Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Induction of Defense Response Against Rhizoctonia solani in Cucumber Plants by Endophytic Bacterium Bacillus thuringiensis GS1

  • Seo, Dong-Jun (Division of Applied Bioscience and Biotechnology, Institute of Environmentally-Friendly Agriculture (IEFA), Chonnam National University) ;
  • Nguyen, Dang-Minh-Chanh (Division of Applied Bioscience and Biotechnology, Institute of Environmentally-Friendly Agriculture (IEFA), Chonnam National University) ;
  • Song, Yong-Su (Division of Applied Bioscience and Biotechnology, Institute of Environmentally-Friendly Agriculture (IEFA), Chonnam National University) ;
  • Jung, Woo-Jin (Division of Applied Bioscience and Biotechnology, Institute of Environmentally-Friendly Agriculture (IEFA), Chonnam National University)
  • Received : 2011.07.13
  • Accepted : 2011.11.01
  • Published : 2012.03.28
Download PDF
⟨ Previous Next ⟩

Abstract

An endophytic bacterium, Bacillus thuringiensis GS1, was isolated from bracken (Pteridium aquilinum) and found to have maximal production of chitinase (4.3 units/ml) at 5 days after culture. This study investigated the ability of B. thuringiensis GS1 to induce resistance to Rhizoctonia solani KACC 40111 (RS) in cucumber plants. Chitinase activity was greatest in RS-treated plants at 4 days. ${\beta}$-1,3-Glucanase activity was highest in GS1-treated plants at 5 days. Guaiacol peroxidase (GPOD) activity increased continuously in all treated plants for 5 days. Ascorbate peroxidase (APX) activity in RS-treated plants was increased 1.5-fold compared with the control at 4 days. Polyphenol oxidase (PPO) activity in RS-treated plants was increased 1.5-fold compared with the control at 3 days. At 5 days after treatment, activity staining revealed three bands with chitinase activity (Ch1, Ch2, and Ch3) on SDS-PAGE of cucumber plants treated with GS1+RS, whereas only one band was observed for RS-treated plants (Ch2). One GPOD isozyme (Gp1) was also observed in response to treatment with RS and GS1+RS at 4 days. One APX band (Ap2) was present on the native-PAGE gel of the control, and GS1- and GS1+RS-treated plants at 1 day. PPO bands (Po1 and Po2) from RS- and GS1+RS-treated plants were stronger than in the control and GS1-treated plants upon native-PAGE at 5 days. Taken together, these results indicate that the induction of PR proteins and defense-related enzymes by B. thuringiensis GS1 might have suppressed the damping-off caused by R. solani KACC 40111 in cucumber plants.

Keywords

References

  1. Arakane, Y. and D. Koga. 1999. Purification and characterization of a novel chitinase isozyme from yam tuber. Biosci. Biotechnol. Biochem. 63: 1895-1901. https://doi.org/10.1271/bbb.63.1895
  2. Asaka, O. and M. Shoda. 1996. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilus RB14. Appl. Environ. Microbiol. 62: 397-404.
  3. Baker, K. F. and R. J. Cook. 1974. Biological Control of Plant Pathogens. American Phytopathological Society, St. Paul, MN.
  4. Bakker, P. A. H. M., C. M. J. Pieterse, and L. C. Van Loon. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97: 239-243. https://doi.org/10.1094/PHYTO-97-2-0239
  5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitiation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  6. Brewer, M. T. and R. P. Larkin. 2005. Efficacy of several potential biocontrol organisms against Rhizoctonia solani on potato. Crop Prot. 24: 939-950. https://doi.org/10.1016/j.cropro.2005.01.012
  7. Brurberg, M. B., I. F. Nes, and V. G. H. Eijsink. 1996. Comparative studies of chitinase A and B from Serratia marcescens. Microbiology 142: 1581-1589. https://doi.org/10.1099/13500872-142-7-1581
  8. Caruso, C., G. Chilosi, C. Caporale, L. Leonardi, L. Bertini, P. Margo, and V. Buonocore. 1999. Induction of pathogenesis-related proteins in germinating wheat seeds infected with Fusarium culmorum. Plant Sci. 140: 107-120.
