Fungal endophytes: unique plant inhabitants with great promises

Abstract

Fungal endophytes residing in the internal tissues of living plants occur in almost every plant on earth from the arctic to the tropics. The endophyte–host relationship is described as a balanced symbiotic continuum ranging from mutualism through commensalism to parasitism. This overview will highlight selected aspects of endophyte diversity, host specificity, endophyte–host interaction and communication as well as regulation of secondary metabolite production with emphasis on advanced genomic methods and their role in improving our current knowledge of endophytic associations. Furthermore, the chemical potential of endophytic fungi for drug discovery will be discussed with focus on the detection of pharmaceutically valuable plant constituents as products of fungal biosynthesis. In addition, selected examples of bioactive metabolites reported in recent years (2008–2010) from fungal endophytes residing in terrestrial plants are presented grouped according to their reported biological activities.

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References

  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 96:34–42

    PubMed  Article  Google Scholar 

  2. Aly AH, Edrada-Ebel R, Indriani ID, Wray V, Müller WEG, Frank T, Zirrgiebel U, Schächtele C, Kubbutat MHG, Lin WH, Proksch P, Ebel R (2008) Cytotoxic metabolites from the fungal endophyte Alternaria sp. and their subsequent detection in its host plant Polygonum senegalense. J Nat Prod 71:972–980

    CAS  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  4. Amna T, Puri SC, Verma V, Sharma JP, Khajuria RK, Musarrat J, Spiteller M, Qazi GN (2006) Bioreactor studies on the endophytic fungus Entrophospora infrequens for the production of an anticancer alkaloid camptothecin. Can J Microbiol 52:189–196

    CAS  PubMed  Article  Google Scholar 

  5. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66

    Article  Google Scholar 

  6. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549

    PubMed  Article  Google Scholar 

  7. Arnold AE, Mejia 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 USA 100:15649–15654

    CAS  PubMed  Article  Google Scholar 

  8. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206

    CAS  PubMed  Article  Google Scholar 

  9. Bacon CW, White JF (2000) Microbial endophytes. Dekker, New York, pp 341–388

    Google Scholar 

  10. Bae H, Sicher RC, Kim MS, Kim S-H, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, Samuels GJ, Choi IY, Holmes KA (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464

    CAS  PubMed  Article  Google Scholar 

  12. Barengo N, Sieber TN, Holdenrieder O (2000) Diversity of endophytic mycobiota in leaves and twigs of pubescent birch (Betula pubescens). Sydowia 52:305–320

    Google Scholar 

  13. Bashyal B, Li JY, Strobel GA, Hess WM (1999) Seimatoantlerium nepalense, an endophytic taxol producing coelomycete from Himalayan yew (Taxus wallachiana). Mycotaxon 72:33–42

    Google Scholar 

  14. Blankenship JD, Spiering MJ, Wilkinson HH, Fannin FF, Bush LP, Schardl CL (2001) Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media. Phytochemistry 58:395–401

    CAS  PubMed  Article  Google Scholar 

  15. Boberg JB, Ihrmark K, Lindahl BD (2011) Decomposing capacity of fungi commonly detected in Pinus sylvestris needle litter. Fungal Ecol 4:110–114

    Article  Google Scholar 

  16. Bode HB, Walker M, Zeeck A (2000) Cladospirones B to I from Sphaeropsidales sp. F-24′707 by variation of culture conditions. Eur J Org Chem 2000:3185–3193

    Article  Google Scholar 

  17. Bode HB, Bethe B, Hofs R, Zeek A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. Chembiochem 3:619–627

    CAS  PubMed  Article  Google Scholar 

  18. Bok JW, Keller NP (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3:527–535

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Botella L, Diez JJ (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18

    Article  Google Scholar 

  20. Calvo AM, Wilson RA, Bok JW, Keller NP (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66:447–459

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. Christensen MJ, Bennett RJ, Schmid J (2002) Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycol Res 106:93–106

    Article  Google Scholar 

  22. Cueto M, Jensen PR, Kauffman C, Fenical W, Lobkovsky E, Clardy J (2001) Pestalone, a new antibiotic produced by a marine fungus in response to bacterial challenge. J Nat Prod 64:1444–1446

