Mechanism of Interaction of Endophytic Microbes with Plants

  • Neethu Sahadevan
  • E. K. Radhakrishnan
  • Jyothis Mathew


Microbial association with seeds as endophyte may play significant role in its germination and seedling establishment. However, the microbial communities associated with seeds and its diversity are still unexplored due to the difficulties in the characterization of spermosphere and its temporary duration and also due to the complexity of interactions involved. The rapidly changing spermosphere is a microbiologically rich area where interactions between seed and associated microbial communities take place. Recent technological advances are giving us significant promises to study the characteristics of seed exudates, microbial communities, and their mechanisms of interactions with seed and soil. In this chapter, we focused on the current understanding concerning the spermosphere and endophytic microbes that have been isolated from seeds of different plant species. Endophytic colonization route and mode of transmission to the seeds and mechanisms of interaction are also considered under the purview of this chapter. In addition, examples of recent techniques used for the characterization of seed microbiome are also given.


Spermosphere Microbial community Vertical transmission Mechanisms Characterization 


  1. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saudi Univ Sci 26:1–20. Scholar
  2. Ahmad I, Ahmad F, Pichtel J (2011) Microbes and microbial technology: agricultural and environmental applications, pp 1–516.
  3. Ali S, Duan J, Charles TC, Glick BR (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198. Scholar
  4. Aswathy AJ, Jasim B, Jyothis M, Radhakrishnan EK (2012) Identification of two strains of Paenibacillus sp. as indole 3 acetic acid-producing rhizome-associated endophytic bacteria from Curcuma longa. 3 Biotech 3:219–224. Scholar
  5. Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740. Scholar
  6. Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570. Scholar
  7. Bacilio-jim M, Aguilar-flores S, Ventura-zapata E, Eduardo P, Perez-Capos E, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chematactic response of endophytic bacteria. Plant Soil 249:271–277. Scholar
  8. Bacilio-Jiménez M, Aguilar-Flores S, Del Valle MV, Pérez A, Zepeda A, Zenteno E (2001) Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol Biochem 33:167–172. Scholar
  9. Baker BKF, Smith SH (1966) Literature pertaining to this review was completed in April 1966, 311Google Scholar
  10. Basheer J, Ravi A, Mathew J, Krishnankutty RE (2018) Assessment of plant-probiotic performance of novel endophytic Bacillus sp. in talc-based formulation. Probiotics Antimicrob Proteins 1–8.
  11. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. Scholar
  12. Buyer JS, Roberts DP, Russek-Cohen E (1999) Microbial community structure and function in the spermosphere as affected by soil and seed type. Can J Microbiol 45:138–144. Scholar
  13. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345. Scholar
  14. Chen MM, Zhu YG, Su YH, Chen BD, Fu BJ, Marschner P (2007) Effects of soil moisture and plant interactions on the soil microbial community structure. Eur J Soil Biol 43:31–38. Scholar
  15. Chithra S, Jasim B, Mathew J, Radhakrishnan EK (2017) Endophytic Phomopsis sp. colonization in Oryza sativa was found to result in plant growth promotion and piperine production. Physiol Plant 160:437–446. Scholar
  16. Cottyn B, Regalado E, Lanoot B, De Cleene M, Mew TW, Swings J (2001) Bacterial populations associated with rice seed in the tropical environment. Phytopathology 91:282–292. Scholar
  17. Croes S, Weyens N, Janssen J, Vercampt H, Colpaert JV, Carleer R, Vangronsveld J (2013) Bacterial communities associated with Brassica napus L. grown on trace element-contaminated and non-contaminated fields: a genotypic and phenotypic comparison. Microb Biotechnol 6:371–384. Scholar
  18. Díaz Herrera S, Grossi C, Zawoznik M, Groppa MD (2016) Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiol Res 186–187:37–43. Scholar
  19. Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL, Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14. Scholar
  20. Gagne-Bourgue F, Aliferis KA, Seguin P, Rani M, Samson R, Jabaji S (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol 114:836–853. Scholar