  9. Chen, G. and K. Asada. 1989. Ascorbate peroxidase in tea leaves: Occurrence of two isozymes and the difference in their enzymatic and molecular properties. Plant Cell Physiol. 30: 987-998.
  10. Chittor, J. M., J. E. Leach, and F. F. White. 1999. Induction of peroxidase during defense against pathogens. In: Pathogenesisrelated Proteins in Plants. CRC Press, Boca Raton, FL.
  11. Cordero, M. J., D. Raventos, and B. San Segundo. 1992. Induction of PR-proteins in germinating maize seeds infected with the fungus Fusarium moniliforme. Physiol. Mol. Plant Pathol. 41: 189-200. https://doi.org/10.1016/0885-5765(92)90010-S
  12. De Vleesschauwer, D., P. Cornelis, and M. Hofte. 2006. Redoxactive pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Mol. Plant Microbe Interact. 19: 1406-1419. https://doi.org/10.1094/MPMI-19-1406
  13. Driss, F., M. Kallassy-Award, N. Zouari, and S. Jaoua. 2005. Molecular characterization of a novel chitinase from Bacillus thuringiensis subsp. kurstaki. J. Appl. Microbiol. 99: 945-953. https://doi.org/10.1111/j.1365-2672.2005.02639.x
  14. Duzhak, A. B., Z. I. Panfilova, T. G. Duzhak, and E. A. Vasyunina. 2009. Extracellular chitinase of mutant superproducing strain Serratia marcescens M-1. Biochemistry 74: 257-263.
  15. Edreva, A. 2005. Pathogenesis-related proteins: Research progress in the last 15 years. Gen. Appl. Plant Physiol. 31: 105-124.
  16. Frank, J. A. and S. S. Leach. 1980. Comparison of tuberborne and soilborne inoculums in rhizoctonia disease of potato. Phytopathology 70: 51-53. https://doi.org/10.1094/Phyto-70-51
  17. Fu, J. and B. Huang. 2001. Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ. Exp. Bot. 45: 105-114. https://doi.org/10.1016/S0098-8472(00)00084-8
  18. Gayoso, C., F. Pomar, F. Merino, and M. A. Bernal. 2004. Oxidative metabolism and phenolic compounds in Capsicum annuum L. var. annuum infected by Phytophthora capsici Leon. Sci. Hort. 102: 1-13. https://doi.org/10.1016/j.scienta.2003.11.015
  19. Haran, S., H. Schickler, A. Oppenheim, and I. Chet. 1995. New components of the chitinolytic system of Trichoderma harzianum. Mycol. Res. 99: 441-446. https://doi.org/10.1016/S0953-7562(09)80642-4
  20. Jeger, M. J., G. A. Hide, P. H. J. F. Van Den Boogert, A. J. Termorshuizen, and P. Van Baarlen. 1996. Pathology and control of soil-borne fungal pathogens of potato. Potato Res. 39: 437-469. https://doi.org/10.1007/BF02357949
  21. Jung, W. J., K. N. An, Y. L. Jin, R. D. Park, K. T. Lim, K. Y. Kim, and T. H. Kim. 2003. Biological control of damping-off caused by Rhizoctonia solani using chitinase-producing Paenibacillus illinoisensis KJA-424. Soil Biol. Biochem. 35: 1261-1264. https://doi.org/10.1016/S0038-0717(03)00187-1
  22. Jung, W. J., Y. L. Jin, Y. C. Kim, K. Y. Kim, R. D. Park, and T. H. Kim. 2004. Inoculation of Paenibacillus illinoisensis alleviates root mortality, activates of lignifications-related enzymes, and induction of the isozymes in pepper plants infected by Phytophthora capsici. Biol. Control 30: 645-652. https://doi.org/10.1016/j.biocontrol.2004.03.006
  23. Jung, W. J., F. Mabood, T. H. Kim, and D. Smith. 2007. Induction of pathogenesis-related proteins during biocontrol of Rhizoctonia solani with Pseudomonas aureofaciens in soybean (Glycine max L. Merr.) plants. Biocontrol 52: 895-904. https://doi.org/10.1007/s10526-007-9089-x
