Meta-analysis Reveals That the Genus Pseudomonas Can Be a Better Choice of Biological Control Agent against Bacterial Wilt Disease Caused by Ralstonia solanacearum

Chandrasekaran, Murugesan;Subramanian, Dharaneedharan;Yoon, Ee;Kwon, Taehoon;Chun, Se-Chul

  • Received : 2015.11.02
  • Accepted : 2016.02.02
  • Published : 2016.06.01


Biological control agents (BCAs) from different microbial taxa are increasingly used to control bacterial wilt caused by Ralstonia solanacearum. However, a quantitative research synthesis has not been conducted on the role of BCAs in disease suppression. Therefore, the present study aimed to meta-analyze the impacts of BCAs on both Ralstonia wilt disease suppression and plant (host) growth promotion. The analysis showed that the extent of disease suppression by BCAs varied widely among studies, with effect size (log response ratio) ranging from -2.84 to 2.13. The disease incidence and severity were significantly decreased on average by 53.7% and 49.3%, respectively. BCAs inoculation also significantly increased fresh and dry weight by 34.4% and 36.1%, respectively on average. Also, BCAs inoculation significantly increased plant yield by 66%. Mean effect sizes for genus Pseudomonas sp. as BCAs were higher than for genus Bacillus spp. Among antagonists tested, P. fluorescens, P. putida, B. cereus, B. subtilis and B. amyloliquefaciens were found to be more effective in general for disease reduction. Across studies, highest disease control was found for P. fluorescens, annual plants, co-inoculation with more than one BCA, soil drench and greenhouse condition were found to be essential in understanding plant responses to R. solanacearum. Our results suggest that more efforts should be devoted to harnessing the potential beneficial effects of these antagonists, not just for plant growth promoting traits but also in mode of applications, BCAs formulations and their field studies should be considered in the future for R. solanacearum wilt disease suppression.


