Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Two Bacterial Entophytes Eliciting Both Plant Growth Promotion and Plant Defense on Pepper (Capsicum annuum L.)

  • Kang, Seung-Hoon (Laboratory of Microbial Genomics, Systems Microbiology Research Center, KRIBB) ;
  • Cho, Hyun-Soo (Laboratory of Microbial Genomics, Systems Microbiology Research Center, KRIBB) ;
  • Cheong, Hoon (Laboratory of Microbial Genomics, Systems Microbiology Research Center, KRIBB) ;
  • Ryu Choong-Min (Laboratory of Microbial Genomics, Systems Microbiology Research Center, KRIBB) ;
  • Kim, Ji-Hyun (Laboratory of Microbial Genomics, Systems Microbiology Research Center, KRIBB) ;
  • Park, Seung-Hwan (Laboratory of Microbial Genomics, Systems Microbiology Research Center, KRIBB)
  • Published : 2007.01.31
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Abstract

Plant growth-promoting rhizobacteria (PGPR) have the potential to be used as microbial inoculants to reduce disease incidence and severity and to increase crop yield. Some of the PGPR have been reported to be able to enter plant tissues and establish endophytic populations. Here, we demonstrated an approach to screen bacterial endophytes that have the capacity to promote the growth of pepper seedlings and protect pepper plants against a bacterial pathogen. Initially, out of 150 bacterial isolates collected from healthy stems of peppers cultivated in the Chungcheong and Gyeongsang provinces of Korea, 23 putative endophytic isolates that were considered to be predominating and representative of each pepper sample were selected. By phenotypic characterization and partial 16S rDNA sequence analysis, the isolates were identified as species of Ochrobacterium, Pantoea, Pseudomonas, Sphingomonas, Janthinobacterium, Ralstonia, Arthrobacter, Clavibacter, Sporosarcina, Acidovorax, and Brevundimonas. Among them, two isolates, PS4 and PS27, were selected because they showed consistent colonizing capacity in pepper stems at the levels of $10^6-10^7CFU/g$ tissue, and were found to be most closely related to Pseudomonas rhodesiae and Pantoea ananatis, respectively, by additional analyses of their entire 16S rDNA sequences. Drenching application of the two strains on the pepper seedlings promoted significant growth of peppers, enhancing their root fresh weight by 73.9% and 41.5%, respectively. The two strains also elicited induced systemic resistance of plants against Xanthomonas axonopodis pv. vesicatoria.