  24. Jung, W. J., R. D. Park, F. Mabood, A. Souleimanov, and D. Smith. 2011. Effects of Pseudomonas aureofaciens 63-28 on defense responses in soybean plants infected by Rhizoctonia solani. J. Microbiol. Biotechnol. 21: 379-386
  25. Kavino, M., S. Harish, N. Kumar, T. Saravanakumar Damodaran, K. Soorianathasundaram, and R. Samiyappan. 2007. Rhizosphere and endophytic bacteria for induction of systemic resistance of banana plantlets against bunchy top virus. Soil Biol. Biochem. 39: 1087-1098. https://doi.org/10.1016/j.soilbio.2006.11.020
  26. Koga, D., Y. Sasaki, Y. Uchiumi, N. Hiral, Y. Arakane, and Y. Nagamatsu. 1997. Purification and characterization of Bombyx mori chitinases. Insect Biochem. Mol. Biol. 27: 757-767. https://doi.org/10.1016/S0965-1748(97)00058-1
  27. Kolattukudy, P. E., R. Mohan, M. A. Bajar, and B. A. Sherf. 1992. Plant peroxidase gene expression and function. Biochem. Soc. Trans. 20: 333-337.
  28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-683. https://doi.org/10.1038/227680a0
  29. Liu, M., Q. X. Cai, H. Z. Liu, B. H. Zhang, J. P. Yan, and Z. M. Yuan. 2002. Chitinolytic activity in Bacillus thuringiensis and their synergistic effects on larvicidal activity. J. Appl. Microbiol. 58: 840-849.
  30. Lingappa, Y. and J. L. Lockwood. 1962. Chitin media for selective isolation and culture of Actinomycetes. Phytopathology 52: 317-323.
  31. Lumsden, R. D. and G. C. Papavizas. 1988. Biological control of soilborne plant pathogens. Am. J. Alter. Agric. 3: 98-101. https://doi.org/10.1017/S0889189300002253
  32. Magnin-Robert, M., P. Trotel-Aziz, D. Quantinet, and S. Biagianti. 2007. Biological control of Botrytis cinerea by selected grapevine-associated bacteria and stimulation of chitinase and ${\beta}$-1,3-glucanase activities under field conditions. Eur. J. Plant Pathol. 118: 43-57. https://doi.org/10.1007/s10658-007-9111-2
  33. Mohammadi, M. and H. Kazemi. 2002. Change in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci. 162: 491-498. https://doi.org/10.1016/S0168-9452(01)00538-6
  34. Monreal, J. and E. T. Reese. 1969. The chitinase of Serratia marcescens. Can. J. Microbiol. 15: 689-696. https://doi.org/10.1139/m69-122
  35. Nguyen, V. N., Y. J. Kim, K. T. Oh, W. J. Jung, and R. D. Park. 2008. Antifungal activity of chitinases from Trichoderma aureoviride DY-59 and Rhizopus microsporus VS-9. Curr. Microbiol. 56: 28-32. https://doi.org/10.1007/s00284-007-9033-4
  36. Ohya, T., Y. Morimura, H. Saji, T. Mihara, and T. Ikawa. 1997. Purification and characterization of ascorbate peroxidase in roots of Japanese radish. Plant Sci. 125: 137-145. https://doi.org/10.1016/S0168-9452(97)00063-0
  37. Pan, S. Q., X. S. Ye, and J. Kue. 1989. Direct detection of ${\beta}$-1,3-glucanase isozymes on polyacrylamide electrophoresis and isoelectrofocusing gels. Anal. Biochem. 182: 136-140. https://doi.org/10.1016/0003-2697(89)90730-6
  38. Paranidharan, V., A. Palaniswami, P. Vidhyasekaran, and R. Velazhahan. 2003. Induction of enzymatic scavengers of active oxygen species in rice in response to infection by Rhizoctonia solani. Acta Physiol. Plant. 25: 91-96. https://doi.org/10.1007/s11738-003-0041-0
  39. Parry, D. W. 1990. Diseases of potato, pp. 276-280. In: Plant Pathology in Agriculture. Cambridge University Press, Cambridge.
