Fungal Endophytes and Their Secondary Metabolites: Role in Sustainable Agriculture

  • Anamika
  • Samiksha Joshi
  • Manvika Sahgal
  • Sharda Sahu
  • Anil Prakash


In today’s constantly changing scenario, there is an increase in the use of novel and useful bioactive compounds for solving myriad of problems mankind faces, viz. appearance of drug-resistant bacteria, emergence of life-threatening viruses, increasing incidences of fungal infections in the world’s population and problems in eliminating food scarcity from some areas of the globe to help human populations. Fungal endophytes though not extensively studied yet are potent source of novel natural products useful in industry, agriculture and medicine. Each of the 300,000 plant species existing on earth is host to one or more endophytes. Till date about one tenth of an estimated one million plant species have been studied for fungal endophytes which are considerably diverse. This chapter deals with the range of bioactive metabolites produced by the fungal endophytes studied so far with emphasis on those useful in increasing food production.


Endophytic fungi Bioactive metabolites Volatile compounds Tripartite interaction Signalling molecules 



Authors Sharda Sahu and Anil Prakash gratefully acknowledge the financial support provided by DBT-Builder Programme, Barkatullah University, Bhopal. Manvika Sahgal acknowledges the financial assistance provided by ICAR-GOI and Director Experiment Station, GBPUAT, Pantnagar-India.


  1. Akello J, Dubois T, Gold CS, Coyne D, Nakavuma J, Paparu P (2007) Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J Invertebr Pathol 96(1):34–42PubMedCrossRefGoogle Scholar
  2. Akello J, Dubois T, Coyne D, Kyamanywa S (2008) Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Prot 27(11):1437–1441CrossRefGoogle Scholar
  3. Akutse KS, Maniania NK, KKM F, Van den Berg J, Ekesi S (2013) Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecol 6(4):293–301CrossRefGoogle Scholar
  4. Arai T, Mikami Y, Fukushima K, Utsumi T, Yazawa K (1973) A new antibiotic, leucinostatin, derived from Penicillium lilacinum. J Antibiot 26(3):157–161PubMedCrossRefGoogle Scholar
  5. 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 100(26):15649–15654PubMedCrossRefPubMedCentralGoogle Scholar
  6. Azeem M, Rajarao GK, Terenius O, Nordlander G, Nordenhem H, Nagahama K, Borg-Karlson AK (2013) A fungal metabolite masks the host plant odor for the pine weevil (Hylobius abietis). Fungal Ecol 13:103–111CrossRefGoogle Scholar
  7. Azevedo JL, Maccheroni W Jr, Pereira JO, de Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3(1):15–16CrossRefGoogle Scholar
  8. Bacon CW, Hills NS (1996) Symptomless grass endophytes: products of coevolutionary symbioses and their role in the ecological adaptation of grasses. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants. American Phytopathologycal Society Press, St. Paul, pp 155–178Google Scholar
  9. Bacon CW, Porter JK, Robins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microbiol 34:576–581PubMedPubMedCentralGoogle Scholar
  10. Ball OJP, Miles CO, Prestidge RA (1997) Ergopeptide alkaloids and Neotyphodium lolli-mediated resistance in perennial ryegrass against adult Heteronychus arator (Coleoptera: Scarabaeidae). J Econ Entomol 90:1382–1391CrossRefGoogle Scholar
  11. Bandara WM, Seneviratne G, Kulasooriya SA (2006) Interactions among endophytic bacteria and fungi: effects and potentials. J Biosci 31(5):645–650PubMedCrossRefGoogle Scholar
  12. Benz F, Knüsel F, Nüesch J, Treichler H, Voser W, Nyfeler R, Keller-Schierlein W (1974) Stoffwechselprodukte von Mikroorganismen 143. Mitteilung. Echinocandin B, ein neuartiges Polypeptid-Antibioticum aus Aspergillus nidulans var. echinulatus: Isolierung und Bausteine. Helv Chim Acta 57(8):2459–2477CrossRefGoogle Scholar
  13. Bills GF, Giacobbe RA, Lee SH, Peláez F, Tkacz JS (1992) Tremorgenic mycotoxins, paspalitrem A and C, from a tropical Phomopsis. Mycol Res 96(11):977–983CrossRefGoogle Scholar
  14. Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211CrossRefGoogle Scholar
  15. Boberg JB, Ihrmark K, Lindahl BD (2011) Decomposing capacity of fungi commonly detected in Pinus sylvestris needle litter. Fungal Ecol 4(1):110–114CrossRefGoogle Scholar
  16. Boyle R, McLean S, Foley W, Davies NW, Peacock EJ, Moore B (2001) Metabolites of dietary 1, 8-cineole in the male koala (Phascolarctos cinereus). Comp Biochem Physiol C: Toxicol Pharmacol 129(4):385–395Google Scholar
  17. Brady SF, Clardy J (2000) CR377, a new pentaketide antifungal agent isolated from an endophytic fungus. J Nat Prod 63(10):1447–1448PubMedCrossRefGoogle Scholar
