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Exploring the Benefits of Endophytic Fungi via Omics

  • Hasnahana Chetia
  • Debajyoti Kabiraj
  • Biju Bharali
  • Sunita Ojha
  • Manash Pratim Barkataki
  • Dharitri Saikia
  • Tinka Singh
  • Ponnala Vimal Mosahari
  • Pragya Sharma
  • Utpal BoraEmail author
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Endophytic fungi constitute a remarkably diverse, ubiquitous group of eukaryotes with the ability to synthesize secondary metabolites of clinical significance. Their presence has an advantageous effect on growth and health of host plants under duress. They have also been envisaged as a source of diverse medicinal compounds since the discovery of taxol, a prominent anti-cancer drug. In this chapter, we have discussed how resident endophytic fungi aids the host plant in tackling various forms of biotic and abiotic stresses. Their therapeutic potential, viz. cancer cytotoxicity, immunomodulatory, anti-parasitic and anti-pathogenic potential have also been reviewed here. This chapter also explores the plethora of literature available for genomics, metagenomics, transcriptomics, proteomics and metabolomics of endophytic fungi alongside their available web-resources. Applications of omics-based studies on these mutualistic biotrophs have been instrumental in discovery of many unanswered and novel aspects of their biosynthetic potential and overall biology. Data reservoir on fungal endophytes has been constantly growing over the past decades and this reservoir can pave the route of future exploration of these beneficial organisms in therapeutics, biology and evolution via emergent and evolving modes of analysis like machine learning and more.

References

  1. Adpressa DA, Loesgen S (2016) Bioprospecting chemical diversity and bioactivity in a marine derived Aspergillus terreus. Chem Biodivers 13(2):253–259PubMedCrossRefPubMedCentralGoogle Scholar
  2. Akiyama H, Fujii K, Yamasaki O, Oono T, Iwatsuki K (2001) Antibacterial action of several tannins against Staphylococcus aureus. J Antimicrob Chemother 48(4):487–491PubMedCrossRefPubMedCentralGoogle Scholar
  3. Ambrose KV, Belanger FC (2012) SOLiD-SAGE of endophyte-infected red fescue reveals numerous effects on host transcriptome and an abundance of highly expressed fungal secreted proteins. PLoS One 7(12):e53214PubMedPubMedCentralCrossRefGoogle Scholar
  4. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100(26):15649–15654. http://www.ncbi.nlm.nih.gov/pubmed/14671327 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Artanti N, Tachibana S, Kardono L, Sukiman H (2011) Screening of endophytic fungi having ability for antioxidative and α-glucosidase inhibitor activities isolated from Taxus sumatrana. Pak J Biol Sci 14(22):1019–1023PubMedCrossRefPubMedCentralGoogle Scholar
  6. Aschehoug ET, Callaway RM, Newcombe G, Tharayil N, Chen S (2014) Fungal endophyte increases the allelopathic effects of an invasive forb. Oecologia 175(1):285–291.  https://doi.org/10.1007/s00442-014-2891-0 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microbiol 34(5):576–581PubMedPubMedCentralGoogle Scholar
  8. Bacon CW, White JF, James F (2018) Biotechnology of endophytic fungi of grasses. CRC, Boca RatonCrossRefGoogle Scholar
  9. Bai Y, Chen B, Li M, Zhou Y, Ren S, Xu Q et al (2017) FPD: a comprehensive phosphorylation database in fungi. Fungal Biol 121(10):869–875PubMedCrossRefPubMedCentralGoogle Scholar
  10. Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G et al (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180(2):501–510. http://www.ncbi.nlm.nih.gov/pubmed/18681935 PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bashyal BP, Wellensiek BP, Ramakrishnan R, Faeth SH, Ahmad N, Gunatilaka AAL (2014) Altertoxins with potent anti-HIV activity from Alternaria tenuissima QUE1Se, a fungal endophyte of Quercus emoryi. Bioorg Med Chem 22(21):6112–6116PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bayat F, Mirlohi A, Khodambashi M (2009) Effects of endophytic fungi on some drought tolerance mechanisms of tall fescue in a hydroponics culture. Russ J Plant Physiol 56(4):510–516.  https://doi.org/10.1134/S1021443709040104 CrossRefGoogle Scholar
  13. Bonants P, Edema M, Robert V (2013) Q-bank, a database with information for identification of plant quarantine plant pest and diseases. EPPO Bull 43(2):211–215CrossRefGoogle Scholar
