Seed Endophytes in Crop Plants: Metagenomic Approaches to Study the Functional Roles and Interactions

  • Priyanka Verma


Seed endophytes play a key role in increasing plant health and growth in both managed and natural ecosystems. These can be applied in agricultural production or for the phytoremediation of pollutants. However, because of their capacity to confer plant beneficial effects, efficient colonization of the plant environment is of utmost importance. The majority of endophytes derives from the soil environment. They may migrate to the rhizosphere and subsequently the rhizoplane of their hosts before they are able to show beneficial effects. These endophytes can also penetrate plant roots, and may move to aerial plant parts. A better understanding on colonization processes has been obtained mostly by microscopic visualization as well as by analyzing the characteristics of mutants carrying disfunctional genes potentially involved in colonization. In this chapter we describe the different metagenomic approaches of seed colonization and survey the known mechanisms responsible for endophytic competence. The understanding of seed colonization processes is important to better predict how endophytes interact with seeds.


Seed endophytes Agriculture Metagenomic approaches Phytoremediation 



The authors are grateful to the Department of Microbiology, Akal College of Basic Science, Eternal University, Himachal Pradesh, for providing the facilities and financial support.


  1. Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genomics Data 6:159–163PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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:e53214PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arachevaleta M, Bacon C, Hoveland C, Radcliffe D (1989) Effect of the tall fescue endophyte on plant response to environmental stress. Agron J 81:83–90CrossRefGoogle Scholar
  4. Araújo WL, Marcon J, Maccheroni W, van Elsas JD, van Vuurde JW, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68:4906–4914PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bacon C, Hinton D (1997) Isolation and culture of endophytic bacteria and fungi. ASM Press, Washington, DCGoogle Scholar
  6. Barac T et al (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583PubMedCrossRefPubMedCentralGoogle Scholar
  7. Barnett MJ, Toman CJ, Fisher RF, Long SR (2004) A dual-genome symbiosis chip for coordinate study of signal exchange and development in a prokaryote–host interaction. Proc Natl Acad Sci 101:16636–16641PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bartholdy B, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals 14:33–42PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bashan Y, Harrison SK, Whitmoyer RE (1990) Enhanced growth of wheat and soybean plants inoculated with Azospirillum brasilense is not necessarily due to general enhancement of mineral uptake. Appl Environ Microbiol 56:769–775PubMedPubMedCentralGoogle Scholar
  10. Bezerra J, Santos M, Svedese V, Lima D, Fernandes M, Paiva L, Souza-Motta C (2012) Richness of endophytic fungi isolated from Opuntia ficus-indica mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 28:1989–1995PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bhuyan S, Bandyopadhyay P, Yadava P (2015) Extraction of proteins for two-dimensional gel electrophoresis and proteomic analysis from an endophytic fungus. Protoc Exch. doi
  12. Bischoff KM, Wicklow DT, Jordan DB, de Rezende ST, Liu S, Hughes SR, Rich JO (2009) Extracellular hemicellulolytic enzymes from the maize endophyte Acremonium zeae. Curr Microbiol 58:499–503PubMedCrossRefPubMedCentralGoogle Scholar
  13. Brinkerhoff L, Hunter R (1963) Internally infected seed as a source of inoculum for the primary cycle of bacterial blight of cotton. Phytopathology 53:1397–1401Google Scholar
