehman, S., Sul-tan, P., Qazi, P., Suden, P., et al. (2008). Isolation and identification of an endophytic strain of Fusarium oxysporum producing podophyllotoxin from Juniperus recurva. World J. Microbiol. Biotech-nol. 24, 1115–1121.
54. Kusari, S., Lamshöft, M., and Spiteller, M. (2009). Aspergillus fumigatus Fre-senius, an endophytic fungus from Juniperus communis L. Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. J. Appl. Microbiol. 107, 1019–1030.
55. Lazo, J. S., Tamura, K., Vogt, A., Jung, J. K., Rodriguez, S., Balachandran, R., et al. (2001). Antimitotic actions of a novel analog of the fungal metabolite palmarumycin CP1. J. Pharma-col. Exp. Ther. 296, 364–371.
56. Lehtonen, P., Helander, M., Wink, M., Sporer, F., and Saikkonen, K. (2005). Transfer of endophyte-origin defen-sive alkaloids from a grass to a hemiparasitic plant. Ecol. Lett. 8, 1256–1263.
57. Leyns, F., De Cleene, M., Swings, J. G., and De Ley, J. (1984). The host range of the genus Xanthomonas. Bot. Rev. 50, 308–356.
58. Li, E., Jiang, L., Guo, L., Zhang, H., and Che, Y. (2008a). Pestalachlorides A– C, antifungal metabolites from the plant endophytic fungus Pestalotiop-sis adusta. Bioorg. Med. Chem. 16, 7894–7899.
59. Li, E., Tian, R., Liu, S., Chen, X., Guo, L., and Che, Y. (2008b). Pestalotheols A-D, bioactive metabolites from the plant endophytic fungus Pestalotiop-sis theae. J. Nat. Prod. 71, 664–668.
60. Li, J. Y., Strobel, G., Harper, J., Lobkovsky, E., and Clardy, J. (2000). Cryptocin, a potent tetramic acid antimycotic from the endophytic fungus Cryptosporiopsis cf. quercina. Org. Lett. 2, 767–770.
61. Liu, L., Liu, S., Chen, X., Guo, L., and Che, Y. (2009). Pestalofones A–E, bioactive cyclohexanone derivatives from the plant endophytic fungus Pestalotiopsis fici. Bioorg. Med. Chem. 17, 606–613.
62. Lodeiro, S., Xiong, Q., Wilson, W. K., Ivanova, Y., Smith, M. L., May, G. S., et al. (2009). Protostadienol biosyn-thesis and metabolism in the pathogenic fungus Aspergillus fumigatus. Org. Lett. 11, 1241–1244.
63. Lösgen, S., Magull, J., Schulz, B., Draeger, S., and Zeeck, A. (2008). Isofusidienols: novel chromone-3-oxepines produced by the endo-phytic fungus Chalara sp. European J. Org. Chem. 2008, 698–703.
64. Lu, H., Zou, W. X., Meng, J. C., Hu, J., and Tan, R. X. (2000). New bioac-tive metabolites produced by Col-letotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci. 151, 67–73.
65. Martínez-Luis, S., Della-Togna, G., Coley, P. D., Kursar, T. A., Ger-wick, W. H., and Cubilla-Rios, L. (2008). Antileishmanial constituents of the Panamanian endophytic fungus Edenia sp. J. Nat. Prod. 71, 2011–2014.
66. Miller, J. D., MacKenzie, S., Foto, M., Adams, G. W., and Findlay, J. A. (2002). Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce bud-worm growth rate. Mycol. Res. 106, 471–479.
67. Misumi, Y., Miki, K., Takatsuki, A., Tamura, G., and Ikehara, Y. (1986). Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 261, 11398–11403.
68. Moore, J. H., Davis, N. D., and Diener, U. L. (1972). Mellein and 4-hydroxymellein production by Aspergillus ochraceus Wilhelm. Appl. Microbiol. 23, 1067–1072.
69. Moule, Y., Jemmali, M., and Rousseau, N. (1976). Mechanism of the inhibition of transcription by PR toxin, a mycotoxin from Penicillium roqueforti. Chem. Biol. Interact. 14, 207–216.
