Literature data on acyl homoserine lactones (AHL), a novel class of bacterial mediator molecules involved in a remote signal transduction, have been analyzed and summarized. Their involvement in auto-reception of bacterial population quantitative parameters called “quorum sensing” (QS) is discussed. The QS phenomenon and its components are related to the regulation of plant and bacteria physiological processes including bio-film formation, phytohormone synthesis, plasmid transfer, production of virulent factors, etc. A special attention is given to the AHL involvement in plant growth and development regulation, prospects of their application in crops priming biotechnology, modeling of protection responses and development of genetic resistance in nonresistant plants.
Keywords: acyl homoserine lactone, biofilm, autoinductor, plant priming biotechnology
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1. Babenko, L.M., Kosakivska, I.V., Skaterna, T.D. & Kharchenko, O.V. (2013). Plant lipoxygenase at adaptation to influence of abiotic stress factors. Bull. Kharkov. Natl. Agr. Univ., No. 2, pp. 6-19 [in Ukrainian].
2. Boubriak, O.A., Akimkina, T.V., Dmitriev, O.P., Grodzinsky, D.M. & Boubriak, I.I. (2013). Search for molecular markers for optimization presowing processing (priming) of seeds. Bull. Kharkov. Natl. Agr. Univ., No. 2, pp. 47-57 [in Ukrainian].
3. Gostev, V.V. & Sidorenko, S.V. (2010). Bacterial biofilms and infections. Zhurn. infektologii, No. 2(3), pp. 4-15 [in Russian].
4. Kolupaev, Yu.E. & Karpets, Yu.V. (2010). Formation of adaptive reactions of plants to the action of abiotic stresses. Kiev: Osnova [in Russian].
5. Krestetska, S.L. & Nesterenko, A.M. (2007). Autoinduction and signal transduction: communication systems in microbial populations. Annals of Mechnicov Institute, No. 1, pp. 4-9 [in Ukrainian].
6. Moshynets, O.V. & Kosakivska, I.V. (2010). Phytosphere ecology: plant-microbial interactions. 1. structure functional characteristic of rhizo-, endo- and phyllosphere. Bull. Kharkov. Natl. Agr. Univ., No. 2(20), pp. 19-35 [in Ukrainian].
7. Moshynets, O.V., Shpylova, S.P., Spiers, A.J. & Kosakivska, I.V. (2010). The phytosphere of Brassica napus L. as a niche for Pseudomonas fluorescens SBW25. Dopov. Nac. akad. nauk Ukr., No. 12, pp. 150-153 [in Ukrainian].
8. Oleskin, A.V., Botvinko, I.V. & Tsavkelova, E.A. (2000). Colony organization and intracellular communication in microorganisms. Microbiology, No. 3, pp. 309-327 [in Russian]. https://doi.org/10.1007/BF02756730
9. Bai, X., Todd, C.D., Desikan, R. & Yang, Y. (2012). N-3-oxo-decanoyl-L-homoserinelactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in muny bean. Plant Physiol., No. 158, pp. 725-736. https://doi.org/10.1104/pp.111.185769
10. Bassler, B. (2002). Small talk. Cell-to-cell communication in bacteria. Cell, No. 109(4), pp. 421-424. https://doi.org/10.1016/S0092-8674(02)00749-3
11. Beckers, G.J., Jaskiewicz, M., Liu, Y., Underwood W.R., He S.Y., Zhang S. & Conrath, U. (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell., No. 21, pp. 944-953. https://doi.org/10.1105/tpc.108.062158
12. Beckers, G.J. & Spoel, S.H. (2006). Fine-tuning plant defense signaling: salicylate versus jasmonate. Plant Biol. (Stuttg.), No. 8, pp. 1-10.
