Applied Microbiology and Biotechnology

, Volume 99, Issue 13, pp 5383–5390 | Cite as

Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology

  • Parijat Kusari
  • Souvik Kusari
  • Michael Spiteller
  • Oliver KayserEmail author


Quorum sensing, the cell-to-cell communication system mediated by autoinducers, is responsible for regulation of virulence factors, infections, invasion, colonization, biofilm formation, and antibiotic resistance within bacterial populations. Concomitantly, quorum quenching is a process that involves attenuation of virulence factors by inhibiting or degrading quorum signaling autoinducers. Survival of endophytic microorganisms, commonly known as endophytes, in planta is a continuous mêlée with invading pathogens and pests. In order to survive in their microhabitats inside plants, endophytes have co-evolved to not only utilize an arsenal of biologically active defense compounds but also impede communication between invading pathogens. Such antivirulence strategies prevent pathogens from communicating with or recognizing each other and thus, colonizing plants. The quenching phenomena often involves microbial crosstalk within single or mixed population(s) vis-à-vis gene expression, and production/modulation of quenching enzymes coupled to various antagonistic and synergistic interactions. This concept is particularly interesting because it can be biotechnologically translated in the future to quorum inhibiting antivirulence therapies without triggering resistance in bacteria, which is currently a major problem worldwide that cannot be tackled only with antimicrobial therapies. In this mini-review, we highlight the quorum quenching capacity of endophytes with respect to attenuation of virulence factors and aiding in plant defense response. Further, benefits and potential challenges of using such systems in biotechnology are discussed.


Quorum sensing Quorum quenching Endophytes Virulence factors Autoinducer Drug resistance 



We gratefully acknowledge the Ministry of Innovation, Science, Research, and Technology of the State of North Rhine-Westphalia, Germany and TU Dortmund for funding.

Conflict of interest

The authors declare no conflict of interest.


