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 Pathology Journal

Volumn 29, Issue 2, 2013, Pages 182-192

  Ryu, Choong Min ^a,b   Choi, Hye Kyung ^a   Lee, Chi Ho ^d   Murphy, John F ^c   Lee, Jung Kee ^d   Kloepper, Joseph W ^c  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

^c AUBURN UNIVERSITY   (United States)

^d PaiChai University   (South Korea)

Author keywords

AiiA; N Acyl homoserine lactone; Plant growth promoting rhizobacteria; Quorum sensing

Indexed keywords

BACTERIA (MICROORGANISMS); CUCUMBER MOSAIC VIRUS; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; PECTOBACTERIUM CAROTOVORUM SUBSP. CAROTOVORUM; PSEUDOMONAS SYRINGAE PV. TABACI; RHIZOBIALES; RHIZOBIUM; SERRATIA MARCESCENS;

EID: 84885723377     PISSN: 15982254     EISSN: 20939280     Source Type: Journal    
DOI: 10.5423/PPJ.SI.11.2012.0173     Document Type: Article

References (44)

1. Audenaert, K., Pattery, T., Cornelis, P. and Höfte, M. 2002. Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: Role of salicylic acid, pyochelin, and pyocyanin. Mol. Plant-Microbe Interact. 15:1147-1156.
2. Cho, H. S., Park, S. Y., Ryu, C.-M., Kim, J. F., Kim, J. G. and 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.
3. Cortes-Barco, A. M., Goodwin, P. H. and Hsiang, T. 2010a. Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathol. 59:643-653.
4. Cortes-Barco, A. M., Hsiang, T. and Goodwin, P. H. 2010b. Induced systemic resistance against three foliar diseases of Agrostis stolonifera by (2R,3R)-butanediol or an isoparaffin mixture. Ann. Appl. Biol. 157:179-189.
5. De Vleesschauwer, D. and Hofte, M. 2009. Rhizobacteria-induced systemic resistance. Adv. Bot. Res. 51:223-281.
6. Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F. and Zhang, L. H. 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acylhomoserine lactonase. Nature 411: 813-817.
7. Enebak, S. A. and Carey, W. A. 2000. Evidence for induced systemic protection to fusiform rust in loblolly pine by plant growth-promoting rhizobacteria. Plant Dis. 84:306-308.
8. Fray, R. G., Throup, J. P., Wallace, A., Daykin, M., Williams, P., Stewart, G. S. A. B. and Grierson, D. 1999. Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nature Biotechnol. 17:1017-1020.
9. Fray, R. G. 2002. Altering plant-microbe interaction through artificially manipulating bacterial quorum sensing. Ann. Bot. 89:245-53.
10. Hahm, M. S., Sumayo, M., Hwang, Y. J., Jeon, S. A., Park, S. J., Lee, J. Y., Ahn, J. H., Kim, B. S., Ryu, C. M. and Ghim, S. Y. 2012. Biological control and plant growth promoting capacity of rhizobacteria on pepper under greenhouse and field conditions. J. Microbiol. 50:380-385.
11. Kloepper, J. W., Tuzun, S. and Kuc, J. A. 1992. Proposed definitions related to induced disease resistance. Biocontrol Sci. Technol. 2:349-351.
12. Kloepper, J. W., Ryu, C.-M. and. Zhang, S. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-1266.
13. Kloepper, J. W. and Ryu, C.-M. 2006. Bacterial endophytes as elicitors of induced systemic resistance. In: Soil Biology, eds. by B. S. Schulz, C. Boyle and T. N. Sieber, Volume 9 Microbial Root Endophytes. pp. 33-52. Berlin Heidelberg: SpringerVerlag. Germany.
14. Kovacikova, G., Lin, W. and Skorupski, K. 2005. Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetateresponsive LysR-type regulator AlsR in Vibrio Cholerae. Mol. Microbiol. 57:420-433.
15. Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anolles, G., Rolfe, B. G. and Bauer, W. D. 2003. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. USA 100:1444-1449.
16. Miller, M. B. and Bassler, B. L. 2001. Quorum sensing in bacteria Annu. Rev. Microbiol. 55:165-199.
17. Moons, P., Van Houdt, R., Vivijs, B., Michiels, C. M. and Aertsen, A. 2011. Integrated regulation of acetoin fermentation by quorum sensing and pH in Serratia plymuthica RVH1. Appl. Environ. Microbiol. 77: 3422-3427.
18. Morello, J. E., Pierson, E. A. and Pierson, L. S. 3rd. 2004. Negative cross-communication among wheat rhizosphere bacteria: effect on antibiotic production by the biological control bacterium Pseudomonas aureofaciens 30-84. Appl. Environ. Microbiol. 70:3103-3109.
19. Murphy, J. F., Reddy, M. S., Ryu, C.-M., Kloepper, J. W. and Li, R. 2003. Rhizobacteria-mediated growth promotion of tomato leads to protection against Cucumber mosaic virus. Phytopathology 93:1301-1307.
20. Naylor, M., Murphy, A. M., Berry, J. O. and Carr, J. P. 1998. Salicylic acid can induce resistance to plant virus movement. Mol. Plant-Microbe Interact. 11:860-868.