13. Beneduzi, A., Ambrosini, A. & Passaglia, L.M. (2012). Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet. Mol. Biol., No. 35, pp. 1044-1051. https://doi.org/10.1590/S1415-47572012000600020
14. Berg, G. (2009). Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol., No. 84, pp. 11-18. https://doi.org/10.1007/s00253-009-2092-7
15. Brader, G., Compant, S., Mitter, B. Trognitz, F. & Sessitsch, A. (2014). Metabolic potential of endophytic bacteria. Curr. Opin. Biotechnol., No. 27, pp. 30-37. https://doi.org/10.1016/j.copbio.2013.09.012
16. Conrath, U., Pieterse, C. & Mauch-Mani, B. (2002). Priming in plant-pathogen interactions. Trends Plant Sci., No. 7, pp. 210-216. https://doi.org/10.1016/S1360-1385(02)02244-6
17. Farah, C., Vera, M., Morin, D., Dominique H., Jerez, C.A. & Guiliani, N. (2005). Evidence for a functional quorum-sensing type AI-1 system in the extermophilic bacterium Acidithibacillus ferrooxidans. AEM, No. 7(11), pp. 7033-7040. https://doi.org/10.1128/AEM.71.11.7033-7040.2005
18. Fukua, W., Winans, S. & Greenberg, E. (1994). Quorum sensing in bacteria: the LuxR/LuxI family of cell density responsive transcriptional regulators. J. Bacteriol., No. 176, pp. 269-275. https://doi.org/10.1128/jb.176.2.269-275.1994
19. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol., No. 43, pp. 205-227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
20. Gonzalez, J.E. & Marketon, M.M. (2003). Quorum sensing in nitrogen-fixing rhizobia. Microbiol. Mol. Biol. Rev., No. 67, pp. 574-592. https://doi.org/10.1128/MMBR.67.4.574-592.2003
21. Hernandez-Reyes, C., Schenk, S.T., Neumann, C., Kogel, K.H. & Schikora, A. (2014). N-acyl-homoserine lactone-producing bacteria protect plants against plant and human pathogens . Microbiol. Biotechnol., No. 7, pp. 580-588. https://doi.org/10.1111/1751-7915.12177
22. Iida, A., Ohnishi, Y. & Horinouchi, S. (2008). Control of acetic acid fermentation by quorum sensing via N-acylhomoserine lactones in Gluconacetobacter intermedius. J. Bacteriol., No. 190 (7), pp. 2546-2555. https://doi.org/10.1128/JB.01698-07
23. Iida, A., Ohnishi, Y. & Horinouchi, S. (2009). Identification and characterization of target genes of the GinI/GinR quorum-sensing system in Gluconacetobacter intermedius . Microbiology, No. 155, pp. 3021-3032. https://doi.org/10.1099/mic.0.028613-0
24. Jaskiewicz, M., Conrath, U. & Peterhansel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response . EMBO Rep., No. 12, pp. 50-55. https://doi.org/10.1038/embor.2010.186
25. Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J. & Greenberg, J.T. (2009). Priming in systemic plant immunity. Science, No. 324, pp. 89-91. https://doi.org/10.1126/science.1170025
26. Kievit, T. & Iglewsky, B. (2000). Bacterial quorum sensing in pathogenic relationships. Infect. Immun., No. 68 (9), pp. 4839-4849. https://doi.org/10.1128/IAI.68.9.4839-4849.2000
27. Koornneef, A. & Pieterse, C.M. (2008). Cross talk in defense signaling. Plant Physiol., No. 146, pp. 839-844. https://doi.org/10.1104/pp.107.112029
28. 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-acylhomoserine lactones, the bacterial quorum-sensing signals. Mol. Plant-Microbe. Interact., No. 25, pp. 677-683. https://doi.org/10.1094/MPMI-10-11-0274
29. Losick, R. & Kaiser, D. (1997). Why and how bacteria communicate. Sci. Amer., No. 276(2), pp. 68-73. https://doi.org/10.1038/scientificamerican0297-68
30. Luna, E., Bruce, T.J., Roberts, M.R., Flors, V. & Ton, J. (2012). Next-generation systemic acquired resistance. Plant Physiol., No. 158, pp. 844-853. https://doi.org/10.1104/pp.111.187468
31. Manos, J. Arthur, J., Rose, B., Tingpej, P., Fung, C., Curtis, M., Webb, J.S., Hu, H., Kjelleberg, S., Gorrell, M.D., Bye, P. & Harbour, C. (2008). Transcriptome analyses and biofilm-forming characteristics of a clonal Pseudomonas aeruginosa from the cystic fibrosis lung. J. Med. Microbiol., No. 57, pp. 1454—1465. https://doi.org/10.1099/jmm.0.2008/005009-0
32. Mark, J., Mandel, M.S., Wollenberg, E.V. Stabb, E.V, Visick, K.L. & Ruby, E.G. (2003). A single regulatory gene is sufficient to alter bacterial host range. Nature, No. 458, pp. 215-218.