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Debbab A, Aly AH, Edrada-Ebel RA, Wray V, Müller WEG, Totzke F, Zirrgiebel U, Schächtele C, Kubbutat MHG, Lin WH, Mosaddak M, Hakiki A, Proksch P, Ebel R (2009) Bioactive metabolites from the endophytic fungus Stemphylium globuliferum isolated from Mentha pulegium. J Nat Prod 72:626–631

    CAS  PubMed  Article  Google Scholar 

  24. Dowzer CE, Kelly JM (1989) Cloning of the CreA gene from Aspergillus nidulans: a gene involved in carbon catabolite repression. Curr Genet 15:457–459

    CAS  PubMed  Article  Google Scholar 

  25. Duong LM, Jeewon R, Lumyong S, Hyde KD (2006) DGGE coupled with ribosomal DNA gene phylogenies reveal uncharacterized fungal phylotypes. Fungal Divers 23:121–138

    Google Scholar 

  26. Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69:1121–1124

    CAS  PubMed  Article  Google Scholar 

  27. Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integr Comp Biol 42:360–368

    PubMed  Article  Google Scholar 

  28. Frisvad JC, Andersen B, Thrane U (2008) The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycol Res 112:231–240

    CAS  PubMed  Article  Google Scholar 

  29. Fuchser J, Zeeck A (1997) Secondary metabolites by chemical screening, 34.—Aspinolides and aspinonene/aspyrone co-metabolites, new pentaketides produced by Aspergillus ochraceus. Liebigs Ann 1997:87–95

    Article  Google Scholar 

  30. Gamboa MA, Laureano S, Bayman P (2002) Measuring diversity of endophytic fungi in leaf fragments: does size matter? Mycopathologia 156:41–45

    PubMed  Article  PubMed Central  Google Scholar 

  31. Gangadevi V, Muthumary J (2008a) Taxol, an anticancer drug produced by an endophytic fungus Bartalinia robillardoides Tassi, isolated from a medicinal plant, Aegle marmelos Correa ex Roxb. World J Microbiol Biotechnol 24:717–724

    CAS  Article  Google Scholar 

  32. Gangadevi V, Muthumary J (2008b) Isolation of Colletotrichum gloeosporioides, a novel endophytic taxol-producing fungus from the leaves of a medicinal plant, Justicia gendarussa. Mycol Balc 5:1–4

    Google Scholar 

  33. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327

    PubMed  Article  Google Scholar 

  34. Garcia-Effron G, Park S, Perlin DS (2009) Correlating echinocandin MIC and kinetic inhibition of fks1 mutant glucan synthases for Candida albicans: implications for interpretive breakpoints. Antimicrob Agents Chemother 53:112–122

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254

    Article  Google Scholar 

  36. Ge HM, Peng H, Guo ZK, Cui JT, Song YC, Tan RX (2010) Bioactive alkaloids from the plant endophytic fungus Aspergillus terreus. Planta Med 76:822–824

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. Germaine K, Keogh E, Garcia-Cabellos G, Borremans B, Lelie D, Barac T, Oeyen L, Vangronsveld J, Moore FP, Moore ERB, Campbell CD, Ryan D, Dowling DN (2004) Colonisation of poplar trees by gfp expressing bacterial endophytes. FEMS Microbiol Ecol 48:109–118

    CAS  PubMed  Article  Google Scholar 

  38. Ghimire SR, Charlton ND, Bell JD, Krishnamurthy YL, Craven KD (2011) Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Divers 47:19–27

    Article  Google Scholar 

  39. Glauser G, Gindro K, Fringeli J, De Joffrey J-P, Rudaz S, Wolfender J-L (2009) Differential analysis of mycoalexins in confrontation zones of grapevine fungal pathogens by ultrahigh pressure liquid chromatography/time-of-flight mass spectrometry and capillary nuclear magnetic resonance. J Agric Food Chem 57:1127–1134

    CAS  PubMed  Article  Google Scholar 

  40. González V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42

    Article  Google Scholar 

  41. Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implication of their occurrence. J Nat Prod 69:509–526

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. Guo B, Wang Y, Sun X, Tang K (2008) Bioactive natural products from endophytes: a review. Appl Biochem Microbiol 44:136–142

    CAS  Article  Google Scholar 

  43. Halmschlager E, Butin H, Donabauer E (1993) Endophytic fungi in leaves and twigs of Quercus petrea. Eur J For Pathol 23:51–63

