Potential Role of Endophytes in Sustainable Agriculture-Recent Developments and Future Prospects

  • Pranay JainEmail author
  • Ram Kumar Pundir
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 15)


Discovery of new solutions for the establishment of sustainable agricultural is essential that may avoid the heavy use of fertilizers and pesticides as a reliance of productivity booster. Plant associative beneficial microbes are expected to harness their contribution in integrated pest management schemes over the coming decades. There is global ever growing demand for implanting ecologically compatible and ecofriendly practices in agriculture, capable of providing adequate solutions for improving agriculture productivity. For these reasons, the endophytes prove to be an important alternative practice for long. The term endophyte is used to define those microorganisms which colonize in the plant tissues. These microorganisms induce plant growth using several mechanistic approaches such as biological nitrogen fixation, phytohormone production, phosphate solubilization, inhibition of ethylene biosynthesis, and tolerance to abiotic stresses by inducing resistance in plant to counteract against pathogenic attacks or by the release of secondary metabolites such as enzymes, siderophore, and antibiotics. The major factor that is contributing in sustainable agriculture involves choice of the plant, its age, and endophytic microorganisms which could adapt themselves in the plant tissues to be inhabited in. The basic knowledge of this kind of symbiotic relationship would assist in increasing crop production by using them as bioinoculants. The research on the ecology of endophytic bacteria will be most important contributing factor to capitalize on the agricultural returns from these microbes.


Agriculture sustainability Beneficial microorganisms Endophytes Plant growth-promoting potential 



The authors are grateful to the Hon’ble Vice-Chancellor, Kurukshetra University, Kurukshetra, for providing infrastructural facilities to carry out research on endophytes and Science and Engineering Research Board, Department of Science and Technology, New Delhi, for providing necessary funds. The authors are also grateful to Director, University Institute of Engineering and Technology (UIET), Kurukshetra University, Kurukshetra, Haryana (India), and the Management of Ambala College of Engineering and Applied Research (ACE), Devsthali, Ambala, Haryana (India), for their valuable support.


  1. Ahuja A, Ghosh SB, D’Souza SF (2007) Isolation of a starch utilizing, phosphate solubilizing fungus on buffered medium and its characterization. Bioresour Technol 98:3408–3411PubMedCrossRefGoogle Scholar
  2. Akello J, Dubois T, Coyne D, Kyamanywa S (2008) Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Protec 27(11):1437–1441Google Scholar
  3. Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6:159–163PubMedPubMedCentralCrossRefGoogle Scholar
  4. Akiyama K, Hayashi H (2001) Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots. Biosci Biotech Biochem 66:762–769CrossRefGoogle Scholar
  5. Anuar EN, Nulit R, Idris AS (2015) Growth promoting effects of endophytic fungus Phlebia GanoEF3 on oil palm (Elaeis guineensis) seedlings. Int J Agric Biol 17:135–141Google Scholar
  6. Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe DE (1989) Effect of tall fescue endophyte on plant response to environmental stress. Agron J 81:83–90CrossRefGoogle Scholar
  7. Azevedo JL, Maccheroni WJr, Pereira JO, Araujo WL (2000) Endophytic microorganisms: a review oninsect control and recent advances on tropical plants. Elect J Biotechnol 3:40–65Google Scholar
  8. Azevedo JL, Maccheroni JW, Araujo WL (2002) Microorganisms endophytic and its role in tropical plants. In: Biotechnology: Adv Agric Agribus 233–268Google Scholar
  9. Bacon CW, Hinton DM (2007) Bacterial endophytes: the endophytic niche, its occupants, and its utility. In: Gnanamanickam SS (ed.) Plant associated bacteria. Springer Science and Business Media, pp 155–194Google Scholar
  10. Bacon CW, White JF (2000) Microbial endophytes. Marcel Deker Inc., New York, pp 99–101Google Scholar
  11. Bal HB, Subhasis D, Tushar KD, Tapan KA (2013) ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants. Bas Microbiol 53(12):972–984CrossRefGoogle Scholar
  12. Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588PubMedCrossRefGoogle Scholar
  13. Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146:234–243PubMedCrossRefGoogle Scholar
  14. Barka AE, Gognies S, Nowak J, Audran J-C, Belarbi A (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Contr 24:135–142CrossRefGoogle Scholar