33. Marketon, M.M., Glenn, S.A., Eberhard, A. & Gonzalez, J.E. (2003). Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J. Bacteriol., No. 185, pp. 325-331. https://doi.org/10.1128/JB.185.1.325-331.2003
34. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anollés, G., Rolfe, B.G., Bauer, W.D. (2003). Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. USA, No. 100, pp. 1444-1449. https://doi.org/10.1073/pnas.262672599
35. McLean, R.J., Pierson, L.S. & Fuqua, C. (2004). A simple screening protocol for the identification of quorum signal antagonists. J. Microbiol. Methods., No. 58, pp. 351-360. https://doi.org/10.1016/j.mimet.2004.04.016
36. Nadeem, S.M., Ahmad, M., Zahir, Z.A., Javaid, A. & Ashraf, M. (2013). The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv., No. 32, pp. 429-448.
37. Natelson, S. & Natelson, E.A. (1989). Preparation of D-, DL- and L-homoserine lactone from methionine. Microchem. J., No. 40, pp. 226-232. https://doi.org/10.1016/0026-265X(89)90074-X
38. Normander, B. & Prosser, J. L. (2000). Bacterial origin and community composition in the barley phytosphere as a function of habitat and presowing conditions. Appl. Environ. Microbiol., No. 66, pp. 4372-4377. https://doi.org/10.1128/AEM.66.10.4372-4377.2000
39. Ortiz-Castro, R., Martinez-Trujillo, M. & Lopez-Bucio, J. (2008). N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ., No. 31, pp. 1497-1509. https://doi.org/10.1111/j.1365-3040.2008.01863.x
40. Palmer, A.G., Senechal, A.C., Mukherjee, A., Ané, J.M. & Blackwell, H.E. (2014). Plant responses to bacterial N-acyl-L-homoserine lactones are dependent on enzymatic degradation to L-homoserine. ACS Chem. Biol., No. 9, pp. 1834-1845. https://doi.org/10.1021/cb500191a
41. Parsek, M., Val, D., Hanzelka, B., Cronan, J. & Greenberg, E.P. (1999). Acyl homoserine lactone quorum-sensing signal generation. Proc. Natl. Acad. Sci. USA, No. 96, pp. 4360-4365. https://doi.org/10.1073/pnas.96.8.4360
42. Rasmann, S., De Vos, M., Casteel, C.L., Tian, D., Halitschke, R., Sun, J.Y., Agrawal, A.A., Felton, G.W. & Jander, G. (2012). Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol., No. 158, pp. 854-863. https://doi.org/10.1104/pp.111.187831
43. Ortíz-Castro, R., Contreras-Cornejo, H.A., Macías-Rodríguez, L. & López-Bucio, J. (2009). The role of microbial signals in plant growth and development. Plant Signal. Behav., No. 4 (8), pp. 701-712. https://doi.org/10.4161/psb.4.8.9047
44. Revenchon, S., Bouillant, M.L., Salmond, G. & Nasser, W. (1998). Integration of the quorum-sensing system in the regulatory networks controlling virulence factor synthesis in Erwinia chrysanthemii. Mol. Microbiol., No. 29, pp. 1407-1418. https://doi.org/10.1046/j.1365-2958.1998.01023.x
45. Salmond, G.P.C., Bycroft, B.W., Stewart, C.S.A.B. & Williams, P. (1995). The bacterial "enigma": cracking the code of cell-cell communication. Mol. Microbiol., No. 16 (4), pp. 615-624. https://doi.org/10.1111/j.1365-2958.1995.tb02424.x
46. Schenk, S. & Schikora, A. (2015). AHL-priming function via oxylipin and salicylic acid. Front. Plant Sci., No. 5, pp. 784-794. https://doi.org/10.3389/fpls.2014.00784
