Abstract
Quorum sensing regulation, mediated by N-acyl homoserine lactone signals, produced by strain Serratia plymuthica HRO-C48 isolated from the rhizosphere of oilseed rape, was found to be responsible for this strain’s ability to produce the broad spectrum antibiotic pyrrolnitrin. In this study, we have shown that some other biocontrol-related traits of strain HRO-C48, such as protection of cucumbers against Pythium apahnidermatum damping-off disease, induced systemic resistance to Botrytis cinerea grey mold in bean and tomato plants, and that colonisation of the rhizosphere also depends on AHL signalling. The results prove that quorum sensing regulation may be generally involved in interactions between plant-associated bacteria, fungal pathogens and host plants.
Similar content being viewed by others
Abbreviations
- AHLs:
-
N-acyl-homoserine lactones
- ISR:
-
induced systemic resistance
- PGPR:
-
plant growth-promoting rhizobacteria
- QS:
-
quorum sensing
- VOCs:
-
volatile organic compounds
- BCA:
-
biocontrol agent
References
Bauer, W. D., & Mathesius, U. (2004). Plant responses to bacterial quorum sensing signals. Current Opinion in Plant Biology, 7, 429–433. doi:10.1016/j.pbi.2004.05.008.
Benhamou, N., Gagné, S., Le Quéré, D., & Dehbi, L. (2000). Bacterial-mediated induced resistance in cucumber : beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathology, 90, 45–56. doi:10.1094/PHYTO.2000.90.1.45.
Berg, G. (2000). Diversity of antifungal and plant-associated Serratia plymuthica strains. Journal of Applied Microbiology, 88, 952–960. doi:10.1046/j.1365-2672.2000.01064.x.
Berg, G., Krechel, A., Ditz, M., Sikora, R. A., Ulrich, A., & Hallmann, J. (2005). Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiology Ecology, 51, 215–229. doi:10.1016/j.femsec.2004.08.006.
Chet, I., & Chernin, L. (2002). Biocontrol, Microbial agents in soil. In G. Bitton (Ed.), Encyclopedia of Environmental Microbiology (pp. 450–465). New York: Willey & Sons Inc.
Chin-A-Woeng, T. F. C., Bloemberg, G. V., & Lugtenberg, B. J. J. (2003). Phenazines and their role in biocontrol by Pseudomonas bacteria. The New Phytologist, 157, 503–523. doi:10.1046/j.1469-8137.2003.00686.x.
de Vleeschauwer, D., & Höfte, M. (2007). Using Serratia plymuthica to control fungal pathogens of plant. CAB Reviews, 2, 046.
Fekete, A., Frommberger, M., Rothballer, M., Li, X., Englmann, M., Fekete, J., et al. (2007). Identification of bacterial N-acylhomoserine lactones (AHLs) with a combination of ultra-performance liquid chromatography (UPLC), ultra-high-resolution mass spectrometry, and in-situ biosensors. Analytical and Bioanalytical Chemistry, 387, 455–467. doi:10.1007/s00216-006-0970-8.
Frankowski, J., Lorito, M., Scala, F., Schmid, R., Berg, G., & Bahl, H. (2001). Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Archives of Microbiology, 176, 421–426. doi:10.1007/s002030100347.
Heungens, K., & Parke, J. L. (2000). Zoospore homing and infection events: effects of the biocontrol bacterium Burkholderia cepacia AMMDR1 on two oomycete pathogens of pea (Pisum sativum L.). Applied and Environmental Microbiology, 66, 5192–5200. doi:10.1128/AEM.66.12.5192-5200.2000.
Kai, M., Effmert, U., Berg, G., & Piechulla, B. (2007). Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Archives of Microbiology, 187, 351–360. doi:10.1007/s00203-006-0199-0.
Kalbe, C., Marten, P., & Berg, G. (1996). Members of the genus Serratia as beneficial rhizobacteria of oilseed rape. Microbiological Research, 151, 433–439.
Kurze, S., Dahl, R., Bahl, H., & Berg, G. (2001). Biological control of soil-borne pathogens in strawberry by Serratia plymuthica HRO-C48. Plant Disease, 85, 529–534. doi:10.1094/PDIS.2001.85.5.529.
Landa, B. B., Mavrodi, O. V., Raaijmakers, J. M., McSpadden Gardener, B. B., Thomashow, L. S., & Weller, D. M. (2002). Differential ability of genotypes of 2,4-diacetylphloroglucinol- producing Pseudomonas fluorescens strains to colonize the roots of pea plants. Applied and Environmental Microbiology, 68, 3226–3237. doi:10.1128/AEM.68.7.3226-3237.2002.
Liu, X., de Bore, W., Berg, G., & Chernin, L. (2004). N-acyl homoserine lactones produced by strains of Collimonas, Herbaspirillum, and Serratia species (Poster presented at the ASM Conference on Cell-Cell Communication in Bacteria, Banff, Alberta, Canada)
Liu, X., Bimerew, M., Ma, Y., Muller, H., Ovadis, M., Eberl, L., et al. (2007). Quorum-sensing signaling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica. FEMS Microbiology Letters, 270, 299–305. doi:10.1111/j.1574-6968.2007.00681.x.