  14. Brakhage AA, Schuemann J, Bergmann S, Scherlach K, Schroeckh V, Hertweck C (2008) Activation of fungal silent gene clusters: a new avenue to drug discovery. In: Petersen F, Amstutz R (eds) Natural compounds as drugs. Progress in drug research, vol 66. Birkhäuser, Basel, pp 1–12CrossRefGoogle Scholar
  15. Channabasava, Govindappa M (2014) First report of anticancer agent, lapachol producing endophyte, Aspergillus niger of Tabebuia argentea and its in vitro cytotoxicity assays. Bangladesh J Pharmacol 9(1):129–139CrossRefGoogle Scholar
  16. Chaudhary VB, Rúa MA, Antoninka A, Bever JD, Cannon J, Craig A et al (2016) MycoDB, a global database of plant response to mycorrhizal fungi. Sci Data 3:160028PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111(1):89–97.  https://doi.org/10.1111/j.1469-8137.1989.tb04222.x CrossRefGoogle Scholar
  18. Clay K (1987) Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia 73(3):358–362.  https://doi.org/10.1007/BF00385251 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Clay K, Holah H (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Forensic Sci Int 285(5434):1742–1745. http://www.ncbi.nlm.nih.gov/pubmed/10481011 Google Scholar
  20. Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G (2004) MycoBank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22Google Scholar
  21. Cui J, Guo S, Xiao P (2011) Antitumor and antimicrobial activities of endophytic fungi from medicinal parts of Aquilaria sinensis. J Zhejiang Univ Sci B 12(5):385–392PubMedPubMedCentralCrossRefGoogle Scholar
  22. de Fávaro LCL, de Sebastianes FLS, Araújo WL (2012) Epicoccum nigrum P16, a sugarcane endophyte, produces antifungal compounds and induces root growth. PLoS One 7(6):e36826PubMedPubMedCentralCrossRefGoogle Scholar
  23. Desale MG, Bodhankar MG (2013) Antimicrobial activity of endophytic fungi isolated from Vitex negundo Linn. Int J Curr Microbiol App Sci 2(12):389–395Google Scholar
  24. Deshmukh SK, Mishra PD, Kulkarni-Almeida A, Verekar S, Sahoo MR, Periyasamy G et al (2009) Anti-inflammatory and anticancer activity of ergoflavin isolated from an endophytic fungus. Chem Biodivers 6(5):784–789PubMedCrossRefGoogle Scholar
  25. Dhankhar S, Dhankhar S, Parkash YJ (2013) Investigations towards new antidiabetic drugs from fungal endophytes associated with salvadora oleoides decne. Med Chem (Los Angeles) 9:624–632Google Scholar
  26. Du F-Y, Li X, Li X-M, Zhu L-W, Wang B-G (2017) Indolediketopiperazine alkaloids from Eurotium cristatum en-220, an endophytic fungus isolated from the marine alga Sargassum thunbergii. Mar Drugs 15(12):24PubMedCentralCrossRefGoogle Scholar
  27. Ekanayake PN, Rabinovich M, Guthridge KM, Spangenberg GC, Forster JW, Sawbridge TI (2013) Phylogenomics of fescue grass-derived fungal endophytes based on selected nuclear genes and the mitochondrial gene complement. BMC Evol Biol 13(1):270PubMedPubMedCentralCrossRefGoogle Scholar
  28. Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllumpeltatum produce podophyllotoxin. J Nat Prod 69(8):1121–1124PubMedCrossRefPubMedCentralGoogle Scholar
  29. Firrincieli A, Otillar R, Salamov A, Schmutz J, Khan Z, Redman RS et al (2015) Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1. Front Microbiol 6:978PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gangadevi V, Muthumary J (2009) Taxol production by Pestalotiopsis terminaliae, an endophytic fungus of Terminalia arjuna (arjun tree). Biotechnol Appl Biochem 52(1):9–15PubMedCrossRefPubMedCentralGoogle Scholar
  31. Gazis R, Kuo A, Riley R, LaButti K, Lipzen A, Lin J et al (2016) The genome of Xylona heveae provides a window into fungal endophytism. Fungal Biol 120(1):26–42PubMedCrossRefPubMedCentralGoogle Scholar
  32. Ghabooli M, Khatabi B, Ahmadi FS, Sepehri M, Mirzaei M, Amirkhani A et al (2013) Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J Proteome 94:289–301CrossRefGoogle Scholar
  33. Gianoulis TA, Griffin MA, Spakowicz DJ, Dunican BF, Alpha CJ, Sboner A et al (2012) Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet 8(3):e1002558PubMedPubMedCentralCrossRefGoogle Scholar
  34. Giridharan P, Verekar SA, Khanna A, Mishra PD, Deshmukh SK (2012) Anticancer activity of sclerotiorin, isolated from an endophytic fungus Cephalotheca faveolata Yaguchi, Nishim. and Udagawa. Indian J Exp Biol 50:464–468PubMedPubMedCentralGoogle Scholar
  35. Godstime O, Felix E, Jewo Augustina O, Christopher E (2014) Mechanisms of antimicrobial actions of phytochemicals against enteric pathogens – a review. J Pharm Chem Biol Sci 2(22):77–85Google Scholar