  15. Baverstock J, Elliot SL, Alderson PG, Pell JK (2005) Response of the entomopathogenic fungus Pandora neoaphidis to aphid-induced plant volatiles. J Invert Pathol 89(2):157–164CrossRefGoogle Scholar
  16. Betina V (1984) Indole derived tremorgenic toxins. In: Betina V (ed). Mycotoxins production, isolation, separation and purification. Developments in food science, vol 8. Elsevier, New York, p 415Google Scholar
  17. Bezerra JDP, Santos MGS, Svedese VM (2012) Richness of endophytic fungi isolated from Opuntia ficus-indica Mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 28(5):1989–1995PubMedCrossRefGoogle Scholar
  18. Bhagobaty RK, Joshi SR (2009) Promotion of seed germination of Green gram and Chick pea by Penicillium verruculosum RS7PF, a root endophytic fungus of Potentilla fulgens L. Adv Biotechnol 16–18Google Scholar
  19. Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis(Hubner) (Lepidoptera: Pyralidae) by endophyticBeauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211CrossRefGoogle Scholar
  20. Bing LA, Lewis LC (1992) Temporal relantionshipsbetween Zea mays, Ostrinia nubilalis (Hubner) (Lep: Pyralidae) and endophytic Beauveria bassiana (Balsamo) Vuillemin. Entomophaga 37:525–536CrossRefGoogle Scholar
  21. Bischoff JF, White JF Jr (2005) Evolutionary development of the Clavicipitaceae. In: Dighton J, White JF, Oudemans P (eds) The fungal community: its organization and role in the ecosystem. CRC Press, Boca RatonGoogle Scholar
  22. Bischoff KM, WicklowDT Jordan D et al (2009) Extracellular hemi cellulolytic enzymes from the maize endophyte Acremoniumzeae. Curr Microbiol 58(5):499–503PubMedCrossRefGoogle Scholar
  23. Bjornberg KE, Jonas E, Marstorp H, Tidaker P (2015) The role of biotechnology in sustainable agriculture: views and perceptions among key factors n the Sweedish food supply chain. Sustainability 7(6):7512–7529CrossRefGoogle Scholar
  24. Boddey RM (1995) Biological nitrogen fixation in sugarcane: a key to energetically viable biofuel production. Crit Rev Plant Sci 14:209–266CrossRefGoogle Scholar
  25. Boddey RM, de Oliveira OC, Urquiaga S, Reis VM, Olivares FL, Baldani VLD, Döbereiner J (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant Soil 174:195–209CrossRefGoogle Scholar
  26. Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotech 27:30–37PubMedPubMedCentralCrossRefGoogle Scholar
  27. Burd GI, Dixon DG, Glick BR (1998) A plant growth promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668PubMedPubMedCentralGoogle Scholar
  28. Cao L, Qiu Z, You J, Tan H, Zhou S (2005) Isolation and characterization of endophytic Streptomycesantagonists of Fusarium wilt pathogen from surface sterilized banana roots. FEMS Microbiol Lett 247:147–152. doi: 10.1016/j.femsle.2005.05.006 PubMedCrossRefGoogle Scholar
  29. Carroll G (1986) Fungal associates of woody plants asinsect antagonists in leaves and stems. In: Inarbosa P, Krischik VA, Jones CG (eds) Microbial mediation of plant herbivore interactions. Wiley, New York, pp 253–271Google Scholar
  30. Carroll GC (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2–9CrossRefGoogle Scholar
  31. Castillo UF, Strobel GA, Ford EJ, Hess WM, Porter H, Jensen JB, Albert H, Robison R, Condron MA, Teplow DB, Stevens D, Yaver D (2002) Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology 148(9):P2675–P2685CrossRefGoogle Scholar
  32. Choi WY, Rim SO, Lee JH, Lee JM, Lee IJ, Cho KJ (2005) Isolation of gibberellins-producing fungi from the root of several Sesamum indicum plants. J Microbiol Biotechnol 15:22–28Google Scholar
  33. Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87(5):455–462CrossRefGoogle Scholar
  34. Compant S, Duffy B, Nowak J, Clément C, Ait Barka E (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microb 71:4951–4959CrossRefGoogle Scholar
  35. Dobereiner J, Boddey RM (1981) Nitrogen fixation in association with graminae. Current perspectives in nitrogen fixation. Aust Acad Sci 305–312Google Scholar
  36. El-Shatoury S, El-Kraly O, El-Kazzaz W, Dewedar A (2009) Antimicrobial activities of Actinomycetes inhabiting Achillea fragrantissima (Family: Compositae) Egypt J Nat Toxins 6(2):1–15Google Scholar
  37. El-Tarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupine caused by Plectosporium tabacinum. Aust J Bot 51:257–266. doi: 10.1071/BT02107 CrossRefGoogle Scholar
  38. El-Tarabily KA, Sivasithamparam K (2006) Nonstreptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem 38:1505–1520. doi: 10.1016/j.soilbio.2005.12.017 CrossRefGoogle Scholar
