Applied Microbiology and Biotechnology

, Volume 99, Issue 7, pp 2955–2965 | Cite as

Plant-endophyte symbiosis, an ecological perspective

  • Zahoor Ahmed Wani
  • Nasheeman Ashraf
  • Tabasum Mohiuddin
  • Syed Riyaz-Ul-HassanEmail author


Endophytism is the phenomenon of mutualistic association of a plant with a microorganism wherein the microbe lives within the tissues of the plant without causing any symptoms of disease. In addition to being a treasured biological resource, endophytes play diverse indispensable functions in nature for plant growth, development, stress tolerance, and adaptation. Our understanding of endophytism and its ecological aspects are overtly limited, and we have only recently started to appreciate its essence. Endophytes may impact plant biology through the production of diverse chemical entities including, but not limited to, plant growth hormones and by modulating the gene expression of defense and other secondary metabolic pathways of the host. Studies have shown differential recruitment of endophytes in endophytic populations of plants growing in the same locations, indicating host specificity and that endophytes evolve in a coordinated fashion with the host plants. Endophytic technology can be employed for the efficient production of agricultural and economically important plants and plant products. The rational application of endophytes to manipulate the microbiota, intimately associated with plants, can help in enhancement of production of agricultural produce, increased production of key metabolites in medicinal and aromatic plants, as well as adaption to new bio-geographic regions through tolerance to various biotic and abiotic conditions. However, the potential of endophytic biology can be judiciously harnessed only when we obtain insight into the molecular mechanism of this unique mutualistic relationship. In this paper, we present a discussion on endophytes, endophytism, their significance, and diverse functions in nature as unraveled by the latest research to understand this universal natural phenomenon.


Endophytes Endophytism Multitrophic interaction Phytoremediation Plant adaptation Systems biology approach 



ZAW and TM are grateful to the Council of Scientific and Industrial Research (CSIR), India, for their respective fellowships. SRH and NA acknowledge the financial support obtained from CSIR 12th FYP projects “PMSI” (BSC0117) and “SIMPLE” (BSC0109) of the Council of Scientific and Industrial Research (CSIR), New Delhi, India. This review paper bears the institutional manuscript number IIIM/1757/2015.

Conflict of interest

The authors report no declarations of interest.


