Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Adonizio AL, Downum K, Bennett BC, Mathee K (2006) Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 105:427–435

  • Aly AH, Debbab A, Proksch P (2013) Fungal endophytes—secret producers of bioactive plant metabolites. Pharmazie 68:499–505

    CAS  PubMed  Google Scholar 

  • 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 158:725–736

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 95:194–202

    CAS  PubMed  Article  Google Scholar 

  • 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 49:551–555

    CAS  PubMed  Article  Google Scholar 

  • Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Callow JA, Callow ME (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings. Nat Commun 2:244

    PubMed  Article  Google Scholar 

  • 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 782847

  • 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 101:5048–5052

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 60:14–23

    CAS  PubMed  Article  Google Scholar 

  • 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 12:115–124

    CAS  PubMed  Article  Google Scholar 

  • Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3:541–548

    CAS  PubMed  Article  Google Scholar 

  • 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 111:4280–4284

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Dichschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369

    Article  Google Scholar 

  • 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 97:3526–3531

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 411:813–817

  • 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 44:1331–1339

    PubMed Central  PubMed  Article  Google Scholar 

  • Estrela AB, Abraham WR (2010) Combining biofilm-controlling compounds and antibiotics as a promising new way to control biofilm infections. Pharmaceuticals 3:1374–1393

    CAS  PubMed Central  Article  Google Scholar 

  • 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 77:1351–1358

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 111:28–67

    CAS  PubMed  Article  Google Scholar 

  • 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 125:204–208

    CAS  PubMed  Article  Google Scholar 

  • 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 178:6618–6622

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harjai K, Kumar R, Singh S (2010) Garlic blocks quorum sensing and attenuates the virulence of Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 58:161–168

    CAS  PubMed  Article  Google Scholar 

  • Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131

    PubMed Central  PubMed  Article  Google Scholar 

  • 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 8:1–11

    Article  Google Scholar 

  • Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 12:4661–4696

    PubMed Central  PubMed  Article  Google Scholar 

  • 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 5:1857–1870

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 78:2410–2421

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 49:354–360

    CAS  PubMed  Article  Google Scholar 

  • Kim S-H, Park H-D (2013) Ginger Extract Inhibits Biofilm Formation by Pseudomonas aeruginosa PA14. PLoS ONE 8, e76106

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Koh KH, Tham FY (2011) Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. J Microbiol Immunol Infect 44:144–148

    PubMed  Article  Google Scholar 

  • 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 60:137–151

    Article  Google Scholar 

  • 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 98:7173–7183

    CAS  PubMed  Article  Google Scholar 

  • 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 106:771–788

    CAS  PubMed  Article  Google Scholar 

  • 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 77:2577–2584

    CAS  PubMed  Article  Google Scholar 

  • Kusari S, Singh S, Jayabaskaran C (2014d) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303

    CAS  PubMed  Article  Google Scholar 

  • LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 68:3919–3924

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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):e00143–15

    PubMed Central  PubMed  Article  Google Scholar 

  • 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 11:26

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 25:677–683

    CAS  PubMed  Article  Google Scholar 

  • 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 12:5503–5526

    PubMed Central  PubMed  Article  Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199

    CAS  PubMed  Article  Google Scholar 

  • Moebius N, Üzüm Z, Dijksterhuis J, Lackner G, Hertweck C (2014) Active invasion of bacteria into living fungal cells. eLife 3, e03007

    PubMed Central  PubMed  Article  Google Scholar 

  • 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 25:149–162

    CAS  PubMed  Article  Google Scholar 

  • 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 13:109–126

    CAS  PubMed  Article  Google Scholar 

  • 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 317:53–57

    CAS  Article  Google Scholar 

  • Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 194:615–622

  • 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 31:1497–1509

    PubMed  Article  Google Scholar 

  • 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 164:749–760

    CAS  PubMed  Article  Google Scholar 

  • Rajesh PS, Rai VR (2013) Hydrolytic enzymes and quorum sensing inhibitors from endophytic fungi of Ventilago madraspatana Gaertn. Biocatal Agric Biotechnol 2:120–124

    Google Scholar 

  • 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 443:290–295

    CAS  PubMed  Article  Google Scholar 

  • 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 169:561–569

    CAS  PubMed  Article  Google Scholar 

  • 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 98:3401–3412

    CAS  PubMed  Article  Google Scholar 

  • Sandoz KM, Mitzimberg SM, Schuster M (2007) Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 104:15876–15881

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Schenk ST, Stein E, Kogel K-H, Schikora A (2012) Arabidopsis growth and defense are modulated by bacterial quorum sensing molecules. Plant Signal Behav 7:178–181

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • 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 55:1187–1192

    CAS  PubMed  Article  Google Scholar 

  • Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, Bjarnsholt T, de Nys R, Givskov M (2008) Quorum sensing antagonism from marine organisms. Mar Biotechnol 10:56–63

    CAS  PubMed  Article  Google Scholar 

  • Sorrentino F, Roy I, Keshavarz T (2010) Impact of linoleic acid supplementation on lovastatin production in Aspergillus terreus cultures. Appl Microbiol Biotechnol 88:65–73

    CAS  PubMed  Article  Google Scholar 

  • Tait K, Hutchison Z, Thompson FL, Munn CB (2010) Quorum sensing signal production and inhibition by coral-associated vibrios. Environ Microbiol Rep 2:145–150

  • 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 111:100–116

    CAS  PubMed  Article  Google Scholar 

  • 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 57:11186–11193

    CAS  PubMed  Article  Google Scholar 

  • Ulrich RL (2004) Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis. Appl Environ Microbiol 70:6173–6180

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Vattem DA, Mihalik K, Crixell SH, McLean RJ (2007) Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78:302–310

    CAS  PubMed  Article  Google Scholar 

  • 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 229:73–85

    CAS  Article  Google Scholar 

  • 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 43:7403–7409

    CAS  PubMed  Article  Google Scholar 

  • Zhou Y, Choi Y-L, Sun M, Yu Z (2008) Novel roles of Bacillus thuringiensis to control plant diseases. Appl Microbiol Biotechnol 80:563–572

    CAS  PubMed  Article  Google Scholar 

  • Zhu H, Sun SJ (2008) Inhibition of bacterial quorum sensing-regulated behaviors by Tremella fuciformis extract. Curr Microbiol 57:418–422

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Oliver Kayser.

Additional information

This manuscript is dedicated with best wishes to Professor Dr. Hartmut Laatsch on the occasion of his 69th birthday

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kusari, P., Kusari, S., Spiteller, M. et al. Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology. Appl Microbiol Biotechnol 99, 5383–5390 (2015). https://doi.org/10.1007/s00253-015-6660-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6660-8

Keywords

  • Quorum sensing
  • Quorum quenching
  • Endophytes
  • Virulence factors
  • Autoinducer
  • Drug resistance