Functional Roles of Seed-Inhabiting Endophytes of Rice

  • Gaurav Pal
  • Kanchan Kumar
  • Anand Verma
  • James Francis WhiteJr
  • Satish K. Verma


Endophytic microbes including bacteria and fungi inhabiting in seed tissues have recently gained significant importance owing to a diversity of roles that they play and eventually resulting in improved plant growth as well as plant fitness. Some of the major roles played by seed endophytic microbes include plant growth promotion by enhanced nutrient acquisition or production of growth hormones, nitrogen fixation, phosphate solubilisation, and protection against pathogens as well as abiotic stresses. Since, rice is one of the important staple crop across the globe, there is a great need to explore and decipher the roles of the endophytic community present inside it. This chapter focuses on the diversity and distribution of rice seed endophytes, their transmission along with the various functional roles that they play inside the plants with an aim to provide deep insights on rice seed endophytes as plant growth promoting and biocontrol agents.


Endophytic microbes Rice Plant growth promotion Biocontrol agents 



The authors are grateful to the Department of Plant Biology, Rutgers University, NJ, for research facilities. SKV thanks to UGC, India, for providing a Raman Post Doctoral Fellowship No. F 5-11/2016(IC) for the year 2016–2017 to work in the USA and support as grant, Project-UGC-BSR startup-M14-26. The SKV and RNK are also grateful to the Head and Coordinator of CAS and DST-FIST and PURSE of Botany, BHU, Varanasi, for providing facilities and leave to pursue endophyte research. The authors are also thankful for support from the John E. and Christina C. Craighead Foundation, USDA-NIFA Multistate Project W3147, and the New Jersey Agricultural Experiment Station.


  1. Arnold AE, Maynard Z et al (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3(4):267–274CrossRefGoogle Scholar
  2. Arnold AE, Mejía LC et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100(26):15649–15654PubMedCrossRefPubMedCentralGoogle Scholar
  3. Atugala DM, Deshappriya N (2015) Effect of endophytic fungi on plant growth and blast disease incidence of two traditional rice varieties. J Natl Sci Found 43(2):173Google Scholar
  4. Azevedo JL, Maccheroni W Jr et al (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3(1):15–16CrossRefGoogle Scholar
  5. Barac T, Taghavi S et al (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22(5):583PubMedCrossRefPubMedCentralGoogle Scholar
  6. Barazani O, Friedman J (2001) Allelopathic bacteria and their impact on higher plants. Crit Rev Microbiol 27(1):41–55PubMedCrossRefPubMedCentralGoogle Scholar
  7. Barrow JR, Osuna P (2002) Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. J Arid Environ 51(3):449–459CrossRefGoogle Scholar
  8. Bashan Y, De-Bashan LE (2005) Plant growth-promoting. In: Encyclopedia of soils in the environment, vol 1. Elsevier, Oxford, pp 103–115CrossRefGoogle Scholar
  9. Beltran-Garcia MJ, White JF Jr et al (2014) Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Rep 4:6938PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bertani I, Abbruscato P et al (2016) Rice bacterial endophytes: isolation of a collection, identification of beneficial strains and microbiome analysis. Environ Microbiol Rep 8(3):388–398PubMedCrossRefPubMedCentralGoogle Scholar
  11. Boddey RM, Oliveira OC et al (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant Soil 174(1):195–209CrossRefGoogle Scholar
  12. Brader G, Corretto E et al (2017) Metagenomics of plant microbiomes. In: Functional metagenomics: tools and applications. Springer, Cham, pp 179–200CrossRefGoogle Scholar
  13. Carroll GC (1991) Fungal associates of woody plants as insect antagonists in leaves and stems. In: Microbial mediation of plant-herbivore interactions. Wiley, New York, pp 253–271Google Scholar
