Skip to main content
SpringerLink
Log in

Induction of systemic resistance, root colonisation and biocontrol activities of the rhizospheric strain of Serratia plymuthica are dependent on N-acyl homoserine lactones

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • de Vleeschauwer, D., & Höfte, M. (2007). Using Serratia plymuthica to control fungal pathogens of plant. CAB Reviews, 2, 046.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kalbe, C., Marten, P., & Berg, G. (1996). Members of the genus Serratia as beneficial rhizobacteria of oilseed rape. Microbiological Research, 151, 433–439.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

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

  1. Institute of Life Sciences, Jiangsu University, Zhenjiang, 212013, Jiangsu, China

    Yandong Pang & Xiaoguang Liu

  2. Department of Plant Pathology, Shandong Agricultural University, Taian, China

    Yingxin Ma & Kexiang Gao

  3. The Otto Warburg Centre for Agriculture Biotechnology, Hebrew University of Jerusalem, Rehovot, Israel

    Leonid Chernin

  4. Institute of Environmental Biotechnology, Graz University of Technology, Graz, Austria

    Gabriele Berg

Authors
  1. Yandong Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoguang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yingxin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonid Chernin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gabriele Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kexiang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaoguang Liu.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-008-9411-1

Keywords

Search

Navigation