Biological Control of Rice Bakanae by an Endophytic Bacillus oryzicola YC7007

  • Received : 2015.10.13
  • Accepted : 2016.02.05
  • Published : 2016.06.01


In our previous study, we reported that a novel endophytic bacterium Bacillus oryzicola YC7007 has suppressed bacterial diseases of rice via induced systemic resistance and antibiotic production. This endophytic strain, B. oryzicola YC7007 was used as a biological control agent against bakanae disease of rice caused by Fusarium fujikuroi, and its mechanism of interaction with the pathogen and the rice was further elucidated. Root drenching with B. oryzicola YC7007 suspension reduced the disease severity of bakanae significantly when compared with the untreated controls. The treatments of B. oryzicola YC7007 suspension ($2.0{\times}10^7cfu/ml$) to the rice rhizosphere reduced bakanae severity by 46-78% in pots and nursery box tests containing autoclaved and non-autoclaved soils. Moreover, in the detached rice leaves bioassay, the development of necrotic lesion and mycelial expansion of F. fujikuroi were inhibited significantly by spraying the culture filtrate of B. oryzicola YC7007. Drenching of ethyl acetate extracts of the culture filtrate to the rhizosphere of rice seedlings also reduced the bakanae disease severity in the plant culture dish tests. With the root drenching of B. oryzicola YC7007 suspension, the accumulation of hydrogen peroxide was observed at an early stage of rice seedlings, and a hormonal defense was elicited with and without pathogen inoculation. Our results showed that the strain B. oryzicola YC7007 had a good biocontrol activity against the bakanae disease of rice by direct inhibition, and was also capable of inducing systemic resistance against the pathogen via primed induction of the jasmonic acid pathway.


Bacillus oryzicola;biocontrol;induced systemic resistance;rice bakanae disease


  1. Ahn, I. P., Lee, S. W. and Suh, S. C. 2007. Rhizobacteriainduced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol. Plant-Microbe Interact. 20:759-768.
  2. Alqueres, S., Meneses, C., Rouws, L., Rothballer, M., Baldani, I., Schmid, M. and Hartmann, A. 2013. The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol. Plant-Microbe Interact. 26:937-945.
  3. Amatulli, M. T., Spadaro, D., Gullino, M. L. and Garibaldi, A. 2010. Molecular identification of Fusarium spp. associated with bakanae disease of rice in Italy and assessment of their pathogenicity. Plant Pathol. 59:839-844.
  4. Aslam, Z., Yasir, M., Yoon, H. S., Jeon, C. O. and Chung, Y. R. 2013. Diversity of the bacterial community in the rice rhizosphere managed under conventional and no-tillage practices. J. Microbiol. 51:747-756.
  5. Bais, H. P., Fall, R. and Vivanco, J. M. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134:307-319.
  6. Berg, G., Mahnert, A. and Moissl-Eichinger, C. 2014. Beneficial effects of plant-associated microbes or indoor microbiomes and human health? Front. Microbiol. 5:15.
  7. Bonman, J. M. 1992. Root and crown disease, bakanae. In: Compendium of rice diseases, eds. by R. K. Webster and P. S. Gunnell, pp. 27. APS Press, St. Paul, MN, USA.
  8. Bordiec, S., Paquis, S., Lacroix, H., Dhondt, S., Ait Barka, E., Kauffmann, S., Jeandet, P., Mazeyrat-Gourbeyre, F., Clement, C., Baillieul, F. and Dorey, S. 2011. Comparative analysis of defence responses induced by the endophytic plant growthpromoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J. Exp. Bot. 62:595-603.
  9. Carter, L. L., Leslie, J. F. and Webster, R. K. 2008. Population structure of Fusarium fujikuroi from California rice and water grass. Phytopathology 98:992-998.
  10. Castella, G., Bragulat, M. R., Rubiales, M. V. and Cabanes, F. J. 1997. Malachite green agar, a new selective medium for Fusarium spp. Mycopathologia 137:173-178.
