Abstract
The colonization of plant roots with certain rhizosphere bacteria promotes plant growth and induces long lasting systemic protection against a broad spectrum of plant pathogens. The role of the global regulator, GacS, in the rhizosphere colonist Pseudomonas chlororaphis O6 in stimulating growth promotion and induced resistance against Cucumber mosaic virus was examined in tobacco. Responses were compared in tobacco cvs Samsun and GX3. Root colonization of Samsun with wild-type O6 and the gacS complemented mutant-elicited reduced viral symptoms and viral titre. On GX3, there was little affect on symptoms when roots were colonized by the wild-type, gacS mutant or complemented mutant but colonization by both the wild-type and the gacS mutant lowered viral titre. Wild-type O6 and the gacS mutant caused plant growth to be maintained in both tobacco cultivars after viral infection, although the affect was stronger with GX3 than Samsun. In contrast, although a chemical inducer, benzothiadiazole, reduced symptoms and viral titre in both cultivars, plant growth was suppressed. Our results indicate rhizobacteria-elicited induced viral resistance without a negative impact on growth but there was a differential response between cultivars. Detailed knowledge regarding the mechanisms inherent to these differences between cultivars requires further investigation.
Similar content being viewed by others
References
Dietrich, R., Ploss, K., & Heil, M. (2005) Growth responses and fitness costs after induction of pathogen resistance depend on environmental conditions. Plant, Cell and Environment, 28, 211–222.
Garcia-Ruitz, H., & Murphy, J. F. (2001) Age-related resistance in bell pepper to Cucumber mosaic virus. Annals of Applied Biology, 139, 307–317.
Glick, B. R. (1995) The enhancement of plant growth by free-living bacteria. Canadian Journal of Microbiology, 41, 109–117.
Han, S. H., Lee, S. J., Moon, J. H., Yang, K. Y., Cho, B. H., Kim, K. Y., Kim, Y. W., Lee, M. C., Anderson, A. J., & Kim, Y. C. (2006) GacS-dependent production of 2R, 3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Molecular Plant-Microbe Interactions, 19, 924–930.
Heil, M., & Baldwin, I. (2002) Costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science, 7, 61–67.
Heil, M., Hilpert, A., Kaiser, W., & Linsenmair, K. E. (2000) Reduced growth and seed set following chemical induction of pathogen defence: Does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology, 88, 645–654.
Iavicoli, A., Boutet, E., Buchala, A., & Metraux, J. P. (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions, 16, 851–858.
Jung, J. H., Shin, D. H., Bae, W. C., Hong, S. K., Suh, J. W., Koo, S. H., & Jeong, B. C. (2002) Identification of FM001 as plant growth-promoting substance from Acremonium strictum MJN1 culture. Journal of Microbiology and Biotechnology, 12, 327–330.
Kang, B. R., Han, S. H., Zdor, R. E., Anderson, A. J., Spencer, M., Yang, K. Y., Kim, Y. H., Lee, M. C., Cho, B. H., & Kim, Y. C. (2007) Inhibition of seed germination and induction of systemic disease resistance by Pseudomonas chlororaphis O6 require phenazine production regulated by the global regulator, GacS. Journal of Microbiology and Biotechnology, 17, 586–593.
Kang, B. R., Yang, K. Y., Cho, B. H., Han, T. H., Kim, I. S., Lee, M. C., Anderson, A. J., & Kim, Y. C. (2006) Production of indole-3-acetic acid in the plant beneficial strain Pseudomonas chlororaphis O6 is negatively regulated by the global sensor kinase GacS. Current Microbiology, 52, 473–476.
Kim, M. S, Kim, Y. C., & Cho, B. H. (2004) Gene expression analysis in cucumber leaves primed by root colonization with Pseudomonas chlororaphis O6 upon challenge-inoculation with Corynespora cassicola. Plant Biology, 6, 105–108.
Kim, Y. C., Kim, C. H., Kim, K. Y., & Cho, B. H. (2002) Induced systemic resistance and plant growth promotion of a phosphate-solubilizing bacterium, Enterobacter intermedium 60–2G. Korean Journal of Soil Science and Fertilizer, 35, 223–231.
Kloepper, J. W., Leong, J., Teintze, M., & Schroth, M. N. (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature, 286, 885–886.