  14. Brundrett MC (2006) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In: Microbial root endophytes. Springer, Heidelberg, pp 281–298CrossRefGoogle Scholar
  15. Camilios-Neto D et al (2014) Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genomics 15:378PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345PubMedCrossRefPubMedCentralGoogle Scholar
  17. Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2–9CrossRefGoogle Scholar
  18. Carroll GC (1991) Fungal associates of woody plants as insect antagonists in leaves and stems. In: Barbosa P, Krischik VA, Jones CG (eds) Microbial mediation of plant-herbivore interactions. John Wiley and Son, New York, pp 253–271Google Scholar
  19. Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340:347–355CrossRefGoogle Scholar
  20. Chareprasert S, Piapukiew J, Thienhirun S, Whalley AJ, Sihanonth P (2006) Endophytic fungi of teak leaves Tectona grandis L. and rain tree leaves Samanea saman Merr. World J Microbiol Biotechnol 22:481–486CrossRefGoogle Scholar
  21. Chen C, Bauske E, Musson G, Rodriguez-Kabana R, Kloepper J (1995) Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biol Control 5:83–91CrossRefGoogle Scholar
  22. Chen Y, Mei R, Lu S, Liu L, Kloepper J (1996) The use of yield increasing bacteria (YIB) as plant growth-promoting rhizobacteria in Chinese agriculture. In: Utkhede RS, Gupta VK (eds) Management of soil born diseases. Kalyani Publishers, Ludhiana, pp 165–184Google Scholar
  23. Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744PubMedCrossRefPubMedCentralGoogle Scholar
  24. Das A (2009) Symbiosis: the art of living. In: Varma A, Kharkwal AC (eds) Symbiotic fungi principles and practice. Springer, BerlinGoogle Scholar
  25. De Bary A (1879) Die erscheinung der symbiose. Verlag von Karl J Trübner, StrasbourgGoogle Scholar
  26. Delmotte N et al (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci 106:16428–16433PubMedCrossRefPubMedCentralGoogle Scholar
  27. Devaraju R, Satish S (2011) Endophytic mycoflora of Mirabilis jalapa L. and studies on antimicrobial activity of its endophytic Fusarium sp. Soc Appl Sci 2:75–79Google Scholar
  28. Dinkins RD, Barnes A, Waters W (2010) Microarray analysis of endophyte-infected and endophyte-free tall fescue. J Plant Physiol 167:1197–1203PubMedCrossRefPubMedCentralGoogle Scholar
  29. Dinsdale EA et al (2008) Functional metagenomic profiling of nine biomes. Nature 452:629PubMedCrossRefPubMedCentralGoogle Scholar
  30. Döbereiner J (1992) Recent changes in concepts of plant bacteria interactions: endophytic N2 fixing bacteria. Ciência Cult 44:310–313Google Scholar
  31. Dong Y, Glasner JD, Blattner FR, Triplett EW (2001) Genomic interspecies microarray hybridization: rapid discovery of three thousand genes in the maize endophyte, Klebsiella pneumoniae 342, by microarray hybridization with Escherichia coli K-12 open reading frames. Appl Environ Microbiol 67:1911–1921PubMedPubMedCentralCrossRefGoogle Scholar
  32. Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170PubMedCrossRefPubMedCentralGoogle Scholar
  33. Dudeja S, Giri R, Saini R, Suneja-Madan P, Kothe E (2012) Interaction of endophytic microbes with legumes. J Basic Microbiol 52:248–260PubMedCrossRefPubMedCentralGoogle Scholar
  34. Elango F, Lozano J (1980) Transmission of Xanthomonas manihotis in seed of cassava (Manihot esculenta). Plant Dis 64:784–786CrossRefGoogle Scholar
  35. Espinosa-Urgel M, Salido A, Ramos J-L (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182:2363–2369PubMedPubMedCentralCrossRefGoogle Scholar
  36. Felitti S et al (2006) Transcriptome analysis of Neotyphodium and Epichloë grass endophytes. Fungal Genet Biol 43:465–475PubMedCrossRefPubMedCentralGoogle Scholar