Loh, J., Pierson, E. A., Pierson III, L. S., Stacey, G., & Chatterjee, A. (2002). Quorum sensing in plant-associated bacteria. Current Opinion in Plant Biology, 5, 285–290. doi:10.1016/S1369-5266(02)00274-1.
Ma, Y., Liu, X., Gao, K., Qin, N., Pang, Y., & Shi, C. (2007). Preliminary study on biocontrol potential of rhizobacterium Serratia plymuthica HRO-C48. Journal of Yunnan Agricultural University, 22, 49–53.
McCullagh, M., Utkhede, R., Menzies, J. G., Punja, Z. K., & Paulitz, T. C. (1996). Evaluation of plant growth-promoting rhizobacteria for biological control of Pythium root rot of cucumbers grown in rockwool and effects on yield. European Journal of Plant Pathology, 102, 747–755. doi:10.1007/BF01877149.
Meziane, H., van der Sluis, I., van Loon, L. C., Höfte, M., & Bakker, P. A. H. M. (2005). Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Molecular Plant Pathology, 6, 177–185. doi:10.1111/j.1364-3703.2005.00276.x.
Navazio, L., Aldan, B., Moscatiello, R., Zuppani, A., Woo, S. L., Mariani, P., et al. (2007). Calcium-mediated perception and defense responses activated in plant cells by metabolite mixtures secreted by the biocontrol fungus Trichoderma atroviride. BMC Plant Biology, 30, 41. doi:10.1186/1471-2229-7-41.
Ovadis, M., Liu, X., Gavriel, S., Ismailov, Z., Chet, I., & Chernin, L. (2004). The global regulator genes from biocontrol strain Serratia plymuthica IC1270: cloning, sequencing, and functional studies. Journal of Bacteriology, 186, 4986–4993. doi:10.1128/JB.186.15.4986-4993.2004.
Persello-Carteaux, F., Nussaume, L., & Robaglia, C. (2003). Tales from the underground: molecular plant–rhizobacteria interactions. Plant, Cell & Environment, 26, 189–199. doi:10.1046/j.1365-3040.2003.00956.x.
Pierson III, L. S., Wood, D. W., & Pierson, E. A. (1998). Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annual Review of Phytopathology, 36, 207–225. doi:10.1146/annurev.phyto.36.1.207.
Sarniguet, A., Kraus, J., Henkels, M. D., Muehlchen, A. M., & Loper, J. E. (1995). The sigma factor sigma s affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. Proceedings of the National Academy of Sciences of the United States of America, 92, 12255–12259. doi:10.1073/pnas.92.26.12255.
Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., et al. (2006). Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant, Cell & Environment, 29, 909–918. doi:10.1111/j.1365-3040.2005.01471.x.
Siddiqui, I. A., & Shaukat, S. S. (2005). Phenylacetic acid-producing Rhizoctonia solani represses the biosynthesis of nematicidal compounds in vitro and influences biocontrol of Meloidogyne incognita in tomato by Pseudomonas fluorescens strain CHA0 and its GM derivatives. Journal of Applied Microbiology, 98, 43–55. doi:10.1111/j.1365-2672.2004.02457.x.
Steidle, A., Allesen-Holm, M., Riedel, K., Berg, G., Givskov, M., Molin, S., et al. (2002). Identification and characterization of an N-acylhomoserine lactone-dependent quorum-sensing system in Pseudomonas putida strain IsoF. Applied and Environmental Microbiology, 68, 6371–6382. doi:10.1128/AEM.68.12.6371-6382.2002.
Tran, H., Ficke, A., Asiimwe, T., Höfte, M., & Raaijmakers, J. M. (2007). Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. The New Phytologist, 175, 731–742. doi:10.1111/j.1469-8137.2007.02138.x.
van Houdt, R., Givskov, M., & Michiels, C. W. (2007). Quorum sensing in Serratia. FEMS Microbiology Reviews, 31, 407–424. doi:10.1111/j.1574-6976.2007.00071.x.
van Loon, L. C. (2007). Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Pathology, 119, 243–254. doi:10.1007/s10658-007-9165-1.
Waters, C. M., & Bassler, B. K. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology, 21, 319–346. doi:10.1146/annurev.cellbio.21.012704.131001.
Yan, Z., Reddy, M. S., & Kloepper, J. W. (2003). Survival and colonization of rhizobacteria in a tomato transplant system. Canadian Journal of Microbiology, 49, 383–389. doi:10.1139/w03-051.
Acknowledgements
This work was partially supported by the National Natural Science Foundation of China (grant nos. 30670030 and 30470954) and the senior talent funds of Jiangsu University (07JDG030).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pang, Y., Liu, X., Ma, Y. et al. 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 (2009). https://doi.org/10.1007/s10658-008-9411-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-008-9411-1