Abstract
Endophytic fungi are a group of mutualistic fungi harbored in plant tissues that are known to provide a plethora of fitness benefits to host plants. It is now firmly established that fungal endophytes have a remarkable capability to produce bioactive secondary metabolites including valuable pharmaceutically relevant agents. Unfortunately, efforts to utilize endophytic fungi as sustainable microbial resources for industrial production of compounds have not yet been successful. Recent studies have revealed that endophytic fungi not only interact with their host plant but also engage in complex communication strategies with associated macro- and microorganisms in order to survive and function in their natural habitat. These multifaceted interactions are difficult to introduce and maintain in vitro under artificial fermentation conditions in the laboratory. Our emerging knowledge on the complex interaction between endophytic fungi and associated organisms as well as the host plants provides a silver lining toward industrial exploitation of endophytes. Herein, we highlight the importance of endophytes (particularly endophytic fungi) in plant-microbe associations and discuss future strategies that might be employed to investigate the chemical communication within endophytic microbial communities, which can lead the way toward sustainable industrial production of important compounds using endophytic fungi.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ajikumar PK, Xiao W-H, Tyo KEJ, Wang Y, Simeon F, Leonard E et al (2010) Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70–74
Albuquerque P, Casadevall A (2012) Quorum sensing in fungi—a review. Med Mycol 50:337–345
Arabiodopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arbidopsis interactome map. Science 333:601–607
Arkin AP, Schaffer DV (2011) Network news: innovations in 21st century systems biology. Cell 144:844–849
Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J et al (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464
Bandara HMHN, Lam OLT, Jin LJ, Samaranayake L (2012) Microbial chemical signaling: a current perspective. Crit Rev Microbiol 38:217–249
Bertrand S, Schumpp O, Bohni N, Monod M, Gindro K, Wolfender JL (2013) De novo production of metabolites by fungal co-culture of Trichophyton rubrum and Bionectria ochroleuca. J Nat Prod 76:1157–1165
Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. ChemBioChem 3:619–627
Cano J, Guarro J, Gené J (2004) Molecular and morphological identification of Colletotrichum species of clinical interest. J Clin Microbiol 42:2450–2454
Chithra S, Jasim B, Sachidanandan P, Jyothis M, Radhakrishnan EK (2014) Piperine production by endophytic fungus Colletotrichum gloeosporioides isolated from Piper nigrum. Phytomedicine 21:534–540
Christian N, Whitaker BK, Clay K (2015) Microbiomes: unifying animal and plant systems through the lens of community ecology theory. Front Microbiol 6:869
Clay K, Cheplick GP (1989) Effect of ergot alkaloids from fungal endophyte-infected grasses on fall armyworm (Spodoptera frugiperda). J Chem Ecol 15:169–182
Cui Y, Yi D, Bai X, Sun B, Zhao Y, Zhang Y (2012) Ginkgolide B produced endophytic fungus (Fusarium oxysporum) isolated from Ginkgo biloba. Fitoterapia 83:913–920
Dandekar AA, Chugani S, Greenberg EP (2012) Bacterial quorum sensing and metabolic incentives to cooperate. Science 338:264–266
Deng Y, Wu J, Tao F, Zhang LH (2011) Listening to a new language: DSF-based quorum sensing in gram-negative bacteria. Chem Rev 111:160–173
Dong L-H, Fan S-W, Ling Q-Z, Huang B-B, Wei Z-J (2014) Indentification of huperzine A-producing endophytic fungi isolated from Huperzia serrata. World J Microbiol Biotechnol 30:1011–1017
Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180:190–195
Eldar A (2011) Social conflict drives the evolutionary divergence of quorum sensing. Proc Natl Acad Sci 108:13635–13640
El-Elimat T, Raja HA, Graf TN, Faeth SH, Cech NB, Oberlies NH (2014) Flavonolignans from Aspergillus iizukae, a fungal endophyte of milk thistle (Silybum marianum). J Nat Prod 77:193–199
