The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Determinants of Plant Growth-promoting Ochrobactrum lupini KUDC1013 Involved in Induction of Systemic Resistance against Pectobacterium carotovorum subsp. carotovorum in Tobacco Leaves

  • Sumayo, Marilyn (School of Life Sciences and Institute for Microorganisms, Kyungpook National University) ;
  • Hahm, Mi-Seon (School of Life Sciences and Institute for Microorganisms, Kyungpook National University) ;
  • Ghim, Sa-Youl (School of Life Sciences and Institute for Microorganisms, Kyungpook National University)
  • Received : 2012.09.13
  • Accepted : 2012.11.07
  • Published : 2013.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

The plant growth-promoting rhizobacterium Ochrobactrum lupini KUDC1013 elicited induced systemic resistance (ISR) in tobacco against soft rot disease caused by Pectobacterium carotovorum subsp. carotovorum. We investigated of its factors involved in ISR elicitation. To characterize the ISR determinants, KUDC1013 cell suspension, heat-treated cells, supernatant from a culture medium, crude bacterial lipopolysaccharide (LPS) and flagella were tested for their ISR activities. Both LPS and flagella from KUDC1013 were effective in ISR elicitation. Crude cell free supernatant elicited ISR and factors with the highest ISR activity were retained in the n-butanol fraction. Analysis of the ISR-active fraction revealed the metabolites, phenylacetic acid (PAA), 1-hexadecene and linoleic acid (LA), as elicitors of ISR. Treatment of tobacco with these compounds significantly decreased the soft rot disease symptoms. This is the first report on the ISR determinants by plant growth-promoting rhizobacteria (PGPR) KUDC1013 and identifying PAA, 1-hexadecene and LA as ISR-related compounds. This study shows that KUDC1013 has a great potential as biological control agent because of its multiple factors involved in induction of systemic resistance against phytopathogens.