  36. Govindappa M, Sadananda TS, Channabasava, Ramachandra YL, Chandrappa CP, Padmalatha RS et al (2015) In vitro and in vivo antidiabetic activity of lectin (N-acetylgalactosamine, 64 kDa) isolated from endophytic fungi, Alternaria species from Viscum album on alloxan induced diabetic rats. Integr Obes Diabetes 1(1):11–19Google Scholar
  37. Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69(3):509–526. http://www.ncbi.nlm.nih.gov/pubmed/16562864 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Guo B, Dai J-R, Ng S, Huang Y, Leong C, Ong W et al (2000) Cytonic acids A and B: novel tridepside inhibitors of hCMV protease from the endophytic fungus Cytonaema species. J Nat Prod 63(5):602–604PubMedCrossRefPubMedCentralGoogle Scholar
  39. Guo Z, Gai C, Cai C, Chen L, Liu S, Zeng Y et al (2017) Metabolites with insecticidal activity from Aspergillus fumigatus JRJ111048 isolated from mangrove plant acrostichum specioum endemic to hainan island. Mar Drugs 15(12):381PubMedCentralCrossRefGoogle Scholar
  40. Hua MDS, Senthil Kumar R, Shyur LF, Cheng Y Bin, Tian Z, Oelmüller R, et al (2017) Metabolomic compounds identified in Piriformospora indica-colonized chinese cabbage roots delineate symbiotic functions of the interaction. Sci Rep 7(1)Google Scholar
  41. Jalgaonwala RE, Mohite BV, Mahajan RT (2011) A review: natural products from plant associated endophytic fungi. J Microbiol Biotechnol Res 1(2):21–32Google Scholar
  42. Jogawat A, Vadassery J, Verma N, Oelmüller R, Dua M, Nevo E et al (2016) PiHOG1, a stress regulator MAP kinase from the root endophyte fungus Piriformospora indica, confers salinity stress tolerance in rice plants. Sci Rep 6(1):36765PubMedPubMedCentralCrossRefGoogle Scholar
  43. Johnson LJ, Johnson RD, Schardl CL, Panaccione DG (2003) Identification of differentially expressed genes in the mutualistic association of tall fescue with Neotyphodium coenophialum. Physiol Mol Plant Pathol 63(6):305–317. https://www.sciencedirect.com/science/article/pii/S0885576504000384 CrossRefGoogle Scholar
  44. Joseph B, Priya RM (2011) Bioactive compounds from endophytes and their potential in pharmaceutical effect: a review. Am J Biochem Mol Biol 1(3):291–309CrossRefGoogle Scholar
  45. Kamal N, Viegelmann C, Clements C, Edrada-Ebel R (2016) Metabolomics-guided isolation of anti-trypanosomal metabolites from the endophytic fungus Lasiodiplodia theobromae. Planta Med 83(6):565–573PubMedCrossRefPubMedCentralGoogle Scholar
  46. Kang X, Liu C, Liu D, Zeng L, Shi Q, Qian K et al (2016) The complete mitochondrial genome of huperzine A-producing endophytic fungus Penicillium polonicum. Mitochondrial DNA B 1(1):202–203CrossRefGoogle Scholar
  47. Kaul S, Sharma T, Dhar MK (2016) Omics tools for better understanding the plant-endophyte interactions. Front Plant Sci 7:955. http://www.ncbi.nlm.nih.gov/pubmed/27446181 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant [Internet] 59(4):609–619.  https://doi.org/10.1007/s10535-015-0549-3 CrossRefGoogle Scholar
  49. Kemler M, Garnas J, Wingfield MJ, Gryzenhout M, Pillay K-A, Slippers B (2013) Ion torrent PGM as tool for fungal community analysis: a case study of endophytes in Eucalyptus grandis reveals high taxonomic diversity. PLoS One 8(12):e81718PubMedPubMedCentralCrossRefGoogle Scholar
  50. Khan AL, Hamayun M, Ahmad N, Hussain J, Kang S-M, Kim Y-H et al (2011) Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and Glycine max. L. J Microbiol Biotechnol 21(9):893–902. http://www.ncbi.nlm.nih.gov/pubmed/21952365 PubMedCrossRefPubMedCentralGoogle Scholar
  51. Khan AL, Hamayun M, Kang S-M, Kim Y-H, Jung H-Y, Lee J-H et al (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3. http://www.ncbi.nlm.nih.gov/pubmed/22235902 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Khan AL, Waqas M, Hamayun M, Al-Harrasi A, Al-Rawahi A, Lee I-J (2013) Co-synergism of endophyte Penicillium resedanum LK6 with salicylic acid helped Capsicum annuum in biomass recovery and osmotic stress mitigation. BMC Microbiol 13(1):51. http://www.ncbi.nlm.nih.gov/pubmed/23452409 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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(7):1208PubMedCrossRefPubMedCentralGoogle Scholar
  54. Kim H-Y, Choi GJ, Lee HB, Lee S-W, Lim HK, Jang KS et al (2007) Some fungal endophytes from vegetable crops and their anti-oomycete activities against tomato late blight. Lett Appl Microbiol 44(3):332–337. http://www.ncbi.nlm.nih.gov/pubmed/17309513 PubMedCrossRefPubMedCentralGoogle Scholar