  37. Firrincieli A et al (2015) Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1. Front Microbiol 6:978PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fisher P, Petrini O, Scott HL (1992) The distribution of some fungal and bacterial endophytes in maize (Zea mays L.). New Phytol 122:299–305CrossRefGoogle Scholar
  39. Fouts DE et al (2008) Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4:e1000141PubMedPubMedCentralCrossRefGoogle Scholar
  40. Fox R, Manners J, Myers A (1972) Ultrastructure of tissue disintegration and host reactions in potato tubers infected by Erwinia carotovora var. atroseptica. Potato Res 15:130–145CrossRefGoogle Scholar
  41. Fryar S, Yuen T, Hyde K, Hodgkiss I (2001) The influence of competition between tropical fungi on wood colonization in streams. Microb Ecol 41:245–251PubMedCrossRefPubMedCentralGoogle Scholar
  42. Fukasawa Y, Osono T, Takeda H (2009) Effects of attack of saprobic fungi on twig litter decomposition by endophytic fungi. Ecol Res 24:1067CrossRefGoogle Scholar
  43. Gagné S, Richard C, Rousseau H, Antoun H (1987) Xylem-residing bacteria in alfalfa roots. Can J Microbiol 33:996–1000CrossRefGoogle Scholar
  44. Gangadevi V, Muthumary J (2008) Isolation of Colletotrichum gloeosporioides, a novel endophytic taxol-producing fungus from the leaves of a medicinal plant, Justicia gendarussa. Mycol Balc 5:1–4Google Scholar
  45. Gardner JM, Feldman AW, Zablotowicz RM (1982) Identity and behavior of xylem-residing bacteria in rough lemon roots of Florida citrus trees. Appl Environ Microbiol 43:1335–1342PubMedPubMedCentralGoogle Scholar
  46. Gehring CA, Cobb NS, Whitham TG (1997) Three-way interactions among ectomycorrhizal mutualists, scale insects, and resistant and susceptible pinyon pines. Am Nat 149:824–841PubMedCrossRefPubMedCentralGoogle Scholar
  47. Germaine K (2007) Construction of endophytic xenobiotic degrader bacteria for improving the phytoremediation of organic pollutants. PhD thesis, Institute of Technology Carlow, CarlowGoogle Scholar
  48. Glienke-Blanco C, Aguilar-Vildoso CI, Vieira MLC, Barroso PAV, Azevedo JL (2002) Genetic variability in the endophytic fungus Guignardia citricarpa isolated from citrus plants. Genet Mol Biol 25:251–255CrossRefGoogle Scholar
  49. Goodman R (1982) The infection process. Phytopathogenic prokaryotes 1:31–62CrossRefGoogle Scholar
  50. Granér G, Persson P, Meijer J, Alström S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224:269–276PubMedCrossRefPubMedCentralGoogle Scholar
  51. Grum M, Camloh M, Rudolph K, Ravnikar M (1998) Elimination of bean seed-borne bacteria by thermotherapy and meristem culture. Plant Cell Tissue Organ Cult 52:79–82CrossRefGoogle Scholar
  52. Guo L et al (2015) A host plant genome (Zizania latifolia) after a century-long endophyte infection. Plant J 83:600–609PubMedCrossRefPubMedCentralGoogle Scholar
  53. Hallmann J, Kloepper J, Rodriguez-Kabana R, Sikora R (1995) Endophytic rhizobacteria as antagonists of Meloidogyne incognita on cucumber. Phytopathology 85:136Google Scholar
  54. Hamayun M et al (2009) 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. He X et al (2012) Diversity and decomposition potential of endophytes in leaves of a Cinnamomum camphora plantation in China. Ecol Res 27:273–284CrossRefGoogle Scholar
  56. Hert DG, Fredlake CP, Barron AE (2008) Advantages and limitations of next-generation sequencing technologies: a comparison of electrophoresis and non-electrophoresis methods. Electrophoresis 29:4618–4626PubMedCrossRefPubMedCentralGoogle Scholar
  57. Hettich RL, Pan C, Chourey K, Giannone RJ (2013) Metaproteomics: harnessing the power of high performance mass spectrometry to identify the suite of proteins that control metabolic activities in microbial communities. ACS Publications, Washington, DCGoogle Scholar
  58. Hollis JP (1951) Bacteria in healthy potato tissue. Phytopathology 41:350–366Google Scholar
  59. Huang J-S (1986) Ultrastructure of bacterial penetration in plants. Annu Rev Phytopathol 24:141–157CrossRefGoogle Scholar