  18. Breen JP (1992) Temperature and seasonal effects on expression of Acremonium endophyte-enhanced resistance to Schizaphis graminum (Homoptera: Aphididae). Environ Entomol 21:68–74CrossRefGoogle Scholar
  19. Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114(1):1PubMedPubMedCentralCrossRefGoogle Scholar
  20. Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96(4):281–286CrossRefGoogle Scholar
  21. Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69(1):2–9CrossRefGoogle Scholar
  22. Caruso M, Colombo AL, Fedeli L, Pavesi A, Quaroni S, Saracchi M, Ventrella G (2000) Isolation of endophytic fungi and actinomycetes taxane producers. Ann Microbiol 50(1):3–14Google Scholar
  23. Castrillo LA, Griggs MH, Ranger CM, Reding ME, Vandenberg JD (2011) Virulence of commercial strains of Beauveria bassiana and Metarhizium brunneum (Ascomycota: Hypocreales) against adult Xylosandrus germanus (Coleoptera: Curculionidae) and impact on brood. Biol Control 58(2):121–126CrossRefGoogle Scholar
  24. Chapela IH, Petrini O, Hagmann L (1991) Monolignol glucosides as specific recognition messengers in fungus-plant symbioses. Physiol Mol Plant Pathol 39(4):289–298CrossRefGoogle Scholar
  25. Cherry AJ, Lomer CJ, Djegui D, Schulthess F (1999) Pathogen incidence and their potential as microbial control agents in IPM of maize stem borers in West Africa. BioControl 44(3):301–327CrossRefGoogle Scholar
  26. Cherry AJ, Banito A, Djegui D, Lomer C (2004) Suppression of the stem-borer Sesamia calamistis (Lepidoptera; Noctuidae) in maize following seed dressing, topical application and stem injection with African isolates of Beauveria bassiana. Int J Pest Manag 50(1):67–73CrossRefGoogle Scholar
  27. Chiron N, Michelot D (2005) Odeurs des champignons: chimie et rôle dans les interactions biotiques-une revue. Cryptogam Mycol 26(4):299–364Google Scholar
  28. Clay K (1988a) Fungal endophytes of grasses. A defensive mutualism between plants and fungi. Ecology 69:10–16CrossRefGoogle Scholar
  29. Clay K (1988b) Fungal endophytes of grasses. Their potential as biocontrol agents. Mycol Res 92:1–12CrossRefGoogle Scholar
  30. Contreras-Cornejo HA, Macías-Rodríguez L, Herrera-Estrella A, López-Bucio J (2014) The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission. Plant Soil 379(1–2):261–274CrossRefGoogle Scholar
  31. Crous PW, Braun U, Groenewald JZ (2007) Mycosphaerella is polyphyletic. Stud Mycol 58:1–32PubMedPubMedCentralCrossRefGoogle Scholar
  32. Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39(7):840–859PubMedCrossRefGoogle Scholar
  33. de Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43(3):237–256CrossRefGoogle Scholar
  34. Deckert RJ, Melville LH, Peterson RL (2001) Structural features of a Lophodermium endophyte during the cryptic life-cycle phase in the foliage of Pinus strobus. Mycol Res 105(8):991–997CrossRefGoogle Scholar
  35. Demain AL (1980) Microbial production of primary metabolites. Naturwissenschaften 67(12):582–587PubMedCrossRefGoogle Scholar
  36. Dew RK, Boissonneault GA, Gay N, Boling JA, Cross RJ, Cohen DA (1990) The effect of the endophyte (Acremonium coenophialum) and associated toxin (s) of tall fescue on serum titer response to immunization and spleen cell flow cytometry analysis and response to mitogens. Vet Immunol Immunopathol 26(3):285–295PubMedCrossRefGoogle Scholar
  37. Dourado MN, Neves AAC, Santos DS, Araújo WL (2015) Biotechnological and agronomic potential of endophytic pink-pigmented methylotrophic methylobacterium spp. Hindawi Publishing Corporation. BioMed Res Int 2015:909016 19 pagesPubMedPubMedCentralCrossRefGoogle Scholar
  38. Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38(6):665–703PubMedCrossRefGoogle Scholar
  39. Ezquer I, Li J, Ovecka M, Baroja-Fernández E, Muñoz FJ, Montero M, Etxeberria E (2010) Microbial volatile emissions promote accumulation of exceptionally high levels of starch in leaves in mono-and dicotyledonous plants. Plant Cell Physiol 51(10):1674–1693PubMedCrossRefGoogle Scholar
  40. Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42(2):360–368PubMedCrossRefGoogle Scholar
  41. Fialho MB, Ferreira LFR, Monteiro RTR, Pascholati SF (2011) Antimicrobial volatile organic compounds affect morphogenesis-related enzymes in Guignardia citricarpa, causal agent of citrus black spot. Biocontrol Sci Tech 21(7):797–807CrossRefGoogle Scholar
  42. Findlay JA, Li G, Penner PE, Miller JD (1995a) Novel diterpenoid insect toxins from a conifer endophyte. J Nat Prod 58(2):197–200CrossRefGoogle Scholar
  43. Findlay JA, Buthelezi S, Lavoie R, Peña-Rodriguez L, Miller JD (1995b) Bioactive isocoumarins and related metabolites from conifer endophytes. J Patural Prod 58(11):1759–1766CrossRefGoogle Scholar
  44. Findlay S, Carreiro M, Krischik V, Jones CG (1996) Effects of damage to living plants on leaf litter quality. Ecol Appl 6(1):269–275CrossRefGoogle Scholar