  1. Adonizio AL, Downum K, Bennett BC, Mathee K (2006) Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 105:427–435Google Scholar
  2. Aly AH, Debbab A, Proksch P (2013) Fungal endophytes—secret producers of bioactive plant metabolites. Pharmazie 68:499–505PubMedGoogle Scholar
  3. Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-l-homoserine- lactone activates auxin-induced adventitious root formation via hydrogen peroxide-and nitric oxide-dependent cyclic GMP signaling in mungbean. Plant Physiol 158:725–736PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bai Z-Q, Lin X, Wang Y, Wang J, Zhou X, Yang B, Liu J, Yang X, Wang Y, Liu Y (2014) New phenyl derivatives from endophytic fungus Aspergillus flavipes AIL8 derived of mangrove plant Acanthus ilicifolius. Fitoterapia 95:194–202PubMedCrossRefGoogle Scholar
  5. Bodini SF, Manfredini S, Epp M, Valentini S, Santori F (2009) Quorum sensing inhibition activity of garlic extract and p-coumaric acid. Lett Appl Microbiol 49:551–555PubMedCrossRefGoogle Scholar
  6. Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37PubMedCentralPubMedCrossRefGoogle Scholar
  7. Callow JA, Callow ME (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings. Nat Commun 2:244PubMedCrossRefGoogle Scholar
  8. Chankhamhaengdecha S, Hongvijit S, Srichaisupakit A, Charnchai P, Panbangred W (2013) Endophytic Actinomycetes: a novel source of potential acyl homoserine lactone degrading enzymes. Biomed Res Int 2013: Article ID 782847Google Scholar
  9. Chen H, Fujita M, Feng Q, Clardy J, Fink GR (2004) Tyrosol is a quorum-sensing molecule in Candida albicans. Proc Natl Acad Sci U S A 101:5048–5052PubMedCentralPubMedCrossRefGoogle Scholar
  10. Cho H-S, Park S-Y, Ryu C-M, Kim JF, Kim J-G, Park S-H (2007) Interference of quorum sensing and virulence of the rice pathogen Burkholderia glumae by an engineered endophytic bacterium. FEMS Microbiol Ecol 60:14–23PubMedCrossRefGoogle Scholar
  11. Claessen D, Rozen DE, Kuipers OP, Søgaard-Andersen L, van Wezel GP (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12:115–124PubMedCrossRefGoogle Scholar
  12. Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3:541–548PubMedCrossRefGoogle Scholar
  13. Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci U S A 111:4280–4284PubMedCentralPubMedCrossRefGoogle Scholar
  14. Dichschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369CrossRefGoogle Scholar
  15. Dong Y-H, Xu J-L, Li X-Z, Zhang L-H (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci U S A 97:3526–3531PubMedCentralPubMedCrossRefGoogle Scholar
  16. Dong Y-H, Wnag L-H, Xu J-L, Zhang H-B, Zhang X-F, Zhang L-H (2001) Quenching quorum-sensing dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817Google Scholar
  17. Dourado MN, Bogas AC, Pomini AM, Andreote FD, Quecine MC, Marsaioli AJ, Araújo WL (2013) Methylobacterium-plant interaction genes regulated by plant exudate and quorum sensing molecules. Braz J Microbiol 44:1331–1339PubMedCentralPubMedCrossRefGoogle Scholar
  18. Estrela AB, Abraham WR (2010) Combining biofilm-controlling compounds and antibiotics as a promising new way to control biofilm infections. Pharmaceuticals 3:1374–1393PubMedCentralCrossRefGoogle Scholar
  19. Figueroa M, Jarmusch AK, Raja HA, El-Elimat T, Kavanaugh JS, Horswill AR, Cooks RG, Cech NB, Oberlies NH (2014) Polyhydroxyanthraquinones as quorum sensing inhibitors from the guttates of Penicillium restrictum and their analysis by desorption electrospray ionization mass spectrometry. J Nat Prod 77:1351–1358PubMedCentralPubMedCrossRefGoogle Scholar
  20. Galloway WRJD, Hodgkinson JT, Bowden SD, Welch M, Spring DR (2011) Quorum sensing in gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem Rev 111:28–67PubMedCrossRefGoogle Scholar
  21. Girennavar B, Cepeda ML, Soni KA, Vikram A, Jesudhasan P, Jayaprakasha GK, Pillai SD, Patil BS (2008) Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. Int J Food Microbiol 125:204–208PubMedCrossRefGoogle Scholar
  22. Givskov M, de Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD, Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178:6618–6622PubMedCentralPubMedGoogle Scholar
  23. Harjai K, Kumar R, Singh S (2010) Garlic blocks quorum sensing and attenuates the virulence of Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 58:161–168PubMedCrossRefGoogle Scholar
  24. Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131PubMedCentralPubMedCrossRefGoogle Scholar
  25. Higgins KL, Arnold AE, Coley PD, Kursar TA (2014) Communities of fungal endophytes in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecol 8:1–11CrossRefGoogle Scholar