  21. Gamalero E (2011) Bacteria in agrobiology: plant nutrient management.
  22. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. Scholar
  23. Glick BR, Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15. Scholar
  24. Green SJ, Inbar E, Michel FC, Hadar Y, Minz D (2006) Succession of bacterial communities during early plant development: transition from seed to root and effect of compost amendment. Appl Environ Microbiol 72:3975–3983. Scholar
  25. Hirsch PR, Mauchline TH, Clark IM (2010) Culture-independent molecular techniques for soil microbial ecology. Soil Biol Biochem 42:878–887. Scholar
  26. Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant-Microbe Interact 20:619–626. Scholar
  27. James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant-Microbe Interact 15:894–906. Scholar
  28. Jasim B, John Jimtha C, Jyothis M, Radhakrishnan EK (2013) Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regul 71:1–11. Scholar
  29. Jasim B, Jimtha John C, Shimil V, Jyothis M, Radhakrishnan EK (2014a) Studies on the factors modulating indole-3-acetic acid production in endophytic bacterial isolates from Piper nigrum and molecular analysis of ipdc gene. J Appl Microbiol 117:786–799. Scholar
  30. Jasim B, Joseph AA, John CJ, Mathew J, Radhakrishnan EK (2014b) Isolation and characterization of plant growth promoting endophytic bacteria from the rhizome of Zingiber officinale. 3 Biotech 4:197–204. Scholar
  31. Jasim B, Anish MC, Shimil V, Jyothis M, Radhakrishnan EK (2015a) Studies on plant growth promoting properties of fruit-associated bacteria from Elettaria cardamomum and molecular analysis of ACC deaminase gene. Appl Biochem Biotechnol 177:175–189. Scholar
  32. Jasim B, Geethu PR, Mathew J, Radhakrishnan EK (2015b) Effect of endophytic Bacillus sp. from selected medicinal plants on growth promotion and diosgenin production in Trigonella foenum-graecum. Plant Cell Tissue Organ Cult 122:565–572. Scholar
  33. Jasim B, Mathew J, Radhakrishnan EK (2016) Identification of a novel endophytic Bacillus sp. from Capsicum annuum with highly efficient and broad spectrum plant probiotic effect. J Appl Microbiol 121:1079–1094. Scholar
  34. Jasim B, Sahadevan N, Chithra S, Mathew J, Radhakrishnan EK (2018) Epigenetic modifier based enhancement of piperine production in endophytic Diaporthe sp. PF20. Proc Natl Acad Sci India B Biol Sci
  35. Jayakumar A, Krishna A, Mohan M, Nair IC, Radhakrishnan EK (2018) Plant growth enhancement, disease resistance, and elemental modulatory effects of plant probiotic endophytic Bacillus sp. Fcl1. Probiotics Antimicrob Proteins 1–9.
  36. Jimtha John C, Jishma P, Karthika NR, Nidheesh KS, Ray JG, Mathew J, Radhakrishnan EK (2017) Pseudomonas fluorescens R68 assisted enhancement in growth and fertilizer utilization of Amaranthus tricolor (L.). 3 Biotech 7:2–7. Scholar
  37. Jishma P, Hussain N, Chellappan R, Rajendran R, Mathew J, Radhakrishnan EK (2017) Strain-specific variation in plant growth promoting volatile organic compounds production by five different Pseudomonas spp. as confirmed by response of Vigna radiata seedlings. J Appl Microbiol 123:204–216. Scholar
  38. 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:e20396. Scholar
  39. Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44. Scholar
  40. Kageyama K, Nelson EB (2003) Differential inactivation of seed exudate stimulation of Pythium ultimum sporangium germination by Enterobacter cloacae influences biological control efficacy on different plant species. Appl Environ Microbiol 69:1114–1120. Scholar