  14. Chatterjee A, Valasubramanian R et al (1996) Isolation of ant mutants of Pseudomonas fluorescens strain Pf7-14 altered in antibiotic production, cloning of ant+ DNA, and evaluation of the role of antibiotic production in the control of blast and sheath blight of rice. Biol Control 7(2):185–195CrossRefGoogle Scholar
  15. Cheplick GP, Clay K et al (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111(1):89–97CrossRefGoogle Scholar
  16. Cho SJ, Lim WJ et al (2003) Endophytic colonization of balloon flower by antifungal strain Bacillus sp. CY22. Biosci Biotechnol Biochem 67(10):2132–2138PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cho HS, Park SY et al (2007) Interference of quorum sensing and virulence of the rice pathogen Burkholderia glumae by an engineered endophytic bacterium. FEMS Microbiol Ecol 60(1):14–23PubMedCrossRefPubMedCentralGoogle Scholar
  18. Clay K (1989) Clavicipitaceous endophytes of grasses: their potential as biocontrol agents. Mycol Res 92(1):1–12CrossRefGoogle Scholar
  19. Compant S, Clément C et al (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42(5):669–678CrossRefGoogle Scholar
  20. Cottyn B, Regalado E et al (2001) Bacterial populations associated with rice seed in the tropical environment. Phytopathology 91(3):282–292PubMedCrossRefPubMedCentralGoogle Scholar
  21. De Vleesschauwer D, Djavaheri M et al (2008) Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol 148(4):1996–2012PubMedPubMedCentralCrossRefGoogle Scholar
  22. Doty SL, Oakley B et al (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 47(1):23–33CrossRefGoogle Scholar
  23. Dunne C, Crowley JJ et al (1997) Biological control of Pythium ultimum by Stenotrophomonas maltophilia W81 is mediated by an extracellular proteolytic activity. Microbiology 143(12):3921–3931CrossRefGoogle Scholar
  24. Elbeltagy A, Nishioka K et al (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46(3):617–629CrossRefGoogle Scholar
  25. Elbeltagy A, Nishioka K et al (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67(11):5285–5293PubMedPubMedCentralCrossRefGoogle Scholar
  26. Farooq M, Jabran K et al (2011) The role of allelopathy in agricultural pest management. Pest Manag Sci 67:493–506PubMedCrossRefPubMedCentralGoogle Scholar
  27. Feng Y, Shen D et al (2006) Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100(5):938–945PubMedCrossRefPubMedCentralGoogle Scholar
  28. Fisher PJ, Petrini O (1992) Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L.). New Phytol 120(1):137–143CrossRefGoogle Scholar
  29. Fravel DR (1988) Role of antibiosis in the biocontrol of plant diseases. Annu Rev Phytopathol 26(1):75–91CrossRefGoogle Scholar
  30. Freeman EM (1904) The seed-fungus of Lolium temulentum L., the darnel. Philos Trans R Soc Lond B 196(214–224):1–27CrossRefGoogle Scholar
  31. Gagne-Bourgue F, Aliferis KA et al (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol 114(3):836–853PubMedCrossRefPubMedCentralGoogle Scholar
  32. Glass AD (1989) Plant mineral nutrition. An introduction to current concepts. Jones and Bartlett, BostonGoogle Scholar
  33. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41(2):109–117CrossRefGoogle Scholar
  34. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251(1):1–7PubMedCrossRefPubMedCentralGoogle Scholar
  35. Glick BR, Penrose DM et al (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190(1):63–68PubMedCrossRefPubMedCentralGoogle Scholar
  36. Gond SK, Bergen MS, Torres MS, White Jr JF (2015) Endophytic bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87PubMedCrossRefPubMedCentralGoogle Scholar
  37. Gyaneshwar P, James EK et al (2001) Endophytic colonization of rice by a diazotrophic strain of Serratia marcescens. J Bacteriol 183:2634–2645PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hallmann J, Quadt-Hallmann A et al (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43(10):895–914CrossRefGoogle Scholar