  39. El-Tarabily KA, Hardy GE, St J, Sivasithamparam K (2010) Performance of three endophytic actinomycetes in relation to plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber under commercial field production conditions in the United Arab Emirates. Eur J Plant Pathol 128:527–539. doi: 10.1007/s10658-010-9689-7 CrossRefGoogle Scholar
  40. Fahey W (1988) Endophytic bacteria for the delivery of agrochemicals to plants. In: Cutler HG (ed) Biologically active natural products. American Chemical Society, Washington, DC, pp 120–128CrossRefGoogle Scholar
  41. Fernandez O, Theocharis A, Bordiec S, Feil R, Dhont-Cordelier S, Bailleuil F, Clement C, Fontaine F, Ait Barka E (2013) Interaction between Burkholderia phytofirmans and grapevine: link between modulation of carbohydrate metabolism and induced tolerance to low temperatures. In: Schneider C, Leifert C, Feldmann F (eds) Endophytes for plant protection: the state of the art. Deutsche Phytomedizinische Gesellschaft, BraunschweigGoogle Scholar
  42. Foley JA, Defries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309(5734):570–574PubMedCrossRefGoogle Scholar
  43. Fouda AH, El-Din Hassan S, Eid AM, El-Din Ewais E (2015) Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss). Ann Agric Sci 60(1):95–104Google Scholar
  44. Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750PubMedCrossRefGoogle Scholar
  45. Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87CrossRefGoogle Scholar
  46. Gangwar M, Dogra S, Gupta UP, Kharwar RN (2014) Diversity and biopotential of endophytic actinomycetes from three medicinal plants in India. Afr J Microbiol Res 8(2):184–191. doi: 10.5897/AJMR2012.2452 CrossRefGoogle Scholar
  47. Giménez C, Cabrera R, Reina M, Coloma-González A (2007) Fungal endophytes and their role in plant protection. Curr Org Chem 11:707–720CrossRefGoogle Scholar
  48. Gómez-Vidal S, Salinas J, Tena M, Lopez-Llorca LV (2009) Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi. Electrophoresis 30(17):2996–3005PubMedCrossRefGoogle Scholar
  49. Gough C, Galera C, Vasse J, Webster G, Cocking EC, Denarie J (1997) Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol Plant Microbe Interact 10:560–570PubMedCrossRefGoogle Scholar
  50. Griffith GW, Hedger JN (1994) The breeding biology of biotypes of the witches’ broom pathogen of cacao, Crinipellis perniciosa. Heredity 72:278–289CrossRefGoogle Scholar
  51. Haddad N, Krimi Z, Raio A (2013) Endophytic bacteria from weeds promotes growth of tomato plants in vitro and in greenhouse. In: Schneider C, Leifert C, Feldmann F (eds) Endophytes for plant protection: the state of the art. Deutsche Phytomedizinische Gesellschaft, BraunschweigGoogle Scholar
  52. Halmann J, Quadt-Hallmann A, Mahaffee WF (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  53. Hamayun M, Khan SA, Ahmad N, Khan AL, Rehman G, Sohn EY, Kim SK, Joo GJ, Lee I-J (2009a) Phoma herbarum as a new gibberellin producing and plant growth-promoting fungus. J Microbiol Biotechnol 19:1244–1249PubMedGoogle Scholar
  54. Hamayun M, Khan SA, Ahmad N, Tang DS, Kang SM, Sohn E-Y, Hwang YH, Shin DH, Lee BH, Kim JG, Lee I-J (2009b) Cladosporium sphaerospermum as a new plant growth promoting endophyte from the roots of Glycine max (L.) Merr. World J Microbiol Biotechnol 25:627–632CrossRefGoogle Scholar
  55. Hamayun M, Khan SA, Khan MA, Khan AL, Kang SM, Kim SK, Joo GJ, Lee IJ (2009c) Gibberellin production by pure cultures of a new strain of Aspergillus fumigatus. World J Microbiol Biotechnol 25:1785–1792CrossRefGoogle Scholar
  56. Hamayun M, Khan SA, Khan AL, Rehman G, Kim Y-H, Iqbal I, Hussain J, Sohn E-Y, Lee I-J (2010) Gibberllin production and plant growth promotion from pure cultures of Cladosporium sp.MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia 102(5):989–995PubMedCrossRefGoogle Scholar
  57. Hart MM, Trevors JT (2005) Microbe management: application of mycorrhyzal fungi in sustainable agriculture. Front Ecol Environ 3:533–539CrossRefGoogle Scholar
  58. Hasan HAH (2002) Gibberellin and auxin production by plant root fungi and their biosynthesis under salinity-calcium interaction. Rostlinná Výroba 48:101–106Google Scholar
  59. Hassan SED, Liu A, Bittman S, Forge TA, Hunt DE, Hijri M, St-Arnaud M (2013) Impact of 12-year field treatments withorganic and inorganic fertilizers on crop productivity and mycorrhizalcommunity structure. Biol Fertil Soil 49:1109–1121CrossRefGoogle Scholar
  60. Hawksworth DL (2004) Fungal diversity and its implications for genetic resource collections. Stud Mycol 50:9–18Google Scholar
  61. He X, Han G, Lin Y et al (2012) Diversity and decomposition potential of endophytes in leaves of a Cinnamomum camphora plantation in China. Ecol Res 27(2):273–284CrossRefGoogle Scholar