  60. Jacobs MJ, Bugbee WM, Gabrielson DA (1985) Enumeration, location, and characterization of endophytic bacteria within sugar beet roots. Can J Bot 63:1262–1265CrossRefGoogle Scholar
  61. Johnson NC, Graham JH, Smith F (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585CrossRefGoogle Scholar
  62. 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 63:305–317CrossRefGoogle Scholar
  63. Jones WJ (2010) High-throughput sequencing and metagenomics. Estuar Coasts 33:944–952CrossRefGoogle Scholar
  64. Joseph B, Priya RM (2011) Bioactive compounds from Endophytes and their potential in American. J Biochem Mol Biol 1:291–309Google Scholar
  65. Jumpponen A, Jones KL, Mattox JD, Yaege C (2010) Massively parallel 454-sequencing of fungal communities in Quercus spp. ectomycorrhizas indicates seasonal dynamics in urban and rural sites. Mol Ecol 19:41–53PubMedCrossRefPubMedCentralGoogle Scholar
  66. Kaul S, Gupta S, Ahmed M, Dhar MK (2012) Endophytic fungi from medicinal plants: a treasure hunt for bioactive metabolites. Phytochem Rev 11:487–505CrossRefGoogle Scholar
  67. Knief C et al (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378PubMedCrossRefPubMedCentralGoogle Scholar
  68. Korkama-Rajala T, Müller MM, Pennanen T (2008) Decomposition and fungi of needle litter from slow-and fast-growing Norway spruce (Picea abies) clones. Microb Ecol 56:76PubMedCrossRefPubMedCentralGoogle Scholar
  69. Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648–657PubMedCrossRefPubMedCentralGoogle Scholar
  70. Kuan T-L, Minsavage G, Gabrielson R (1985) Detection of Xanthomonas campestris pv. Carotae in carrot seed. Plant Dis 69:758–760CrossRefGoogle Scholar
  71. Kumar S, Kaushik N, Edrada-Ebel R, Ebel R, Proksch P (2011) Isolation, characterization, and bioactivity of endophytic fungi of Tylophora indica. World J Microbiol Biotechnol 27:571–577CrossRefGoogle Scholar
  72. Kumaresan V (2002) Endophytes assemblages in young mature and senescent leaves of Rhizophora apiculata: evidence for the role of endophytes in mangrove litter degradation. Fungal Divers 9:81–91Google Scholar
  73. Kusari S, Singh S, Jayabaskaran C (2014) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303PubMedCrossRefPubMedCentralGoogle Scholar
  74. Lalande R, Bissonnette N, Coutlée D, Antoun H (1989) Identification of rhizobacteria from maize and determination of their plant-growth promoting potential. Plant Soil 115:7–11CrossRefGoogle Scholar
  75. Lee S, Flores-Encarnacion M, Contreras-Zentella M, Garcia-Flores L, Escamilla J, Kennedy C (2004) Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome c biogenesis genes. J Bacteriol 186:5384–5391PubMedPubMedCentralCrossRefGoogle Scholar
  76. Lery LM, Hemerly AS, Nogueira EM, von Krüger WM, Bisch PM (2011) Quantitative proteomic analysis of the interaction between the endophytic plant-growth-promoting bacterium Gluconacetobacter diazotrophicus and sugarcane. Mol Plant-Microbe Interact 24:562–576PubMedCrossRefPubMedCentralGoogle Scholar
  77. Lewis D (1985) Symbiosis and mutualism: crisp concepts and soggy semantics. In: Boucher DH (ed) The biology of mutualism. Oxford University Press, OxfordGoogle Scholar
  78. Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. J Ind Microbiol Biotechnol 36:1171PubMedCrossRefPubMedCentralGoogle Scholar
  79. López-López A, Rogel MA, Ormeno-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327PubMedCrossRefPubMedCentralGoogle Scholar
  80. Lu C, Shen Y (2007) A novel ansamycin, naphthomycin K from Streptomyces sp. J Antibiot 60:649PubMedCrossRefPubMedCentralGoogle Scholar
  81. Mahaffee W et al (1997) Spatial and temporal colonization of Phaseolus vulgaris by the bacterial endophytes Pseudomonas fluorescens strain 89B-27 and Enterobacter asburiae strain JM22. Appl Environ Microbiol.