    Article  Google Scholar 

  44. Harper JK, Arif AM, Ford EJ, Strobel GA Jr, Porco JA, Tomer DP, Oneill KL, Heider EM, Grant DM (2003) Pestacin: a 1,3-dihydro isobenzofuran from Pestalotiopsis microspora possessing antioxidant and antimycotic activities. Tetrahedron 59:2471–2476

    CAS  Article  Google Scholar 

  45. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    CAS  PubMed  Article  Google Scholar 

  46. Hendry SJ, Boddy L, Lonsdale D (2002) Abiotic variables effect differential expression of latent infections in beech (Fagus sylvatica). New Phytol 155:449–460

    Article  Google Scholar 

  47. Hensens OD, Ondeyka JG, Dombrowski AW, Ostlind DA, Zink DL (1999) Isolation and structure of nodulisporic acid A1 and A2, novel insecticides from a Nodulisporium sp. Tetrahedron Lett 40:5455–5458

    CAS  Article  Google Scholar 

  48. Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    CAS  PubMed  Article  Google Scholar 

  49. Herrera-Carillo Z, Torres MS, Singh AP, Vorsa N, Gianfagna T, Meyer W, White JF Jr (2009) Phenolic, flavonoid and antioxidant profiling for cool-season grasses with and without endophyte. Proceedings of the 18th Annual Rutgers Turfgrass Symposium. Rutgers University, New Brunswick, p 43

    Google Scholar 

  50. Higgins KL, Arnold AE, Miadlikowska J, Sarvate SD, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555

    CAS  PubMed  Article  Google Scholar 

  51. Ho WH, To PC, Hyde KD (2003) Induction of antibiotic production of freshwater fungi using mix-culture fermentation. Fungal Divers 12:45–51

    Google Scholar 

  52. Hoffman MT, Arnold AE (2008) Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycol Res 112:331–344

    CAS  PubMed  Article  Google Scholar 

  53. Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 90:248–253

    CAS  PubMed  Article  Google Scholar 

  54. Huang W-Y, Cai Y-Z, Hyde KD, Corke H, Sun M (2007a) Endophytic fungi from Nerium oleander L (Apocynaceae): main constituents and antioxidant activity. World J Microbiol Biotechnol 23:1253–1263

    CAS  Article  Google Scholar 

  55. Huang W-Y, Cai Y-Z, Xing J, Corke H, Sun M (2007b) A potential antioxidant resource: endophytic fungi from medicinal plants. Econ Bot 61:14–30

    CAS  Article  Google Scholar 

  56. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

    Google Scholar 

  57. Hynes MJ (1975) Studies on the role of the AreA gene in the regulation of nitrogen catabolism in Aspergillus nidulans. Aust J Biol Sci 28:301–313

    CAS  PubMed  Article  Google Scholar 

  58. Jeewon R, Liew ECY, Hyde KD (2004) Phylogenetic evaluation of species nomenclature of Pestalotiopsis in relation to host association. Fungal Divers 17:39–55

    Google Scholar 

  59. Kaneko R, Kaneko S (2004) The effect of bagging branches on levels of endophytic fungal infection in Japanese beech leaves. For Pathol 34:65–78

    Article  Google Scholar 

  60. Kogel K-H, Franken P, Hückelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363

    PubMed  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  62. Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Divers 17:69–90

    CAS  Google Scholar 

  63. Kumaresan V, Suryanarayanan TS (2002) Endophyte assemblages in young, mature and senescent leaves of Rhizophora apiculata: evidence for the role of endophytes in mangrove litter degradation. Fungal Divers 9:81–91

    Google Scholar 

  64. Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71:159–162

    CAS  PubMed  Article  Google Scholar 

  65. Kusari S, Lamshöft M, Spiteller M (2009a) Aspergillus fumigatus Fresenius, an endophytic fungus from Juniperus communis L Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. J Appl Microbiol 107:1019–1030

    CAS  PubMed  Article  Google Scholar 

  66. Kusari S, Zühlke S, Spiteller M (2009b) An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J Nat Prod 72:2–7

    CAS  PubMed  Article  Google Scholar 

  67. Kwak S-S, Choi M-S, Park Y-G, Yoo J-S, Liu J-R (1995) Taxol content in the seeds of Taxus spp. Phytochemistry 40:29–32