  62. Jalgaonwala RE, Mohite BV, Mahajan RT (2011) A review: natural products from plant associated endophytic fungi. J Microbiol Biotech Res 1(2):21–32Google Scholar
  63. Jallow MFA, Dugassa-Gobena D, Vidal S (2004) Indirect interaction between and unspecialized endophytic fungus and a polyphagous moth. Basic Appl Ecol 5(2):183–191CrossRefGoogle Scholar
  64. Janarthine Rylo Sona S, Eganathan P (2012) Plant growth promoting endophytic Sporosarcina aquimarina SjAM 16103 isolated from the pneumatophores of Avicennia marina L. Int J Microbiol 12: doi: 10.1155/2012/532060
  65. Jankiewicz U, Kołtonowicz M (2012) The involvement of Pseudomonas bacteria in induced systemic resistance in plants. Prikl Biokhim Mikrobiol 48:276–281PubMedGoogle Scholar
  66. Jerry B (1994) A role of endophytic fungi in regulating nutrients and energy in plants within a desert ecosystem. International symposium and workshop on desertification in developed countries. Accessed on 2011/10/25Google Scholar
  67. Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33:797–802CrossRefGoogle Scholar
  68. Joseph B, Mini Priya R (2011) Bioactive compounds fromendophytes and their potential in pharmaceutical effect: a review. Am J Biochem Mol Biol 1(3):291–309CrossRefGoogle Scholar
  69. Kawaguchi M, Sydn K (1996) The excessive production of indole-3-acetic acid and its significance in studies of the biosynthesis of this regulator of plant growth and development. Plant Cell Physiol 37:1043–1048PubMedCrossRefGoogle Scholar
  70. Kawaide H (2006) Biochemical and molecular analysis of gibberellins biosynthesis in fungi. Biosci Biotech Biochem 70:583–590CrossRefGoogle Scholar
  71. Khan SA, Hamayun M, Yoon HJ, Kim H-Y, Suh SJ, Hwang SK, Kim JM, Lee I-J, Choo YS, Yoon UH, Kong WS, Lee BM, Kim JG (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:231PubMedPubMedCentralCrossRefGoogle Scholar
  72. Khan AA, Jilani G, Akhtar MS, Naqvi SMS, Rasheed M (2009a) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. J Agric Biol Sci 1:48–58Google Scholar
  73. Khan SA, Hamayun M, Kim HY, Yoon HJ, Lee IJ, Kim JG (2009b) Gibberellin production and plant growth promotion by a newly isolated strain of Gliomastix murorum. World J Microbiol Biotechnol 25:829–833CrossRefGoogle Scholar
  74. Khan SA, Hamayun M, Kim HY, Yoon HJ, Seo JC, Choo YS, Lee I-J, Kim SD, Rhee IK, Kim JG (2009c) A new strain of Arthrinium phaeospermum isolated from Carex kobomugi Ohwi is capable of gibberellin production. Biotechnol Lett 31:283–287PubMedCrossRefGoogle Scholar
  75. Khan AL, Hamayun M, Ahmad N, Waqas M, Kang SM, Kim YH, Lee IJ (2011a) Exophiala sp. LHL08 reprograms Cucumis sativus to higher growth under abiotic stresses. Physiol Plant 143(4):329–343PubMedCrossRefGoogle Scholar
  76. Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011b) Ameliorative symbiosis of endophyte (Penicillium funiculosum sp. LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49(8):852–862PubMedCrossRefGoogle Scholar
  77. Khan AL, Hamayun M, Kim YH, Kang SM, Lee JH, Lee IJ (2011c) Gibberellins producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, isoflavonoids production and plant growth in salinity stress. Process Biochem 46:440–447CrossRefGoogle Scholar
  78. Kloepper JW, Ryu CM (2006) Bacterial endophytes as elicitors of induced systemic resistance. Soil Biol 9:33–52CrossRefGoogle Scholar
  79. Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. Microbial Endophytes, pp 199–233Google Scholar
  80. Kuklinsky-Sobral K, Araujo WL, Mendonca C, Geran LC, Piskala A, Azevedo JL (2004) Isolationand characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251PubMedCrossRefGoogle Scholar
  81. Ladha JK, Reddy PM (2000) Steps towards nitrogen fixation in Rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. International Rice Research Institute, Manila, Philippines, pp 33–46Google Scholar
  82. Lana TG, Azevedo JL, Pomella AWV, Monteiro RTR, Silva CB, Araujo WL (2011) Endophytic and pathogenic isolates of the cacao fungal pathogen Moniliophthora perniciosa (Tricholomataceae) are indistinguishable based on genetic and physiological analysis. Genet Mol Res 10:326–334PubMedCrossRefGoogle Scholar
  83. Li J, Zhao G-Z, Huang H-Y et al (2012) Isolation and characterization of culturable endophytic actinobacteria associated with Artemisia annua L. Antony van Leeuwenhoek 101(3):515–527CrossRefGoogle Scholar
  84. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Ann Rev Microbiol 63:541–556CrossRefGoogle Scholar
  85. Luo S, Xu T, Chen L et al (2012) Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Appl Microbiol Biotechnol 93(4):1745–1753PubMedCrossRefGoogle Scholar