70. Muromtsev, G., Voblikova, V., Kobrina, N., Koreneva, V., Krasnopolskaya, L., and Sadovskaya, V. (1994). Occur-rence of fusicoccanes in plants and fungi. J. Plant Growth Regul. 13, 39–49.
71. Noble, H. M., Langley, D., Sidebot-tom, P. J., Lane, S. J., and Fisher, P. J. (1991). An echinocandin from an endophytic Cryptosporiopsis sp. and Pezicula sp. in Pinus sylvestris and Fagus sylvatica. Mycol. Res. 95, 1439–1440.
72. Okamura, N., Haraguchi, H., Hashimoto, K., and Yagi, A. (1993). Altersolanol-related antimicrobial compounds from a strain of Alternaria solani. Phytochemistry 34, 1005–1009.
73. Payne, G. A., and Widstrom, N. W. (1992). Aflatoxin in maize. Crit. Rev. Plant Sci. 10, 423–440.
74. Pendse, G. S., and Mujumdar, A. M. (1986). Recent Advances in Cytocha-lasans. London: Chapman and Hall.
75. Pimentel, D. (2009). “Pesticides and pest control,” in Integrated Pest Man-agement: Innovation-Development Process, eds R. Peshin and A. K. Dhawan (Dordrecht: Springer), 83–87.
76. Pongcharoen, W., Rukachaisirikul, V., Phongpaichit, S., Kühn, T., Pelz-ing, M., Sakayaroj, J., et al. (2008). Metabolites from the endophytic fungus Xylaria sp. PSU-D14. Phyto-chemistry 69, 1900–1902.
77. Pongcharoen, W., Rukachaisirikul, V., Phongpaichit, S., Rungjindamai, N., and Sakayaroj, J. (2006). Pimarane diterpene and cytochalasin derivatives from the endophytic fungus Eutypella scoparia PSU-D44. J. Nat. Prod. 69, 856–858.
78. Powell, R. G., and Petroski, R. J. (1992). Alkaloid toxins in endophyte-infected grasses. Nat. Toxins 1, 163–170.
79. Qiao, M. F., Ji, N. Y., Liu, X. H., Li, K., Zhu, Q. M., and Xue, Q. Z. (2010). Indoloditerpenes from an algicolous isolate of Aspergillus oryzae. Bioorg. Med. Chem. Lett. 20, 5677–5680.
80. Qin, J. C., Zhang, Y. M., Gao, J. M., Bai, M. S., Yang, S. X., Laatsch, H., et al. (2009). Bioactive metabolites produced by Chaetomium globosum, an endophytic fungus isolated from Ginkgo biloba. Bioorg. Med. Chem. Lett. 19, 1572–1574.
81. Robens, J., and Cardwell, K. (2003). The costs of mycotoxin management to the USA: management of aflatoxins in the United States. Toxin Rev. 22, 139–152.
82. Rowan, D. D. (1993). Lolitrems, peramine and paxilline – mycotox-ins of the ryegrass endophyte inter-action. Agric. Ecosyst. Environ. 44, 103–122.
83. Rukachaisirikul, V., Sommart, U., Phongpaichit, S., Sakayaroj, J., and Kirtikara, K. (2008). Metabolites from the endophytic fungus Pho-mopsis sp. PSU-D15. Phytochem. Lett. 69, 783–787.
84. Schardl, C. L. (2010). The epichloae, symbionts of the grass subfamily Poöideae. Ann. Mo. Bot. Gard. 97, 646–665.
85. Schulz, B., Sucker, J., Aust, H. J., Krohn, K., Ludewig, K., Jones, P. G., et al. (1995). Biologically active secondary metabolites of endophytic Pezicula species. Mycol. Res. 99, 1007–1015.
86. Serrano-Wu, M. H., St. Laurent, D. R., Mazzucco, C. E., Stickle, T. M., Bar-rett, J. F., Vyas, D. M., et al. (2002). Oxime derivatives of sordaricin as potent antifungal agents. Bioorg. Med. Chem. Lett. 12, 943–946.
87. Shin, D. S., Oh, M. N., Yang, H. C., and Oh, K. B. (2005). Biological charac-terization of periconicins, bioactive secondary metabolites, produced by Periconia sp. OBW-15. J. Microbiol. Biotechnol. 15, 216–219.
88. Shurtleff, M. C. A., and Averre, C. W. (2000). Diagnosing Plant Diseases Caused by Nematodes. Minneapolis: APS Press.