  45. Findlay JA, Buthelezi S, Li GQ, Seveck M, Miller JD (1997) Insect toxins from an endophytic fungus from wintergreen. J Nat Prod 60:1214–1215CrossRefGoogle Scholar
  46. Fraatz MA, Zorn H (2010) Fungal flavors. In: Esser K, Hofrichter M (eds) The mycota X: industrial applications. Springer, Heidelberg, pp 249–268Google Scholar
  47. Georg GI, Chen TT, Ojima I, Vyas DM (1994) Taxane anticancer agents. Basic science current status, American Chemical Society. Symposium Series no. 583. American Chemical Society, Washington, DCGoogle Scholar
  48. Glenn AE, Bacon CW, Price R, Hanlin RT (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88:369–383CrossRefGoogle Scholar
  49. Golo PS, Gardner DR, Grilley MM, Takemoto JY, Krasnoff SB, Pires MS, Roberts DW (2014) Production of destruxins from Metarhizium spp. fungi in artificial medium and in endophytically colonized cowpea plants. PLoS One 9(8):e104946PubMedPubMedCentralCrossRefGoogle Scholar
  50. Götz M, Dammann U, Schulz B, Boyle C (2000) Influence of colonization of the apoplast by endophytic fungi on the nutrient status of the host plant. Abstracts, third international congress on symbiosis, Marburg, p 78Google Scholar
  51. Greenfield M, Pareja R, Ortiz V, María I, Jiménez G, Fernando E, Vega, Parsa S (2015) A novel method to scale up fungal endophyte isolations. Biocontrol Sci Tech 25(10):1208–1212CrossRefGoogle Scholar
  52. Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA (2010) Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiology 156(12):3814–3829PubMedCrossRefGoogle Scholar
  53. Gunatilaka AL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69(3):509–526PubMedPubMedCentralCrossRefGoogle Scholar
  54. Guo LD, Hyde KD, Liew ECY (2000) Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 147(3):617–630CrossRefGoogle Scholar
  55. Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47(6):453–467PubMedCrossRefGoogle Scholar
  56. Halmschlager E, Butin H, Donaubauer E (1993) Endophytic fungi in leaves and twigs of Quercus petraea. Eur J For Pathol 23(1):51–63CrossRefGoogle Scholar
  57. Harper JK, Arif AM, Ford EJ, Strobel GA, Porco JA, Tomer DP, Grant DM (2003) Pestacin: a 1, 3-dihydro isobenzofuran from Pestalotiopsis microspora possessing antioxidant and antimycotic activities. Tetrahedron 59(14):2471–2476CrossRefGoogle Scholar
  58. Herrera-Carillo Z, Torres MS, Singh AP, Vorsa N, Gianfagna T, Meyer W, White Jr JF (2009) Phenolic, flavonoid and antioxidant profiling for cool-season grasses with and without endophyte. In: Proceedings of the 18th annual rutgers turfgrass symposium, vol 12, January 2009Google Scholar
  59. Hofer P, Vermette P, Groleau D (2011) Introducing a new bioengineered bug: Methylobacterium extorquens tuned as a microbial bioplastic factory. Bioeng Bug 2(2):71–79CrossRefGoogle Scholar
  60. Holighaus G, Weißbecker B, von Fragstein M, Schütz S (2014) Ubiquitous eight-carbon volatiles of fungi are infochemicals for a specialist fungivore. Chemoecology 24(2):57–66CrossRefGoogle Scholar
  61. Horakova K, Betina V (1976) Cytotoxic activity of macrocyclic metabolites from fungi. Neoplasma 24(1):21–27Google Scholar
  62. Horn WS, Simmonds MS, Schwartz RE, Blaney WM (1996) Variation in production of Phomodiol and Phomopsolide B by Phomopsis spp. Mycologia 88:588–595CrossRefGoogle Scholar
  63. Huang Z, Wang B, Eaves DH, Shikany JM, Pace RD (2007) Phenolic compound profile of selected vegetables frequently consumed by African Americans in the Southeast United States. Food Chem 103(4):1395–1402CrossRefGoogle Scholar
  64. Hung R, Lee S, Bennett JW (2013) Arabidopsis thaliana as a model system for testing the effect of Trichoderma volatile organic compounds. Fungal Ecol 6(1):19–26CrossRefGoogle Scholar
  65. Inamdar AA, Moore JC, Cohen RI, Bennett JW (2012) A model to evaluate the cytotoxicity of the fungal volatile organic compound 1-octen-3-o1 in human embryonic stem cells. Mycopathologia 173:13–20PubMedCrossRefGoogle Scholar
  66. Ishii T, Hayashi K, Hida T, Yamamoto Y, Nozaki Y (2000) TAN-1813, a novel Ras-farnesyltransferase inhibitor produced by Phoma sp. J Antibiot 53(8):765–778PubMedCrossRefGoogle Scholar
  67. Ju Y, Sacalis JN, Still CC (1998) Bioactive flavonoids from endophyte-infected blue grass (Poa ampla). J Agric Food Chem 46:3785–3788CrossRefGoogle Scholar
  68. Jumpponen ARI, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140(2):295–310CrossRefGoogle Scholar
  69. Kaiser R (2006) Flowers and fungi use scents to mimic each other. Science 311:806–807PubMedCrossRefGoogle Scholar
  70. Kaul S, Sharma T, Dhar MK (2016) Omics tools for better understanding the plant–endophyte interactions. Front Plant Sci.