  86. Machungo C, Losenge T, Kahangi E, Coyne D, Dubois T, Kimenju J (2009) Effect of endophytic Fusarium oxysporum on growth of tissue-cultured Banana plants. Afr J Hort Sci 2:160–167Google Scholar
  87. MacMillan J (2002) Occurrence of gibberellins in vascular plants, fungi and bacteria. J Plant Growth Reg 20:387–442CrossRefGoogle Scholar
  88. Maheshwari DK (2013) Bacteria in Agrobiology: disease management. Springer Science & Business Media, Heidelberg, Germany, p 495CrossRefGoogle Scholar
  89. Maheshwari DK, Dheeman S, Agarwal M (2015) Phytohormone producing PGPR for sustainable agriculture. In: Maheshwari DK (ed) Bacterial metabolite in sustainable agroecosystem. Springer International Publishing, pp 159–182Google Scholar
  90. Mahmoud RS, Narisawa K (2013) A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS One 8(11):e78746. doi: 10.1371/journal.pone.0078746 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Malinowski DP, Belesky DP (1999) Neotyphodium coenophialum- endophyte infection affects the ability of tall fescue to use sparingly available phosphorus. J Plant Nutr 22:835–853CrossRefGoogle Scholar
  92. Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil 227(1–2):115–126CrossRefGoogle Scholar
  93. Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar specific bacterial endophyte community in potato roots. Microb Ecol 60(1):157–166PubMedCrossRefGoogle Scholar
  94. Marella S (2014) Bacterial endophytes in sustainable crop production: applications, recent developments and challenges ahead. Int J Life Sci Res 2(2):46–56Google Scholar
  95. Mariano RLR, Silveira EB, Assis SMP (2004) Importancia de bacterias promotoras de crescimento e de biocontrole de doencas de plantas para uma agricultura sustentavel. An Acad Pernamb Cien Agron Recife 1:89–111Google Scholar
  96. Marina S, Angel M, Silva-Flores MA, Cervantes-Badillo MG, Rosales- Saavedra MT, Islas-Osuna MA, Casas-Flores S (2011) The plant growth-promoting fungus Aspergillus ustus promotes growth and induces resistance against different lifestyle pathogens in Arabidopsis thaliana. J Microbiol Biotechnol 21(7):686–696CrossRefGoogle Scholar
  97. Mastretta C, TaghaviS, van der Lelie D et al (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremed 11(3):251–267Google Scholar
  98. McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–268CrossRefGoogle Scholar
  99. Miche L, Balandreau J (2001) Effects of rice seed surface sterilization with hypochlorite on inoculated Burkholderia vietnamiensis. Appl Environ Microbiol 67:3046–3052PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ming Q, Su C, Zheng C, Jia M, Zhang Q, Zhang H, Rahman K, Han T, Qin L (2013) Elicitors fromthe endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J Exp Bot (E-pub ahead of print)Google Scholar
  101. Muller 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(7):1801–1810PubMedCrossRefGoogle Scholar
  102. Muńoz A, Gandía M, Harries E, Carmona L, Read ND, Marcos JF (2013) Understanding the mechanism of action of cell penetrating antifungal peptides using the rationally designed hexapeptide PAF26 as a model. Fungal Biol Rev 26:146–155CrossRefGoogle Scholar
  103. Muthukumarasamy R, Cleenwerck I, Revathi G, Vadivelu M, Janssens D, Hoste B, Gum KU, Park K, Son CY, Sa T, Caballero-Mellado J (2005) Natural association of Gluconoacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28:277–286PubMedCrossRefGoogle Scholar
  104. Nadeem A, Hamayun M, Khan SA, Khan AL, Lee IJ, Shin DH (2010) Gibberellin-producing endophytic fungi isolated from Monochoria vaginalis. J Microbiol Biotechnol 20(12):1744–1749Google Scholar
  105. Nath R, Sharma GD, Barooah M (2012) Efficiency of tricalcium phosphate solubilization by two different endophytic Penicillium sp. isolated from tea (Camelia sinensis L.). Er. J Exp Biol 2(4):1354–1358Google Scholar
  106. Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014) Drought stress amelioration in wheat throughinoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73:121–131CrossRefGoogle Scholar
  107. Newman L, Reynolds C (2005) Bacteria and phyto-remediation: new uses for endophytic bacteria in plants. Trend Biotechnol 23:6–8CrossRefGoogle Scholar
  108. Ngamau CN, Matiru VN, Tani A, Muthuri CW (2014) Potential use of endophytic bacteria as biofertilizer for sustainable banana (Musa spp.) production. Afr J Hort Sci 8:1–11Google Scholar
  109. Nigris S, Baldan E, Zottini M, Squartini A, Baldan B (2013) Is the bacterial endophyte community, living in Glera (Vitis vinifera) plants, active in biocontrol? In: Schneider C, Leifert C, Feldmann F (eds) Endophytes for plant protection: the state of the art. Deutsche Phytomedizinische Gesellschaft, BraunschweigGoogle Scholar