47. Schenk, S.T., Hernandez-Reyes, C., Samans, B., Stein, E., Neumann, C., Schikora, M., Reichelt, M., Mithofer, A., Becker, A., Kogel, K.H. & Schikora, A. (2014). N-Acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell., No. 26, pp. 2708-2723. https://doi.org/10.1105/tpc.114.126763
48. Schikora, A., Schenk, S.T., Stein, E., Molitor, A., Zuccaro, A. & Kogel, K.H. (2011). N-Acyl-homoserine lactone confers resistance towards biotrophic and hemibiotrophic pathogens via altered activation of AtMPK. Plant Physiol., No. 57, pp. 1407-1418. https://doi.org/10.1104/pp.111.180604
49. Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Van Breusegem, F., Eberl, L., Hartmann, A. & Langebartels, C. (2006). Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ., No. 29, pp. 909-918. https://doi.org/10.1111/j.1365-3040.2005.01471.x
50. Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B. & Mauch-Mani, B. (2012). Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol., No. 158, pp. 835-843. https://doi.org/10.1104/pp.111.191593
51. Spoel, S.H. & Dong, X. (2008). Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe, No. 3, pp. 348-351. https://doi.org/10.1016/j.chom.2008.05.009
52. Teplitski, M., Robinson, J.B. & Bauer, W.D. (2000). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe Interact., No. 13, pp. 637-648. https://doi.org/10.1094/MPMI.2000.13.6.637
53. Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M.N., Métraux, J.P. & Mauch-Mani, B. (2005). Dissecting the b-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell., No. 17, pp. 987-999. https://doi.org/10.1105/tpc.104.029728
54. Tsai, C.H., Singh, P., Chen, C.W., Thomas, J., Weber, J., Mauch-Mani, B. & Zimmerli, L. (2011). Priming for enhanced defense responses by specific inhibition of the Arabidopsis response to coronatine. Plant J., No. 65, pp. 469-479. https://doi.org/10.1111/j.1365-313X.2010.04436.x
55. van Elsas, J.D., Tumer, S. & Bailey, M.J. (2003). Horizontal gene transfer in the phytosphere. New Phytol., No. 157, pp. 525-537. https://doi.org/10.1046/j.1469-8137.2003.00697.x
56. van Peer, P., Punte, H.L. M., De Weger, L. A. & Schippers, B. (1990). Characterization of root surface and endorhizosphere Pseudomonas in relation to their colonization of roots. Appl. Environ. Microbiol., No. 56, pp. 2462-2470.
57. van Wees, S.C., De Swart, E.A., van Pelt, J.A., van Loon, L.C. & Pieterse, C.M.J. (2000). Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, No. 97, pp. 8711-8716. https://doi.org/10.1073/pnas.130425197
58. von Rad, U., Klein, I., Dobrev, P.I., Kottova, J., Zazimalova, E., Fekete, A., Hartmann, A, Schmitt-Kopplin, P. & Durner, J. (2009). Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta, No. 229, pp. 73-85.
59. Whitehead, N., Barnard, A., Slater, H., Simpson, N.J. & Salmond, G.P. (2001). Quorum sensing in Gram-negative bacteria. FEMS Microbiol. Rev., No. 25, pp. 365-404. https://doi.org/10.1111/j.1574-6976.2001.tb00583.x
60. Zarkani, A.A., Stein, E., Rohrich, C.R., Schikora, M., Evguenieva-Hackenberg, E., Degenkolb, T., Vilcinskas, A., Klug, G., Kogel, K.H. & Schikora, A. (2013). Homoserine lactones influence the reaction of plants to rhizobia. Int. J. Mol. Sci., No. 4, pp. 17122-17146. https://doi.org/10.3390/ijms140817122