    CAS  Article  Google Scholar 

  68. Lehtonen P, Helander M, Wink M, Sporer F, Saikkonen K (2005) Transfer of endophyte origin defensive alkaloids from a grass to hemiparasitic plant. Ecol Lett 8:1256–1263

    Article  Google Scholar 

  69. 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 20:259–264

    CAS  Article  Google Scholar 

  70. Li LY, Scattler I, Deng ZW, Groth I, Walther G, Menzel K-D, Peschel G, Grabley S, Lin WH (2008) A-seco-oleane-type triterpenes from Phomopsis sp. (strain HKI0458) isolated from the mangrove plant Hibiscus tiliaceus. Phytochemistry 69:511–517

    CAS  PubMed  Article  Google Scholar 

  71. Lingqi Z, Bo G, Haiyan L, Songrong Z, Hua S, Su G, Rongcheng W (2000) Preliminary study on the isolation of endophytic fungus of Catharanthus roseus and its fermentation to produce products of therapeutic value. Zhong Cao Yao 31:805–807

    Google Scholar 

  72. Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. J Ind Microbiol Biotechnol 36:1171–1177

    CAS  PubMed  Article  Google Scholar 

  73. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant—three way symbiosis required for thermal tolerance. Science 315:513–515

    PubMed  Article  CAS  Google Scholar 

  74. Martin JF (2000) Molecular control of expression of penicillin biosynthesis genes in fungi: regulatory proteins interact with a bidirectional promoter region. J Bacteriol 182:2355–2362

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. Martìnez-Luis S, Della-Togna G, Coley PD, Kursar TA, Gerwick WH, Cubilla-Rios L (2008) Antileishmanial constituents of the Panamanian endophytic fungus Edenia sp. J Nat Prod 71:2011–2014

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  76. Meinke PT, Colletti SL, Fisher MH, Wyvratt MJ, Shih TL, Ayer MB, Li C, Lim J, Ok D, Salva S, Warmke LM, Zakson M, Michael BF, deMontigny P, Ostlind DA, Fink D, Drag M, Schmatz DM, Shoop WL (2009) Discovery of the development candidate N-tert-butyl nodulisporamide: a safe and efficacious once monthly oral agent for the control of fleas and ticks on companion animals. J Med Chem 52:3505–3515

    CAS  PubMed  Article  Google Scholar 

  77. Metz A, Haddad A, Worapong J, Long D, Ford E, Hess WM, Strobel GA (2000) Induction of the sexual stage of Pestalotiopsis microspora, a taxol producing fungus. Microbiology 146:2079–2089

    CAS  PubMed  Article  Google Scholar 

  78. Moricca S, Ragazzi A (2008) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology 98:380–386

    CAS  PubMed  Article  Google Scholar 

  79. Motyl MR, Tan C, Liberator P, Giacobbe R, Racine F, Hsu M, Nielsen-Kahn J, Douglan C, Bowman J, Hammond M, Balkovec J, Greenlee M, Meng D, Parker D, Peel M, Fan W, Mamai A, Hong J, Orr M, Ouvray G, Perrey D, Liua H, Jones M, Nelson K, Ogbu C, Lee S, Li K, Kirwan R, Note A, Sligar J, Martensen P (2010) MK-3118, an oral enfumafungin with potent in vitro activity against Candida and Aspergillus spp. 50th Interscience Conference on Antimicrobial Agents and Chemotherapy F1–847

  80. Müller MM, Valjakka R, Suokko A, Hantula J (2001) Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol Ecol 10:1801–1810

    PubMed  Article  Google Scholar 

  81. Murali TS, Suryanarayanan TS, Geeta R (2006) Endophytic Phomopsis species: host range and implications for diversity estimates. Can J Microbiol 52:673–680

    CAS  PubMed  Article  Google Scholar 

  82. Nadeem M, Rikhari HC, Kumar A, Palni LMS, Nandi SK (2002) Taxol content in the bark of Himalayan Yew in relation to tree age and sex. Phytochemistry 60:627–631

    CAS  PubMed  Article  Google Scholar 

  83. Oh D-C, Kauffman CA, Jensen PR, Fenical W (2007) Induced production of emericellamides A and B from the marine-derived fungus Emericella sp. in competing co-culture. J Nat Prod 70:515–520