  82. Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil 227:115–126CrossRefGoogle Scholar
  83. Mano H, Tanaka F, Watanabe A, Kaga H, Okunishi S, Morisaki H (2006) Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 21:86–100CrossRefGoogle Scholar
  84. 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 60:157–166PubMedCrossRefPubMedCentralGoogle Scholar
  85. Maron P-A, Ranjard L, Mougel C, Lemanceau P (2007) Metaproteomics: a new approach for studying functional microbial ecology. Microb Ecol 53:486–493PubMedCrossRefPubMedCentralGoogle Scholar
  86. Martínez-García PM, Ruano-Rosa D, Schilirò E, Prieto P, Ramos C, Rodríguez-Palenzuela P, Mercado-Blanco J (2015) Complete genome sequence of Pseudomonas fluorescens strain PICF7, an indigenous root endophyte from olive (Olea europaea L.) and effective biocontrol agent against Verticillium dahliae. Stand Genomic Sci 10:10PubMedPubMedCentralCrossRefGoogle Scholar
  87. Mastretta C et al (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267CrossRefGoogle Scholar
  88. McInroy JA, Kloepper JW (1995) Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 173:337–342CrossRefGoogle Scholar
  89. Molina LG, Cordenonsi da Fonseca G, GLd M, de Oliveira LFV, JBd C, Kulcheski FR, Margis R (2012) Metatranscriptomic analysis of small RNAs present in soybean deep sequencing libraries. Genet Mol Biol 35:292–303PubMedPubMedCentralCrossRefGoogle Scholar
  90. Mousa WK, Raizada MN (2013) The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front Microbiol 4:65PubMedPubMedCentralCrossRefGoogle Scholar
  91. Mukhopadhyay K, Garrison NK, Hinton DM, Bacon CW, Khush GS, Peck HD, Datta N (1996) Identification and characterization of bacterial endophytes of rice. Mycopathologia 134:151–159PubMedCrossRefPubMedCentralGoogle Scholar
  92. Müller MM, Valjakka R, Suokko A, Hantula J (2001) Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol Ecol 10:1801–1810PubMedCrossRefPubMedCentralGoogle Scholar
  93. Mundt JO, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32:694–698PubMedPubMedCentralGoogle Scholar
  94. Musson G, McInroy J, Kloepper J (1995) Development of delivery systems for introducing endophytic bacteria into cotton. Biocontrol Sci Tech 5:407–416CrossRefGoogle Scholar
  95. Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:250693CrossRefGoogle Scholar
  96. Neilands J (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedCrossRefPubMedCentralGoogle Scholar
  97. Nikolic B, Schwab H, Sessitsch A (2011) Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch Microbiol 193:665–676PubMedCrossRefPubMedCentralGoogle Scholar
  98. Old KM, Nicolson TH (1978) The root cortex as part of a microbial continuum. In: Loutit MW, Miles JAR (eds) Microbial ecology. SpringerVerlag, Berlin, pp 291–294CrossRefGoogle Scholar
  99. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 409:78PubMedCrossRefPubMedCentralGoogle Scholar
  100. Osono T (2003) Effects of prior decomposition of beech leaf litter by phyllosphere fungi on substrate utilization by fungal decomposers. Mycoscience 44:0041–0045CrossRefGoogle Scholar
  101. Osono T (2006) Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Can J Microbiol 52:701–716PubMedCrossRefPubMedCentralGoogle Scholar
  102. Osono T, Hirose D (2009) Effects of prior decomposition of Camellia japonica leaf litter by an endophytic fungus on the subsequent decomposition by fungal colonizers. Mycoscience 50:52–55CrossRefGoogle Scholar
  103. Parker MP (1995) Plant fitness variation caused by different mutualist genotypes. Ecology 76:1525–1535CrossRefGoogle Scholar
  104. Parker MA (1999) Mutualism in metapopulations of legumes and rhizobia. Am Nat 153:S48–S60PubMedCrossRefPubMedCentralGoogle Scholar
  105. Patriquin D, Döbereiner J (1978) Light microscopy observations of tetrazolium-reducing bacteria in the endorhizosphere of maize and other grasses in Brazil. Can J Microbiol 24:734–742PubMedCrossRefPubMedCentralGoogle Scholar
  106. Patriquin D, Döbereiner J, Jain D (1983) Sites and processes of association between diazotrophs and grasses. Can J Microbiol 29:900–915CrossRefGoogle Scholar
  107. Petrini O (1986) Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, Van Den Huevel J (eds) Microbiology of the phyllosphere. Cambridge University Press, Cambridge, pp 175–187Google Scholar