Keywords

References

  1. Alonso, L., Cuesta, E. P. and Gilliland, S. E. 2003. Production of free conjugated linoleic acid by Lactobacillus acidophilus and Lactobacillus casei of human intestinal origin. J. Dairy Sci. 86:1941−1946.
  2. Babalola, O. O. 2010. Beneficial bacteria of agricultural importance. Biotechnol. Lett. 32:1559−1570.
  3. Cameron, R.K., Dixon, R. and Lamb, C. 1994. Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J. 5:715−725. https://doi.org/10.1111/j.1365-313X.1994.00715.x
  4. Chin, S. F., Liu, W., Storkson, J. M., Ha, Y. L. and Pariza, M. W. 1992. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J. Food Comp. Anal. 5:185−197.
  5. Chin-A-Woeng, T. F. C., Bloemberg, G. V., van der Bij, A. J., van der Drift, K. M. G. M., Schripsema, J., Kroon, B., Scheffer R. J., Keel, C., Bakker, P. A. H. M., Tichy, H. V., de Brujin, F. J. Thomas-Oaters, J. E. and Lugtenberg, B. J. J. 1998. Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Mol. Plant-Microbe Interact. 11:1069−77.
  6. Dunne, C., Möenne-Loccoz, Y., McCarthy, J., Higgins, P., Powell, J., Dowling, D. N. and O'Gara, F. 1998. Combining proteolytic and phloroglucinol-producing bacteria for improved control of Pythium-mediated damping-off of sugar beet. Plant Pathol. 47:299−307.
  7. Fries, L. 1977. Growth regulating effects of phenylacetic acid and phydroxy-phenylacetic acid on Fucus spiralis L. (Phaecophyceae, Fucales) in axenic culture. Phycology 16:451−455.
  8. Gomez-Gomez, L. and Boller, T. 2002. Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7:251−256. https://doi.org/10.1016/S1360-1385(02)02261-6
  9. Haas, D. and Keel, C. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 41:117− 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. 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. Ham, M. S., Park, Y. M., Sung, H. R., Sumayo, M., Ryu, C. M., Park, S. H. and Ghim, S.-Y. 2009. Characterization of rhizo-bacteria isolated from family Solanaceae plants in Dokdo island. Kor. J. Microbiol. Biotechnol. 37:110−117.
  12. Han, S. H., Anderson, J. A., Yang, K. W., Cho, B. H., Kim, K. Y., Lee, M. C., Kim, Y. H. and Kim, Y. C. 2006. Multiple determinants influence root colonization and induction of induced systemic resistance by Pseudomonas chlororaphis O6. Mol. Plant Pathol. 7:463−472.
  13. Hwang, B. K., Lim, S. W., Kim, B. S., Lee, J. Y. and Moon, S. S. 2001. Isolation and in vivo and in vitro antifungal activity of phenylacetic acid and sodium phenylacetate from Streptomyces humidus. Appl. Environ. Microbiol. 67:3739−3745.
  14. Isogai, Y., Okamoto, T. and Koizumi, T. 1967. Isolation of indole-3-acetamide, 2-phenylacetamide and indole-3-carboxaldehyde from etiolated seedlings of Phaseolus. Chem. Pharm. Bull. Tokyo.15:151−158.
  15. Jetiyanon, K. and Kloepper, J. W. 2002. Mixtures of plant-growth promoting rhizobacteria for induction of systemic resistance against multiple diseases. Biol. Control 24:285−291.
  16. Kamilova, F., Validov, S., Azarova, T., Mulders, I. and Lugtenberg, B. 2005. Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ. Microbiol. 7:1809-17. https://doi.org/10.1111/j.1462-2920.2005.00889.x
  17. Kloepper, J. W., Tuzun, S. and Kuc, J. A. 1992. Proposed definitions related to induced disease resistance. Biocontrol Sci. Tech. 2:349−351.
  18. Kumar, V., Bhatnagar, A. K. and Srivastava, J. N. 2011. Antibacterial activity of crude extracts of Spirulina platensis and its structural elucidation of bioactive compound. J. Med. Plants. Res. 5:7043−7048.
  19. Lee, J. Y., Kim, H. S., Kim, K. D. and Hwang, B. K. 2004. In vitro anti-oomycete and in vivo control efficacy of phenylacetic acid against Phytophthora capsici. Plant Pathol. J. 20:177−183.
  20. Leeman, M., van Pelt, J. A., Den Ouden, F. M., Heinsbroek, M., Bakker, P. A. H. M. and Schippers, B. 1995. Induction of systemic resistance against Fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85:1021−1027. https://doi.org/10.1094/Phyto-85-1021
  21. Liu, S., Weibin, R., Jing, L., Hua, X., Jingan, W., Yubao, G. and Jingguo, W. 2008. Biological control of phytopathogenic fungi by fatty acids. Mycopathologia 166:93−102. https://doi.org/10.1007/s11046-008-9124-1
  22. Lugtenberg, B. and Kamilalova, F. 2009. Plant growth promoting rhizobacteria. Annu. Rev. Microbiol. 63:541−556.
  23. Macouzet, M., Lee, B. H. and Robert, N. 2009. Production of conjugated linoleic acid by probiotic Lactobacillus acidophilus La-5. J. Appl. Microbiol. 106:1886−1891.
  24. Meindl, T., Boller, T. and Felix, G. 2000. The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell 12:1783−1794.
  25. Meziane, H., van der Sluis, I., van Loon, L. C., Hofte, M. and Bakker, P. A. H. M. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177−185.