89. Silva, G. H., De Oliveira, C. M., Teles, H. L., Pauletti, P. M., Castro-Gamboa, I., Silva, D. H. S., et al. (2010). Sesquiterpenes from Xylaria sp., an endophytic fungus associated with Piper aduncum (Piperaceae). Phy-tochem. Lett. 3, 164–167.
90. Silva, G. H., Teles, H. L., Zanardi, L. M., Marx Young, M. C., Eberlin, M. N., Hadad, R., et al. (2006). Cadinane sesquiterpenoids of Pho-mopsis cassiae, an endophytic fungus associated with Cassia spectabilis (Leguminosae). Phytochemistry 67, 1964–1969.
91. Singh, M. P., Janso, J. E., Luckman, S. W., Brady, S. F., Clardy, J., Greenstein, M., et al. (2000). Biological activity of guanacastepene, a novel diterpenoid antibiotic produced by an uniden-tified fungus CR115. J. Antibiot. 53, 256–261.
92. Soliman, S. S. M., Tsao, R., and Raizada, M. N. (2011). Chemical inhibitors suggest endophytic fungal paclitaxel is derived from both mevalonate and non-mevalonate-like pathways. J. Nat. Prod. 74, 2497–2504.
93. Spiering, M. J., Moon, C. D., Wilkin-son, H. H., and Schardl, C. L. (2005). Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 169, 1403–1414.
94. Stähelin, H. F., and von Wartburg, A. (1991). The chemical and biological route from podophyllotoxin gluco-side to etoposide: ninth Cain memo-rial award lecture. Cancer Res. 51, 5–15.
95. Stierle, A., Strobel, G., and Stierle, D. (1993). Taxol and taxane production by Taxomyces andreanae, an endo-phytic fungus of Pacific yew. Science 260, 214–216.
96. Stierle, A., Strobel, G., Stierle, D., Grothaus, P., and Bignami, G. (1995). The search for a taxol-producing microorganism among the endophytic fungi of the Pacific yew, Taxus brevifolia. J. Nat. Prod. 58, 1315–1324.
97. Stone, J., Bacon, C. W., and White, J. F. (2000). “An overview of endophytic microbes: endophytism defined,” in Microbial Endophytes, eds C. W. Bacon and J. F. White (New York: Marcel Dekker), 3–29.
98. Strange, R. N., and Scott, P. R. (2005). Plant disease: a threat to global food security. Annu. Rev. Phytopathol. 43, 83–116.
99. Strobel, G., and Daisy, B. (2003). Bio-prospecting for microbial endo-phytes and their natural prod-ucts. Microbiol. Mol. Biol. Rev. 67, 491–502.
100. Strobel, G. A., Miller, R. V., Martinez-Miller, C., Condron, M. M., Teplow, D. B., and Hess, W. M. (1999). Cryp-tocandin, a potent antimycotic from the endophytic fungus Cryptospori-opsis cf. quercina. Microbiology 145, 1919–1926.
101. Strobel, G. A., Torczynski, R., and Bol-lon, A. (1997). Acremonium sp. – a leucinostatin A producing endo-phyte of European yew (Taxus bac-cata). Plant Sci. 128, 97–108.
102. Sudo, K., Konno, K., Shigeta, S., and Yokota, T. (1998). Inhibitory effects of podophyllotoxin derivatives on Herpes simplex virus repli-cation. Antivir. Chem. Chemother. 9, 263–267.
103. Sutton, J. C. (1982). Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can. J. Plant Pathol. 4, 195–209.
104. Thresh, J. M., and Cooter, R. J. (2005). Strategies for controlling Cassava Mosaic virus disease in Africa. Plant Pathol. 54, 587–614.
105. Tse, B., Balkovec, J. M., Blazey, C. M., Hsu, M. J., Nielsen, J., and Schmatz, D. (1998). Alkyl side-chain derivatives of sordaricin as potent antifun-gal agents against yeast. Bioorg. Med. Chem. Lett. 8, 2269–2272.
106. Tudzynski, P., Correia, T., and Keller, U. (2001). Biotechnology and genetics of ergot alkaloids. Appl. Microbiol. Biotechnol. 57, 593–605.
