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.


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
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
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
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
Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37
Callow JA, Callow ME (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings. Nat Commun 2:244
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
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
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
Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3:541–548
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
Dichschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369
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
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
Estrela AB, Abraham WR (2010) Combining biofilm-controlling compounds and antibiotics as a promising new way to control biofilm infections. Pharmaceuticals 3:1374–1393
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
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
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
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
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
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
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
Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619
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
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
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
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
Kim S-H, Park H-D (2013) Ginger Extract Inhibits Biofilm Formation by Pseudomonas aeruginosa PA14. PLoS ONE 8, e76106
Koh KH, Tham FY (2011) Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. J Microbiol Immunol Infect 44:144–148
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
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
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
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
Kusari S, Singh S, Jayabaskaran C (2014d) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303
LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111
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
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
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
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
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
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
Moebius N, Üzüm Z, Dijksterhuis J, Lackner G, Hertweck C (2014) Active invasion of bacteria into living fungal cells. eLife 3, e03007
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
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
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
Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518
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
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
Rajesh PS, Rai VR (2013) Hydrolytic enzymes and quorum sensing inhibitors from endophytic fungi of Ventilago madraspatana Gaertn. Biocatal Agric Biotechnol 2:120–124
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
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
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
Sandoz KM, Mitzimberg SM, Schuster M (2007) Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 104:15876–15881
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
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
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
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
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
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
Ulrich RL (2004) Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis. Appl Environ Microbiol 70:6173–6180
Vattem DA, Mihalik K, Crixell SH, McLean RJ (2007) Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78:302–310
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
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
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
Zhu H, Sun SJ (2008) Inhibition of bacterial quorum sensing-regulated behaviors by Tremella fuciformis extract. Curr Microbiol 57:418–422
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
Corresponding author
Additional information
This manuscript is dedicated with best wishes to Professor Dr. Hartmut Laatsch on the occasion of his 69th birthday
Rights and permissions
About this article
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
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