  26. Milborrow, B. V., Purse, J. G. and Wightman, F. 1975. On the auxin activity of phenylacetic acid. Ann. Bot. 39:1143−1146.
  27. Ogawa, J., Kishino, S., Ando, A., Sugimoto, S., Mihara, K. and Shimizu, S. 2005. Production of conjugated fatty acids by lactic acid bacteria. J. Biosci. Bioeng. 100:355−364.
  28. Ongena, M., Jourdan, E., Schafer, M., Kech, C., Budzikiewicz, H., Luxen, A. and Thonart, P. 2005. Isolation of an N-alkylated benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Mol. Plant-Microbe Interact. 18:562−569.
  29. Park, M. R., Kim, Y. C., Park, J. Y., Han, S. H., Kim, K. Y., Lee, S. W. and Kim, I. S. 2008. Identification of an ISR-related metaboliteproduced by Pseudomonas chlororaphis O6 against wildfire pathogen Pseudomonas syringae pv. tabaci in tobacco. J. Microbiol. Biotechnol. 18:1659−1662.
  30. Park, M. R., Kim, Y. C., Lee, S. and Kim, I. S. 2009. Identification of an ISR-related metabolite produced by rhizobacterium Klebsiella oxytoca C1036 active against soft-rot disease pathogen in tobacco. Pest Manag. Sci. 65:1114−1117.
  31. Reitz, M., Rudolph, K., Schröder, I., Hoffmann-Hergarten, S., Hallmann, J. and Sikora R. A. 2000. Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl. Environ. Microbiol. 66:3515−3518.
  32. Rezania, S., Amirmozaffari, N., Bahman Tabarraei, B., Jeddi-Tehrani, M., Zarei, O., Alizadeh, R., Masjedian, F. and Amir Hassan Zarnani, A. H. 2011. Extraction, purification and characterization of lipopolysaccharide from Escherichia coli and Salmonella typhi. Avicenna J. Med. Biotech. 3:3−9.
  33. Rohilla, R., Singh, U.S. and Singh, R. L. 2002. Mode of action of acibenzolar-S-methyl against sheath blight of rice, caused by Rhizoctonia solani Kühn. Pest. Manag. Sci. 58:63−69.
  34. Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W. and Pare, P. W. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017−1026.
  35. Ryu, C. M., Kim, J., Choi, O., Park, S. Y., Park, S. H. and Park, C. S. 2005. Nature of a root-associated Paenibacillys polymyxa from field-grown winter barley in Korea. J. Microbiol. Biotechnol. 15:984−991.
  36. Sarwar, M. and Franckenberger, W. T. Jr. 1995. Fate of lphenylalanine in soil and its effect on plant growth. Soil Sci. Soc. Amer. J. 59:1625−1630.
  37. Siddiquee, S. Cheond, B. E., Taslima, K. Kausar, H. and Hasan M. M. 2012. Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. J. Chromatogr. Sci. 50:358−367.
  38. Slininger, P. J., Burkhead, K. D. and Schisler, D. A. 2004. Antifungal and sprout regulatory bioactivities of phenylacetic acid, indole-3-acetic acid, and tyrosol isolated from the potato dry rot suppressive bacterium Enterobacter cloacae S11:T:07. J. Ind. Microbiol. Biotechnol. 31:517−524.
  39. Somers, E., Ptacek, D. Gysegom, P., Srinivasan, M. and Vanderleyden, J. 2005. Azospirillum brasilense produces the auxinlike phenylacetic acid by using the key enzyme for indole-3-acetic acid biosynthesis. Appl. Environ. Microbiol. 71:1803−1810.
  40. Taguchi, F., Shimizu, R., Nakajima, R., Toyoda, K., Shiraishi, T. and Ichinose, Y. 2003. Differential effects of flagellins from Pseudomonas syringae pv. tabaci, tomato and glycinea on plant defense response. Plant Physiol. Biochem. 41:165−174.
  41. Tosi, L. and Zazzerini, A. 2000. Interactions between Plasmopara helianthi, Glomus mosseae and two plant activators in sunower plants. Eur. J. Plant Pathol. 106:735−744.
  42. van Loon, L. C., Bakker, P. A. H. M. and Pieterse, C. M. J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453−483.
  43. van Peer, R. and Schippers, B. 1992. Lipopolysaccharides of plant growth promoting Pseudomonas spp. strain WCS417r induce resistance in carnation to Fusarium wilt. Neth. J. Pl. Path. 98: 129−139.
  44. van Peer, R., Niemann, G. J. and Schippers, B. 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728−34.
  45. Walters, D., Raynor, L., Mitchell, A., Walker, R. and Walker, K. 2004. Antifungal activities of four fatty acids against plant pathogenic fungi. Mycopathologia 157:87−90.
  46. Wei, G., Kloepper, J. W. and Tuzun, S. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth promoting rhizobacteria. Phytopathology 81:1508−1512.
  47. Whatley, M. H., Hunter, N., Cantrell, M. A., Hendrick, C. A., Keegstra, K. and Sequeira, L. 1980. Lipopolysaccharide composition of the wilt pathogen, Pseudomonas solanacearum: correlation with hypersensitive response in tobacco. Plant Physiol. 65:557−559.
  48. Zakaria, N. A., Ibrahim, D., Fariza Shaida, S. F. and Afifah Supardy, N. A. 2011. Phytochemical composition and antibacterial potential of hexane extract from Malaysian red algae, Acanthophora spicifera (Vahl) Borgesen. World Appl. Sci. J. 15: 496−501.
  49. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D. G., Felix, G. and Boller, T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764−767.