Keywords

References

  1. Bottini, R., F. Cassan, and P. Piccoli. 2004. Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 65: 497-503
  2. Cao, L., Z. Qiu, J. You, H. Tan, and S. Zhou. 2004. Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Lett. Appl. Microbiol. 39: 425-430 https://doi.org/10.1111/j.1472-765X.2004.01606.x
  3. Chanway, C. P. 1997. Introduction of tree roots with plant growth promoting soil bacteria: An emerging technology for reforestation. Forest Sci. 43: 99-112
  4. Cheong, H., S.-Y. Park, C.-M. Ryu, J. F. Kim, S.-H. Park, and C. S. Park. 2005. Diversity of root-associated Paenibacillus spp. in winter crops from the southern part of Korea. J. Microbiol. Biotechnol. 15: 1286-1298
  5. Chung, E., C.-M. Ryu, S.-K. Oh, R. N. Kim, J. M. Park, H. S. Cho, S. Lee, J. S. Moon, S.-H. Park, and D. Choi. 2006. Suppression of pepper SGT1 and SKP1 causes severe retardation of plant growth and compromises basal resistance. Physiol. Plant. 126: 605-617
  6. Compant, S., B. J. Nowak, C. Clement, and E. Ait Barka. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: Principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71: 4951-4959 https://doi.org/10.1128/AEM.71.9.4951-4959.2005
  7. Compant, S., B. B. Reiter, A. Sessitsch, J. Nowak, C. Clement, and E. Ait Barka. 2005. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl. Environ. Microbiol. 71: 1685-1693 https://doi.org/10.1128/AEM.71.4.1685-1693.2005
  8. Dickie, G. A. and C. R. Bell. 1995. A full factorial analysis of nine factors influencing in vitro antagonistic screens for potential biocontrol agents. Can. J. Microbiol. 41: 284- 293 https://doi.org/10.1139/m95-039
  9. Downing, K. J., G. Leslie, and J. A. Thomson. 2000. Biocontrol of the sugarcane borer Eldana saccharina by expression of the Bacillus thuringiensis cry1Ac7 and Serratia marcescens chiA genes in sugarcane-associated bacteria. Appl. Environ. Microbiol. 66: 2804-2810 https://doi.org/10.1128/AEM.66.7.2804-2810.2000
  10. Emmert, E. A. and J. Handelsman. 1999. Biocontrol of plant disease: A (Gram-) positive perspective. FEMS Microbiol. Lett. 171: 1-9 https://doi.org/10.1111/j.1574-6968.1999.tb13405.x
  11. Garbeva, P., L. S. Overbeek, J. W. van Vuurde, and J. D. van Elsas. 2001. Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb. Ecol. 41: 369-383 https://doi.org/10.1007/s002480000096
  12. Glick, B. R. 1995. The enhancement of plant growth by freeliving bacteria. Can. J. Microbiol. 41: 109-117 https://doi.org/10.1139/m95-015
  13. Glick, B. R. 1999. Overview of plant growth-promoting bacteria, pp. 1-13. In B. R. Glick, C. L. Patten, G. Holguin, and D. M. Penrose (eds.), Biochemical and Genetic Mechanisms Used by Plant Growth Promoting Bacteria. Imperial College Press, London
  14. Halmann, J., A. Quadt-Hallmann, and J. W. Kloepper. 1997. Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43: 895-914 https://doi.org/10.1139/m97-131
  15. Hallmann, J., A. Quadt-Hallmann, W. G. Miller, R. A. Sikora, and S. E. Lindow. 2001. Endophytic colonization of plants by the biocontrol agent Rhizobium etli G12 in relation to Meloidogyne incognita infection. Phytopathology 91: 415- 422 https://doi.org/10.1094/PHYTO.2001.91.4.415
  16. Handelsman, J. and K. Stabb. 1996. Biocontrol of soil-borne plant pathogens. Plant Cell 8: 1855-1869 https://doi.org/10.1105/tpc.8.10.1855
  17. Heil, M. and I. Baldwin. 2002. Costs of induced resistance: Emerging experimental support for a slippery concept. Trend. Plant Sci. 7: 61-67 https://doi.org/10.1016/S1360-1385(01)02186-0
  18. Heil, M., A. Hilpert, W. Kaiser, and K. E. Linsenmair. 2000. Reduced growth and seed set following chemical induction of pathogen defence: Does systemic acquired resistance (SAR) incur allocation costs? J. Ecol. 88: 645-654 https://doi.org/10.1046/j.1365-2745.2000.00479.x
  19. Hwang, B. K. and C. H. Kim. 1995. Phytophthora blight of pepper and its control in Korea. Plant Dis. 79: 221-227 https://doi.org/10.1094/PD-79-0221
  20. James E. K. and F. L. Olivares. 1998. Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit. Rev. Plant Sci. 17: 77-119 https://doi.org/10.1016/S0735-2689(98)00357-8
  21. Jetiyanon, K. and J. W. Kloepper. 2002. Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol. Contr. 24: 285-291 https://doi.org/10.1016/S1049-9644(02)00022-1
  22. Kim, J. S., S. W. Kwon, F. Jordan, and J. C. Ryu. 2003. Analysis of bacterial community structure in bulk soil, rhizosphere soil, and root samples of hot pepper plants using FAME and 16S rDNA clone libraries. J. Microbiol. Biotechnol. 13: 236-242
  23. Kloepper, J. W. and M. N. Schroth. 1978. Plant growthpromoting rhizobacteria on radishes, pp. 879-882. In Station de pathologie vegetale et phyto-bacteriologie (ed.), Proceedings of the 4th International Conference on Plant Pathogenic Bacteria, vol. II. Gilbert-Clarey, Tours
  24. Kloepper, J. W. 1992. Plant growth-promoting rhizobacteria as biological control agents, pp. 255-274. In F. B. Metting Jr. (ed.), Soil Microbial Ecology: Applications in Agricultural and Environmental Management. Marcel Dekker Inc., N.Y