107. Ueno, Y., Sato, N., Ito, T., Ueno, I., Enomoto, M., and Tsunoda, H. (1980). Chronic toxicity and hepa-tocarcinogenicity of (+) rugulosin, an anthraquinoid mycotoxin from Penicillium species: preliminary sur-veys in mice. J. Toxicol. Sci. 5, 295–302.
108. Wallwey, C., and Li, S. (2011). Ergot alkaloids: structure diversity, biosyn-thetic gene clusters and functional proof of biosynthetic genes. Nat. Prod. Res. 28, 496–510.
109. Wang, F., Jiao, R., Cheng, A., Tan, S., and Song, Y. (2007). Antimicrobial potentials of endophytic fungi resid-ing in Quercus variabilis and brefeldin A obtained from Cladospo-rium sp. World J. Microbiol. Biotech-nol. 23, 79–83.
110. Weerapreeyakul, N., Anorach, R., Khuansawad, T., Yenjai, C., and Isaka, M. (2007). Synthesis of bioreductive esters from fungal compounds. Chem. Pharm. Bull. 55, 930–935.
111. Wei, C., Hansen, B. S., Vaughan, M. H., and McLaughlin, C. S. (1974). Mechanism of action of the mycotoxin trichodermin A, 12,13-epoxytrichothecene. Proc. Natl. Acad. Sci. U.S.A. 71, 713–717.
112. Wicklow, D. T., and Poling, S. M. (2009). Antimicrobial activity of pyrrocidines from Acremonium zeae against endophytes and pathogens of maize. Phytopathology 99, 109–115.
113. Wicklow, D. T., Roth, S., Deyrup, S. T., and Gloer, J. B. (2005). A protec-tive endophyte of maize: Acremo-nium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium ver-ticillioides. Mycol. Res. 109, 610–618.
114. Wilkinson, H. H., Siegel, M. R., Blanken-ship, J. D., Mallory, A. C., Bush, L. P., and Schardl, C. L. (2000). Contri-bution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol. Plant Microbe Interact. 13, 1027–1033.
115. World Health Organization (WHO). (2012). Tuberculosis: Fact-sheet March 2012. Available at: http://www.Who.Int/mediacentre/factsheets/fs104/en/index.html
116. Yarwood, C. E. (1932). Ampelomyces quisqualis on clover mildew. Phy-topathology 22, 31.
117. Yoshihara, T., Togiya, S., Koshino, H., Sakamura, S., Shimanuki, T., Sato, T., et al. (1985). Three fungitoxic cyclopentanoid sesquiterpenes from stromata of Epichloe typhina. Tetrahedron Lett. 26, 5551–5554.
118. Yuan, L., Zhao, P. J., Ma, J., Lu, C. H., and Shen, Y. M. (2009). Labdane and tetranorlabdane diterpenoids from Botryosphaeria sp. MHF, an endo-phytic fungus of Maytenus hookeri. Helv. Chim. Acta 92, 1118–1125.
119. Zhang, D. X., Nagabhyru, P., Blanken-ship, J. D., and Schardl, C. L. (2010). Are loline alkaloid levels regulated in grass endophytes by gene expres-sion or substrate availability? Plant Signal. Behav. 5, 1419–1422.
120. Zhao, J., Mou, Y., Shan, T., Li, Y., Zhou, L., Wang, M., et al. (2010). Antimicrobial metabolites from the endophytic fungus Pichia guillier-mondii isolated from Paris poly-phylla var. Yunnanensis. Molecules 15, 7961–7970.
121. Zhou, L., Zhao, J., Shan, T., Cai, X., and Peng, Y. (2010a). Spiro-bisnaphthalenes from fungi and their biological activi-ties. Mini Rev. Med. Chem. 10, 977–989.
122. Zhou, X., Zhu, H., Liu, L., Lin, J., and Tang, K. (2010b). A review: recent advances and future prospects of taxol-producing endophytic fungi. Appl. Microbiol. Biotechnol. 86, 1707–1717.
123. Zou, W. X., Meng, J. C., Lu, H., Chen, G. X., Shi, G. X., Zhang, T. Y., et al. (2000). Metabolites of Col-letotrichum gloeosporioides, an endo-phytic fungus in Artemisia mon-golica. J. Nat. Prod. 63, 1529–1530.