  55. Kim JA, Jeon J, Kim K-T, Choi G, Park S-Y, Lee H-J et al (2017) Draft genome sequence of an endophytic fungus,Gaeumannomyces sp. strain JS-464, isolated from a reed plant, Phragmites communis. Genome Announc 5(31):e00734-17PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kim TY, Jang JY, Yu NH, Chi WJ, Bae C-H, Yeo JH et al (2018) Nematicidal activity of grammicin produced by Xylaria grammica KCTC 13121BP against Meloidogyne incognita. Pest Manag Sci 74(2):384–391PubMedCrossRefPubMedCentralGoogle Scholar
  57. Kodama Y, Shumway M, Leinonen R, International Nucleotide Sequence Database Collaboration (2012) The sequence read archive: Explosive growth of sequencing data. Nucleic Acids Res 40(D1):D54–D56PubMedCrossRefPubMedCentralGoogle Scholar
  58. Kumar S, Aharwal RP, Shukla H, Rajak RC, Sandhu SS (2014) Endophytic fungi: as a source of antimicrobials bioactive compounds. World J Pharm Pharm Sci 3(2):1179–1197Google Scholar
  59. Kusari S, Spiteller M (2012) Metabolomics of endophytic fungi producing associated plant secondary metabolites: progress, challenges and opportunities. In: Roessner U (ed) Metabolomics. InTech, LondonGoogle Scholar
  60. Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71(2):159–162PubMedCrossRefGoogle Scholar
  61. 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(3):1019–1030PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kusari S, Zühlke S, Košuth J, Čellárová E, Spiteller M (2009b) Light-independent metabolomics of endophytic Thielavia subthermophila provides insight into microbial hypericin biosynthesis. J Nat Prod 72(10):1825–1835PubMedCrossRefPubMedCentralGoogle Scholar
  63. Kusari S, Zühlke S, Spiteller M (2009c) An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J Nat Prod 72(1):2–7PubMedCrossRefGoogle Scholar
  64. 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(4):764–775PubMedCrossRefPubMedCentralGoogle Scholar
  65. Kusari S, Verma VC, Lamshoeft M, Spiteller M (2012) An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J Microbiol Biotechnol 28(3):1287–1294PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lata R, Chowdhury S, Gond SK, White JF (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66(4):268–276.  https://doi.org/10.1111/lam.12855 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Lee C, Kim S, Li W, Bang S, Lee H, Lee HJ et al (2017) Bioactive secondary metabolites produced by an endophytic fungus Gaeumannomyces sp. JS0464 from a maritime halophyte Phragmites communis. J Antibiot (Tokyo) 70(6):737–742CrossRefGoogle Scholar
  68. Lehtonen PT, Helander M, Siddiqui SA, Lehto K, Saikkonen K (2006) Endophytic fungus decreases plant virus infections in meadow ryegrass (Lolium pratense). Biol Lett 2(4):620–623. http://www.ncbi.nlm.nih.gov/pubmed/17148304 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Li B, Tang M, Tang K, Zhao L, Guo S (2012) Screening for differentially expressed genes in Anoectochilus roxburghii (Orchidaceae) during symbiosis with the mycorrhizal fungus Epulorhiza sp. Sci China Life Sci 55(2):164–171PubMedCrossRefPubMedCentralGoogle Scholar
  70. Lignanların A, Ve Bitkiler Ö, Dağılımı A, Konuklugil B (1995) The importance of aryltetralin (podophyllum) lignans and their distribution in the plant kingdom. J Fac Pharm Ankara 2422(13):301–302Google Scholar
  71. Lyons PC, Evans JJ, Bacon CW (1990) Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiol 92(3):726–732. http://www.ncbi.nlm.nih.gov/pubmed/16667341 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses. Crop Sci 40(4):923. https://www.crops.org/publications/cs/abstracts/40/4/923 CrossRefGoogle Scholar
  73. Malinowski DP, Brauer DK, Belesky DP (1999) The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus deficiency. J Agron Crop Sci 183(1):53–60.  https://doi.org/10.1046/j.1439-037x.1999.00321.x CrossRefGoogle Scholar
  74. Marquez 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(5811):513–515. http://www.ncbi.nlm.nih.gov/pubmed/17255511 PubMedCrossRefPubMedCentralGoogle Scholar
  75. Miller AN, Bates ST (2017) The Mycology Collections Portal (MyCoPortal). IMA Fungus 8(2):65–66Google Scholar
  76. Mishra VK, Singh G, Passari AK, Yadav MK, Gupta VK, Singh BP (2016a) Distribution and antimicrobial potential of endophytic fungi associated with ethnomedicinal plant Melastoma malabathricum L. J Environ Biol 37(2):229–237Google Scholar