  25. Kloepper, J. W., S. Tuzun, and J. Kuc. 1992. Proposed definitions related to induced disease resistance. Biocontrol Sci. Technol. 2: 349-351 https://doi.org/10.1080/09583159209355251
  26. Kloepper, J. W., R. Rodriguez-Kabana, G. W. Zehnder, J. Murphy, E. Sikora, and C. Fernandez. 1999. Plant rootbacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Austral. J. Plant Pathol. 28: 27-33 https://doi.org/10.1071/AP99004
  27. Kloepper, J. W., C.-M. Ryu, and. S. Zhang. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94: 1259-1266 https://doi.org/10.1094/PHYTO.2004.94.11.1259
  28. Kloepper, J. W. and C.-M. Ryu. 2006. Bacterial endophytes as elicitors of induced systemic resistance, pp. 33-52. In B. Schulz, C. Boyle, and T. Sieber (eds.), Microbial Root Endophytes. Kluwer Inc
  29. Krechel, A., A. Faupel, J. Hallmann, A. Ulrich, and G. Berg. 2002. Potato-associated bacteria and their antagonistic potential towards plant-pathogenic fungi and the plantparasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Can. J. Microbiol. 48: 772-786 https://doi.org/10.1139/w02-071
  30. Kuklinsky-Sobral, J., W. L. Araujo, R. Mendes, O. I. Geraldi, A. A. Pizzirani-Kleiner, and J. L. Azevedo. 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 6: 1244-1251 https://doi.org/10.1111/j.1462-2920.2004.00658.x
  31. Lee, H. J., K. H. Park, J. H. Shim, R. D. Park, Y. W. Kim, J. Y. Cho, H. Hwangbo, Y. C. Kim, G. S. Cha, H. B. Krishnan, and K. Y. Kim. 2005. Quantitative changes of plant defense enzymes in biocontrol of pepper (Capsicium annuum L.) late blight by antagonistic Bacillus subtilis HJ927. J. Microbiol. Biotechnol. 15: 1073-1079
  32. Lucas Garcia, J. A., M. Schloter, T. Durkaya, A. Hartmann, and F. J. Gutierrez Manero. 2003. Colonization of pepper roots by a plant growth promoting Pseudomonas fluorescens strain. Biol. Fertil. Soils 6: 381-385
  33. Oh, S.-K., S. Lee, E. Chung, J. M. Park, S. H. Yu, C.-M. Ryu, and D. Choi. 2006. Insight into Types I and II nonhost resistance using expression patterns of defense-related genes in tobacco. Planta 223: 1101-1107 https://doi.org/10.1007/s00425-006-0232-1
  34. Pernezny, K. L., P. D. Roberts, J. F. Murphy, and N. P. Goldberg. 2003. Compendium of Pepper Diseases. 1st Ed. APS Press, St. Paul, MN, U.S.A
  35. Reiter, B., U. Pfeifer, H. Schwab, and A. Sessitsch. 2002. Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica. Appl. Environ. Microbiol. 68: 2261-2268 https://doi.org/10.1128/AEM.68.5.2261-2268.2002
  36. Ryu, C.-M., M. A. Farag, C.-H. Hu, M. S. Reddy, H. X. Wei, P. W. Pare, and J. W. Kloepper. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 4927-4932
  37. Ryu, C.-M., C.-H. Hu, M. S. Reddy, and J. W. Kloepper. 2003. Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytol. 160: 413-420 https://doi.org/10.1046/j.1469-8137.2003.00883.x
  38. Ryu, C.-M., M. Farag, C.-H. Hu, M. S. Reddy, P. Pare, and J. W. Kloepper. 2004. Bacterial volatiles induced systemic resistance in Arabidopsis. Plant Physiol. 134: 1017-1026 https://doi.org/10.1104/pp.103.026583
  39. Ryu, C.-M., J. Kim, O. Choi, S.-Y. Park, S.-H. Park, and C. S. Park. 2005. Nature of a root-associated Paenibacillus polymyxa from field-grown winter barley in Korea. J. Microbiol. Biotechnol. 12: 984-991
  40. Ryu, C.-M., J. Kim, O. Choi, S. H. Kim, and C. S. Park. 2006. Improvement of biological control capacity of Paenibacillus polymyxa E681 by seed pelleting on sesame. Biol. Control (in press)
  41. Ryu, C.-M., J. F. Murphy, K. S. Mysore, and J. W. Kloepper. 2004. 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. Plant J. 39: 381-392 https://doi.org/10.1111/j.1365-313X.2004.02142.x
  42. Sambrook, J. and D. W. Russel. 2001. Molecular Cloning: A Laboratory Manual, 3rd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A
  43. Sessitsch, A., B. Reiter, and G. Berg. 2004. Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can. J. Microbiol. 50: 239-249 https://doi.org/10.1139/w03-118
  44. Timmusk, S., B. Nicander, U. Granhall, and E. Tillberg. 1999. Cytokinin production by Paenibacillus polymyxa. Soil Biol. Biochem. 31: 1847-1852 https://doi.org/10.1016/S0038-0717(99)00113-3
  45. Van Loon, L. C., P. A. Bakker, and C. M. Pierterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopath. 36: 453-483 https://doi.org/10.1146/annurev.phyto.36.1.453
  46. Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26: 379-407 https://doi.org/10.1146/annurev.py.26.090188.002115
  47. Wei, G., J. W. Kloepper, and S. Tuzun. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81: 1508-1512 https://doi.org/10.1094/Phyto-81-1508
  48. Zheng, H. Z., Y. W. Kim, H. J. Lee, R. D. Park, W. J. Jung, Y. C. Kim, S. H. Lee, T. H. Kim, and K. Y. Kim. 2004. Quantitative changes of PR proteins and antioxidative enzymes in response to Glomus intraradices and Phytophthora capsici in pepper (Capsicum annuum L.) plants. J. Microbiol. Biotechnol. 14: 553-562
  49. Zinniel, D. K., P. Lambrecht, N. B. Harris, Z. Feng, D. Kuczmarski, P. Higley, C. A. Ishimaru, A. Arunakumari, R. G. Barletta, and A. K. Vidaver. 2002. Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl. Environ. Microbiol. 68: 2198-2208 https://doi.org/10.1128/AEM.68.5.2198-2208.2002