Bacterial quorum sensing compounds are important modulators of microbe-plant interactions

Frontiers in Plant Science

Volumn 5, Issue APR, 2014, Pages

  Hartmann, Anton ^a   Rothballer, Michael ^a   Hense, Burkhard A ^a   Schröder, Peter ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Endophytic bacteria; Innate immunity; Mutualists; N acyl homoserine lactones; Quorum sensing; Systemic responses

Indexed keywords

EID: 84901036641     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00131     Document Type: Article

References (36)

1. Alqueres, S., Menses, C., Rouws, L., Rothballer, M., Baldani, I., Schmid, M., et al. (2013). The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus strain PAL5. Mol. Plant-Microbe Interact. 26, 937-945. doi: 10.1094/MPMI-12-12-0286-R
2. Bai, X., Todd, C. D., Desikan, R., Yang, Y., and 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 mung bean. Plant Physiol. 158, 725-736. doi: 10.1104/pp.111.185769
3. Barriuso, J., Solano, B. R., Fray, R. G., Cámara, M., Hartmann, A., and Gutierrez Manero, F. J. (2008). Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria. Plant Biotech. J. 6, 442-452. doi: 10.1111/j.1467-7652.2008.00331.x
4. Bauer, W. D., and Mathesius, U. (2004). Plant responses to bacterial quorum sensing signals. Curr. Opin. Plant Biol. 7, 429-433. doi: 10.1016/j.pbi.2004.05.008
5. Chalupowicz, L., Barash, I., Panijel, M., Sessa, G., and Manulis-Sasson, S. (2009). Regulatory interaction between quorum-sensing, auxin, cytokinin, and the hrp regulon in relation to gall formation and epiphytic fitness of Pantoea agglomerans pv. Gypsophilae. Mol. Plant Microbe Interact. 22, 849-856. doi: 10.1094/MPMI-22-7-0849
6. Delalande, L., Faure, D., Raffoux, A., Uroz, S., D'Angelo-Picard, C., Elasri, M., et al. (2005). N-hexanoyl-L-homoserine lactone, a mediator of bacterial quorum sensing regulation, exhibits plant-dependent. FEMS Microbiol. Ecol. 52, 13-50.
7. Eberl, L. (1999). N-acyl-homoserine lactone-mediated gene regulation in Gram-negative bacteria. Syst. Appl. Microbiol. 22, 493-506. doi: 10.1016/S0723-2020(99)80001-0
8. Gao, M., Teplitski, M., Robinson, J. B., and Bauer, W. D. (2003). Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol. Plant Microbe Interact. 16, 827-834. doi: 10.1094/MPMI.2003.16.9.827
9. Garcia-Gutiérrez, L., Zeriouh, H., Romero, D., Cubero, J., de Vicente, A., and Pérez-Garcia A. (2013). The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate-and salicylic acid-dependent defence response. Microb. Biotechnol. 6, 264-274. doi: 10.1111/1751-7915.12028
10. Götz, C., Fekete, A., Gebefügi, I., Forczek, S., Fuksová, K., Li, X., et al. (2007). Uptake, degradation and chiral discrimination of N-acyl-D/L-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal. Bioanal. Chem. 389, 1447-1457. doi: 10.1007/s00216-007-1579-2
11. Hartmann, A., Gantner, S., Schuhegger, R., Steidle, A., Dürr, C., Schmid, M., et al. (2004). "N-acyl-homoserine lactones of rhizosphere bacteria trigger systemic resistance in tomato plants" in Biology of Molecular Plant-Microbe Interactions, Vol. 4, eds B. Lugtenberg, I. Tikhonovich, and N. Provorov (St. Paul, Minnesota: MPMI-Press), 554-556.
12. Hartmann, A., and Schikora, A. (2012). Quorum sensing of bacteria and trans-kingdom interactions of N-acyl homoserine lactones with eukaryotes. J. Chem. Ecol. 38, 704-713. doi: 10.1007/s10886-012-0141-7
13. Hense, B. A., Kuttler, C., Müller, J., Rothballer, M., Hartmann, A., and Kreft, J.-U. (2007). Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5, 230-239. doi: 10.1038/nrmicro1600
14. Janeway, C. A. Jr., and Medzhitov, R. (2002). Innate immune recognition. Annu. Rev. Immunol. 20, 197-216. doi: 10.1146/annurev.immunol.20.083001.084359
15. Jin, G., Liu, F., Ma, H., Hao, S., Zhao, Q., Bian, Z., et al. (2012). Two G-protein-coupled-receptor candidates, Cand2 and Cand7, are involved in Arabidopsis root growth mediated by the bacterial quorum-sensing signals N-acyl-homoserine lactones. Biochem. Biophys. Res. Commun. 417, 991-995. doi: 10.1016/j.bbrc.2011.12.066
16. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
17. Joseph, C. M., and Phillips, D. A. (2003). Metabolites from soil bacteria affect plant water relations. Plant Physiol. Biochem. 41, 189-192. doi: 10.1016/S0981-9428(02)00021-9