  1. Albrectsen BR, Björkén L, Varad A, Hagner A, Wedin M, Karlsson J, Jansson S (2010) Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance. Fungal Divers 41:17–28Google Scholar
  2. Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845PubMedGoogle Scholar
  3. Arnold AE (2007) Understanding the diversity of foliar fungal endophytes: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66Google Scholar
  4. Arnold AE, Lutzoni F (2007) Diversity and Host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology 88:541–549PubMedGoogle Scholar
  5. Backman PA, Sikora RA (2008) Endophytes: An emerging tool for biological control. Biol Control 46:1–3Google Scholar
  6. Bao X, Roossinck MJ (2013) Multiplexed interactions: viruses of endophytic fungi. Adv Virus Res 86:37–57PubMedGoogle Scholar
  7. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577PubMedGoogle Scholar
  8. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18PubMedGoogle Scholar
  9. Bitas V, Kim HS, Bennett JW, Kang S (2013) Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant Microbe Interact 26:835–843PubMedGoogle Scholar
  10. Boller T (1995) Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:189–214Google Scholar
  11. Botella L, Díez JJ (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18Google Scholar
  12. Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37PubMedCentralPubMedGoogle Scholar
  13. Chen L, Zhang QY, Jia M, Ming QL, Yue W, Rahman K, Qin LP, Han T (2014) Endophytic fungi with antitumor activities: Their occurrence and anticancer compounds. Crit Rev Microbiol 24:1–20Google Scholar
  14. Cheplick GP (2007) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exp Bot 60:202–210Google Scholar
  15. Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson JP, Koolaard WR, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45:84–93PubMedGoogle Scholar
  16. Conn VM, Walker AR, Franco CM (2008) Endophytic actinobacteria induces defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218PubMedGoogle Scholar
  17. Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci 103:18450–18457PubMedCentralPubMedGoogle Scholar
  18. Doty SL, Oakley B, Xin G, Kang JW, Singleton G, Khan Z, Vajzovic A, Staley JT (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 47:23–33Google Scholar
  19. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedGoogle Scholar
  20. Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180:190–195PubMedGoogle Scholar
  21. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2014) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci. doi: 10.1073/pnas.1414592112 Google Scholar
  22. Ek-Ramos MJ, Zhou W, Valencia CU, Antwl JB, Kalns LL, Morgan GD, Kerns DL, Sword GA (2013) Spatial and Temporal Variation in Fungal Endophyte Communities Isolated from Cultivated Cotton (Gossypium hirsutum). PLoS One 8:e66049PubMedCentralPubMedGoogle Scholar
  23. Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131:61–67Google Scholar
  24. Elvira-Recuenco M, Van Vuurde JWL (2000) Natural incidence of endophytic bacteria in pea cultivars under field conditions. Can J Microbiol 46:1036–1041PubMedGoogle Scholar
  25. Ezra D, Hess WH, Strobel GA (2004) New endophytic isolates of M. albus, a volatile antibiotic-producing fungus. Microbiol 150:4023–4031Google Scholar
  26. Fahey JW, Dimock MB, Tomasino SF, Taylor JM, Carlson PS (1991) Genetically engineered endophytes as biocontrol agents: a case study in industry. Microb Ecol Leaves 401–411Google Scholar
  27. Freeman S, Rodriguez RJ (1993) Genetic conversion of a fungal pathogen to a nonpathogenic, endophytic mutualist. Science 260:75–78PubMedGoogle Scholar
  28. Friesen ML (2012) widespread fitness alignment in the legume–rhizobium symbiosis. New Phytol 194:1096–1111PubMedGoogle Scholar
  29. Glazebrook J (2005) Contrasting Mechanisms of Defense against Biotrophic and Necrotrophic Pathogens. Annu Rev Phytopathol 43:205–227PubMedGoogle Scholar
  30. Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA (2010) Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiol 156:3814–3829Google Scholar
  31. Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implication of their occurrence. J Nat Prod 69:509–526PubMedCentralPubMedGoogle Scholar
  32. Gundel PE, Martinez-Ghersa MA, Omacini M, Cuyeu R, Pagano E, Rios R, Ghersa CM (2012) Mutualism effectiveness and vertical transmission of symbiotic fungal endophytes in response to host genetic background. Evol Appl 5:838–884PubMedCentralPubMedGoogle Scholar