  39. Hardoim PR, van Overbeek LS et al (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471CrossRefGoogle Scholar
  40. Hardoim PR, Nazir R et al (2013) The new species Enterobacter oryziphilus sp. nov. and Enterobacter oryzendophyticus sp. nov. are key inhabitants of the endosphere of rice. BMC Microbiol 13(1):164PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hodgson S, Cates C et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4(8):1199–1208PubMedPubMedCentralCrossRefGoogle Scholar
  42. Holguin G, Patten CL (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. World Scientific, LondonGoogle Scholar
  43. Hollis J (1949) Location of bacteria in healthy potato tissue. Phytopathology 39(1):9–10Google Scholar
  44. Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42(10):1825–1831Google Scholar
  45. Hornok L (2000) Genetically modified microorganisms in biological control. Növényvédelem 36(5):229–237Google Scholar
  46. Hoysted GA, Kowal J et al (2018) A mycorrhizal revolution. Curr Opin Plant Biol 44:1–6PubMedCrossRefPubMedCentralGoogle Scholar
  47. Hurek T, Reinhold-Hurek B et al (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J Bacteriol 176(7):1913–1923PubMedPubMedCentralCrossRefGoogle Scholar
  48. Irizarry I, White JF (2017) Application of bacteria from non-cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. J Appl Microbiol 122(4):1110–1120PubMedCrossRefPubMedCentralGoogle Scholar
  49. Ji SH, Gururani MA et al (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169(1):83–98PubMedCrossRefPubMedCentralGoogle Scholar
  50. Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6(6):e20396PubMedPubMedCentralCrossRefGoogle Scholar
  51. Johnston-Monje D, Lundberg DS et al (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil 405(1–2):337–355CrossRefGoogle Scholar
  52. Kaga H, Mano H, Tanaka F, Watanabe A, Kaneko S, Morisaki H (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ 24(2):154–162PubMedCrossRefPubMedCentralGoogle Scholar
  53. Kandel SL, Joubert PM et al (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5(4):77PubMedCentralCrossRefGoogle Scholar
  54. Kim J, Kim JG et al (2004) Quorum sensing and the LysR-type transcriptional activator ToxR regulate toxoflavin biosynthesis and transport in Burkholderia glumae. Mol Microbiol 54(4):921–934PubMedCrossRefPubMedCentralGoogle Scholar
  55. Kong CH, Wang P et al (2008) Impact of allelochemical exuded from allelopathic rice on soil microbial community. Soil Biol Biochem 40(7):1862–1869CrossRefGoogle Scholar
  56. Krishnan P, Bhat R et al (2012) Isolation and functional characterization of bacterial endophytes from Carica papaya fruits. J Appl Microbiol 113(2):308–317PubMedCrossRefPubMedCentralGoogle Scholar
  57. Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46(1):57–71CrossRefGoogle Scholar
  58. Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587PubMedPubMedCentralCrossRefGoogle Scholar
  59. Larran S, Simon MR et al (2016) Endophytes from wheat as biocontrol agents against tan spot disease. Biol Control 92:17–23CrossRefGoogle Scholar
  60. Li HY, Wei DQ et al (2012) Endophytes and their role in phytoremediation. Fungal Divers 54(1):11–18CrossRefGoogle Scholar
  61. Liu Y, Zuo S et al (2012) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194(12):1001–1012PubMedCrossRefPubMedCentralGoogle Scholar
  62. Liu Y, Zuo S et al (2013) Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Ann Microbiol 63(1):71–79CrossRefGoogle Scholar
  63. Loaces I, Ferrando L et al (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microb Ecol 61(3):606–618PubMedCrossRefPubMedCentralGoogle Scholar
  64. Lodewyckx C, Vangronsveld J et al (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21(6):583–606CrossRefGoogle Scholar