  71. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73(1):35–37CrossRefGoogle Scholar
  72. Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite–what decides? Curr Opin Plant Biol 9(4):358–363PubMedCrossRefGoogle Scholar
  73. Korpi A, Jarnberg J, Pasanen A-L (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193PubMedCrossRefGoogle Scholar
  74. Koshino H, Terada SI, Yoshihara T, Sakamura S, Shimanuki T, Sato T, Tajimi A (1988) Three phenolic acid derivatives from stromata of Epichloë typhina on Phleum pratense. Phytochemistry 27(5):1333–1338CrossRefGoogle Scholar
  75. Koshino T, Yoshihara S, Sakamura T, Shimanuki T, Sato A, Tajimi (1989) A ring B aromatic sterol from stromata of Epichloë typhina. Phytochemistry 28:771–772CrossRefGoogle Scholar
  76. Koshino H, Yoshihara T, Okuno M, Sakamura S, Tajimi A, Shimanuki T (1992) Gamahonolides A, B, and gamahorin, novel antifungal compounds from stromata of Epichloë typhina on Phleum pratense. Biosci Biotechnol Biochem 56(7):1096–1099PubMedCrossRefGoogle Scholar
  77. Krohn K, Michel A, Flörke U, Aust HJ, Draeger S, Schulz B (1994) Biologically active metabolites from fungi, 5. Palmarumycins C1–C16 from Coniothyrium sp.: isolation, structure elucidation, and biological activity. Eur J Org Chem 1994(11):1099–1108Google Scholar
  78. Krohn K, Michel A, Romer E, Florke U, Aust HJ, Draeger S, Schulz B (1996) Biologically active secondary metabolites from fungi 6: phomosines AC. Two new biaryl ethers and one new arylbenzyl ether from Phomopsis sp. Nat Prod Lett 8:43–48CrossRefGoogle Scholar
  79. Krohn K, Bahramsari R, Flörke U, Ludewig K, Kliche-Spory C, Michel A, Antus S (1997) Dihydroisocoumarins from fungi: isolation, structure elucidation, circular dichroism and biological activity. Phytochemistry 45(2):313–320PubMedCrossRefPubMedCentralGoogle Scholar
  80. Krohn K, Florke U, John M, Root N, Steingrover K, Aust HJ, Draeger S, Schulz B, Antus S, Simonyi M, Zsila F (2001) Biologically active metabolites from fungi part 16. New preussomerins J, K and L from an endophytic fungus: structure elucidation, crystal structure analysis and determination of absolute configuration by CD calculations. Tetrahedron 57:4343–4348CrossRefGoogle Scholar
  81. Kumar S, Kaushik N (2012) Metabolites of endophytic fungi as novel source of biofungicide: a review. Phytochem Rev 11(4):507–522CrossRefGoogle Scholar
  82. Kusari S, Singh S, Jayabaskaran C (2014) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:6Google Scholar
  83. Lee JC, Lobokovsky NB, Strobel GA, Clardy JC (1995) Subglutinol A and B: immunosuppresive compounds from the endophytic fungus Fusarium subglutinans. J Org Chem 60:7076–7077CrossRefGoogle Scholar
  84. Lee SO, Kim HY, Choi GJ, Lee HB, Jang KS, Choi YH, Kim JC (2009) Mycofumigation with Oxyporus latemarginatus EF069 for control of postharvest apple decay and Rhizoctonia root rot on moth orchid. J Appl Microbiol 106(4):1213–1219PubMedCrossRefGoogle Scholar
  85. Leuchtmann A (1992) Systematics, distribution, and host specificity of grass endophytes. Nat Toxins 1(3):150–162PubMedCrossRefGoogle Scholar
  86. Li JY, Strobel G, Sidhu R, Hess WM, Ford EJ (1996) Endophytic taxol-producing fungi from bald cypress, Taxodium distichum. Microbiology 142(8):2223–2226PubMedCrossRefGoogle Scholar
  87. Li JY, Sidhu RS, Ford EJ, Long DM, Hess WM, Strobel GA (1998) The induction of taxol production in the endophytic fungus—Periconia sp from Torreya grandifolia. J Ind Microbiol Biotech 20:259–264CrossRefGoogle Scholar
  88. Liang B, Lehmann J, Solomon D, Sohi S, Thies JE, Skjemstad JO, Wirick S (2008) Stability of biomass-derived black carbon in soils. Geochim Cosmochim Acta 72(24):6069–6078CrossRefGoogle Scholar
  89. Lingham RB, Silverman KC, Bills GF, Cascales C, Sanchez M, Jenkins RG, Mochales S (1993) Chaetomella acutiseta produces chaetomellic acids A and B which are reversible inhibitors of farnesyl-protien transferase. Appl Microbiol Biotechnol 40(2–3):370–374PubMedGoogle Scholar
  90. Liu CH, Zou WX, Lu H, Tan RX (2001) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88(3):277–282PubMedCrossRefGoogle Scholar