    CAS  PubMed  Article  Google Scholar 

  84. Ondeyka JG, Helms GL, Hensens OD, Goetz MA, Zink DL, Tsipouras A, Shoop WL, Slayton L, Dombrowski AW, Polishook JD, Ostlind DA, Tsou NN, Ball RG, Singh SB (1997) Nodulisporic acid A, a novel and potent insecticide from a Nodulisporium sp. isolation, structure determination, and chemical transformations. J Am Chem Soc 119:8809–8816

    CAS  Article  Google Scholar 

  85. Onishi J, Meinz M, Thompson J, Curotto J, Dreikorn S, Rosenbach M, Douglas C, Abruzzo G, Flattery A, Kong L, Cabello A, Vicente F, Pelaez F, Diez MT, Martin I, Bills G, Giacobbe R, Dombrowski A, Schwartz R, Morris S, Harris G, Tsipouras A, Wilson K, Kurtz MB (2000) Discovery of novel antifungal (1,3)-β-D-glucan synthase inhibitors. Antimicrob Agents Chemother 44:368–377

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. 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 33:77–86

    Google Scholar 

  87. Pandey AK, Reddy MS, Suryanarayanan TS (2003) ITS-RFLP and ITS sequence analysis of a foliar endophytic Phyllosticta from different tropical trees. Mycol Res 107:439–444

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  88. Pang K-L, Vrijmoed LLP, Goh TK, Plaingam N, Jones EBG (2008) Fungal endophytes associated with Kandelia candel (Rhizophoraceae) in Mai Po Nature Reserve, Hong Kong. Bot Mar 51:171–178

    Article  Google Scholar 

  89. 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 3:338–346

    Article  Google Scholar 

  90. Peláez F, Cabello A, Platas G, Díez MT, González A, Basilio A, Martín I, Vincente F, Bills GF, Giacobbe RA, Schwartz RE, Onishi JC, Meinz MS, Arbruzzo GK, Flattery AM, Kong L, Kurtz MB (2000) The discovery of enfumafungin, a novel antifungal compound produced by endophytic Hormonema species, biological activity, and taxonomy of the producing organisms. Syst Appl Microbiol 23:333–343

    PubMed  Article  Google Scholar 

  91. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197

    Google Scholar 

  92. Pettit RK (2009) Mixed fermentation for natural product drug discovery. Appl Microbiol Biotechnol 83:19–25

    CAS  PubMed  Article  Google Scholar 

  93. Priti V, Ramesha BT, Singh S, Ravikanth G, Ganeshaiah KN, Suryanarayanan TS, Shaanker RU (2009) How promising are endophytic fungi as alternative sources of plant secondary metabolites? Curr Sci 97:477–478

    Google Scholar 

  94. Puri SC, Verma V, Amna T, Qazi GN, Spiteller M (2005) An endophytic fungus from Nothapodytes foetida that produces camptothecin. J Nat Prod 68:1717–1719

    CAS  PubMed  Article  Google Scholar 

  95. Puri SC, Nazir A, Chawla R, Arora R, Riyaz-Ul-Hasan S, Amna T, Ahmed B, Verma V, Singh S, Sagar R, Sharma A, Kumar R, Sharma RK, Qazi GN (2006) The endophytic fungus Trametes hirsuta as a novel alternative source of podophyllotoxin and related aryl tetralin lignans. J Biotechnol 122:494–510

    CAS  PubMed  Article  Google Scholar 

  96. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716

    Article  Google Scholar 

  97. Redman RS, Sheehan KB, Stout TG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581

    CAS  PubMed  Article  Google Scholar 

  98. Richardson MD, Chapman GW, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-infected tall fescue. Crop Sci 32:1060–1061

    CAS  Article  Google Scholar 

  99. Rocha ACS, Garcia D, Uetanabaro APT, Carneiro RTO, Araújo IS, Mattos CRR, Góes-Neto A (2011) Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Divers 47:75–84

    Article  Google Scholar 

  100. Rodrigues KF, Samuels GJ (1999) Fungal endophytes of Spondias mombin leaves in Brazil. J Basic Microbiol 39:131–135

    Article  Google Scholar 

  101. 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 59:1109–1114

    CAS  PubMed  Article  Google Scholar 

  102. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME Nat 2:404–416

    Article  Google Scholar 

  103. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    CAS  PubMed  Article  Google Scholar 