  108. Pirttilä AM, Laukkanen H, Pospiech H, Myllylä R, Hohtola A (2000) Detection of intracellular bacteria in the buds of scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66:3073–3077PubMedPubMedCentralCrossRefGoogle Scholar
  109. Pleban S, Ingel F, Chet I (1995) Control of Rhizoctonia solani and Sclerotium rolfsii in the greenhouse using endophytic Bacillus spp. Eur J Plant Pathol 101:665–672CrossRefGoogle Scholar
  110. Posada F, Vega FE (2006) Inoculation and colonization of coffee seedlings (Coffea arabica L.) with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycoscience 47:284–289CrossRefGoogle Scholar
  111. Premjanu N, Jayanthy C (2012) Endophytic fungi a repository of bioactive compounds-a review. Intl J Inst Phar Life Sci 2:135–162Google Scholar
  112. Promputtha I, Hyde KD, McKenzie EH, Peberdy JF, Lumyong S (2010) Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers 41:89–99CrossRefGoogle Scholar
  113. Pullen CB et al (2003) Occurrence and non-detectability of maytansinoids in individual plants of the genera Maytenus and Putterlickia. Phytochemistry 62:377–387PubMedCrossRefPubMedCentralGoogle Scholar
  114. Qiu X, Pei Y, Wang Y, Zhang F (1990) Isolation of pseudomonads from cotton plants and their effect on seedling diseases. Acta Phytophylacica Sinica 17:303–306Google Scholar
  115. Qiu M, Xie R, Shi Y, Chen H, Wen Y, Gao Y, Hu X (2010) Isolation and identification of endophytic fungus SX01, a red pigment producer from Ginkgo biloba L. World J Microbiol Biotechnol 26:993–998CrossRefGoogle Scholar
  116. Quadt-Hallmann A, Kloepper J (1996) Immunological detection and localization of the cotton endophyte Enterobacter asburiae JM22 in different plant species. Can J Microbiol 42:1144–1154CrossRefGoogle Scholar
  117. Quadt-Hallmann A, Hallmann J, Kloepper J (1997) Bacterial endophytes in cotton: location and interaction with other plant-associated bacteria. Can J Microbiol 43:254–259CrossRefGoogle Scholar
  118. Rand FV, Cash LC (1921) Stewart’s disease of corn. J Agric Res 21:263–264Google Scholar
  119. Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921PubMedCrossRefPubMedCentralGoogle Scholar
  120. Rodriguez RJ et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404PubMedCrossRefPubMedCentralGoogle Scholar
  121. Roos IM, Hattingh M (1983) Scanning electron microscopy of Pseudomonas syringae pv, morsprunorum on sweet cherry leaves. J Phytopathol 108:18–25CrossRefGoogle Scholar
  122. Russell JR et al (2011) Biodegradation of polyester polyurethane by endophytic fungi. Appl Environ Microbiol 77:6076–6084PubMedPubMedCentralCrossRefGoogle Scholar
  123. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9PubMedCrossRefPubMedCentralGoogle Scholar
  124. Schaad NW, Cheong S, Tamaki S, Hatziloukas E, Panopoulos NJ (1995) A combined biological and enzymatic amplification (BIO-PCR) technique to detect Pseudomonas syringae pv. Phaseolicola in bean seed extracts. Phytopathology 85:243–246CrossRefGoogle Scholar
  125. Schaad NW, Jones JB, Chun W (2001) Laboratory guide for the identification of plant pathogenic bacteria, vol 3. APS Press, UrbanaGoogle Scholar
  126. Selim K, El-Beih A, AbdEl-Rahman T, El-Diwany A (2011) Biodiversity and antimicrobial activity of endophytes associated with Egyptian medicinal plants. Mycosphere 2:669–678CrossRefGoogle Scholar
  127. Sessitsch A et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36PubMedCrossRefPubMedCentralGoogle Scholar
  128. Sette L, Passarini M, Delarmelina C, Salati F, Duarte M (2006) Molecular characterization and antimicrobial activity of endophytic fungi from coffee plants. World J Microbiol Biotechnol 22:1185–1195CrossRefGoogle Scholar
  129. Sharrock K, Parkes S, Jack H, Rees-George J, Hawthorne B (1991) Involvement of bacterial endophytes in storage rots of buttercup squash (Cucurbita maxima D. hybrid ‘Delica’). N Z J Crop Hortic Sci 19:157–165CrossRefGoogle Scholar
  130. Sheibani-Tezerji R, Rattei T, Sessitsch A, Trognitz F, Mitter B (2015) Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress. MBio 6:e00621–e00615PubMedPubMedCentralCrossRefGoogle Scholar
  131. Singh SK, Strobel GA, Knighton B, Geary B, Sears J, Ezra D (2011) An endophytic Phomopsis sp. possessing bioactivity and fuel potential with its volatile organic compounds. Microb Ecol 61:729–739PubMedCrossRefPubMedCentralGoogle Scholar