  11. Chung, E. J., Hossain, M. T., Khan, A., Kim, K. H., Jeon, C. O. and Chung, Y. R. 2015. Bacillus oryzicola sp. nov., an endophytic bacterium isolated from the root of rice with antimicrobial, plant-growth promoting and systemic resistanceinducing activities in rice. Plant Pathol. J. 31:152-164.
  12. Coutinho, B. G., Licastro, D., Mendonca-Previato, L., Camara, M. and Venturi, V. 2015. Plant-influenced gene expression in the rice endophyte Burkholderia kururiensis M130. Mol. Plant-Microbe Interact. 28:10-21.
  13. Crane, J. M., Gibson, D. M., Vaughan, R. H. and Bergstrom, G. C. 2013. Iturin levels on wheat spikes linked to biological control of Fusarium head blight by Bacillus amyloliquefaciens. Phytopathology 103:146-155.
  14. De Vleesschauwer, D., Djavaheri, M., Bakker, P. A. and Hofte, M. 2008. Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acidrepressible multifaceted defense response. Plant Physiol. 148:1996-2012.
  15. De Vleesschauwer, D., Van Buyten, E., Satoh, K., Balidion, J., Mauleon, R., Choi, I. R., Vera-Cruz, C., Kikuchi, S. and Hofte, M. 2012. Brassinosteroids antagonize gibberellinand salicylate-mediated root immunity in rice. Plant Physiol. 158:1833-1846.
  16. De Vleesschauwer, D., Yang, Y., Cruz, C. V. and Hofte, M. 2010. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol. 152:2036-2052.
  17. Dimkic, I., Zivkovic, S., Beric, T., Ivanovic, Z., Gavrilovic, V., Stankovic, S. and Fira, D. 2013. Characterization and evaluation of two Bacillus strains, SS-12.6 and SS-13.1, as potential agents for the control of phytopathogenic bacteria and fungi. Biol. Control 65:312-321.
  18. Fanata, W. I., Lee, K. H., Son, B. H., Yoo, J. Y., Harmoko, R., Ko, K. S., Ramasamy, N. K., Kim, K. H., Oh, D. B., Jung, H. S., Kim, J. Y., Lee, S. Y. and Lee, K. O. 2013. N-glycan maturation is crucial for cytokinin-mediated development and cellulose synthesis in Oryza sativa. Plant J. 73:966-979.
  19. Gnanamanickam, S. S. 2009. An overview of progress in biological control. In: Biological control of rice diseases:Progress in biological control Series, ed. by S. S. Gnanamanickam, pp. 43-51. Springer, Dordrecht, Netherlands.
  20. Goswami, R. S. and Kistler, H. C. 2004. Heading for disaster:Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5:515-525.
  21. Harrach, B. D., Baltruschat, H., Barna, B., Fodor, J. and Kogel, K. H. 2013. The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol. Plant-Microbe Interact. 26:599-605.
  22. Kazempour, M. N. and Elahinia, S. A. 2007. Biological control of Fusarium fujikuroi , the causal agent of bakanae disease by rice associated antagonistic bacteria. Bulg. J. Agric. Sci. 13:393-408.
  23. Kim, C. K. 1981. Ecological studies of bakanae disease of rice caused by Gibberella fujikuroi. Kor. J. Plant Prot. 20:146-150.
  24. McSpadden Gardener, B. B. 2004. Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94:1252-1258.
  25. McSpadden Gardener, B. B. 2010. Biocontrol of plant pathogens and plant growth promotion by Bacillus. In: Recent developments in management of plant diseases, eds. by U. Gisi, I. Chet and M. Lodovica Gullino, pp. 71-79. Springer, Dordrecht, Netherlands.
  26. Mendes, R., Kruijt, M., de Bruijn, I., Dekkers, E., van der Voort, M., Schneider, J. H., Piceno, Y. M., DeSantis, T. Z., Andersen, G. L., Bakker, P. A. and Raaijmakers, J. M. 2011. Deciphering the rhizosphere microbiome for diseasesuppressive bacteria. Science 332:1097-1100.