  104. Roncal T, Cordobés S, Sterner O, Ugalde U (2002) Conidiation in Penicillium cyclopium is induced by conidiogenone, an endogenous diterpene. Eukaryot Cell 1:823–829

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. Rudgers JA, Koslow JM, Clay K (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol Lett 7:42–51

    Article  Google Scholar 

  106. Sabzalian MR, Mirlohi A (2010) Neotyphodium endophytes trigger salt resistance in tall and meadow fescues. J Plant Nutr Soil Sci 173:952–957

    Article  CAS  Google Scholar 

  107. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74

    Article  Google Scholar 

  108. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  109. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9:275–280

    CAS  PubMed  Article  Google Scholar 

  110. Schardl CL, Liu J-S, White JF, Finkel RA, An Z, Siegel MR (1991) Molecular phylogenetic relationships of nonpathogenic grass mycosymbionts and clavicipitaceous plant pathogens. Plant Syst Evol 178:27–41

    CAS  Article  Google Scholar 

  111. Schroeckh V, Scherlach K, Nützmann H-W, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA 106:14558–14563

    CAS  PubMed  Article  Google Scholar 

  112. Schulz B, Boyle C, Draeger S, Römmert A-K, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004

    CAS  Article  Google Scholar 

  113. Schwartz RE, Smith SK, Onishi JC, Meinz M, Kurtz MB, Giacobbe RA, Wilson KE, Liesch J, Zink D, Horn W, Morris S, Cabello A, Vicente F (2000) The isolation and structure determination of enfumafungin, a triterpene glycoside antifungal agent from the fermentation of a Hormonema sp. J Am Chem Soc 122:4882–4886

    CAS  Article  Google Scholar 

  114. Shwab EK, Keller NP (2008) Regulation of secondary metabolite production in filamentous ascomycetes. Mycol Res 112:225–230

    CAS  PubMed  Article  Google Scholar 

  115. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89

    Article  Google Scholar 

  116. Sieber T, Hugentobler C (1987) Endophytic fungi in leaves and twigs of healthy and diseased beech trees (Fagus sylvatica L.). Eur J For Pathol 17:411–425

    Article  Google Scholar 

  117. Staniek A, Woerdenbag HJ, Kayser O (2008) Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery. J Plant Interact 3:75–93

    CAS  Article  Google Scholar 

  118. Stierle A, Stobel 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

    CAS  PubMed  Article  Google Scholar 

  119. Stierle A, Strobel GA, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260:214–216

    CAS  PubMed  Article  Google Scholar 

  120. Strobel GA (2002) Microbial gifts from rain forests. Can J Plant Pathol 24:14–20

    Article  Google Scholar 

  121. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. Strobel GA, Hess WM, Ford E, Sidhu RS, Yang X (1996a) Taxol from fungal endophytes and the issue of biodiversity. J Ind Microbiol 17:417–423

    CAS  Google Scholar 

  123. Strobel GA, Yang X, Sears J, Kramer R, Sidhu R, Hess WM (1996b) Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallachiana. Microbiology 142:435–440

    CAS  PubMed  Article  Google Scholar 

  124. Strobel G, Ford E, Worapong J, Harper JK, Arif AM, Grant DM, Fung PCW, Chau RMW (2002) Isopestacin, an isobenzofuranone from Pestalotiopsis microspora, possessing antifungal and antioxidant activities. Phytochemistry 60:179–183

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  125. Sun X, Guo L-D, Hyde KD (2011) Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47:85–95

    Article  Google Scholar 

  126. Suryanarayanan TS, Vijaykrishna D (2001) Fungal endophytes of aerial roots of Ficus benghalensis. Fungal Divers 8:155–161

    Google Scholar 

  127. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19

    Article  Google Scholar 

  128. Susan DC (2004) Endophytic-host selectivity of Discula umbrinella on Quercus alba and Quercus rubra characterized by infection, pathogenicity and mycelial compatibility. Eur J Plant Pathol 110:713–721

    Article  Google Scholar 

  129. Szewczyk E, Chiang Y-M, Oakley CE, Davidson AD, Wang CCC, Oakley BR (2008) Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans. Appl Environ Microbiol 74:7607–7612

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  130. Tabet N (2006) Acetylcholinesterase inhibitors for Alzheimer’s disease: anti-inflammatories in acetylcholine clothing! Age Ageing 35:336–338