  26. Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619PubMedCentralPubMedCrossRefGoogle Scholar
  27. Hong K-W, Koh C-L, Sam C-K, Yin Y-F, Chan K-G (2012) Quorum quenching revisited—from signal decays to signaling confusion. Sensors 12:4661–4696PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hosni T, Moretti C, Devescovi G, Suarez-Moreno ZR, Fatmi MB, Guarnaccia C, Pongor S, Onofri A, Buonaurio R, Venturi V (2011) Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J 5:1857–1870PubMedCentralPubMedCrossRefGoogle Scholar
  29. Jakobsen TH, Bragason SK, Phipps RK, Christensen LD, van Gennip M, Alhede M, Skindersoe M, Larsen TO, Høiby N, Bjarnsholt T, Givskov M (2012) Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl Environ Microbiol 78:2410–2421PubMedCentralPubMedCrossRefGoogle Scholar
  30. Khan MS, Zahin M, Hasan S, Husain FM, Ahmad I (2009) Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett Appl Microbiol 49:354–360PubMedCrossRefGoogle Scholar
  31. Kim S-H, Park H-D (2013) Ginger Extract Inhibits Biofilm Formation by Pseudomonas aeruginosa PA14. PLoS ONE 8, e76106PubMedCentralPubMedCrossRefGoogle Scholar
  32. Koh KH, Tham FY (2011) Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. J Microbiol Immunol Infect 44:144–148PubMedCrossRefGoogle Scholar
  33. Kusari P, Kusari S, Spiteller M, Kayser O (2013) Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers 60:137–151CrossRefGoogle Scholar
  34. Kusari P, Kusari S, Lamshoeft M, Sezgin S, Spiteller M, Kayser O (2014a) Quorum quenching is an antivirulence strategy employed by endophytic bacteria. Appl Microbiol Biotechnol 98:7173–7183PubMedCrossRefGoogle Scholar
  35. Kusari P, Kusari S, Spiteller M, Kayser O (2014b) Biocontrol potential of endophytes harbored in Radula marginata (liverwort) from the New Zealand ecosystem. Antonie Van Leeuwenhoek 106:771–788PubMedCrossRefGoogle Scholar
  36. Kusari S, Lamshoeft M, Kusari P, Gottfried S, Zühlke S, Louven K, Hentschel U, Kayser O, Spiteller M (2014c) Endophytes are hidden producers of maytansine in Putterlickia roots. J Nat Prod 77:2577–2584PubMedCrossRefGoogle Scholar
  37. Kusari S, Singh S, Jayabaskaran C (2014d) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303PubMedCrossRefGoogle Scholar
  38. LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111PubMedCentralPubMedCrossRefGoogle Scholar
  39. Lee SJ, Park S, Lee J, Yum D, Koo B, Lee J (2002) Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl Environ Microbiol 68:3919–3924PubMedCentralPubMedCrossRefGoogle Scholar
  40. Leonhardt I, Spielberg S, Weber M, Albrecht-Eckardt D, Bläss M, Claus R, Barz D, Scherlach K, Hertweck C, Löffler J, Hünniger K, Kurzai O (2015) The fungal quorum-sensing molecule farnesol activates innate immune cells but suppresses cellular adaptive immunity. mBio 6(2):e00143–15PubMedCentralPubMedCrossRefGoogle Scholar
  41. Liu X, Jia J, Popat R, Ortori CA, Li J, Diggle SP, Gao K (2011) Characterisation of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style. BMC Microbiol 11:26PubMedCentralPubMedCrossRefGoogle Scholar
  42. Liu F, Bian Z, Jia Z, Zhao Q, Song S (2012) The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl-homoserine lactones, the bacterial quorum-sensing system. Mol Plant Microbe Interact 25:677–683PubMedCrossRefGoogle Scholar
  43. Martín-Rodríguez AJ, Reyes F, Martín J, Pérez-Yépez J, León-Barrios M, Couttolenc A, Espinoza C, Trigos A, Martín VS, Norte M, Fernández JJ (2014) Inhibition of bacterial quorum sensing by extracts from aquatic fungi: first report from marine endophytes. Mar Drugs 12:5503–5526PubMedCentralPubMedCrossRefGoogle Scholar
  44. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199PubMedCrossRefGoogle Scholar
  45. Moebius N, Üzüm Z, Dijksterhuis J, Lackner G, Hertweck C (2014) Active invasion of bacteria into living fungal cells. eLife 3, e03007PubMedCentralPubMedCrossRefGoogle Scholar
  46. Molino PJ, Childs S, Eason Hubbard MR, Carey JM, Burgman MA, Wetherbee R (2009) Development of the primary bacterial microfouling layer on antifouling and fouling release coatings in temperate and tropical environments in Eastern Australia. Biofouling 25:149–162PubMedCrossRefGoogle Scholar
  47. Natrah FM, Defoirdt T, Sorgeloos P, Bossier P (2011a) Disruption of bacterial cell-to-cell communication by marine organisms and its relevance to aquaculture. Mar Biotechnol 13:109–126PubMedCrossRefGoogle Scholar
  48. Natrah FMI, Kenmegne MM, Wiyoto W, Sorgeloos P, Bossier P, Defoirdt T (2011b) Effects of micro-algae commonly used in aquaculture on acyl-homoserine lactone quorum sensing. Aquaculture 317:53–57CrossRefGoogle Scholar
  49. Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518PubMedCentralPubMedGoogle Scholar