  91. Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151(1):67–73CrossRefGoogle Scholar
  92. Macías-Rubalcava ML, Hernández-Bautista BE, Oropeza F, Duarte G, González MC, Glenn AE, Anaya AL (2010) Allelochemical effects of volatile compounds and organic extracts from Muscodor yucatanensis, a tropical endophytic fungus from Bursera simaruba. J Chem Ecol 36(10):1122–1131PubMedCrossRefGoogle Scholar
  93. Madelin MF (1963) Diseases caused by hyphomycetous fungi. In: Steinhaus E (ed) Insect pathology. An advanced treatise, vol 2. Academic, New York, pp 233–272CrossRefGoogle Scholar
  94. Metz AM, Haddad A, Worapong J, Long DM, Ford EJ, Hess WM, Strobel GA (2000) Induction of the sexual stage of Pestalotiopsis microspora, a taxol-producing fungus. Microbiology 146(8):2079–2089PubMedCrossRefGoogle Scholar
  95. Miller JD (2001) Factors that affect the occurrence of fumonisin. Environ Health Perspect 109(Suppl 2):321PubMedPubMedCentralCrossRefGoogle Scholar
  96. Minerdi D, Bossi S, Gullino ML, Garibaldi A (2009) Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 11:844–854PubMedCrossRefGoogle Scholar
  97. Minerdi D, Bossi S, Maffei ME, Gullino ML, Garibaldi A (2011) Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol Ecol 76(2):342–351PubMedCrossRefGoogle Scholar
  98. Moricca S, Ragazzi A (2008) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology 98(4):380–386PubMedCrossRefGoogle Scholar
  99. Müller A, Faubert P, Hagen M, zu Castell W, Polle A, Schnitzler JP, Rosenkranz M (2013) Volatile profiles of fungi–chemotyping of species and ecological functions. Fungal Genet Biol 54:25–33PubMedCrossRefGoogle Scholar
  100. Naznin HA, Kiyohara D, Kimura M, Miyazawa M, Shimizu M, Hyakumachi M (2014) Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS One 9(1):e86882PubMedPubMedCentralCrossRefGoogle Scholar
  101. Ngwene B, Boukail S, Söllner L, Franken P, Andrade-Linares DR (2016) Phosphate utilization by the fungal root endophyte Piriformospora indica. Plant Soil 405(1–2):231–241CrossRefGoogle Scholar
  102. O’Hanlon KA, Knorr K, Jørgensen LN, Nicolaisen M, Boelt B (2012) Exploring the potential of symbiotic fungal endophytes in cereal disease suppression. Biol Control 63(2):69–78CrossRefGoogle Scholar
  103. Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4(8):701–712PubMedPubMedCentralCrossRefGoogle Scholar
  104. Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4(3):357–374PubMedPubMedCentralCrossRefGoogle Scholar
  105. Oses R, Valenzuela S, Freer J, Sanfuentes E, Rodriguez J (2008) Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Divers 33(7):77–86Google Scholar
  106. Pagans E, Font X, Sánchez A (2006) Emission of volatile organic compounds from composting of different solid wastes: abatement by biofiltration. J Hazard Mater 131(1):179–186PubMedCrossRefPubMedCentralGoogle Scholar
  107. Parfitt D, Hunt J, Dockrell D, Rogers HJ, Boddy L (2010) Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol 3(4):338–346CrossRefGoogle Scholar
  108. Parsa S, García-Lemos AM, Castillo K, Ortiz V, López-Lavalle LAB, Braun J, Vega FE (2016) Fungal endophytes in germinated seeds of the common bean, Phaseolus vulgaris. Fungal Biol 120(5):783–790PubMedPubMedCentralCrossRefGoogle Scholar
  109. Patterson CG, Potter DA, Fannin FF (1992) Feeding deterrency of alkaloids from endophyte-infected grasses to Japanese beetle grubs. Entomol Exp Appl 61:285CrossRefGoogle Scholar
  110. Pedrini N, Ortiz-Urquiza A, Zhang S, Keyhani NO (2013) Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: hydrocarbon oxidation within the context of a host-pathogen interaction. Front Microbiol 4:24PubMedPubMedCentralCrossRefGoogle Scholar
  111. Peipp H, Sonnenbichler J (1992) Secondary fungal metabolites and their biological activities, II. Occurrence of antibiotic compounds in cultures of Armillaria ostoyae growing in the presence of an antagonistic fungus or host plant cells. Biol Chem Hoppe Seyler 373(2):675–684PubMedCrossRefGoogle Scholar
  112. Peters S, Dammeyer B, Schulz B (1998a) Endophyte-host interactions. I. Plant defense reactions to endophytic and pathogenic fungi. Symbiosis 25(1–3):193–211Google Scholar