  33. Heath KD (2010) Intergenomic epistasis and co-evolutionary constraint in plants and rhizobia. Evolution 64:1446–1458PubMedGoogle Scholar
  34. Heil M, Bostock RM (2002) Induced systemic resistance (ISR) against pathogens in the context of Induced Plant defences. Ann Bot 89:503–512PubMedCentralPubMedGoogle Scholar
  35. Herrera J, Khidir HH, Eudy DM, Porras-Alfaro A, Natvig DO, Sinsabaugh RL (2010) Shifting fungal endophyte communities colonize Bouteloua gracilis: effect of host tissue and geographical distribution. Mycologia 102:1012–1026PubMedGoogle Scholar
  36. Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2003) Effects of Neotyphodium endophytes on growth, reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass Forage Sci 58:407–415Google Scholar
  37. Higgins KL, Arnold AE, Coley P, Kursar T (2014) Communities of fungal endophyte in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecol 8:1–11Google Scholar
  38. Iqbal J, Nelson JA, McCulley RL (2013) Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant Soils 364:15–27Google Scholar
  39. Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ (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 12:3PubMedCentralPubMedGoogle Scholar
  40. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215–236Google Scholar
  41. Kiers ET, Ratcliff WC, Denison RF (2013) Single-strain inoculation may create spurious correlations between legume fitness and rhizobial fitness. New Phytol 198:4–6PubMedGoogle Scholar
  42. Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite - what decides? Curr Opin Plant Biol 9:358–363PubMedGoogle Scholar
  43. Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71Google Scholar
  44. Kusari S, Spiteller M (2012) Are we ready for industrial production of bioactive plant secondary metabolites utilizing endophytes? Nat Prod Rep 28:1203–1207Google Scholar
  45. Kusari S, Zuhlke S, Spiteller M (2009) An endophytic fungus from Camptotheca acuminate that produces camptothecin and analogues. J Nat Prod 72:2–7PubMedGoogle Scholar
  46. Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798PubMedGoogle Scholar
  47. Kusari S, Singh S, Jayabaskaran C (2014) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303PubMedGoogle Scholar
  48. Lahrmann U, Dinga Y, Banhara A, Rath M, Hajirezaeid MR, Döhlemanna S, Wirénd NV, Parniskeb M, Zuccaroa A (2013) Host-related metabolic cues affect colonization strategies of a root endophyte. Proc Natl Acad Sci 110:13965–13970PubMedCentralPubMedGoogle Scholar
  49. Lebeis SL (2014) The potential for give and take in plant–microbiome relationships. Front Plant Sci 5:287PubMedCentralPubMedGoogle Scholar
  50. Li TY, Zeng HL, Ping Y, Lin H, Fan XL, Guo ZG, Zhang CF (2007) Construction of a stable expression vector for Leifsonia xyli subsp. cynodontis and its application in studying the effect of the bacterium as an endophytic bacterium in rice. FEMS Microbiol Lett 267:176–183PubMedGoogle Scholar
  51. Li CH, Shi L, Han Q, Hu HL, Zhao MW, Tang CM, Li SP (2012) Biocontrol of verticillium wilt and colonization of cotton plants by an endophytic bacterial isolate. J Appl Microbiol 113:641–651PubMedGoogle Scholar
  52. Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52:1–14Google Scholar
  53. Mallette ND, Knighton WB, Strobel GA, Carlson RP, Peyton BM (2012) Resolution of volatile fuel compound profiles from Ascocoryne sarcoides: a comparison by proton transfer reaction-mass spectrometry and solid phase microextraction gas chromatography–mass spectrometry. AMB Express 2:23PubMedCentralPubMedGoogle Scholar
  54. 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 315:513–515PubMedGoogle Scholar
  55. Mathys J, De-Cremer K, Timmermans P, Kerckhove SV, Lievens B, Vanhaecke M, Cammue BP, De-Coninck B (2012) Genome wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatumT382 against Botrytis cinerea infection. Front Plant Sci 3:108PubMedCentralPubMedGoogle Scholar
  56. Mendoza AR, Sikora RA (2009) Biological control of Radopholus similis by co application of the mutualistic endophyte Fusarium oxysporum strain 162, the egg pathogen Paecilomyces lilacinuss train 251 and the antagonistic bacteria Bacillus firmus. Bio Control 54:263–272Google Scholar
  57. Mitter B, Petric A, Shin MW, Chain PS, Hauberg-Lotte L, Reinhold Hurek B, Nowak J, Sessitsch A (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120PubMedCentralPubMedGoogle Scholar
  58. Moricca S, Ragazzi A (2008) Fungal endophytes in Mediterranean oak forests: A lesson from Disculaquercina. Phytopathology 98:380–386PubMedGoogle Scholar