  77. Mishra VK, Passari AK, Singh BP (2016b) In vitro antimycotic and biosynthetic potential of fungal endophytes associated with Schima Wallichii. In: Kumar P et al (eds) Current trends in disease diagnostics. Springer International, Basel, pp 367–381CrossRefGoogle Scholar
  78. Mishra VK, Passari AK, Chandra P, Leo VV, Kumar B, Gupta VK, Singh BP (2017a) Determination and production of antimicrobial compounds by Aspergillus clavatonanicus strain MJ31, an endophytic fungus from Mirabilis jalapa L. using UPLC-ESI-MS/MS and TD GC-MS. PLoS One 12(10):1–24.  https://doi.org/10.1371/journal.pone.0186234 CrossRefGoogle Scholar
  79. Mishra VK, Passari AK, Leo VV, Singh BP (2017b) Molecular diversity and detection of endophytic fungi based on their antimicrobial biosynthetic genes. In: Singh BP, Gupta VK (eds) Molecular markers in mycology, fungal biology. Springer International, Basel, pp 1–35.  https://doi.org/10.1007/978-3-319-34106-4_1 CrossRefGoogle Scholar
  80. Molina G, Pimentel MR, Bertucci TCP, Pastore GM (2012) Application of fungal endophytes in biotechnological processes. Chem Eng Trans 27:289–294Google Scholar
  81. Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8(4):450–456. https://www.sciencedirect.com/science/article/pii/S1369526605000683 PubMedCrossRefPubMedCentralGoogle Scholar
  82. Na R, Jiajia L, Dongliang Y, Yingzi P, Juan H, Xiong L et al (2016) Indentification of vincamine indole alkaloids producing endophytic fungi isolated from Nerium indicum, Apocynaceae. Microbiol Res 192:114–121PubMedCrossRefPubMedCentralGoogle Scholar
  83. Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:250693CrossRefGoogle Scholar
  84. Nicolás C, Hermosa R, Rubio B, Mukherjee PK, Monte E (2014) Trichoderma genes in plants for stress tolerance- status and prospects. Plant Sci 228:71–78PubMedCrossRefPubMedCentralGoogle Scholar
  85. Nicoletti R, Fiorentino A (2015) Plant bioactive metabolites and drugs produced by endophytic fungi of spermatophyta. Agriculture 5(4):918–970CrossRefGoogle Scholar
  86. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM et al (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188(1):223–241PubMedCrossRefPubMedCentralGoogle Scholar
  87. Orr SP, Rudgers JA, Clay K (2005) Invasive plants can inhibit native tree seedlings: testing potential allelopathic mechanisms. Plant Ecol 181(2):153–165.  https://doi.org/10.1007/s11258-005-5698-6 CrossRefGoogle Scholar
  88. Osbourn A (2010) Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends Genet 26(10):449–457PubMedCrossRefPubMedCentralGoogle Scholar
  89. Pandi M, Manikandan R, Muthumary J (2010) Anticancer activity of fungal taxol derived from Botryodiplodia theobromae Pat., an endophytic fungus, against 7, 12 dimethyl benz(a)anthracene (DMBA)-induced mammary gland carcinogenesis in Sprague dawley rats. Biomed Pharmacother 64(1):48–53PubMedCrossRefPubMedCentralGoogle Scholar
  90. Passari AK, Mishra VK, Singh G, Singh P, Kumar B, Gupta VK, Sharma RK, Saikia R, Donovan A, Singh BP (2017) Insights into the functionality of endophytic actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci Rep 7(11809):1–17.  https://doi.org/10.1038/s41598-017-12235-4 CrossRefGoogle Scholar
  91. Philippe G (2016) Lolitrem B and indole diterpene alkaloids produced by endophytic fungi of the genus Epichloë and their toxic effects in livestock. Toxins (Basel) 8(2):47. http://www.mdpi.com/2072-6651/8/2/47 CrossRefGoogle Scholar
  92. Phongpaichit S, Nikom J, Rungjindamai N, Sakayaroj J, Hutadilok-Towatana N, Rukachaisirikul V et al (2007) Biological activities of extracts from endophytic fungi isolated from Garcinia plants. FEMS Immunol Med Microbiol 51(3):517–525CrossRefGoogle Scholar
  93. Powthong P, Jantrapanukorn B, Thongmee A, Suntornthiticharoen P (2013) Screening of antimicrobial activities of the endophytic fungi isolated from Sesbania grandiflora (L.) Pers. J Agric Sci Technol 15:1513–1522Google Scholar
  94. Prabavathy D, Valli Nachiyar C (2013) Antimicrobial and antidiabetic activity of an endophytic fungi isolated from Adathoda beddomei. Int J Pharm Pharm Sci 5(3):780–783Google Scholar
  95. Premalatha K, Kalra A (2013) Molecular phylogenetic identification of endophytic fungi isolated from resinous and healthy wood of Aquilaria malaccensis, a red listed and highly exploited medicinal tree. Fungal Ecol 6(3):205–211CrossRefGoogle Scholar