  65. Loganathan P, Nair S (2003) Crop-specific endophytic colonization by a novel, salt-tolerant, N2-fixing and phosphate-solubilizing Gluconacetobacter sp. from wild rice. Biotechnol Lett 25(6):497–501PubMedCrossRefPubMedCentralGoogle Scholar
  66. Lopez DC (2015) Ecological roles of two entomopathogenic endophytes: Beauveria bassiana and Purpureocillium lilacinum in cultivated cotton. Texas A&M UniversityGoogle Scholar
  67. Lucas JA, García-Villaraco A et al (2013) Structural and functional study in the rhizosphere of Oryza sativa L. plants growing under biotic and abiotic stress. J Appl Microbiol 115(1):218–235PubMedCrossRefPubMedCentralGoogle Scholar
  68. Luo S, Xu T 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):1745–1753PubMedCrossRefPubMedCentralGoogle Scholar
  69. Ma Y, Prasad MNV et al (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258PubMedCrossRefPubMedCentralGoogle Scholar
  70. Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117PubMedCrossRefPubMedCentralGoogle Scholar
  71. Mathan S (2016) Isolation of endophytic fungi from marine algae and its bioactivity. Int J Res Pharm Biomed Sci 4(1):45–49Google Scholar
  72. Menn FM, Easter JP et al (2008) Genetically engineered microorganisms and bioremediation, 2nd ed. Biotechnology Set, pp 441–463Google Scholar
  73. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55(1):165–199PubMedCrossRefPubMedCentralGoogle Scholar
  74. Mitter B, Petric A et al (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 4:120PubMedPubMedCentralCrossRefGoogle Scholar
  75. Mukhopadhyay K, Garrison NK et al (1996) Identification and characterization of bacterial endophytes of rice. Mycopathologia 134(3):151–159PubMedCrossRefPubMedCentralGoogle Scholar
  76. Murphy BR, Doohan FM et al (2015) Fungal root endophytes of a wild barley species increase yield in a nutrient-stressed barley cultivar. Symbiosis 65(1):1–7CrossRefGoogle Scholar
  77. Nandakumar R, Babu S et al (2001) Induction of systemic resistance in rice against sheath blight disease by Pseudomonas fluorescens. Soil Biol Biochem 33(4–5):603–612CrossRefGoogle Scholar
  78. Narula S, Anand RC et al (2013) Beneficial traits of endophytic bacteria from field pea nodules and plant growth promotion of field pea. J Food Legumes 26(3 and 4):73–79Google Scholar
  79. Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23(1):6–8PubMedCrossRefPubMedCentralGoogle Scholar
  80. Okunishi S, Sako K et al (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environ 20(3):168–177CrossRefGoogle Scholar
  81. Palumbo JD, Yuen GY et al (2005) Mutagenesis of β-1,3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95(6):701–707PubMedCrossRefPubMedCentralGoogle Scholar
  82. Paungfoo-Lonhienne C, Rentsch D et al (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS One 5:e11915PubMedPubMedCentralCrossRefGoogle Scholar
  83. Perotti R (1926) On the limits of biological enquiry in soil science. Proc Int Soc Soil Sci 2:146–161Google Scholar
  84. Pirttilä AM, Laukkanen H et al (2000) Detection of intracellular bacteria in the buds of Scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66(7):3073–3077PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pirttilä AM, Pospiech H et al (2003) Two endophytic fungi in different tissues of Scots pine buds (Pinus sylvestris L.). Microb Ecol 45(1):53–62PubMedCrossRefPubMedCentralGoogle Scholar
  86. Pleban S, Chernin L et al (1997) Chitinolytic activity of an endophytic strain of Bacillus cereus. Lett Appl Microbiol 25(4):284–288PubMedCrossRefPubMedCentralGoogle Scholar
  87. Prieto KR, Echaide-Aquino F et al (2017) Endophytic bacteria and rare earth elements; promising candidates for nutrient use efficiency in plants. In: Plant macronutrient use efficiency: molecular and genomic perspectives in crop plants. Elsevier, pp 285–306Google Scholar