Cited by

  1. Microbial Community Dynamics and Response to Plant Growth-Promoting Microorganisms in the Rhizosphere of Four Common Food Crops Cultivated in Hydroponics vol.73, pp.2, 2017, https://doi.org/10.1007/s00248-016-0855-0
  2. Searching ISR determinant/s from Bacillus subtilis IAGS174 against Fusarium wilt of tomato vol.60, pp.2, 2015, https://doi.org/10.1007/s10526-014-9636-1
  3. Phenylacetic Acid Is ISR Determinant Produced by Bacillus fortis IAGS162, Which Involves Extensive Re-modulation in Metabolomics of Tomato to Protect against Fusarium Wilt vol.7, 2016, https://doi.org/10.3389/fpls.2016.00498
  4. Identification of a Potential ISR Determinant from Pseudomonas aeruginosa PM12 against Fusarium Wilt in Tomato vol.8, 2017, https://doi.org/10.3389/fpls.2017.00848
  5. The bacterial community in the rhizosphere of Kimchi cabbage restructured by volatile compounds emitted from rhizobacterium Proteus vulgaris JBLS202 vol.105, 2016, https://doi.org/10.1016/j.apsoil.2016.03.020
  6. Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy vol.12, pp.6, 2017, https://doi.org/10.1371/journal.pone.0179957
  7. Diterpenoid phytoalexin factor, a bHLH transcription factor, plays a central role in the biosynthesis of diterpenoid phytoalexins in rice vol.84, pp.6, 2015, https://doi.org/10.1111/tpj.13065
  8. Linoleic acid-induced expression of defense genes and enzymes in tobacco vol.171, pp.18, 2014, https://doi.org/10.1016/j.jplph.2014.08.015
  9. pp.0031-949X, 2018, https://doi.org/10.1094/PHYTO-04-18-0118-R
  10. Exogenous application of phenylacetic acid promotes root hair growth and induces the systemic resistance of tobacco against bacterial soft-rot pathogen Pectobacterium carotovorum subsp. carotovorum vol.45, pp.11, 2018, https://doi.org/10.1071/FP17332
  11. Modulation of plant chemistry by beneficial root microbiota vol.35, pp.5, 2018, https://doi.org/10.1039/C7NP00057J
  12. Ochrobactrum quorumnocens sp. nov., a quorum quenching bacterium from the potato rhizosphere, and comparative genome analysis with related type strains vol.14, pp.1, 2019, https://doi.org/10.1371/journal.pone.0210874