  96. Prestidge RA (1993) Causes and control of perennial ryegrass staggers in New Zealand. Agric Ecosyst Environ 44(1–4):283–300. https://www.sciencedirect.com/science/article/pii/016788099390051P CrossRefGoogle Scholar
  97. Pretsch A, Nagl M, Schwendinger K, Kreiseder B, Wiederstein M, Pretsch D et al (2014) Antimicrobial and anti-inflammatory activities of endophytic fungi Talaromyces wortmannii extracts against acne-inducing bacteria. PLoS One 9(6):e97929PubMedPubMedCentralCrossRefGoogle Scholar
  98. Puri SC, Verma V, Amna T, Qazi GN, Spiteller M (2005) An endophytic fungus from Nothapodytes foetida that produces camptothecin. J Nat Prod 68(12):1717–1719PubMedCrossRefGoogle Scholar
  99. 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(4):494–510PubMedCrossRefPubMedCentralGoogle Scholar
  100. Ramos HP, Braun GH, Pupo MT, Said S (2010) Antimicrobial activity from endophytic fungi Arthrinium state of Apiospora montagnei Sacc. and Papulaspora immersa. Braz Arch Biol Technol 53(3):629–632CrossRefGoogle Scholar
  101. Ranadive K, Jagtap N, Khare H (2017) Fungifromindia: the first online initiative to document fungi from India. IMA Fungus 8(2):67–69. http://www.imafungus.org/Issue/82/MycoLens.pdf Google Scholar
  102. Rank C, Larsen TO, Frisvad JC (2010) Functional systems biology of Aspergillus. In: Aspergillus molecular biology and genomics. p 173–198Google Scholar
  103. Redondo-Gómez S (2013) Abiotic and biotic stress tolerance in plants. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer India, New Delhi, pp 1–20.  https://doi.org/10.1007/978-81-322-0807-5_1 CrossRefGoogle Scholar
  104. Richardson MD, Chapman GW, Hoveland CS, Bacon CW (1992) Sugar alcohols in endophyte-infected tall fescue under drought. Crop Sci 32(4):1060. https://www.crops.org/publications/cs/abstracts/32/4/CS0320041060 CrossRefGoogle Scholar
  105. 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(5):1109–1114PubMedCrossRefGoogle Scholar
  106. Rodriguez RJ, White Jr JF, Arnold AE, Redman RS (2009). Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330.  https://doi.org/10.1111/j.1469-8137.2009.02773.x CrossRefGoogle Scholar
  107. Rouhier N, Koh CS, Gelhaye E, Corbier C, Favier F, Didierjean C et al (2008) Redox based anti-oxidant systems in plants: Biochemical and structural analyses. Biochim Biophys Acta 1780(11):1249–1260. https://www.sciencedirect.com/science/article/pii/S0304416507002991 PubMedCrossRefPubMedCentralGoogle Scholar
  108. Rouxel T, Grandaubert J, Hane JK, Hoede C, Van De Wouw AP, Couloux A et al (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2(1)Google Scholar
  109. Rudgers JA, Orr S (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97(2):247–255.  https://doi.org/10.1111/j.1365-2745.2008.01478.x CrossRefGoogle Scholar
  110. Saikkonen K, Young CA, Helander M, Schardl CL (2016) Endophytic Epichloë species and their grass hosts: from evolution to applications. Plant Mol Biol 90(6):665–675PubMedCrossRefPubMedCentralGoogle Scholar
  111. Sandhu SS, Kumar S, Aharwal RP (2014) Isolation and identification of endophytic fungi from Ricinus communis linn. and their antibacterial activity. Int J Res Pharm Chem 4(3):611–618Google Scholar
  112. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55(1):315–340PubMedCrossRefPubMedCentralGoogle Scholar
  113. Schwarz M, Köpcke B, Weber RWS, Sterner O, Anke H (2004) 3-Hydroxypropionic acid as a nematicidal principle in endophytic fungi. Phytochemistry 65(15):2239–2245PubMedCrossRefPubMedCentralGoogle Scholar
  114. Seetharaman P, Gnanasekar S, Chandrasekaran R, Chandrakasan G, Syed A, Hodhod MS et al (2017) Isolation of limonoid compound (Hamisonine) from endophytic fungi Penicillium oxalicum LA-1 (KX622790) of Limonia acidissima L. for its larvicidal efficacy against LF vector, Culex quinquefasciatus (Diptera: Culicidae). Environ Sci Pollut Res 24(26):21272–21282CrossRefGoogle Scholar
  115. Shen M, Zhao DK, Qiao Q, Liu L, Wang JL, Cao GH et al (2015) Identification of glutathione S-transferase (GST) genes from a dark septate endophytic fungus (Exophiala pisciphila) and their expression patterns under varied metals stress. PLoS One 10(4):e0123418PubMedPubMedCentralCrossRefGoogle Scholar
  116. Shinozuka H, Hettiarachchige IK, Shinozuka M, Cogan NOI, Spangenberg GC, Cocks BG et al (2017) Horizontal transfer of a ß-1,6-glucanase gene from an ancestral species of fungal endophyte to a cool-season grass host. Sci Rep 7(1):9024PubMedPubMedCentralCrossRefGoogle Scholar