  41. Khan S, Zaidi A, Ahmad E (2014) Phosphate solubilizing microorganisms.
  42. Liu Y, Zuo S, Xu L, Zou Y, Song W (2012) Study on diversity of endophytic bacterial communities in seeds of hybrid maize and their parental lines. Arch Microbiol 194:1001–1012. Scholar
  43. López-López A, Rogel MA, Ormeño-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 33:322–327. Scholar
  44. Lugtenberg BJ, Kravchenko LV, Simons M (1999) Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ Microbiol 1:439–446. Scholar
  45. Madmony A, Chernin L, Pleban S, Pelag E, Riov J (2005) Enterobacter cloacae, an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbiol 50:209–216CrossRefGoogle Scholar
  46. Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis – model and research methods. Soil Biol Biochem 43:883–894. Scholar
  47. Mastretta C, Taghavi S, Van Der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267. Scholar
  48. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530. Scholar
  49. Mckellar ME, Nelson EB (2003) Compost-induced suppression of Pythium damping-off is mediated by fatty-acid-metabolizing seed-colonizing microbial communities. Microbiology 69:452–460. Scholar
  50. Mehrabi-Koushki M, Rouhani H, Mahdikhani-Moghaddam E (2012) Differential display of abundantly expressed genes of Trichoderma harzianum during colonization of tomato-germinating seeds and roots. Curr Microbiol 65:524–533. Scholar
  51. Moter A, Göbel UB (2000) Fluorescence in situ hybridization (FISH) for direct visualization of microorganisms. J Microbiol Methods 41:85–112. Scholar
  52. Mukhopadhyay K, Garrison NK, Hinton DM, Bacon CW, Khush GS, Peck HD, Datta N (1996) Identification and characterization of bacterial endophytes of rice. Mycopathologia 134:151–159. Scholar
  53. Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309. Scholar
  54. Ofek M, Hadar Y, Minz D (2011) Colonization of cucumber seeds by bacteria during germination. Environ Microbiol 13:2794–2807. Scholar
  55. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801. Scholar
  56. Pirttila AM, Laukkanen H, Pospiech H, Myllyla R, Hohtola A (2000) Detection of intracellular bacteria in the buds of scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66:3073–3077. Scholar
  57. Puente ME, Li CY, Bashan Y (2009) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401. Scholar
  58. Ramsey PW, Rillig MC, Feris KP, Holben WE, Gannon JE (2006) Choice of methods for soil microbial community analysis: PLFA maximizes power compared to CLPP and PCR-based approaches. Pedobiologia (Jena) 50:275–280. Scholar
  59. Ringelberg D, Foley K, Reynolds CM (2012) Bacterial endophyte communities of two wheatgrass varieties following propagation in different growing media. Can J Microbiol 58:67–80. Scholar
  60. Roberts DP, Kobayashi DY (2011) Impact of spatial heterogeneity within spermosphere and rhizosphere environments on performance of bacterial biological control agents. Bact Agrobiol Crop Ecosyst 61–96.
  61. Roberts DP, Baker CJ, McKenna L, Liu S, Buyer JS, Kobayashi DY (2009) Influence of host seed on metabolic activity of Enterobacter cloacae in the spermosphere. Soil Biol Biochem 41:754–761. Scholar
  62. Rohini S, Aswani R, Kannan M, Sylas VP, Radhakrishnan EK (2018) Culturable endophytic bacteria of ginger rhizome and their remarkable multi-trait plant growth-promoting features. Curr Microbiol 75:505–511. Scholar
  63. Röling WFM, Ferrer M, Golyshin PN (2010) Systems approaches to microbial communities and their functioning. Curr Opin Biotechnol 21:532–538. Scholar
  64. Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57CrossRefGoogle Scholar
  65. Ruiza D, Agaras B, de Werrab P, Wall LG, Valverde C (2011) Characterization and screening of plant probiotic traits of bacteria isolated from rice seeds cultivated in Argentina. J Microbiol 49:902–912. Scholar
  66. Sabu R, Aswani R, Jishma P, Jasim B, Mathew J, Radhakrishnan EK (2017a) Plant growth promoting endophytic Serratia sp. ZoB14 protecting ginger from fungal pathogens. Proc Natl Acad Sci India B Biol Sci.