21. Niu, D. D., Liu, H. X., Jiang, C. H., Wang, Y. P., Wang, Q. Y., Jin, H. L. and Guo, J. H. 2011. The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol. Plant-Microbe Interact. 24:533-542.
22. Pang, Y., Liu, X., Ma, Y., Chernin, L., Berg, G. and Gao, K. 2009. Induction of systemic resistance, root colonisation and iocontrol activities of the rhizospheric strain of Serratia plymuthica are dependent on N-acyl homoserine lactones. Eur. J. Plant Pathol. 124:261-268.
23. Pierson, L. S. 3rd, Wood, D. W. and Pierson, E. A. 1998. Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annu. Rev. Phytopathol. 36:207-25.
24. Press, C. M., Loper, J. E. and Kloepper, J. W. 2001. Role of iron in rhizobacteria-mediated induced systemic resistance of cucumber. Phytopathology 91:593-598.
25. Press, C. M., Wilson, M., Tuzun, S. and Kloepper, J. W. 1997. Salicylic acid produced by Serratia marcescens 90-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol. Plant-Microbe Interact. 10:761-768.
26. Rao, B., Zhang, L. Y., Sun, J., Su, G., Wei, D., Chu, J., Zhu, J. and Shen, Y. 2012. Characterization and regulation of the 2,3-butanediol pathway in Serratia marcescens. Appl. Microbiol. Biotechnol. 93:2147-2159.
27. Raupach, G. S., Liu, L., Murphy, J. F., Tuzun, S. and Kloepper, J. W. 1996. Induced systemic resistance in cucumber and tomato against cucumber mosaic cucumovirus using plant growthpromoting rhizobacteria (PGPR). Plant Dis. 80:891-894.
28. Reimmann, C., Ginet, N., Michel, L., Keel, C., Michaux, P., Krishnapillai, V., Zala, M., Heurlier, K., Triandafillu, K., Harms, H., Defago, G. and Haas, D. 2002. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148:923-932.
29. Robert-Seilaniantz, A., Grant, M. and Jones, J. D. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 2011: 49:317-43.
30. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y. and Hunt, M. D. 1996. Systemic acquired resistance. Plant Cell 8:1809-1819.
31. Ryu, C.-M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W. and Paré, P. W. 2004a. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017-1026.
32. Ryu, C.-M., Murphy, J. F., Mysore, K. S. and Kloepper, J. W. 2004b. Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic aciddependent signaling pathway. Plant J. 39:381-392.
33. Schaefer, A. L., Hanzelka, B. L., Parsek, M. R. and Greenberg, E. P. 2000. Detection, purication, and structural elucidation of the acylhomoserine lactone inducer of Vibrio scheri luminescence and other related molecules. Methods Enzymol. 305:288-301.
34. Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E. Jr., Rinehart, K. L. and Farrand, S. K. 1997. Detecting and characterizing N-acylhomoserine lactone signal molecules by thin-layer chromatography. Proc. Natl. Acad. Sci. USA 94:6036-6041.
35. 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.
36. Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Van Breusegem, F., Eberl, L., Hartmann, A. and Langebartels, C. 2006. Induction of systemic resistance in tomato by N-acyl-L-homoserine lactoneproducing rhizosphere bacteria. Plant Cell Environ. 29:909-918.
37. Teplitski, M., Robinson, J. B. and 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. 13:637-648.
38. Van Houdt, R., Moons, P., Hueso Buj, M. and Michiels, C. W. 2006. N-acyl-L-homoserine lactone quorum sensing controls butanediol fermentation in Serratia plymuthica RVH1 and Serratia marcescens MG1. J. Bacteriol. 188:4570-4572.
39. Van Houdt, R., Moons, P., Aertsen, A., Jansen, A., Vanoirbeek, K., Daykin, M., Williams, P. and Michiels, C. W. 2007. Characterization of a luxI/luxR-type quorum sensing system and N-acyl-homoserine lactone-dependent regulation of exoenzyme and antibacterial component production in Serratia plymuthica RVH1. Res. Microbiol. 158:150-158.
40. Whiteley, M., Lee, K. M. and Greenberg, E. P. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 96:13904-13909.
41. Wilson, M., Ezelle, J. E., Press, C. M., Park, K. S., Farrand, S. K., Pierson III L. S. and Kloepper, J. W. 1997. Autoinducer production in Serratia marcescens 90-166. Phytopathology 87:S103.
42. Yang, J. W., Yi, H.-S., Kim, H., Lee, B., Lee, S., Ghim, S.-Y. and Ryu, C.-M. 2011. Whitefly infestation elicits defense responses against bacterial pathogens on the leaf and root and belowground dynamic change of microflora in pepper. J. Ecol. 99:46-56.
43. Zhang, S., Moyne, A.-L., Reddy, M. S. and Kloepper, J. W. 2002. The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol. Control 25:288-296.
44. Zhang, S., Reddy, M. S. and Kloepper J. W. 2004. Tobacco growth enhancement and blue mold disease protection by rhizobacteria: Relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166. Plant Soil 262:277-288.