  117. Shukla ST, Habbu PV, Kulkarni VH, Jagadish KS, Pandey AR, Sutariya VN (2014) Endophytic microbes: a novel source for biologically/pharmacologically active secondary metabolites. Asian J Pharmacol Toxicol 2(3):1–16Google Scholar
  118. Shweta S, Zuehlke S, Ramesha BT, Priti V, Mohana Kumar P, Ravikanth G et al (2010) Endophytic fungal strains of Fusarium solani, from Apodytes dimidiata E. Mey. ex Arn (Icacinaceae) produce camptothecin, 10-hydroxycamptothecin and 9-methoxycamptothecin. Phytochemistry 71(1):117–122PubMedCrossRefPubMedCentralGoogle Scholar
  119. Singh R, Dubey AK (2015) Endophytic actinomycetes as emerging source for therapeutic compounds. Indo Glob J Pharm Sci 5(2):106–116Google Scholar
  120. Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6(2):175–191. http://www.ncbi.nlm.nih.gov/pubmed/21512319 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Soliman SSM, Greenwood JS, Bombarely A, Mueller LA, Tsao R, Mosser DD et al (2015) An endophyte constructs fungicide-containing extracellular barriers for its host plant. Curr Biol 25(19):2570–2576. http://www.ncbi.nlm.nih.gov/pubmed/26412131 PubMedCrossRefPubMedCentralGoogle Scholar
  122. Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS et al (2012) FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res 40(Database issue):D675–D681PubMedCrossRefPubMedCentralGoogle Scholar
  123. Staniek A, Woerdenbag HJ, Kayser O (2008) Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery. J Plant Interact 3(2):75–93CrossRefGoogle Scholar
  124. Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260(5105):214–216PubMedCrossRefPubMedCentralGoogle Scholar
  125. Strobel GA, Pliam NB (1995) Immunosuppressant diterpene compound, p 24Google Scholar
  126. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502PubMedPubMedCentralCrossRefGoogle Scholar
  127. Strobel G, Ford E, Worapong J, Harper JK, Arif AM, Grant DM et al (2002) Isopestacin, an isobenzofuranone from Pestalotiopsis microspora, possessing antifungal and antioxidant activities. Phytochemistry 60(2):179–183PubMedCrossRefPubMedCentralGoogle Scholar
  128. Takeuchi S, Hirayama K, Ueda K, Sakai H, Yonehara H (1958) Blasticidin S, a new antibiotic. J Antibiot (Tokyo) 11(1):1–5. http://www.ncbi.nlm.nih.gov/pubmed/13525246 Google Scholar
  129. Talbot NJ (2015) Plant immunity: a little help from fungal friends. Curr Biol 25(22):R1074–R1076. http://www.ncbi.nlm.nih.gov/pubmed/26583896 PubMedCrossRefPubMedCentralGoogle Scholar
  130. Teles HL, Sordi R, Silva GH, Castro-Gamboa I, Bolzani Vda S, Pfenning LH et al (2006) Aromatic compounds produced by Periconia atropurpurea, an endophytic fungus associated with Xylopia aromatica. Phytochemistry 67(24):2686–2690PubMedCrossRefPubMedCentralGoogle Scholar
  131. Tian J, Liu XC, Liu ZL, Lai D, Zhou L (2016) Larvicidal spirobisnaphthalenes from the endophytic fungus Berkleasmium sp. against Aedes albopictus. Pest Manag Sci 72(5):961–965PubMedCrossRefPubMedCentralGoogle Scholar
  132. Toju H, Tanabe AS, Ishii HS (2016) Ericaceous plant-fungus network in a harsh alpine-subalpine environment. Mol Ecol 25(13):3242–3257PubMedCrossRefPubMedCentralGoogle Scholar
  133. Umashankar T, Govindappa M, Yarappa Lakshmikantha R, Padmalatha Channabasava, RS (2015). Isolation and characterization of coumarin isolated from endophyte, Alternaria species-1 of Crotalaria pallida and its apoptotic action on HeLa cancer cell line. Metabolomics, 5(4), 1–8.Google Scholar
  134. Uzma F, Hashem A, Murthy N, Mohan HD, Kamath PV, Singh BP, Venkataramana M, Gupta VK, Siddaiah CN, Chowdappa S, Alqaeawi AA, Abd Allah EF (2018) Endophytic fungi—alternative sources of cytotoxic compounds: a review. Front Pharmacol 9(309):1–37.  https://doi.org/10.3389/fphar.2018.00309
  135. Vasundhara M, Kumar A, Reddy MS (2016) Molecular approaches to screen bioactive compounds from endophytic fungi. Front Microbiol 7:1774PubMedPubMedCentralCrossRefGoogle Scholar
  136. Visalakchi S, Muthumary J (2010) Taxol (anticancer drug) producing endophytic fungi: an overview. Int J Pharma Bio Sci 1(3):1–9Google Scholar
  137. Wang X, Zhang X, Liu L, Xiang M, Wang W, Sun X et al (2015a) Genomic and transcriptomic analysis of the endophytic fungus Pestalotiopsis fici reveals its lifestyle and high potential for synthesis of natural products. BMC Genomics 16(1):28PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wang X, Zhang X, Liu L, Xiang M, Wang W, Sun X et al (2015b) Genomic and transcriptomic analysis of the endophytic fungus reveals its lifestyle and high potential for synthesis of natural products. BMC Genomics 16:28PubMedPubMedCentralCrossRefGoogle Scholar