  113. Peters S, Draeger S, Aust HJ, Schulz B (1998b) Interactions in dual cultures of endophytic fungi with host and nonhost plant calli. Mycologia 90:360–367CrossRefGoogle Scholar
  114. Petrini O (1991) Fungal endophytes of tree leaves. In: Microbial ecology of leaves. Springer, New York, pp 179–197Google Scholar
  115. Pimenta RS, Moreira da Silva JF, Buyer JS, Janisiewicz WJ (2012) Endophytic fungi from plums (Prunus domestica) and their antifungal activity against Monilinia fructicola. J Food Prot 75(10):1883–1889PubMedCrossRefGoogle Scholar
  116. Pinto C, Rodrigues LS, Azevedo JL, Pereira JO, Carneiro Vieira ML, Labate CA (2000) Symptomless infection of banana and maize by endophytic fungi impairs photosynthetic efficiency. New Phytol 147(3):609–615CrossRefGoogle Scholar
  117. Powell RG, Petroski RJ (1992) Alkaloid toxins in endophyte-infected grasses. Nat Toxins 1(3):163–170PubMedCrossRefGoogle Scholar
  118. Prestidge RA, Gallagher RT (1988) Endophyte conifers resistance to ryegrass: argentine stem weevil larval studies. Ecol Entomol 13:429–435CrossRefGoogle Scholar
  119. Pulici M, Sugawara F, Koshino H, Uzawa J, Yoshida S, Lobkovsky E, Clardy J (1996a) Pestalotiopsins A and B: new caryophyllenes from an endophytic fungus of Taxus brevifolia. J Org Chem 61(6):2122–2124CrossRefGoogle Scholar
  120. Pulici M, Sugawara F, Koshino H, Uzawa J, Yoshida S, Lobkovsky E, Clardy J (1996b) A new isodrimeninol from Pestalotiopsis sp. J Nat Prod 59(1):47–48CrossRefGoogle Scholar
  121. Pulici M, Sugawara F, Koshino H, Okada G, Esumi Y, Uzawa J, Yoshida S (1997) Metabolites of Pestalotiopsis spp., endophytic fungi of Taxus brevifolia. Phytochemistry 46(2):313–319CrossRefGoogle Scholar
  122. Qiu DY, Huang MJ, Fang XH, Zhu C, Zhu ZQ (1994) Isolation of an endophytic fungus associated with Taxus yunnanensis. Acta Mycol Sin 13:314Google Scholar
  123. Quesada-Moraga E, Landa BB, Muñoz-Ledesma J, Jiménez-Diáz RM, Santiago-Alvarez C (2006) Endophytic colonisation of opium poppy, Papaver somniferum, by an entomopathogenic Beauveria bassiana strain. Mycopathologia 161(5):323–329PubMedCrossRefGoogle Scholar
  124. Rai M, Agarkar G (2014) Plant–fungal interactions: what triggers the fungi to switch among lifestyles? Crit Rev Microbiol 42(3):428–438PubMedGoogle Scholar
  125. Reddy NP, Khan APA, Devi UK, Sharma HC, Reineke A (2009) Treatment of millet crop plant (Sorghum bicolor) with the entomopathogenic fungus (Beauveria bassiana) to combat infestation by the stem borer, Chilo partellus Swinhoe (Lepidoptera: Pyralidae). J Asia Pac Entomol 12(4):221–226CrossRefGoogle Scholar
  126. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151(3):705–716CrossRefGoogle Scholar
  127. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298(5598):1581–1581PubMedCrossRefPubMedCentralGoogle Scholar
  128. Richardson MD, Chapman GW, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-infected tall fescue under drought. Crop Sci 32(4):1060–1061CrossRefGoogle Scholar
  129. Riedell WE, Kieckhefer RE, Petroski RJ, Powell RG (1991) Naturally-occurring and synthetic loline alkaloid derivatives: insect feeding behaviour modification and toxicity. J Entomol Sci 26:122–129CrossRefGoogle Scholar
  130. Rocha AC, Garcia D, Uetanabaro AP, Carneiro RT, Araújo IS, Mattos CR, Góes-Neto A (2011) Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Divers 47(1):75–84CrossRefGoogle Scholar
  131. Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114PubMedCrossRefGoogle Scholar
  132. Rowan DD, Latch GCM (1994) In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, pp 169–183Google Scholar
  133. Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357PubMedCrossRefGoogle Scholar
  134. Rudgers JA, Strauss SY (2004) A selection mosaic in the facultative mutualism between ants and wild cotton. Proc R Soc Lond B Biol Sci 271(1556):2481–2488CrossRefGoogle Scholar
  135. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29(1):319–343CrossRefGoogle Scholar
  136. Schardl CL, Phillips TD (1997) Protective grass endophytes: where are they from and where are they going? Plant Dis 81(5):430–438CrossRefGoogle Scholar