  59. Mostert L, Crous PW, Petrini O (2000) Endophytic fungi associated with shoots and leaves of Vitis vinifera, with specific reference to the Phomopsis viticola complex. Sydowia 52:46–58Google Scholar
  60. Mousa WK, Raizada MN (2013) The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front Microbiol 4:65PubMedCentralPubMedGoogle Scholar
  61. Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL (2013) Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol 13:127PubMedCentralPubMedGoogle Scholar
  62. Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: New uses for endophytic bacteria in plants. Trends Biotechnol 23:6–8PubMedGoogle Scholar
  63. Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Bio Control 55:113–128Google Scholar
  64. Partida-Martínez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100PubMedCentralPubMedGoogle Scholar
  65. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial Ecology of Leaves. Springer-Verlag, New York, USA, p 179Google Scholar
  66. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315PubMedGoogle Scholar
  67. Qawasmeh A, Objed HK, Raman A, Wheatley W (2012) Influence of fungal endophyte infection on phenolic content and antioxidant activity in grasses: interaction between Lolium perenne and different strains of Neotyphodium lolii. J Agric Food Chem 60:3381–3388Google Scholar
  68. Rasmussen S, Parsons AJ, Popay A, Xue H, Newman JA (2008) Plant-endophyte-herbivore interactions: More than just alkaloids? Plant Signal Behav 3:974–977PubMedCentralPubMedGoogle Scholar
  69. Redecker D, Kodner R, Graham LE (2000) Glomalean Fungi from the Ordovician. Science 289:1920–1921PubMedGoogle Scholar
  70. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716Google Scholar
  71. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298:1581PubMedGoogle Scholar
  72. Reinhold-Hurek B, Hurek T (2011) Living in side plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443PubMedGoogle Scholar
  73. Rey T, Schornack S (2013) Interactions of beneficial and detrimental root-colonizing filamentous microbes with plant hosts. Genome Biol 14:121PubMedCentralPubMedGoogle Scholar
  74. Riyaz-Ul-Hassan S, Strobel A, Booth E, Knighton B, Floerchinger C, Sears J (2012) Modulation of volatile organic compound formation in the Mycodiesel-producing endophyte Hypoxylon sp. CI-4. Microbiology 158:465–473Google Scholar
  75. Riyaz-Ul-Hassan S, Strobel G, Geary B, Sears J (2013) An endophytic Nodulisporium sp. from Central America producing volatile organic compounds with both biological and fuel potential. J Microbiol Biotechnol 23:29–35PubMedGoogle Scholar
  76. Rodriguez RJ, Roossinck M (2012) Viruses, fungi and plants: cross-kingdom communication and mutualism. Biocomm Fungi. doi: 10.1007/978-94-007-4264-2-14
  77. 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 J 2:404–416PubMedGoogle Scholar
  78. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedGoogle Scholar
  79. Rosenblueth M, Martínez-Romero E (2006) Bacterial Endophytes and Their Interactions with Hosts. Mol Plant Microbe Interact 19:827–837PubMedGoogle Scholar
  80. Rudgers JA, Miller TE, Ziegler SM, Craven KD (2012) There are many ways to be a mutualist: endophyte fungus reduces plant survival but increases population growth. Ecology 93:565–574Google Scholar
  81. Ryan RP, Germaine K, Franks AA, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9PubMedGoogle Scholar
  82. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343Google Scholar
  83. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280PubMedGoogle Scholar
  84. Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968PubMedGoogle Scholar
  85. Schardl CL, Liu J, White JK, Finkel RA, An Z, Siegel M (1991) Molecular phylogenetic relationship of non-pathogenic grass mycosymbionts and clavicipitaceous plant pathogens. Plant Syst Evol 178:27–41Google Scholar
  86. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340PubMedGoogle Scholar
  87. Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce: active biocontrol of Rhizoctonia solani and negligible, short-term ejects on non target microorganisms. FEMS Microbiol Ecol 64:106–116PubMedGoogle Scholar
  88. Schirmbock M, Lorito M, Wang ML, Hayes MK, Atac IA , Scala F, Harman GE, Kubicek CP (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 4364–4370Google Scholar
  89. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–687PubMedGoogle Scholar
  90. Selim KA, El-Beih AA, AbdEl-Rahman TM, El-Diwany A (2012) Biology of Endophytic Fungi. Curr Res Environ Appl Mycol 2:31–82Google Scholar