  139. Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99(7):2955–2965.  https://doi.org/10.1007/s00253-015-6487-3 CrossRefGoogle Scholar
  140. Webber J (1981) A natural biological control of Dutch elm disease. Nature 292(5822):449–451.  https://doi.org/10.1038/292449a0 CrossRefGoogle Scholar
  141. Weig AR, Peršoh D, Werner S, Betzlbacher A, Rambold G (2013) Diagnostic assessment of mycodiversity in environmental samples by fungal ITS1 rDNA length polymorphism. Mycol Prog 12(4):719–725CrossRefGoogle Scholar
  142. Xu X-H, Su Z-Z, Wang C, Kubicek CP, Feng X-X, Mao L-J et al (2015) The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte. Sci Rep 4(1):5783CrossRefGoogle Scholar
  143. Yadav V, Kumar M, Deep AK, Kumar H, Sharma R, Tripathi T et al (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285(34):26532–26544PubMedPubMedCentralCrossRefGoogle Scholar
  144. Yadava P, Bhuyan SK, Bandyopadhyay P, Yadava PK (2015) Extraction of proteins for two-dimensional gel electrophoresis and proteomic analysis from an endophytic fungus. Protoc Exch.  https://doi.org/10.1038/protex.2015.084
  145. Yamaji K, Watanabe Y, Masuya H, Shigeto A, Yui H, Haruma T (2016) Root fungal endophytes enhance heavy-metal stress tolerance of clethra barbinervis growing naturally at mining sites via growth enhancement, promotion of nutrient uptake and decrease of heavy-metal concentration. PLoS One 11(12):e0169089.  https://doi.org/10.1371/journal.pone.0169089 CrossRefPubMedPubMedCentralGoogle Scholar
  146. Yang S (2010) Allelopathic effects of endophytic fungi of Achnatherum inebrians Keng on the seed and seedling of three turf grasses. Acta Agrestia Sinica. http://en.cnki.com.cn/Article_en/CJFDTOTAL-CDXU201001017.htm
  147. Yang Y, Zhao H, Barrero RA, Zhang B, Sun G, Wilson IW et al (2014) Genome sequencing and analysis of the paclitaxel-producing endophytic fungus Penicillium aurantiogriseum NRRL 62431. BMC Genomics 15(1):69PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zhang P, Zhou P-P, Yu L-J (2009) An endophytic taxol-producing fungus from taxus media, Cladosporium cladosporioides MD2. Curr Microbiol 59(3):227–232PubMedCrossRefPubMedCentralGoogle Scholar
  149. Zhang G, Sun S, Zhu T, Lin Z, Gu J, Li D et al (2011) Antiviral isoindolone derivatives from an endophytic fungus Emericella sp. associated with Aegiceras corniculatum. Phytochemistry 72(11–12):1436–1442PubMedCrossRefPubMedCentralGoogle Scholar
  150. Zhang Y, Han T, Ming Q, Wu L, Rahman K, Qin L (2012) Alkaloids produced by endophytic fungi: a review. Nat Prod Commun 7(7):963–968PubMedPubMedCentralGoogle Scholar
  151. Zhang H, Liu R, Yang J, Li H, Zhou F (2017a) Bioactive alkaloids of Aspergillus fumigatus, an endophytic fungus from Astragalus membranaceus. Chem Nat Compd 53(4):802–805CrossRefGoogle Scholar
  152. Zhang S, Wang XN, Zhang XL, Liu XZ, Zhang YJ (2017b) Complete mitochondrial genome of the endophytic fungus Pestalotiopsis fici: features and evolution. Appl Microbiol Biotechnol 101(4):1593–1604PubMedCrossRefPubMedCentralGoogle Scholar
  153. Zhao J, Mou Y, Shan T, Li Y, Zhou L, Wang M et al (2010) Antimicrobial metabolites from the endophytic fungus Pichia guilliermondii isolated from Paris polyphylla var. yunnanensis. Molecules 15(11):7961–7970PubMedPubMedCentralCrossRefGoogle Scholar
  154. Zhao J, Shan T, Mou Y, Zhou L (2011) Plant-derived bioactive compounds produced by endophytic fungi. Mini Rev Med Chem 11(2):159–168CrossRefGoogle Scholar
  155. Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D et al (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7(10):e1002290PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Hasnahana Chetia
    • 1
  • Debajyoti Kabiraj
    • 1
  • Biju Bharali
    • 2
  • Sunita Ojha
    • 1
  • Manash Pratim Barkataki
    • 1
  • Dharitri Saikia
    • 2
  • Tinka Singh
    • 2
  • Ponnala Vimal Mosahari
    • 2
  • Pragya Sharma
    • 3
  • Utpal Bora
    • 1
    • 2
    Email author
  1. 1.Department of Biosciences and BioengineeringIndian Institute of Technology GuwahatiGuwahatiIndia
  2. 2.Centre for the EnvironmentIndian Institute of Technology GuwahatiGuwahatiIndia
  3. 3.Department of Bioengineering and Technology, Gauhati University Institute of Science and Technology (GUIST)Gauhati UniversityGuwahatiIndia

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