  110. Niu D, Liu H, Jiang C, Wang Y, Jin H, Guo J (2011) The plant growth–promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana, by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant Microb 24:533–542CrossRefGoogle Scholar
  111. Okon Y, Labandera-Gonzalez C (1994) Agronomic application of Azospirillum- An evaluation of 20 years worldwide field incubation. Soil Biol Biochem 26:1591–1601CrossRefGoogle Scholar
  112. Panka D, Piesik D, Jeske M, Musial N, Koczwara K (2013) Emission of volatile organic compounds by perennial ryegrass (Lolium perenne, L.)/Neptyphodium lolii association as a defense reaction towards infection by Fusarium poae and Rhizoctonia solani. In: Schneider C, Leifert C, Feldmann F (eds) Endophytes for plant protection: the state of the art. Braunschweig, Deutsche Phytomedizinische Gesellschaft, pp 121–122Google Scholar
  113. Park KH, Lee O, Jung H, Jeong J, Jeon Y, Hwang D, Lee C, Son H (2010) Rapid solubilization of insoluble phosphate by a novel environmental stress-tolerant Burkholderia vietnamiensis M6 isolated from ginseng rhizospheric soil. Appl Microbiol Biotechnol 86:947–955PubMedCrossRefGoogle Scholar
  114. Pennisi E (2001) The push to pit genomics against fungal pathogens. Sci 292:2273–2274CrossRefGoogle Scholar
  115. Peterson RL, Wagg C, Pautler M (2008) Associations between microfungal endophytes and roots: do structural features indicate function? Botany 86:445–456CrossRefGoogle Scholar
  116. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soilborne microbes. Trend Plant Sci 15:507–514CrossRefGoogle Scholar
  117. Posada F, Vega FE (2005) Establishment of the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte in cocoa seedlings (Theobromacacao). Mycologia 97:1195–1200PubMedCrossRefGoogle Scholar
  118. Posada F, Vega FE (2006) Inoculation and colonization of coffee seedlings (Coffea arabica L.) with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycosci 47(5):284–289Google Scholar
  119. Qadri M, Johri S, Shah BA, Khajuria A, Sidiq T, Lattoo SK, Abdin MZ, Riaz-Ul-Hassan S (2013) Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. SpringerPlus 2:8PubMedPubMedCentralCrossRefGoogle Scholar
  120. Rabin LB, Pacovsky RS (1985) Rduced larva growth of two Lepidoptera (Noctuidae) on excised leaves of soybean infected with amycorrhizal fungus. J Econ Entom 78:1358–1363CrossRefGoogle Scholar
  121. Rademacher W (1994) Gibberellin formation in microorganisms. Plant Growth Reg 15:303–314CrossRefGoogle Scholar
  122. Rai M, Acharya D, Singh A (2001) Positive growth responses of the medicinal plantsSpilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128PubMedCrossRefGoogle Scholar
  123. Redecker D, Vonbereswordtwallrabe P, Beck DP (1997) Influence of inoculation with arbuscular mycorrhizal fungi on stable isotopes of nitrogen in Phaseolus vulgaris. Biol Fertil Soil 24:344–346CrossRefGoogle Scholar
  124. Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14(4):435–443PubMedCrossRefGoogle Scholar
  125. Reis VM, Baldani JI, Baldani VLD, Döbereiner J (2000) Biological nitrogen fixation in gramineae and palm trees. Crit Rev Plant Sci 19:227–247CrossRefGoogle Scholar
  126. Ren JH, Ye JR, LiuH XuXL, Wu XQ (2011) Isolation and characterization of a new Burkholderia pyrrocinia strain JK-SH007 as a potential biocontrol agent. World J Microbiol Biotechnol 27(9):2203–2215CrossRefGoogle Scholar
  127. Richardson MD, Chapman GW, Hoveland CS, Bacon CW (1992) Sugar alkohols in endophyte-infected tall fescue. Crop Sci 32:1060–1061CrossRefGoogle Scholar
  128. Rodriguez RJ, Henson J, Volkenburgh EV, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerancein plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefGoogle Scholar
  129. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330PubMedCrossRefGoogle Scholar
  130. Rosenblueth M, Martinez-Romero E (2006) Bacterialendophytes and their interactions with hosts. Mol Plant Microbe Interac J 19(8):827–837CrossRefGoogle Scholar
  131. Rothballer M, Eckert B, Schmid M, Fekete A, Schloter M, Lehner A, Pollmann S, Hartmann A (2008) Endophytic root colonization of gramineous plants by Herbaspirillum frisingense. FEMS Microbiol Ecol 66:85–95PubMedCrossRefGoogle Scholar
  132. Rowan DD, Hunt MB, Gaynor DL (1986) Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae. J Chem Soc, Chem Commun 1986:935–936Google Scholar
  133. Rubini MR, Silva-Ribeiro R, Pomella AWV, Maki C, Araújo WL, Santos DR, Azevedo JL (2005) Diversity of endophytic fungal community of cacao (Theobromacacao) L. and biological control of Crinipellis perniciosa causal agent of Witches’ broom disease. Int J Biol Sci 1:24–33PubMedPubMedCentralCrossRefGoogle Scholar