  67. Sabu R, Soumya KR, Radhakrishnan EK (2017b) Endophytic Nocardiopsis sp. from Zingiber officinale with both antiphytopathogenic mechanisms and antibiofilm activity against clinical isolates. 3 Biotech 7:1–13. Scholar
  68. Sabu R, Aswani R, Nidheesh KS, Ray JG, Remakanthan A, Radhakrishnan EK (2018) Beneficial changes in Capsicum frutescens due to priming by plant probiotic Burkholderia spp. Probiotics Antimicrob Proteins.
  69. Schiltz S, Gaillard I, Pawlicki-Jullian N, Thiombiano B, Mesnard F, Gontier E (2015) A review: what is the spermosphere and how can it be studied? J Appl Microbiol 119:1467–1481. Scholar
  70. Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36. Scholar
  71. Short GE (1976) Carbohydrate exudation from pea seeds: effect of cultivar, seed age, seed color, and temperature. Phytopathology.
  72. Short GE, Lacy ML (1974) Germination of Fusarium solani f. sp. pisi chlamydospores in the spermoshere of pea. Phytopathology 64:558–562CrossRefGoogle Scholar
  73. Simon EW, Harun RMR (1972) Leakage during seed imbibition. J Exp Bot 23:1076–1085. Scholar
  74. Simon HM, Smith KP, Dodsworth JA, Guenthner B, Handelsman J, Goodman RM (2001) Influence of tomato genotype on growth of inoculated and indigenous bacteria in the spermosphere. Appl Environ Microbiol 67:514–520. Scholar
  75. Singh BK, Dawson LA, Macdonald CA, Buckland SM (2009) Impact of biotic and abiotic interaction on soil microbial communities and functions: a field study. Appl Soil Ecol 41:239–248. Scholar
  76. Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537. Scholar
  77. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol 15:971–981. Scholar
  78. Uhlik O, Leewis M, Strejcek M, Musilova L, Leigh MB, Macek T (2014) NIH Public Access 31:154–165.
  79. Vancura V, Hanzlikova A (1972) Root exudates of plants: IV. Differences in chemcial composition of seed and seedlings exudates. Plant Soil 36(2):271–282CrossRefGoogle Scholar
  80. Voisard C, Keel C, Haas D, Defago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8:351–358. Scholar
  81. Wagner M, Nielsen PH, Loy A, Nielsen JL, Daims H (2006) Linking microbial community structure with function: fluorescence in situ hybridization-microautoradiography and isotope arrays. Curr Opin Biotechnol 17:83–91. Scholar
  82. Watt M, Silk WK, Passioura JB (2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Ann Bot 97:839–855. Scholar
  83. Wellington EMH, Berry A, Krsek M (2003) Resolving functional diversity in relation to microbial community structure in soil: exploiting genomics and stable isotope probing. Curr Opin Microbiol 6:295–301. Scholar
  84. Weststeijn EA (1990) Fluorescent Pseudomonas isolate Ell.3 as biocontrol agent for Pythium root rot in tulips. Neth J Plant Pathol 96:261–272CrossRefGoogle Scholar
  85. Windstam S, Nelson EB (2008) Temporal release of fatty acids and sugars in the spermosphere: impacts on Enterobacter cloacae-induced biological control. Appl Environ Microbiol 74:4292–4299. Scholar
  86. Xu M, Sheng J, Chen L, Men Y, Gan L, Guo S, Shen L (2014) Bacterial community compositions of tomato (Lycopersicum esculentum Mill.) seeds and plant growth promoting activity of ACC deaminase producing Bacillus subtilis (HYT-12-1) on tomato seedlings. World J Microbiol Biotechnol 30:835–845. Scholar
  87. Yaryura PM, León M, Correa OS, Kerber NL, Pucheu NL, García AF (2008) Assessment of the role of chemotaxis and biofilm formation as requirements for colonization of roots and seeds of soybean plants by Bacillus amyloliquefaciens BNM339. Curr Microbiol 56:625–632. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Neethu Sahadevan
    • 1
  • E. K. Radhakrishnan
    • 1
  • Jyothis Mathew
    • 1
  1. 1.School of BioSciencesMahatma Gandhi UniversityKottayamIndia

Personalised recommendations