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  131. Tag A, Hicks J, Garifullina G, Ake C Jr, Phillips TD, Beremand M, Keller NP (2000) G-protein signaling mediates differential production of toxic secondary metabolites. Mol Microbiol 38:658–665

    CAS  PubMed  Article  Google Scholar 

  132. Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459

    CAS  PubMed  Article  Google Scholar 

  133. Tejesvi MV, Kajula M, Mattila S, Pirttilä AM (2011) Bioactivity and genetic diversity of endophytic fungi in Rhododendron tomentosum Harmaja. Fungal Divers 47:97–107

    Article  Google Scholar 

  134. Tilburn J, Sarkar S, Widdick DA, Espeso EA, Orejas M, Mungroo J, Penalva MA, Arst HN Jr (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J 14:779–790

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  135. Torres MS, Singh AP, Shah S, Herrera-Carrillo Z, Gianfagna T, White JF Jr, Vorsa N (2009) LC-MS-MS identification and quantification of phenolics in symbiotic tall fescue. Proceedings of the 18th Annual Rutgers Turfgrass Symposium. Rutgers University, New Brunswick, p 54

    Google Scholar 

  136. Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–118

    CAS  PubMed  Article  Google Scholar 

  137. Unterseher M, Schnittler M (2009) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)—different cultivation techniques influence fungal biodiversity assessment. Mycol Res 113:645–654

    PubMed  Article  Google Scholar 

  138. Unterseher M, Schnittler M (2010) Species richness analysis and ITS rDNA phylogeny revealed the majority of cultivable foliar endophytes from beech (Fagus sylvatica). Fungal Ecol 3:366–378

    Article  Google Scholar 

  139. Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, Infante F, Castillo A, Arnold AE (2010) Fungal endophyte diversity in coffee plants from Colombia, Hawai’i, Mexico and Puerto Rico. Fungal Ecol 3:122–138

    Article  Google Scholar 

  140. Verma VC, Kharwar RN, Strobel GA (2009) Chemical and functional diversity of natural products from plant associated endophytic fungi. Nat Prod Commun 4:1511–1532

    CAS  PubMed  Google Scholar 

  141. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Von Wettstein D, Franken P, Kogel K-H (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    CAS  PubMed  Article  Google Scholar 

  142. 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 193:249–253

    CAS  PubMed  Article  Google Scholar 

  143. Wang F-W, Ye Y-H, Ding H, Chen Y-X, Tan R-X, Song Y-C (2010) Benzophenones from Guignardia sp. IFB-E028, an endophyte on Hopea hainanensis. Chem Biodivers 7:216–220

    CAS  PubMed  Article  Google Scholar 

  144. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254

    CAS  PubMed  Article  Google Scholar 

  145. White JF Jr, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446

    CAS  PubMed  Article  Google Scholar 

  146. Wijeratne EMK, Paranagama PA, Marron MT, Gunatilaka MK, Arnold AE, Gunatilaka AAL (2008) Sesquiterpene quinones and related metabolites from Phyllosticta spinarum, a fungal strain endophytic in Platycladus orientalis of the Sonoran desert. J Nat Prod 71:218–222

    CAS  PubMed  Article  Google Scholar 

  147. Wink M (2008) Plant secondary metabolism: diversity, function and its evolution. Nat Prod Commun 3:1205–1216

    CAS  Google Scholar 

  148. Yang Z, Rogers LM, Song Y, Guo W, Kolattukudy PE (2005) Homoserine and asparagine are host signals that trigger in planta expression of a pathogenesis gene in Nectria haematococca. Proc Natl Acad Sci USA 102:4197–4202

    CAS  PubMed  Article  Google Scholar 

  149. Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, Bryan GT, Saikia S, Scott B (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43:679–693

    CAS  PubMed  Article  Google Scholar 

  150. Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771

    CAS  PubMed  Article  Google Scholar 

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Acknowledgment

P.P. wishes to thank BMBF (Bundesministerium für Bildung und Forschung) for continued support.

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Aly, A.H., Debbab, A. & Proksch, P. Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90, 1829–1845 (2011). https://doi.org/10.1007/s00253-011-3270-y

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Keywords

  • Endophytic fungi
  • Host plants
  • Diversity
  • Host specificity
  • Bioactive secondary metabolites