Kloepper, J. W., Tuzun, S., & Kuc, J. (1992) Proposed definitions related to induced disease resistance. Biocontrol Science & Technology, 2, 349–351.
Kloepper, J. W., & Ryu, C.-M. (2006) Bacterial endophytes as elicitors of induced systemic resistance. In: B. Schulz, C. Boyle & T. N. Sieber (Eds.), Soil biology, microbial root endophytes. (Vol. 9, pp. 33–52). Berlin Heidelberg: Springer-Verlag.
Maurhofer, M., Reimmann, C., Schmidli-Sacherer, P., Heeb, S., Haas, D., & Defago, G. (1998) Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology, 88, 678–684.
Murphy, J. F., Reddy, M. S., Ryu, C.-M., Kloepper, J. W., & Li, R. (2003) Rhizobacteria-mediated growth promotion of tomato leads to protection against Cucumber mosaic virus. Phytopathology, 93, 1301–1307.
Pieterse, C. M. J., Van Wees, S. C. M., Hoffland, E., Van Pelt, J. A., & Van Loon, L. C. (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell, 8, 1225–1237.
Pieterse, C. M. J., Van Wees, S. C. M., Ton, J., Van Pelt, J. A., & Van Loon, L. C. (2002) Signaling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biology, 4, 535–544.
Prinsen, E., Costacurta, A., Michiels, K., Vanderleyden, J., & Van Onckelen, H. (1993) Azospirillum brasilense indole-3-acetic acid biosynthesis: Evidence for a non-tryptophan dependent pathway. Molecular Plant-Microbe Interactions, 6, 609–615.
Raupach, G. S., Liu, L., Murphy, J. F., Tuzun, S., & Kloepper, J. W. (1996) Induced systemic resistance against Cucumber mosaic virus cucumovirus using plant growth-promoting rhizobacteria (PGPR). Plant Disease, 80, 891–894.
Ryu, C.-M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W., & Pare, P. W. (2004a) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiology, 134, 1017–1026.
Ryu, C.-M., Farag, M. A., Hu, C. H., Reddy, M. S., Wei, H. X., Pare, P. W., & Kloepper, J. W. (2003) Bacterial volatiles promote growth in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 100, 4927–4932.
Ryu, C.-M., Murphy, J. F., Mysore, K. S., & 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 acid-dependent signaling pathway. The Plant Journal, 39, 381–392.
Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H. Y., & Hunt, M. D. (1996) Systemic acquired resistance. Plant Cell, 8, 1809–1819.
Saleh, S. S., & Glick, B. R. (2001) Involvement of gacS and rpoS in transcriptional regulation of the plant growth-promoting bacteria Enterobacter cloacae CAL2 and UW4. Canadian Journal of Microbiology, 47, 698–705.
Spencer, M., Kim, Y. C., Ryu, C.-M., Kloepper, J. W., Yang, K. Y., & Anderson, A. J. (2003) Induced defence in tobacco by Pseudomonas chlororaphis strain O6 involves at least the ethylene pathway. Physiological and Molecular Plant Pathology, 63, 27–34.
Timmusk, S., Nicander, B., Granhall, U., & Tillberg, E. (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biology and Biochemistry, 31, 1847–1852.
Vallad, G. E., & Goodman, R. M. (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science, 44, 1920–1934.
Van Loon, L. C., Bakker, P. A. H. M., & Pierterse, C. M. J. (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology, 36, 453–483.
Van Peer, P., & Schippers, R. (1992) Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to Fusarium wilt. Netherlands Journal of Plant Pathology, 98, 129–139.
Acknowledgements
This work was supported by a grant from BioGreen 21 programme (code#20050401034716), Rural Development Administration, Republic of Korea, by a grant from the Technology Development Programme for Agriculture and Forestry, Ministry of Agriculture and Forestry, Republic of Korea, and by the Utah State Agricultural Experiment Station, USA.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ryu, CM., Kang, B.R., Han, S.H. et al. Tobacco cultivars vary in induction of systemic resistance against Cucumber mosaic virus and growth promotion by Pseudomonas chlororaphis O6 and its gacS mutant. Eur J Plant Pathol 119, 383–390 (2007). https://doi.org/10.1007/s10658-007-9168-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-007-9168-y