  137. Schardl CL, Liu JS, White JF, Finkel RA, An Z, Siegel MR (1991) Molecular phylogenetic relationships of nonpathogenic grass mycosymbionts and clavicipitaceous plant pathogens. Plant Syst Evol 178(1):27–41CrossRefGoogle Scholar
  138. Schiestl FP, Steinebrunner F, Schulz C, Von Reuss S, Francke W, Weymuth C, Leuchtmann A (2006) Evolution of ‘pollinator’-attracting signals in fungi. Biol Lett 2(3):401–404PubMedPubMedCentralCrossRefGoogle Scholar
  139. Schrank A, Vainstein MH (2010) Metarhizium anisopliae enzymes and toxins. Toxicon 56(7):1267–1274PubMedCrossRefGoogle Scholar
  140. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109(6):661–686PubMedCrossRefPubMedCentralGoogle Scholar
  141. Schulz B, Sucker J, Aust HJ, Krohn K, Ludewig K, Jones PG, Döring D (1995) Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res 99(8):1007–1015CrossRefGoogle Scholar
  142. Schulz B, Römmert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103(10):1275–1283CrossRefGoogle Scholar
  143. Schulz B, Boyle C, Draeger S, Römmert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites** Paper presented at the British Mycological Society symposium on Fungal Bioactive Compounds, held at the University of Wales Swansea on 22–27 April 2001. Mycol Res 106(9)996–1004Google Scholar
  144. Selosse MA, Dubois MP, Alvarez N (2009) Do Sebacinales commonly associate with plant roots as endophytes? Mycol Res 113(10):1062–1069PubMedCrossRefGoogle Scholar
  145. Singh MP, Janso JE, Luckman SW, Brady SF, Clardy J, Greenstein M, Maiese WM (2000) Biological activity of guanacastepene, a novel diterpenoid antibiotic produced by an unidentified fungus CR115. J Antibiot 53(3):256–261PubMedCrossRefGoogle Scholar
  146. Small CLN, Bidochka MJ (2005) Up-regulation of Pr1, a subtilisin-like protease, during conidiation in the insect pathogen Metarhizium anisopliae. Mycol Res 109(3):307–313PubMedCrossRefGoogle Scholar
  147. Song GC, Ryu CM (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819PubMedPubMedCentralCrossRefGoogle Scholar
  148. Splivallo R, Ottonello S, Mello A, Karlovsky P (2011) Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol 189:688–699PubMedCrossRefGoogle Scholar
  149. St Leger RJ, Joshi L, Bidochka MJ, Roberts DW (1996) Construction of an improved mycoinsecticide overexpressing a toxic protease. Proc Natl Acad Sci 93(13):6349–6354PubMedCrossRefGoogle Scholar
  150. Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science-New York Then Washington 260:214–214CrossRefGoogle Scholar
  151. Stierle A, Strobel G, Stierle D, Grothaus P, Bignami G (1995) The search for a taxol-producing microorganism among the endophytic fungi of the Pacific yew, Taxus brevifolia. J Nat Prod 58(9):1315–1324PubMedCrossRefGoogle Scholar
  152. Stierle AA, Stierle DB, Bugni T (1999) Sequoiatones A and B: novel antitumor metabolites isolated from a redwood endophyte. J Org Chem 64(15):5479–5484PubMedCrossRefGoogle Scholar
  153. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 4:491–502CrossRefGoogle Scholar
  154. Strobel G, Yang X, Sears J, Kramer R, Sidhu RS, Hess WM (1996) Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallichiana. Microbiology 142(2):435–440PubMedCrossRefGoogle Scholar
  155. Strobel GA, Torczynski R, Bollon A (1997) Acremonium sp.—a leucinostatin A producing endophyte of European yew (Taxus baccata). Plant Sci 128(1):97–108CrossRefGoogle Scholar
  156. Strobel GA, Miller RV, Martinez-Miller C, Condron MM, Teplow DB, Hess WM (1999) Cryptocandin, a potent antimycotic from the endophytic fungus Cryptosporiopsis cf. quercina. Microbiology 145(8):1919–1926PubMedCrossRefPubMedCentralGoogle Scholar
  157. Strobel G, Ford E, Worapong J, Harper JK, Arif AM, Grant DM, Chau RMW (2002) Isopestacin, an isobenzofuranone from Pestalotiopsis microspora, possessing antifungal and antioxidant activities. Phytochemistry 60(2):179–183PubMedCrossRefGoogle Scholar
  158. Su M, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83CrossRefGoogle Scholar
  159. Sumarah MW, Puniani E, Blackwell BA, Miller JD (2008) Characterization of polyketide metabolites from foliar endophytes of Picea glauca. J Nat Prod 71(8):1393–1398PubMedCrossRefGoogle Scholar