  27. Mew, T. W., Cottyn, B., Pamplona, R., Barrios, H., Xiangmin, L., Zhiyi, C., Fan, L., Nilpanit, N., Arunyanart, P., Kim, P. V. and Du, P. V. 2004. Applying rice seed-associated antagonistic bacteria to manage rice sheath blight in developing countries. Plant Dis. 88:557-564.
  28. Mew, T. W. and Gonzales, P. 2002. Seed-borne fungi causing stem, leaf sheath, and root diseases in rice. In: A handbook of rice seed-borne fungi, eds. by T. W. Mew and P. Gonzales, pp. 31-34. Science Publishers, Enfield, NH, USA; International Rice Research Institute, Makati, Philippines.
  29. Niu, D. D., Liu, H. X., Jiang, C. H., Wang, Y. P., Wang, Q. Y., Jin, H. L. and Guo, J. H. 2011. The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol. Plant-Microbe Interact. 24:533-542.
  30. Ongena, M., Henry, G. and Thonart, P. 2009. The roles of cyclic lipopeptides in the biocontrol activity of Bacillus subtilis. In: Recent developments in management of plant diseases, eds. by U. Gisi, I. Chet and M. Lodovica Gullino, pp. 59-69. Springer, Dordrecht, Netherlands.
  31. Ou, S. H. 1985. Bakanae disease and foot rot. In: Rice disease, 2nd ed., ed. by S. H. Ou, pp. 262-272. Commonwealth Micological Institue, Kew, England.
  32. Park, K. S., Paul, D. and Yeh, W. H. 2006. Bacillus vallismortis EXTN-1- mediated growth promotion and disease suppression in rice. Plant Pathol. J. 22:278-282.
  33. Park, W. S., Choi, H. W., Han, S. S., Shin, D., Shim, H. K., Jung, E. S., Lee, S. W., Lim, C. K. and Lee, Y. H. 2009. Control of bakanae disease of rice by seed soaking into the mixed solution of prochloraz and fludioxonil. Res. Plant Dis. 15:94-100.
  34. Paulitz, T. C. and Belanger, R. R. 2001. Biological control in greenhouse systems. Annu. Rev. Phytopathol. 39:103-133.
  35. Peng, X., Hu, Y., Tang, X., Zhou, P., Deng, X., Wang, H. and Guo, Z. 2012. Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236:1485-1498.
  36. Pieterse, C. M., Leon-Reyes, A., Van der Ent, S. and Van Wees, S. C. 2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308-316.
  37. Qin, X., Liu, J. H., Zhao, W. S., Chen, X. J., Guo, Z. J. and Peng, Y. L. 2013. Gibberellin 20-oxidase gene OsGA20ox3 regulates plant stature and disease development in rice. Mol. Plant-Microbe Interact. 26:227-239.
  38. Qiu, D., Xiao, J., Ding, X., Xiong, M., Cai, M., Cao, Y., Li, X., Xu, C. and Wang, S. 2007. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol. Plant-Microbe Interact. 20:492-499.
  39. Raaijmakers, J. M., De Bruijn, I., Nybroe, O. and Ongena, M. 2010. Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol. Rev. 34:1037-1062.
  40. Rahman, A., Uddin, W. and Wenner, N. G. 2015. Induced systemic resistance responses in perennial ryegrass against Magnaporthe oryzae elicited by semi-purified surfactin lipopeptides and live cells of Bacillus amyloliquefaciens. Mol. Plant Pathol. 16:546-558.
  41. Riemann, M., Haga, K., Shimizu, T., Okada, K., Ando, S., Mochizuki, S., Nishizawa, Y., Yamanouchi, U., Nick, P., Yano, M., Minami, E., Takano, M., Yamane, H. and Iino, M. 2013. Identification of rice Allene Oxide Cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant J. 74:226-238.
  42. Rosales, A. M. and Mew, T. W. 1997. Suppression of Fusarium moniliforme in rice by rice-associated antagonistic bacteria. Plant Dis. 81:49-52.