  88. Reshma P, Naik MK et al (2018) Induced systemic resistance by 2,4-diacetylphloroglucinol positive fluorescent Pseudomonas strains against rice sheath blight. Indian J Exp Biol 56(3):207–212Google Scholar
  89. Ringelberg D, Foley K et al (2012) Bacterial endophyte communities of two wheatgrass varieties following propagation in different growing media. Can J Microbiol 58(1):67–80PubMedCrossRefPubMedCentralGoogle Scholar
  90. Rojas GJ et al (2016) Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities. Microb Ecol 72(1):197–206PubMedCrossRefPubMedCentralGoogle Scholar
  91. Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19(8):827–837PubMedCrossRefPubMedCentralGoogle Scholar
  92. Ruiza D, Agaras B et al (2011) Characterization and screening of plant probiotic traits of bacteria isolated from rice seeds cultivated in Argentina. J Microbiol 49(6):902–912PubMedCrossRefPubMedCentralGoogle Scholar
  93. Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2(11):a012427PubMedPubMedCentralCrossRefGoogle Scholar
  94. Salisbury FB (1994) The role of plant hormones. Plant-environment interactions. Dekker, New York, pp 39–81Google Scholar
  95. Saraf M, Pandya U et al (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169(1):18–29PubMedCrossRefPubMedCentralGoogle Scholar
  96. Schulz B, Römmert AK et al (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103(10):1275–1283CrossRefGoogle Scholar
  97. Shahzad R, Waqas M et al (2016) Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol Biochem 106:236–243PubMedCrossRefPubMedCentralGoogle Scholar
  98. Shearin ZR, Filipek M et al (2018) Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth. Plant Soil 422(1–2):183–194CrossRefGoogle Scholar
  99. Shehata HR, Ettinger CL et al (2016) Genes required for the anti-fungal activity of a bacterial endophyte isolated from a corn landrace grown continuously by subsistence farmers since 1000 BC. Front Microbiol 7:1548PubMedPubMedCentralCrossRefGoogle Scholar
  100. Shields MS, Reagin MJ et al (1995) TOM, a new aromatic degradative plasmid from Burkholderia (Pseudomonas) cepacia G4. Appl Environ Microbiol 61(4):1352–1356PubMedPubMedCentralGoogle Scholar
  101. Siciliano SD, Fortin N et al (2001) Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol 67(6):2469–2475PubMedPubMedCentralCrossRefGoogle Scholar
  102. Stevenson FJ, Cole MA (1999) Cycles of soils: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, New YorkGoogle Scholar
  103. Sun Y, O’Riordan MX (2013) Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv Appl Microbiol 85:93–118PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sziderics AH, Rasche F et al (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53(11):1195–1202PubMedCrossRefPubMedCentralGoogle Scholar
  105. Tholozan JL, Cappelier JM et al (1999) Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells. Appl Environ Microbiol 65(3):1110–1116PubMedPubMedCentralGoogle Scholar
  106. Tramontano WA, Scanlon C (1996) Cell cycle inhibition by butyrate in legume root meristems. Phytochemistry 41:85–88CrossRefGoogle Scholar
  107. Truyens S, Weyens N et al (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol 7(1):40–50CrossRefGoogle Scholar
  108. Tsurumaru H, Okubo T et al (2015) Metagenomic analysis of the bacterial community associated with the taproot of sugar beet. Microbes Environ 30(1):63–69PubMedPubMedCentralCrossRefGoogle Scholar
  109. Vallad GE, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. J Trop Crop Sci 44(6):1920–1934CrossRefGoogle Scholar
  110. Van Loon LC, Bakker PAHM et al (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36(1):453–483PubMedCrossRefPubMedCentralGoogle Scholar
  111. Verma SC, Ladha JK et al (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91(2–3):127–141PubMedCrossRefPubMedCentralGoogle Scholar