  160. Sun X, Guo LD, Hyde KD (2011) Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47(1):85–95CrossRefGoogle Scholar
  161. Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18(4):448–459PubMedCrossRefPubMedCentralGoogle Scholar
  162. Thorn RMS, Greenman J (2012) Microbial volatile compounds in health and disease conditions. J Breath Res 6(2):024001PubMedCrossRefGoogle Scholar
  163. Torres MS, Singh AP, Shah S, Herrera-Carrillo Z, Gianfagna T, White Jr JF, Vorsa N (2009) LC–MS–MS identification and quantification of phenolics in symbiotic tall fescue. In: Proceedings of the 18th Annual Rutgers Turfgrass Symposium, vol 12. New Brunswick, New Jersey: Rutgers University, Center for Interdisciplinary Studies in Turfgrass Science, January 2009Google Scholar
  164. Traber R, Keller-Juslén C, Loosli HR, Kuhn M, Von Wartburg A (1979) Cyclopeptid-Antibiotika aus Aspergillus-Arten. Struktur der Echinocandine C und D. Helv Chim Acta 62(4):1252–1267CrossRefGoogle Scholar
  165. Tudzynski B (1997) Fungal phytohormones in pathogenic and mutualistic associations. In: Plant relationships. Springer, Berlin/Heidelberg, pp 167–184Google Scholar
  166. Tudzynski B, Sharon A (2002) Biosynthesis, biological role and application of fungal phytohormones. In: Industrial applications. Springer, Berlin/Heidelberg, pp 183–211Google Scholar
  167. Unterseher M, Schnittler M (2010) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)–different cultivation techniques influence fungal biodiversity assessment. Mycol Res 113(5):645–654CrossRefGoogle Scholar
  168. Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, Arnold AE (2010) Fungal endophyte diversity in coffee plants from Colombia, Hawai’i, Mexico and Puerto Rico. Fungal Ecol 3(3):122–138CrossRefGoogle Scholar
  169. Verma VC, Singh SK, Solanki R, Prakash S (2011) Biofabrication of anisotropic gold nanotriangles using extract of endophytic Aspergillus clavatus as a dual functional reductant and stabilizer. Nanoscale Res Lett 6:16–22PubMedCrossRefGoogle Scholar
  170. Wagenaar MM, Corwin J, Strobel G, Clardy J (2000) Three new cytochalasins produced by an endophytic fungus in the genus Rhinocladiella. J Nat Prod 63(12):1692–1695PubMedCrossRefGoogle Scholar
  171. Wang J, Li G, Lu H, Zheng Z, Huang Y, Su W (2000) Taxol from Tubercularia sp. strain TF5, an endophytic fungus of Taxus mairei. FEMS Microbiol Lett 193:249–253PubMedCrossRefGoogle Scholar
  172. Wani MC, Taylor HL, Wall ME, Coggon P, McPhail AT (1971). Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemia and antitumor agent from Taxus brevifolia. Journal of the American Chemical Society, 93(9): 2325–2327Google Scholar
  173. Waweru B, Turoop L, Kahangi E, Coyne D, Dubois T (2014) Non-pathogenic fusarium oxysporum endophytes provide field control of nematodes, improving yield of banana (Musa sp.). Biol Control 74:82–88CrossRefGoogle Scholar
  174. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20(2):248–254PubMedCrossRefGoogle Scholar
  175. White JF, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138(4):440–446PubMedCrossRefGoogle Scholar
  176. White Jr JF, Reddy PV, Bacon CW (2000) Biotrophic endophytes of grasses: a systematic appraisal. In: Microbial endophytes. Marcel Dekker, New York, pp 49–62Google Scholar
  177. Yang X, Strobel G, Stierle A, Hess WM, Lee J, Clardy J (1994) A fungal endophyte-tree relationship: Phoma sp. in Taxus wallichiana. Plant Sci 102(1):1–9CrossRefGoogle Scholar
  178. Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Appl Environ Microbiol 78(16):5942–5944PubMedPubMedCentralCrossRefGoogle Scholar
  179. Zou WX, Meng JC, Lu H, Chen GX, Shi GX, Zhang TY, Tan RX (2000) Metabolites of Colletotrichum gloeosporioides, an endophytic fungus in Artemisia mongolica. J Nat Prod 63(11):1529–1530PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Anamika
    • 1
  • Samiksha Joshi
    • 1
  • Manvika Sahgal
    • 1
  • Sharda Sahu
    • 2
  • Anil Prakash
    • 2
  1. 1.Department of MicrobiologyG. B. Pant University of Agriculture & TechnologyPantnagarIndia
  2. 2.Department of MicrobiologyBarkatullah UniversityBhopalIndia

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