  43. Rosales, A. M., Nuque, F. L. and Mew, T. W. 1986. Biological control of bakanae diseases of rice with antagonistic bacteria. Phil. Phytopath. 22:29-35.
  44. Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W. and Pare, P. W. 2004a. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017-1026.
  45. Ryu, C. M., Murphy, J. F., Mysore, K. S. and 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 aciddependent signaling pathway. Plant J. 39:381-392.
  46. Sanchez, L., Courteaux, B., Hubert, J., Kauffmann, S., Renault, J. H., Clement, C., Baillieul, F. and Dorey, S. 2012. Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiol. 160:1630-1641.
  47. Sang, M. K. and Kim, K. D. 2011. Biocontrol activity and primed systemic resistance by compost water extracts against anthracnoses of pepper and cucumber. Phytopathology 101:732-740.
  48. Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., Minami, E., Okada, K., Yamane, H., Kaku, H. and Shibuya, N. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64:204-214.
  49. Singh, P. P., Shin, Y. C., Park, C. S. and Chung, Y. R. 1999. Biological control of fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89:92-99.
  50. Sung, K. C. and Chung, Y. R. 1997. Enhanced suppression of rice sheath blight using combination of bacteria which produce chitinases or antibiotics. In: Plant growth promoting Rhizobacteria: present status and future prospects, eds. by A. Ogoshi, K. Kobayashi, Y. Homma, F. Kodama, N. Konodo and S. Akino, pp. 370-373. OECD, Paris, France.
  51. Ton, J., Pieterse, C. M. and Van Loon, L. C. 1999. Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 12:911-918.
  52. Tung, L. D. and Serrano, E. P. 2011. Effects of warm water in breaking dormancy for rice seed. Omonrice 18:129-136.
  53. Vallad, G. E. and Goodman, R. M. 2004. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci. 44:1920-1934.
  54. van de Mortel, J. E., de Vos, R. C., Dekkers, E., Pineda, A., Guillod, L., Bouwmeester, K., van Loon, J. J., Dicke, M. and Raaijmakers, J. M. 2012. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160:2173-2188.
  55. van Loon, L. C., Rep, M. and Pieterse, C. M. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-162.
  56. Walters, D. and Heil, M. 2007. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 71:3-17.
  57. Walters, D., Walsh, D., Newton, A. and Lyon, G. 2005. Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95:1368-1373.
  58. Weller, D. M., Mavrodi, D. V., van Pelt, J. A., Pieterse, C. M., van Loon, L. C. and Bakker, P. A. 2012. Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403-412.
  59. Xie, X., Zhang, H. and Pare, P. 2009. Sustained growth promotion in Arabidopsis with long term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal. Behav. 4:948-953.
  60. Yang, Y. R., Kim, Y. C., Lee, S. W., Lee, S. W., An, G. G. and Kim, I. S. 2012. Involvement of an efflux transporter in prochloraz resistance of Fusarium fujikuroi CF245 causing rice bakanae disease. J. Kor. Soc. Appl. Biol. Chem. 55:571-574.
  61. Zachow, C., Jahanshah, G., de Bruijn, I., Song, C., Ianni, F., Pataj, Z., Gerhardt, H., Pianet, I., Lammerhofer, M., Berg, G., Gross, H. and Raaijmakers, J. M. 2015. The novel lipopeptide poaeamide of the endophyte Pseudomonas poae re*1-1-14 is involved in pathogen suppression and root colonization. Mol. Plant-Microbe Interact. 28:800-810.
  62. Zhang, X., Wang, C., Zhang, Y., Sun, Y. and Mou, Z. 2012. The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24:4294-4309.
  63. Zhiyi, C., Zhigang, X., Taidong, G., Shoukun, N., Dafu, Y., Fan, L. and Yongfeng, L. 2001. Biological control of rice diseases. In: Seed health and seed-associated microorganisms for rice disease management: limited Proceedings No. 6 series, eds. by T. W. Mew and B. Cottyn, pp. 61-64. International Rice Research Institute, Los Banos, Philippines.

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Grant : Development of the long-lasting and broad-spectrum plant protectants

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