  40. Patil, R. S., V. Ghormade, and M. V. Deshande. 2000. Chitinolytic enzymes: An exploration. Enzyme Microb. Technol. 26: 473-483. https://doi.org/10.1016/S0141-0229(00)00134-4
  41. Peumans, W. J., P. Proost, R. J. Swennen, and C. J. Van Dame. 2002. The abundant class III chitinase homolog in young developing banana fruits behaves as a transient vegetative storage protein and most probably serves as an important supply of amino acids for the synthesis of ripening-associated proteins. Plant Physiol. 130: 1063-1072. https://doi.org/10.1104/pp.006551
  42. Rao, D. H. and L. R. Gowda. 2008. Abundant class III acidic chitinase homologue in tamarind (Tamarindus indica) seed serves as the major storage protein. J. Agric. Food Chem. 56: 2175-2182. https://doi.org/10.1021/jf073183i
  43. Reyes-Ramirez, A., B. I. Escudero-Abarca, G. Aguilar-Uscanga, P. M. Hayward-Jones, and J. E. Barboza-Corona. 2004. Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J. Food Sci. 69: 131-134.
  44. Roby, D., K. Broglie, R. Cressman, P. Biddle, I. Chet, and R. Broglie. 1990. Activation of a bean chitinase promoter in transgenic tobacco plants by phytopathogenic fungi. Plant Cell 2: 999-1007.
  45. Santos, L. S., E. A. Olivera, M. D. Cunha, O. L. T. Machado, A. G. C. Neves-Ferreira, K. V. S. Fernandes, A. O. Carvalho, J. Perales, and V. M. Gomes. 2007. Expression of chitinase in Adenanthera pavonina seedlings. Physiol. Plant. 131: 80-88. https://doi.org/10.1111/j.1399-3054.2007.00945.x
  46. Senthilkumar, M., V. Govindasamy, and K. Annapurna. 2007. Role of antibiosis in suppression of charcoal rot disease by soybean endophyte Paenibacillus sp. HKA-15. Curr. Microbiol. 55: 25-29. https://doi.org/10.1007/s00284-006-0500-0
  47. Shigeoka, S., T. Ishikawa, M. Tamoi, Y. Miyagawa, T. Takeda, Y. Yabuta, and K. Yoshimura. 2002. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53: 1305-1319. https://doi.org/10.1093/jexbot/53.372.1305
  48. Shrestha, C. L., I. Ona, and S. Muthukridhnan. 2008. Chitinase levels in rice cultivars correlate with resistance to the sheath blight pathogen Rhizoctonia solani. Eur. J. Plant Pathol. 120: 69-77.
  49. Song, Y. S., D. J. Seo, B. R. Lee, and W. J. Jung. 2009. Expression patterns of enzymes in different tissues of oil seed rape (Brassica napus L.) seedling. J. Appl. Biol. Chem. 52: 51-57. https://doi.org/10.3839/jabc.2009.010
  50. Taira, T., T. Ohnuma, T. Yamagami, Y. Aso, M. Ishiguro, and M. Ishihara. 2001. Antifungal activity of rye (Secale cereale) seed chitinases: The different binding manner of class I and class II chitinases to the fungal cell walls. Biosci. Biotechnol. Biochem. 66: 970-977.
  51. Thamthiankul, S., S. Suan-Ngay, S. Tantimavanich, and W. Panbangred. 2001. Chitinase from Bacillus thuringiensis subsp. pakistani. Appl. Microbiol. Biotechnol. 56: 395-401. https://doi.org/10.1007/s002530100630
  52. Trudel, J. and A. Asselin. 1989. Detection of chitinase activity after polyacrylamide gel electrophoresis. Anal. Biochem. 178: 362-366. https://doi.org/10.1016/0003-2697(89)90653-2
  53. Van Loon, L. C., P. A. H. M. Baker, and C. M. J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36: 453-483. https://doi.org/10.1146/annurev.phyto.36.1.453
  54. Vinetz, J. M., S. K. Dave, C. A. Specht, K. A. Brameld, B. Xu, R. Hayward, and D. A. Fidock. 1999. The chitinase PfCHT1 from the human malaria parasite Plasmodium falciparum lacks proenzyme and chitin-binding domains and displays unique substrate preferences. Proc. Natl. Acad. Sci. USA 96: 14061-14066. https://doi.org/10.1073/pnas.96.24.14061
  55. Wakelin, A. M. and D. W. M. Leung. 2009. ${\beta}$-1,3-Glucanase activity in the stigma of healthy petunia flowers. Biol. Plant. 51: 69-74.