Esquenazi E, Yang YL, Watrous J, Gerwick WH, Dorrestein PC (2009) Imaging mass spectrometry of natural products. Nat Prod Rep 26:1521–1534
Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69:1121–1124
Feldman M, Al-Quntar A, Polacheck I, Friedman M, Steinberg D (2014) Therapeutic potential of thiazolidinedione-8 as an antibiofilm agent against Candida albicans. PLoS ONE 9:e93225
Flores-Bustamante ZR, Rivera-Orduña FN, MartÃnez-Cárdenas A, Flores-Cotera LB (2010) Microbial paclitaxel: Advances and perspectives. J Antibiot (Tokyo) 63:460–467
Freeman S, Rodriguez RJ (1993) Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78
Goh CH, Vallejos DFV, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39:826–839
Grice CM, Bertuzzi M, Bignell EM (2013) Receptor-mediated signaling in Aspergillus fumigatus. Front Microbiol 4:26
Hao X, Pan J, Zhu X (2013) Taxol producing fungi. Natural products. Springer, Berlin Heidelberg, pp 2797–2812
Howat S, Park B, Oh IS, Jin Y-W, Lee E-K, Loake GJ (2014) Paclitaxel: biosynthesis, production and future prospects. N Biotechnol 31:242–245
Huang Q, Roessner CA, Croteau R, Scott AI (2001) Engineering Escherichia coli for the synthesis of taxadiene, a key intermediate in the biosynthesis of taxol. Bioorganic Med Chem 9:2237–2242
Huxtable RJ (1992) The pharmacology of extinction. J Ethnopharmacol 37:1–11
Jennewein S, Park H, DeJong JM, Long RM, Bollon AP, Croteau RB (2005) Coexpression in yeast of taxus cytochrome P450 reductase with cytochrome p450 oxygenases involved in taxol biosynthesis. Biotechnol Bioeng 89:588–598
Kharwar RN, Mishra A, Gond SK, Stierle A, Stierle D (2011) Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat Prod Rep 28:1208–1228
Kim G, LeBlanc ML, Wafula EK, DePamphilis CW, Westwood JH (2014) Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–811
Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363
Kumar A, Patil D, Rajamohanan PR, Ahmad A (2013) Isolation, purification and characterization of vinblastine and vincristine from endophytic fungus Fusarium oxysporum isolated from Catharanthus roseus. PLoS ONE 8:e71805
Kusari S, Spiteller M (2011) Are we ready for industrial production of bioactive plant secondary metabolites utilizing endophytes? Nat Prod Rep 28:1203–1207
Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71:159–162
Kusari S, Zühlke S, Košuth J, Čellárová E, Spiteller M (2009a) Light-independent metabolomics of endophytic Thielavia subthermophila provides insight into microbial hypericin biosynthesis. J Nat Prod 72:1825–1835
Kusari S, Zühlke S, Spiteller M (2009b) An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J Nat Prod 72:2–7
Kusari S, Zühlke S, Spiteller M (2011) Effect of artificial reconstitution of the interaction between the plant Camptotheca acuminata and the fungal endophyte Fusarium solani on camptothecin biosynthesis. J Nat Prod 74:764–775
Kusari S, Hertweck C, Spiteller M (2012a) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798
Kusari S, Verma VC, Lamshöft M, Spiteller M (2012b) An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J Microbiol Biotechnol 28:1287–1294
Kusari S, Lamshöft M, Kusari P, Gottfried S, Zühlke S, Louven K et al (2014a) Endophytes are hidden producers of maytansine in Putterlickia roots. J Nat Prod 77:2577–2584
Kusari S, Singh S, Jayabaskaran C (2014b) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303
Kusari S, Singh S, Jayabaskaran C (2014c) Rethinking production of Taxol® (paclitaxel) using endophyte biotechnology. Trends Biotechnol 32:304–311
Kusari P, Kusari S, Spiteller M, Kayser O (2015) Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology. Appl Microbiol Biotechnol 99:5383–5390
Kusari P, Kusari S, Eckelmann D, Zühlke S, Kayser O, Spiteller M (2016) Cross-species biosynthesis of maytansine in Maytenus serrata. RSC Adv 6:10011–10016
Lahrmann U, Zuccaro A (2012) Opprimo ergo sum–evasion and suppression in the root endophytic fungus Piriformospora indica. Mol Plant Microbe Interact 25:727–737