  134. Rungin S, Indanand C, Suttiviriya P, Kruasuwan W, Jaemsaeng R, Thamchaipenet A (2012) Plant growth enhancing effects by a siderophore producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105) Antony van Leeuwenhoek 102:463–472 doi: 10.1007/s10482-012-9778-z
  135. Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones EBG (2008) Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oilpalm, Elaeis guineensis, in Thailand. Fungal Divers 33:139–161Google Scholar
  136. Russel JR, Huang J, Anand P et al (2011) Biodegradation of polyester polyurethane by endophytic fungi. Appl Environ Microbiol 77(17):6076–6084Google Scholar
  137. Rutschmann J, Stadler PA (1978) Chemical background. In: Berde B, Schild HO (eds) Ergot alkaloids and related compounds. Springer, Berlin, GermanyGoogle Scholar
  138. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Ann Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  139. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedCrossRefGoogle Scholar
  140. Schulz B, Römmert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103:1275–1283CrossRefGoogle Scholar
  141. Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39:23–32PubMedCrossRefGoogle Scholar
  142. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes- sustainable approach for managing phosphorous deficiency in agricultural soils. SpringerPlus 2:507CrossRefGoogle Scholar
  143. Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller R (2005) The endophyticfungus Piriformospora indica stimulates the expression of nitrate reductase and the starchdegrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeo domain transcription factor that binds to a conserved motif in their promoters. J Bot Chem 280:26241–26247Google Scholar
  144. Shiomi HF, Silva HSAS, de Melo IS, Nunes FV, Bettiol W (2006) Bioprospecting endophytic bacteria for biological control of coffee leaf rust. Sci Agric (Piracicaba, Braz.) 63(1):32–39Google Scholar
  145. Shweta S, Zuehlke S, Ramesha BT, Priti V, Mohana Kumar P, Ravikant G, Spiteller M, Vasudeva R, Uma SR (2010) Endophytic fungal strains of Fusarium solani, from Apodytes dimidiata E.Mey. ex Arn (Icacinaceae) produce camptothecin, 10-hydroxycamptothecin and 9-methoxycamptothecin. Phytochem 71(1):117–122CrossRefGoogle Scholar
  146. Sieber TN (2002) Fungal root endophytes. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, BaselGoogle Scholar
  147. Singh A, Sharma J, Rexer KH, Varma A (2000) Plant productivity determinants beyond minerals, water and light: Piriformospora indica—a revolutionary plant growth promoting fungus. Curr Sci 79:1548–1554Google Scholar
  148. Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainableagriculture and environmental development. Agric Ecosyst Environ 140(3–4):339–353CrossRefGoogle Scholar
  149. Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plant 131(4):581–589PubMedCrossRefGoogle Scholar
  150. Souza SA, Xavier AA, Costa MR, Cardoso AM, Pereira MC, Nietsche S (2013) Endophytic bacterialdiversity in banana ‘Prata Ana’ (Musa spp.) roots. Genetic. Mol Biol 36(2):252–264Google Scholar
  151. Spaepen S, Vanderleyden J (2011) Auxin and plant microbe interaction. Perspect Biol 3:a001438 First published online November 17, 2010. doi: 1101/cshperspect.a001438
  152. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedCrossRefGoogle Scholar
  153. Srivastava R, Mehta CM, Sharma AK (2011) Fusarium pallidoroseum- A new biofertilizer responsible for enhancing plant growth in different crops. Int Res J Microbiol 2(6):192–199Google Scholar
  154. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502PubMedPubMedCentralCrossRefGoogle Scholar
  155. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplartrees. Appl Environ Microbiol 75:748–757PubMedCrossRefGoogle Scholar
  156. Tan HM, Cao LX, He ZF, Su GJ, Lin B, Zhou SN (2006) Isolation of endophytic actinomycetes from different cultivars of tomato and their activities against Ralstonia solanacearum in vitro. World J Microbiol Biotechnol 22:1275–1280. doi: 10.1007/s11274-006-9172-y CrossRefGoogle Scholar
  157. Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050PubMedCrossRefGoogle Scholar
  158. Tefera T, Vidal (2009) Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. Biocontrol 54(5):663–669CrossRefGoogle Scholar
  159. Terekhova VA, Semenova TA (2005) The structure of micromycete communities and their synecologic interactions with basidiomycetes during plant debris decomposition. Microbiol 74(1):91–96CrossRefGoogle Scholar
  160. Thormann MN, Currah RS, Bayley SE (2003) Succession of microfungal assemblages in decomposing peatland plants. Plant Soil 250(2):323–333CrossRefGoogle Scholar