  56. Yedidia, I., N. Benhamou, Y. Kapulnik, and I. Chet. 2000. Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol. Biochem. 38: 863-873. https://doi.org/10.1016/S0981-9428(00)01198-0
  57. Yong, M. E. and P. A. Carroad. 1981. On continuous culture dilution rate. Can. J. Microbiol. 27: 142-144. https://doi.org/10.1139/m81-022
  58. Zouari, N. and S. Jaoua. 1999. Production and characterization of metalloproteases synthesized concomitantly with ${\delta}$-endotoxin by Bacillus thuringiensis subsp. kurstaki strain grown on gruelbased media. Enzyme Microb. Technol. 25: 364-371. https://doi.org/10.1016/S0141-0229(99)00054-X

Cited by

  1. Bacillus thuringiensis colonises plant roots in a phylogeny‐dependent manner vol.86, pp.3, 2013, https://doi.org/10.1111/1574-6941.12175
  2. Comparative tolerances of two Cucumis species to salinity, Rhizoctonia solani and Meloidogyne incognita vol.12, pp.2, 2014, https://doi.org/10.1017/s1479262113000452
  3. Characterisation of endophyticBacillus thuringiensisstrains isolated from wheat plants as biocontrol agents against wheat flag smut vol.24, pp.8, 2014, https://doi.org/10.1080/09583157.2014.904502
  4. Induced defense-related proteins in soybean (Glycine max L. Merrill) plants by Carnobacterium sp. SJ-5 upon challenge inoculation of Fusarium oxysporum vol.239, pp.5, 2012, https://doi.org/10.1007/s00425-014-2032-3
  5. Ecological interactions in the system: Entomopathogenic bacterium Bacillus thuringiensis-phytopathogenic fungus Rhizoctonia solani-host plant Solanum tuberosum vol.8, pp.4, 2015, https://doi.org/10.1134/s1995425515040034
  6. Biotechnological and Agronomic Potential of Endophytic Pink-Pigmented Methylotrophic Methylobacterium spp. vol.2015, pp.None, 2015, https://doi.org/10.1155/2015/909016
  7. Plant-endophyte symbiosis, an ecological perspective vol.99, pp.7, 2012, https://doi.org/10.1007/s00253-015-6487-3
  8. Chitinolytic Bacillus-Mediated Induction of Jasmonic Acid and Defense-Related Proteins in Soybean (Glycine max L. Merrill) Plant Against Rhizoctonia solani and Fusarium oxysporum vol.36, pp.1, 2017, https://doi.org/10.1007/s00344-016-9630-1
  9. Plant growth promotion and suppression of Phytophthora drechsleri damping-off in cucumber by cellulase-producing Streptomyces vol.62, pp.6, 2012, https://doi.org/10.1007/s10526-017-9838-4
  10. Endophytic Bacteria as Effective Agents of New-Generation Biopesticides (Review) vol.54, pp.2, 2012, https://doi.org/10.1134/s0003683818020072
  11. Endophytic Bacteria as Effective Agents of New-Generation Biopesticides (Review) vol.54, pp.2, 2012, https://doi.org/10.1134/s0003683818020072
  12. Chitinases of Bacillus thuringiensis : Phylogeny, Modular Structure, and Applied Potentials vol.10, pp.None, 2012, https://doi.org/10.3389/fmicb.2019.03032
  13. Evaluation of biocontrol potential of Achromobacter xylosoxidans strain CTA8689 against common bean root rot vol.117, pp.None, 2012, https://doi.org/10.1016/j.pmpp.2021.101769