Li SM (2010) Prenylated indole derivatives from fungi: structure diversity, biological activities, biosynthesis and chemoenzymatic synthesis. Nat Prod Rep 27:57–78
Li YF, Tsai KJS, Harvey CJB, Li JJ, Ary BE, Berlew EE et al (2016) Comprehensive curation and analysis of fungal biosynthetic gene clusters of published natural products. Fungal Genet Biol. doi:10.1016/j.fgb.2016.01.012
Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP et al (2015) A new antibiotic kills pathogens without detectable resistance. Nature 517:455–459
Luo Y, Li BZ, Liu D, Zhang L, Chen Y, Jia B et al (2015) Engineered biosynthesis of natural products in heterologous hosts. Chem Soc Rev 44:5265–5290
Lyons PC, Plattner RD, Bacon CW (1986) Occurrence of peptide and clavine ergot alkaloids in tall fescue grass. Science 232:487–489
Mallick EM, Bennett RJ (2013) Sensing of the microbial neighborhood by Candida albicans. PLoS Pathog 9:e1003661
Newman DJ, Cragg GM (2016) Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79:629–661
Nickerson KW, Atkin AL, Hornby JM (2006) Quorum sensing in dimorphic fungi: farnesol and beyond. Appl Environ Microbiol 72:3805–3813
Nisa H, Kamili AN, Nawchoo IA, Shafi S, Shameem N, Bandh SA (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microb Pathog 82:50–59
Nongkhlaw FMW, Joshi SR (2016) Horizontal gene transfer of the non-ribosomal peptide synthetase gene among endophytic and epiphytic bacteria associated with ethnomedicinal plants. Curr Microbiol 72:1–11
Oh DC, 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
Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D et al (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496:528–532
Parthasarathy R, Sathiyabama M (2014) Gymnemagenin-producing endophytic fungus isolated from a medicinal plant Gymnema sylvestre R.Br. Appl Biochem Biotechnol 172:3141–3152
Partida-MartÃnez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100
Photita W, Taylor PWJ, Ford R, Hyde KD, Lumyong S (2005) Morphological and molecular characterization of Colletotrichum species from herbaceous plants in Thailand. Fungal Divers 18:117–133
Pu X, Qu X, Chen F, Bao J, Zhang G, Luo Y (2013) Camptothecin-producing endophytic fungus Trichoderma atroviride LY357: Isolation, identification, and fermentation conditions optimization for camptothecin production. Appl Microbiol Biotechnol 97:9365–9375
Puri SC, Nazir A, Chawla R, Arora R, Riyaz-ul-Hasan S, Amna T et al (2006) The endophytic fungus Trametes hirsuta as a novel alternative source of podophyllotoxin and related aryl tetralin lignans. J Biotechnol 122:494–510
Puri SG, Verma V, Amna T, Qazi GN, Spiteller M (2005) An endophytic fungus from Nothapodytes foetida that produces camptothecin. J Nat Prod 68:1717–1719
Redman RS, Ranson JC, Rodriguez RJ (1999) Conversion of the pathogenic fungus Colletotrichum magna to a nonpathogenic, endophytic mutualist by gene disruption. Mol Plant-Microbe Interact 12:969–975
Rehman S, Shawl AS, Kour A, Andrabi R, Sudan P, Sultan P et al (2008) An endophytic Neurospora sp. from Nothapodytes foetida producing camptothecin. Appl Biochem Micro 44:203–209
Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968
Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci 112:E5013–E5020
Schaefer AL, Greenberg EP, Oliver CM, Oda Y, Huang JJ, Bittan-Banin G et al (2008) A new class of homoserine lactone quorum-sensing signals. Nature 454:595–599
Scherlach K, Hertweck C (2009) Triggering cryptic natural product biosynthesis in microorganisms. Org Biomol Chem 7:1753–1760
Shu S, Zhao X, Wang W, Zhang G, Cosoveanu A, Ahn Y et al (2014) Identification of a novel endophytic fungus from Huperzia serrata which produces huperzine A. World J Microbiol Biotechnol 30:3101–3109
Shweta S, Gurumurthy BR, Ravikanth G, Ramanan US, Shivanna MB (2013) Endophytic fungi from Miquelia dentata Bedd., produce the anti-cancer alkaloid, camptothecine. Phytomedicine 20:337–342
Soen Y (2014) Environmental disruption of host-microbe co-adaptation as a potential driving force in evolution. Front Genet 5:168
Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of pacific yew. Science 260:214–216
Su J, Yang M (2015) Huperzine A production by Paecilomyces tenuis YS-13, an endophytic fungus isolated from Huperzia serrata. Nat Prod Res 29:1035–1041
Suryanarayanan TS (2013) Endophyte research: going beyond isolation and metabolite documentation. Fungal Ecol 6:561–568
Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19
Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459
Tanaka A, Takemoto D, Chujo T, Scott B (2012) Fungal endophytes of grasses. Curr Opin Plant Biol 15:462–468
von Maltzahn G, Flavell RB, Toledo GV, Leff JW, Samayoa P, Marquez LM et al. (2016) Endophytes, associated compositions, and methods of use thereof. United States Patent Application 20160021891
Wada-Katsumata A, Zurek L, Nalyanya G, Roelofs WL, Zhang A, Schal C (2015) Gut bacteria mediate aggregation in the German cockroach. Proc Natl Acad Sci 112:15678–15683
Wang Y, Zeng QG, Zhang ZB, Yan RM, Wang LY, Zhu D (2011) Isolation and characterization of endophytic huperzine A-producing fungi from Huperzia serrata. J Ind Microbiol Biotechnol 38:1267–1278
Wang XJ, Min CL, Ge M, Zuo RH (2014) An endophytic sanguinarine-producing fungus from Macleaya cordata, Fusarium proliferatum BLH51. Curr Microbiol 68:336–341
Wang WX, Kusari S, Sezgin S, Lamshöft M, Kusari P, Kayser O et al (2015) Hexacyclopeptides secreted by an endophytic fungus Fusarium solani N06 act as crosstalk molecules in Narcissus tazetta. Appl Microbiol Biotechnol 99:7651–7662
Wang WX, Kusari S, Laatsch H, Golz C, Kusari P, Strohmann C et al (2016) Antibacterial azaphilones from an endophytic fungus, Colletotrichum sp. BS4. J Nat Prod 79:704–710
Wever WJ, Bogart JW, Baccile JA, Chan AN, Schroeder FC, Bowers AA (2015) Chemoenzymatic synthesis of thiazolyl peptide natural products featuring an enzyme-catalyzed formal [4 + 2] cycloaddition. J Am Chem Soc 137:3494–3497
Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276
Xiong ZQ, Yang YY, Zhao N, Wang Y (2013) Diversity of endophytic fungi and screening of fungal paclitaxel producer from Anglojap yew. Taxus x media. BMC Microbiol 13:71
Xu Y, Masuko S, Takieddin M, Xu H, Liu R, Jing J et al (2011) Chemoenzymatic synthesis of homogeneous ultralow molecular weight heparins. Science 334:498–501
Yang YL, Xu Y, Straight P, Dorrestein PC (2009) Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 5:885–887
Youk H, Lim WA (2014) Secreting and sensing the same molecule allows cells to achieve versatile social behaviors. Science 343:1242782
Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, Bryan GT et al (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43:679–693
Zhang Q, Wei X, Wang J (2012) Phillyrin produced by Colletotrichum gloeosporioides, an endophytic fungus isolated from Forsythia suspensa. Fitoterapia 83:1500–1505
Zhang G, Wang W, Zhang X, Xia Q, Zhao X, Ahn Y et al (2015) De Novo RNA sequencing and transcriptome analysis of Colletotrichum gloeosporioides ES026 reveal genes related to biosynthesis of huperzine A. PLoS ONE 10:e0120809
Zhao XM, Wang ZQ, Shu SH, Wang WJ, Xu HJ, Ahn YJ et al (2013) Ethanol and methanol can improve huperzine A production from endophytic Colletotrichum gloeosporioides ES026. PLoS ONE 8:e61777
Zuck KM, Shipley S, Newman DJ (2011) Induced production of N-formyl alkaloids from Aspergillus fumigatus by co-culture with Streptomyces peucetius. J Nat Prod 74:1653–1657
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Wang, WX., Kusari, S., Spiteller, M. (2016). Unraveling the Chemical Interactions of Fungal Endophytes for Exploitation as Microbial Factories. In: Purchase, D. (eds) Fungal Applications in Sustainable Environmental Biotechnology. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-42852-9_14
Download citation
DOI: https://doi.org/10.1007/978-3-319-42852-9_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-42850-5
Online ISBN: 978-3-319-42852-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)