  112. Verma SK, Gond SK et al (2017a) Fungal endophytes representing diverse habitats and their role in plant protection. In: Developments in fungal biology and applied mycology. Springer, Singapore, pp 135–157Google Scholar
  113. Verma SK, Kingsley K et al (2017b) Seed vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol 122(6):1680–1691PubMedCrossRefPubMedCentralGoogle Scholar
  114. Verma SK, White JF (2018) Indigenous endophytic seed bacteria promote seedling development and defend against fungal disease in browntop millet (L.). J Appl Microbiol 124(3):764–778PubMedCrossRefPubMedCentralGoogle Scholar
  115. Verma SK, Kingsley K et al (2018) Bacterial endophytes from rice cut grass (Leersia oryzoides L.) increase growth, promote root gravitropic response, stimulate root hair formation, and protect rice seedlings from disease. Plant Soil 422(1–2):223–238CrossRefGoogle Scholar
  116. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255(2):571–586CrossRefGoogle Scholar
  117. Vujanovic V, Germida JJ (2017) Seed endosymbiosis: a vital relationship in providing prenatal care to plants. Can J Plant Sci 97(6):972–981Google Scholar
  118. Walitang DI, Kim K et al (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of Rice. BMC Microbiol 17(1):209PubMedPubMedCentralCrossRefGoogle Scholar
  119. White JF (2017) Syntrophic imbalance and the etiology of bacterial endoparasitism diseases. Med Hypotheses 107:14–15PubMedCrossRefPubMedCentralGoogle Scholar
  120. White JC, Wang X et al (2003) Subspecies-level variation in the phytoextraction of weathered p,p′-DDE by Cucurbita pepo. Environ Sci Technol 37(19):4368–4373PubMedCrossRefPubMedCentralGoogle Scholar
  121. White JF, Chen Q et al (2015) Collaboration between grass seedlings and rhizobacteria to scavenge organic nitrogen in soils. AoB Plants 7Google Scholar
  122. White J F, Kingsley K L et al (2018) Reactive oxygen defense against cellular endoparasites and the origin of eukaryotes. Transformative paleobotany: papers to commemorate the life and legacy of Thomas N. Taylor. Elsevier, AmsterdamGoogle Scholar
  123. White JF, Torres MS et al (2019) Evidence for widespread microbivory of endophytic bacteria in roots of vascular plants through oxidative degradation in root cell periplasmic spaces. In: PGPR amelioration in sustainable agriculture: food security and environmental management. Elsevier, LondonGoogle Scholar
  124. Wijesooriya WADK, Deshappriya N (2016) An inoculum of endophytic fungi for improved growth of a traditional rice variety in Sri Lanka. Trop Plant Res 3(3):470–480CrossRefGoogle Scholar
  125. Williams P, Cámara M (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12(2):182–191PubMedCrossRefPubMedCentralGoogle Scholar
  126. Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276CrossRefGoogle Scholar
  127. Yan Z, Reddy MS et al (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92(12):1329–1333PubMedCrossRefPubMedCentralGoogle Scholar
  128. Yumlembam RA, Borkar SG (2014) Assessment of antibacterial properties of medicinal plants having bacterial leaf endophytes against plant pathogenic Xanthomonads. Indian Phytopathol 67(4):353–357Google Scholar
  129. Zhang T, Yao YF (2015) Endophytic fungal communities associated with vascular plants in the high arctic zone are highly diverse and host-plant specific. PLoS One 10(6):e0130051PubMedPubMedCentralCrossRefGoogle Scholar
  130. Zúñiga A, Poupin MJ et al (2013) Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant-Microbe Interact 26(5):546–553PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Gaurav Pal
    • 1
  • Kanchan Kumar
    • 1
  • Anand Verma
    • 1
  • James Francis WhiteJr
    • 2
  • Satish K. Verma
    • 1
  1. 1.Centre of Advanced Study in BotanyBanaras Hindu UniversityVaranasiIndia
  2. 2.Department of Plant BiologyRutgers UniversityNew BrunswickUSA

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