  132. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502PubMedPubMedCentralCrossRefGoogle Scholar
  133. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268PubMedCrossRefPubMedCentralGoogle Scholar
  134. Suryanarayanan TS (2013) Endophyte research: going beyond isolation and metabolite documentation. Fungal Ecol 6:561–568CrossRefGoogle Scholar
  135. Taghavi S et al (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6:e1000943PubMedPubMedCentralCrossRefGoogle Scholar
  136. Tefera T, Vidal S (2009) Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl 54:663–669CrossRefGoogle Scholar
  137. Terekhova V, Semenova T (2005) The structure of micromycete communities and their synecologic interactions with basidiomycetes during plant debris decomposition. Microbiology 74:91–96CrossRefGoogle Scholar
  138. Thormann MN, Currah RS, Bayley SE (2003) Succession of microfungal assemblages in decomposing peatland plants. Plant Soil 250:323–333CrossRefGoogle Scholar
  139. Toju H, Yamamoto S, Sato H, Tanabe AS, Gilbert GS, Kadowaki K (2013) Community composition of root-associated fungi in a Q uercus-dominated temperate forest:“codominance” of mycorrhizal and root-endophytic fungi. Ecol Evol 3:1281–1293PubMedPubMedCentralCrossRefGoogle Scholar
  140. Tombolini R, Jansson JK (1998) Monitoring of GFP-tagged bacterial cells. In: Bioluminescence methods and protocols. Springer, New York, pp 285–298CrossRefGoogle Scholar
  141. Tombolini R, Unge A, Davey ME, de Bruijn FJ, Jansson JK (1997) Flow cytometric and microscopic analysis of GFP-tagged Pseudomonas fluorescens bacteria. FEMS Microbiol Ecol 22:17–28CrossRefGoogle Scholar
  142. Tomsheck AR et al (2010) Hypoxylon sp., an endophyte of Persea indica, producing 1, 8-cineole and other bioactive volatiles with fuel potential. Microb Ecol 60:903–914PubMedCrossRefPubMedCentralGoogle Scholar
  143. Tripathi AK, Verma SC, Chowdhury SP, Lebuhn M, Gattinger A, Schloter M (2006) Ochrobactrum oryzae sp. nov., an endophytic bacterial species isolated from deep-water rice in India. Int J Syst Evol Microbiol 56:1677–1680PubMedCrossRefPubMedCentralGoogle Scholar
  144. Uszkoreit J, Plohnke N, Rexroth S, Marcus K, Eisenacher M (2014) The bacterial proteogenomic pipeline. BMC Genomics 15:S19PubMedPubMedCentralCrossRefGoogle Scholar
  145. Van Hecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:101–109CrossRefGoogle Scholar
  146. Villacieros M et al (2003) Colonization behaviour of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251:47–54CrossRefGoogle Scholar
  147. Visalakchi S, Muthumary J (2009) Antimicrobial activity of the new endophytic Monodictys castaneae SVJM139 pigment and its optimization. Afr J Microbiol Res 3:550–556Google Scholar
  148. Wang Y, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant-Microbe Interact 18:385–396PubMedCrossRefPubMedCentralGoogle Scholar
  149. Wei G, Kloepper JW, Tuzun S (1991) Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81:1508–1512CrossRefGoogle Scholar
  150. Wei G, Kloepper J, Tuzun S (1996) Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions. Phytopathology 86:121Google Scholar
  151. Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276CrossRefGoogle Scholar
  152. Xi C, Lambrecht M, Vanderleyden J, Michiels J (1999) Bi-functional gfp-and gusA-containing mini-Tn5 transposon derivatives for combined gene expression and bacterial localization studies. J Microbiol Methods 35:85–92PubMedCrossRefPubMedCentralGoogle Scholar
  153. Xin G, Zhang G, Kang JW, Staley JT, Doty SL (2009) A diazotrophic, indole-3-acetic acid-producing endophyte from wild. Biol Fertil Soils 45:669–674CrossRefGoogle Scholar
  154. Young C, Bryant M, Christensen M, Tapper B, Bryan G, Scott B (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial. Mol Gen Genomics 274:13–29CrossRefGoogle Scholar
  155. Zgadzaj R et al (2015) A legume genetic framework controls infection of nodules by symbiotic and endophytic bacteria. PLoS Genet 11:e1005280PubMedPubMedCentralCrossRefGoogle Scholar
  156. Zhang X, Ren A, Ci H, Gao Y (2010) Genetic diversity and structure of Neotyphodium species and their host Achnatherum sibiricum in a natural grass–endophyte system. Microb Ecol 59:744–756PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Priyanka Verma
    • 1
  1. 1.Department of MicrobiologyEternal UniversitySirmaurIndia

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