  91. Seo DJ, Nguyen DM, Song YS, Jung WJ (2012) Induction of defense response against Rhizoctonia solani in cucumber plants by endophytic bacterium Bacillus thuringiensis GS1. J Microbiol Biotechnol 22:407–415PubMedGoogle Scholar
  92. Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Houberg-lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36PubMedGoogle Scholar
  93. Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor which binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247PubMedGoogle Scholar
  94. Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress–related genes in leaves. Mol Plant Microbe Interact 21:799–800PubMedGoogle Scholar
  95. Sikora RA, ZumFelde A, Mendoza A, Menjivar R, Pocasangre L (2010) In planta suppressiveness to nematodes and long-term root health stability through biological enhancement - do we need a cocktail? Acta Hort 879:553–560Google Scholar
  96. Singh LP, Gill SG, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191PubMedCentralPubMedGoogle Scholar
  97. Singh RK, Malik N, Singh S (2013) Improved nutrient use efficiency increases plant growth of rice with the use of IAA-overproducing strains of endophytic Burkholderia cepacia strain RRE25. Microb Ecol 66:375–384PubMedGoogle Scholar
  98. Soliman SSM, Trobacher CP, Tsao R, Greenwood JS, Raizada MN (2013) A fungal endophyte induces transcription of genes encoding a redundant fungicide pathway in its host plant. BMC Plant Biol 13:93PubMedCentralPubMedGoogle Scholar
  99. Stepniewska Z, Kuzniar A (2013) Endophytic microorganisms–promising applications in bioremediation of greenhouse gases. Appl Microbiol Biotechnol 97:9589–9596PubMedCentralPubMedGoogle Scholar
  100. Straub D, Rothballer M, Hartmann A, Ludewig U (2013) The genome of the endophytic bacterium H. frisingense GSF30T identifies diverse strategies in the Herbaspirillum genus to interact with plants. Front Microbiol 4:168PubMedCentralPubMedGoogle Scholar
  101. Strobel G (2006) Muscodor albus and its biological promise. J Ind Microbiol Biotechnol 33:514–522PubMedGoogle Scholar
  102. Strobel GA (2015) Bioprospecting-fuels from fungi. Biotechnol Lett. doi: 10.1007/s10529-015-1773-9 PubMedGoogle Scholar
  103. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268PubMedGoogle Scholar
  104. Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, Griffen M, Daniel Spakowicz D, Sears J (2008) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154:3319–3328PubMedGoogle Scholar
  105. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066PubMedCentralPubMedGoogle Scholar
  106. Tikhonovich IA, Provorov NA (2009) From plant–microbe interactions to symbiogenetics: a universal paradigm for the interspecies genetic integration. Ann Appl Biol 154:341–350Google Scholar
  107. Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63:169–180PubMedGoogle Scholar
  108. Van Bael SA, Estrada C, Rehner SA, Santos JF, Wcislo WT (2012) Leaf endophyte load influences fungal garden development in leaf-cutting ants. BMC Ecol 12:23PubMedCentralPubMedGoogle Scholar
  109. Van der Heijden MGA, Engel RS, Riedl R, Siegrist S, Neudecker A, Ineichen, Boller KT, Wiemken A, Sanders IA (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752PubMedGoogle Scholar
  110. Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JP (2002) Extensive fungal diversity in plant roots. Science 295:2051PubMedGoogle Scholar
  111. 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 3:122–138Google Scholar
  112. Wade MJ (2007) The co-evolutionary genetics of ecological interactions. Nat Rev Genet 8:185–195PubMedGoogle Scholar
  113. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391PubMedCentralPubMedGoogle Scholar
  114. Waqas M, Khan AL, Lee IJ (2014) Bioactive chemical constituents produced by endophytes and effects on rice plant growth. J Plant Interact 9:478–487Google Scholar
  115. Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364PubMedGoogle Scholar
  116. White JF Jr, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446PubMedGoogle Scholar
  117. Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Zahoor Ahmed Wani
    • 1
    • 3
  • Nasheeman Ashraf
    • 2
    • 3
  • Tabasum Mohiuddin
    • 2
    • 3
  • Syed Riyaz-Ul-Hassan
    • 1
    • 3
    Email author
  1. 1.Microbial Biotechnology DivisionCSIR-Indian Institute of Integrative MedicineJammu TawiIndia
  2. 2.Plant Biotechnology DivisionCSIR-Indian Institute of Integrative MedicineSrinagarIndia
  3. 3.Academy of Scientific and Innovative ResearchCSIR-Indian Institute of Integrative MedicineJammu TawiIndia

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