  50. Nieto-Penalver CG, Bertini EV, de Figueroa LIC (2012) Identification of N-acyl homoserine lactones produced by Gluconacetobacter diazotrophicus PAL5 cultured in complex and synthetic media. Arch Microbiol 194:615–622Google Scholar
  51. Ortíz-Castro R, Martinez-Trujillo M, López- Bucio J (2008) N-acyl homoserine lactones:a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509PubMedCrossRefGoogle Scholar
  52. Perez-Montano F, Jimenez-Guerrero I, Sanchez-Matamoros C, Lopez-Baena FJ, Ollero FJ, Rodriguez-Carvajal MA, Bellogin RA, Espuny MR (2013) Rice and bean AHL-mimic quorum-sensing signals specifically interfere with the capacity to form biofilms by plant-associated bacteria. Res Microbiol 164:749–760PubMedCrossRefGoogle Scholar
  53. Rajesh PS, Rai VR (2013) Hydrolytic enzymes and quorum sensing inhibitors from endophytic fungi of Ventilago madraspatana Gaertn. Biocatal Agric Biotechnol 2:120–124Google Scholar
  54. Rajesh PS, Rai VR (2014a) Molecular identification of aiiA homologous gene from endophytic Enterobacter species and in silico analysis of putative tertiary structure of AHL-lactonase. Biochem Biophys Res Commun 443:290–295PubMedCrossRefGoogle Scholar
  55. Rajesh PS, Rai VR (2014b) Quorum quenching activity in cell-free lysate of endophytic bacteria isolated from Pterocarpus santalinus Linn., and its effect on quorum sensing regulated biofilm in Pseudomonas aeruginosa PAO1. Microbiol Res 169:561–569PubMedCrossRefGoogle Scholar
  56. Safari M, Amache R, Esmaeilishirazifard E, Keshavarz T (2014) Microbial metabolism of quorum-sensing molecules acyl-homoserine lactones, γ-heptalactone and other lactones. Appl Microbiol Biotechnol 98:3401–3412PubMedCrossRefGoogle Scholar
  57. Sandoz KM, Mitzimberg SM, Schuster M (2007) Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 104:15876–15881PubMedCentralPubMedCrossRefGoogle Scholar
  58. Schenk ST, Stein E, Kogel K-H, Schikora A (2012) Arabidopsis growth and defense are modulated by bacterial quorum sensing molecules. Plant Signal Behav 7:178–181PubMedCentralPubMedCrossRefGoogle Scholar
  59. Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192PubMedCrossRefGoogle Scholar
  60. Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, Bjarnsholt T, de Nys R, Givskov M (2008) Quorum sensing antagonism from marine organisms. Mar Biotechnol 10:56–63PubMedCrossRefGoogle Scholar
  61. Sorrentino F, Roy I, Keshavarz T (2010) Impact of linoleic acid supplementation on lovastatin production in Aspergillus terreus cultures. Appl Microbiol Biotechnol 88:65–73PubMedCrossRefGoogle Scholar
  62. Tait K, Hutchison Z, Thompson FL, Munn CB (2010) Quorum sensing signal production and inhibition by coral-associated vibrios. Environ Microbiol Rep 2:145–150Google Scholar
  63. Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116PubMedCrossRefGoogle Scholar
  64. Truchado P, Gil-Izquierdo A, Tomas-Barberan F, Allende A (2009) Inhibition by chestnut honey of N-acyl-l-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enterocolitica, and Aeromonas hydrophila. J Agric Food Chem 57:11186–11193PubMedCrossRefGoogle Scholar
  65. Ulrich RL (2004) Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis. Appl Environ Microbiol 70:6173–6180PubMedCentralPubMedCrossRefGoogle Scholar
  66. Vattem DA, Mihalik K, Crixell SH, McLean RJ (2007) Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78:302–310PubMedCrossRefGoogle Scholar
  67. von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) The response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85CrossRefGoogle Scholar
  68. Yeon K-M, Lee C-H, Kim J (2009) Magnetic enzyme carrier for effective biofouling control in the membrane bioreactor based on enzymatic quorum quenching. Environ Sci Technol 43:7403–7409PubMedCrossRefGoogle Scholar
  69. Zhou Y, Choi Y-L, Sun M, Yu Z (2008) Novel roles of Bacillus thuringiensis to control plant diseases. Appl Microbiol Biotechnol 80:563–572PubMedCrossRefGoogle Scholar
  70. Zhu H, Sun SJ (2008) Inhibition of bacterial quorum sensing-regulated behaviors by Tremella fuciformis extract. Curr Microbiol 57:418–422PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Parijat Kusari
    • 1
  • Souvik Kusari
    • 2
  • Michael Spiteller
    • 2
  • Oliver Kayser
    • 1
    Email author
  1. 1.Department of Biochemical and Chemical Engineering, Chair of Technical BiochemistryTU DortmundDortmundGermany
  2. 2.Institute of Environmental Research (INFU), Department of Chemistry and Chemical Biology, Chair of Environmental Chemistry and Analytical ChemistryTU DortmundDortmundGermany

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