18. Kravchenko, V. V., Kaufmann, G. F., Mathison, J. C., Scott, D. A., Katz, A. Z., Wood, M. R., et al. (2008). Modulation of gene expression via disruption of NF-κB signalling by a bacterial small molecule. Science 321, 259-263. doi: 10.1126/science.1156499
19. Liu, F., Bian, Z., Jia, Z., Zhao, Q., and 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. doi: 10.1094/MPMI-10-11-0274
20. Liu, X., Bimerew, M., Ma, Y., Müller, H., Ovadis, M., Eberl, L., et al. (2007). Quorum-sensing signaling is required for production of the antobiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica. FEMS Microbiol. Lett. 270, 299-305. doi: 10.1111/j.1574-6968.2007.00681.x
21. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anoliés, G., Rolfe, B. G., et al. (2003). Extensive and specific responses of a eukaryote to bacterial quorum sensing signals. Proc. Natl. Acad. Sci. U.S. A 100, 1444-1449. doi: 10.1073/pnas.262672599
22. Ortíz-Castro, R., Martinez-Trujillo, M., and 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. doi: 10.1111/j.1365-3040.2008.01863.x
23. Pang, Y., Liu, X., Ma, Y., Chernin, L., Berg, G., and Gao, K. (2009). Induction of systemic resistance, root colonisation and biocontrol activities of the rhizospheric strain of Serratia plymuthica are dependent on N-acyl homoserine lactones. Eur. J. Plant Pathol. 124, 261-268. doi: 10.1007/s10658-008-9411-1
24. Pérez-Montano, F., Guasch-Vidal, B., González-Barroso, S., López-Baena, F. J., Cubo, T., Ollero, F. J., et al. (2011). Nodulation-gene-inducing flavonoids increase overall production of autoinducers and expression of N-acyl-homoserine lactone synthesis genes in Rhizobia. Res. Microbiol. 162, 715-723. doi: 10.1016/j.resmic.2011.05.002
25. Ryu, C.-M., Choi, H. K., Lee, C.-H., Murphy, J. F., Lee, J.-K., and Kloepper, J. W. (2013). Modulation of quorum sensing in acyl-homoserine lactone-producing or-degrading tobacco plants leads to alteration of induced systemic resistance elicited by the rhizobacterium Serratia marcescens 90-166. Plant Pathol. J. 29, 182-192. doi: 10.5423/PPJ.SI.11.2012.0173
26. Schenk, S. T., Stein, E., Kogel, K.-H., and Schikora, A. (2012). Arabidopsis growth and defense are modulated by bacterial quorum sensing molecules. Plant Signal. Behav. 7, 178-181. doi: 10.4161/psb.18789
27. Schikora, A., Schenk, S. T., Stein, E., Molitor, A., Zuccaro, A., and Kogel, K.-H. (2011). N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol. 157, 1407-1418. doi: 10.1104/pp.111.180604
28. Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., et al. (2006) Induction of systemic resistance in tomato plants by N-acyl-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ. 29, 909-918. doi: 10.1111/j.1365-3040.2005.01471.x
29. Scott, R. A., Weil, J., Le, P. T., Williams, P., Fray, R. G., von Bodman, S. B., et al. (2006). Long-and short chain plant-produced bacterial N-acyl-homoserine lactones become components of phyllosphere, rhizosphere, and soil. Mol. Plant-Microbe Interact. 19, 227-239. doi: 10.1094/MPMI-19-0227
30. Sieper, T., Forczek, S., Matucha, M., Krämer, P., Hartmann, A., and Schröder, P. (2014). N-acyl-homoserine lactone uptake and systemic transport in barley rest upon active parts of the plant. New Phytol. 201, 545-555. doi: 10.1111/nph.12519
31. Teplitski, M., Mathesius, U., and Rumbaugh, K. P. (2011). Perception and degradation of N-acyl-homoserine lactone quorum sensing signals by mammalian and plant cells. Chem. Rev. 111, 100-116. doi: 10.1021/cr100045m
32. Turner, T. R., James, E. K., and Poole, P. S. (2013). The plant microbiome. Genome Biol. 14, 209-219. doi: 10.1186/gb-2013-14-6-209
33. von Rad, U., Klein, I., Dobrev, P. I., Kottova, J., Zazimalova, E., Fekete, A., et al. (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. doi: 10.1007/s00425-008-0811-4
34. Yi, H.-S., Ryu, C.-M., and Heil, M. (2010). Sweet smells prepare plants for future stress-airborne induction of plant disease immunity. Plant Signal. Behav. 5, 528-531. doi: 10.4161/psb.10984
35. Zamioudis, C., and Pieterse, C. M. J. (2012). Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139-150. doi: 10.1094/MPMI-06-11-0179
36. Zilber-Rosenberg, I., and Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723-735. doi: 10.1111/j.1574-6976.2008.00123.x