  161. Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark, septate endophytic fungus, Heteroconium chaetospira and a nonmycorrhizal plant, Chinese cabbage. Mycology 99:175–184CrossRefGoogle Scholar
  162. Van Bael SA, Maynard Z, Rojas E, Mejia LC, Kyllo DA, Herre EA, Robbins N, Bischoff JF, Arnold AE (2005) Emerging perspectives on the ecological roles of endophytic fungi in tropical plants. In: Dighton J, White JF, Oudemans P (eds) The fungal community: its organization and role inthe ecosystem. CRC Press, Boca RatonGoogle Scholar
  163. van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254CrossRefGoogle Scholar
  164. Vandenbussche F, Fierro AC, Wiedemann G, Reski R, van der Straeten D (2007) Evolutionary conservation of plant gibberellin signaling pathway components. BMC Plant Biol 7:65PubMedPubMedCentralCrossRefGoogle Scholar
  165. Varma A, Verma S, Sudha Nirmal S, Bütehorn B, Franken P (1998) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65(6):2741–2744Google Scholar
  166. Varma A, Verma S, Sudha Sahay N, Butehorn B, Franken P (1999) Piriformospora indica, a cultivableplant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744PubMedPubMedCentralGoogle Scholar
  167. Vega FE, Posada F, Aime MC, Pava-Ripoll M, Infante F, Rehner SA (2008) Entomopathogenic fungal endophytes. Biol Cont 46:72–82Google Scholar
  168. Verma S, Varma A, Rexer KH, Hassel A, Kost G, SarbhoyA Bisen P, Butehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycology 90:896–903CrossRefGoogle Scholar
  169. 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 Piriformis indica reprograms barley to salt-stress tolerance, disease resistance andhigher yield. Proc Natl Acad Sci USA102:13386–13391Google Scholar
  170. Walters D, Walsh D, Newton A, Lyon G (2005) Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95:1368–1373PubMedCrossRefGoogle Scholar
  171. Wang S, Hu T, Jiao Y, Wei J, Cao K (2009) Isolation and characterizationof Bacillus subtilis EB-28, an endophytic bacterium strain displaying biocontrol activity against Botrytis cinerea Pers. Front Agric China 3(3):247–252CrossRefGoogle Scholar
  172. Waqas M, Khan AL, Hamayun M, Kamran M, Kang SM, Kim YH, Lee IJ (2012) Assessment of endophytic fungi cultural filtrate on soybean seed germination. Afr J Biotechnol 11(85):15135–15143Google Scholar
  173. West CP, Gwinn KD (1993) Role of Acremonium in drought, pest and disease tolerance of grasses. In: Hume DE, Latch GCM, Easton HS (eds) Proceedings II International Symposium Acremonium/grass interactions: plenary papers. AgResearch, Grasslanda Research Centre, Palmerston North, NZGoogle Scholar
  174. Xin G, Zhang G, Kang JW, Staley JT, Doty SL (2009) Adiazotrophic, indole-3-acetic acid-producing endophyte from wild cottonwood. Biol Fert Soil 45(6):669–674CrossRefGoogle Scholar
  175. You YH, Yoon H, Kang SM, Shin JH, Choo YS, Lee IJ, Lee JM, Kim JG (2012) Fungal diversity and plant growth promotion of endophyticfungi from six halophytes in Suncheon Bay. J Microbiol Biotechnol 22(11):1549–1556PubMedCrossRefGoogle Scholar
  176. Zabalgogeazcoa I, Ciudad AG, Vázquez de Aldana BR, Criado BG (2006) Effects of the infection by the fungal endophyte Epichloë festucae in the growth and nutrient content of Festuca rubra. Eur J Agron 24:374–384CrossRefGoogle Scholar
  177. Zhang DX, Nagabhyru P, Schardl CL (2009) Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants. Plant Physiol 150(2):1072–1082PubMedPubMedCentralCrossRefGoogle Scholar
  178. Zhang X, Li J, Qi G, Wen K, Lu J, Zhao X (2011) Insecticidal effect of recombinant endophytic bacteriumcontaining Pinelliaternata agglutinin against white backed planthopper, Sogatellafurcifera. Crop Protec 30(11):1478–1484CrossRefGoogle Scholar
  179. Zhang X, Lin L, Zhu Z, Yang X, Wang Y, An Q (2013) Colonization and modulation of host growth and metal uptake by endophytic bacteria of Sedum alfredii. Int J Phytoremediation 15(1):51–64PubMedCrossRefGoogle Scholar
  180. Zhao X, Qi G, Zhang X, LanN, Ma X (2010) Controlling sapsuckinginsect pests with recombinant endophytes expressing plant lectin. Nature Proc vol 21, article 21Google Scholar
  181. Zou WX, Tan RX (1999) Advances in plant science, vol 2. China Higher Education Press, Beijing, pp 183–190Google Scholar

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Authors and Affiliations

  1. 1.Department of BiotechnologyUniversity Institute of Engineering and Technology (UIET), Kurukshetra UniversityHaryanaIndia
  2. 2.Department of BiotechnologyAmbala College of Engineering and Applied Research (ACE)HaryanaIndia

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