biological control;biomass;crop yield;meta-analysis;Ralstonia solanacearum


  1. Vanitha, S. C., Niranjana, S. R., Mortensen, C. N. and Umesha, S. 2009. Bacterial wilt of tomato in Karnataka and its management by Pseudomonas fluorescens. BioControl 54:685-695.
  2. Wei, Z., Yang, X. M., Yin, S. X., Shen, Q. R., Ran, W. and Xu, Y. C. 2011. Efficacy of Bacillus-fortified organic fertilizer in controlling bacterial wilt of tomato in the field. Appl. Soil Ecol. 48:152-159.
  3. Yadeta, K. A. and J. Thomma, B. P. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci. 4:97.
  4. Yuan, S., Wang, L., Wu, K., Shi, J., Wang, M., Yang, X., Shen, Q. and Shen, B. 2014. Evaluation of Bacillus-fortified organic fertilizer for controlling tobacco bacterial wilt in greenhouse and field experiments. Appl. Soil Ecol. 75:86-94.
  5. Zhou, T. T., Li, C. Y., Chen, D., Wu, K., Shen, Q. R. and Shen, B. 2014. phlF- mutant of Pseudomonas fluorescens J2 improved 2,4-DAPG biosynthesis and biocontrol efficacy against tomato bacterial wilt. Biol. Control 78:1-8.
  6. Rosenberg, N. J., Adams, D. C. and Gurevitch, J. 2000. Metawin: statistical software for meta-analysis version 2.0. Sinauer, Sunderland, MA, USA. 128 pp.
  7. Salam, K. P., Thomas, G. J., Beard, C., Loughman, R., MacLeod, W. J. and Salam, M. U. 2013. Application of metaanalysis in plant pathology: a case study examining the impact of fungicides on wheat yield loss from the yellow spot-septoria nodorum blotch disease complex in Western Australia. Food Sec. 5:319-325.
  8. Sarkar, S. and Chaudhuri, S. 2013. Evaluation of the biocontrol potential of Bacillus subtilis, Pseudomonas aeruginosa and Trichoderma viride against bacterial wilt of tomato. Asian J. Biol. Life Sci. 2:146-151.
  9. Seleim, M. A., Saead, F. A., Abd-Alal Moneem, K. M. H. and Abo-Elyousr, K. A. 2011. Biological control of bacterial wilt of tomato by plant growth promoting rhizobacteria. Plant Pathol. J. 10:146-153.
  10. Shan, H., Zhao, M., Chen, D., Cheng, J., Li, J., Feng, Z., Ma, Z. and An, D. 2013. Biocontrol of rice blast by the phenaminomethylacetic acid producer of Bacillus methylotrophicus strain BC79. Crop Prot. 44:29-37.
  11. Singh, N. and Siddiqui, Z. A. 2015. Effects of Bacillus subtilis, Pseudomonas fluorescens and Aspergillus awamori on the wilt-leaf spot disease complex of tomato. Phytoparasitica 43:61-75.
  12. Stiling, P. and Cornelissen, T. 2005. What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol. Control 34:236-246.
  13. Takenaka, S., Sekiguchi, H., Nakaho, K., Tojo, M., Masunaka, A. and Takahashi, H. 2008. Colonization of Pythium oligandrum in the tomato rhizosphere for biological control of bacterial wilt disease analyzed by real-time PCR and confocal laser-scanning microscopy. Phytopathology 98:187-195.
  14. Ojiambo, P. S., Paul, P. A. and Holmes, G. J. 2010. A quantitative review of fungicide efficacy for managing downy mildew in cucurbits. Phytopathology 100:1066-1076.
  15. Ojiambo, P. S. and Scherm, H. 2006. Biological and application-oriented factors influencing plant disease suppression by biological control: a meta-analytical review. Phytopathology 96:1168-1174.
  16. Paul, P. A., Madden, L. V., Bradley, C. A., Robertson, A. E., Munkvold, G. P., Shaner, G., Wise, K. A., Malvick, D. K., Allen, T. W., Grybauskas, A., Vincelli, P. and Esker, P. 2011. Meta-analysis of yield response of hybrid field corn to foliar fungicides in the U.S. Corn Belt. Phytopathology 101:1122-1132.
  17. Paulitz, T. C. and Belanger, R. R. 2001. Biological control in greenhouse systems. Annu. Rev. Phytopathol. 39:103-133.
  18. Peeters, N., Guidot, A., Vailleau, F. and Valls, M. 2013. Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol. Plant Pathol. 14:651-662.
  19. Raaijmakers, J. M., de Bruijn, I. and de Kock, M. J. 2006. Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol. Plant-Microbe Interact. 19:699-710.
  20. Ramesh, R. and Phadke, G. S. 2012. Rhizosphere and endophytic bacteria for the suppression of eggplant wilt caused by Ralstonia solanacearum. Crop Prot. 37:35-41.
  21. Rosenberg, M. S. 2005. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59:464-468.
  22. Rosenberg, M. S., Garrett, K. A., Su, Z. and Bowden, R. L. 2004. Meta-analysis in plant pathology: synthesizing research results. Phytopathology 94:1013-1017.
  23. Lehmann, A., Veresoglou, S. D., Leifheit, E. F. and Rillig, M. C. 2014. Arbuscular mycorrhizal influence on zinc nutrition in crop plants: a meta-analysis. Soil Biol. Biochem. 69:123-131.
  24. Liu, B., Qiao, H., Huang, L., Buchenauer, H., Han, Q., Kang, Z. and Gong, Y. 2009. Biological control of take-all in wheat by endophytic Bacillus subtilis E1R-j and potential mode of action. Biol. Control 49:277-285.
  25. Lugtenberg, B. J. J., Dekkers, L. and Bloemberg, G. V. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39:461-490.
  26. Maji, S. and Chakrabartty, P. K. 2014. Biocontrol of bacterial wilt of tomato caused by Ralstonia solanacearum by isolates of plant growth promoting rhizobacteria. Aust. J. Crop Sci. 8:208-214.
  27. Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S. V., Machado, M. A., Toth, I., Salmond, G. and Foster, G. D. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614-629.
  28. Nelson, M. E., Gent, D. H. and Grove, G. G. 2015. Metaanalysis reveals a critical period for management of powdery mildew on hop cones. Plant Dis. 99:632-640.
  29. Ngugi, H. K., Esker, P. D. and Scherm, H. 2011. Meta-analysis to determine the effects of plant disease management measures:review and case studies on soybean and apple. Phytopathology 101:31-41.
  30. Lehmann, A. and Rillig, M. C. 2015. Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops: a meta-analysis. Soil Biol. Biochem. 81:147-158.
  31. Abo-Elyousr, K. A. M., Ibrahim, Y. E. and Balabel, N. M. 2012. Induction of disease defensive enzymes in response to treatment with acibenzolar-S-methyl (ASM) and Pseudomonas fluorescens Pf2 and inoculation with Ralstonia solanacearum race 3, biovar 2 (phylotype II). J. Phytopathol. 160:382-389.
  32. Almoneafy, A. A., Kakar, K. U., Nawaz, Z., Li, B., Ali saand, M., Chun-lan, Y. and Xie, G.-L. 2014. Tomato plant growth promotion and anti-bacterial related mechanisms of four rhizobacterial Bacillus strains against Ralstonia solacearum. Symbiosis 63:59-70.
  33. Belanger, R. R. and Benyagoub, M. 1997. Challenges and prospects for integrated control of powdery mildews in the greenhouse. Can. J. Plant Pathol. 19:310-314.
  34. Chandrasekaran, M., Sonia, B., Hu, S., Oh, S.-H. and Sa, T. 2014. A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza 24:611-625.
  35. Chen, D., Liu, X., Li, C., Tian, W., Shen, Q. and Shen, B. 2014. Isolation of Bacillus amyloliquefaciens S20 and its application in control of eggplant bacterial wilt. J. Environ. Manage. 137:120-127.
  36. Coll, N. S. and Valls, M. 2013. Current knowledge on the Ralstonia solanacearum type III secretion system. Microb. Biotechnol. 6:614-620.
  37. Cook, R. J. 1993. Making greater use of introduced microorganisms for biological control of plant pathogens. Annu. Rev. Phytopathol. 31:53-80.
  38. Cooper, H. 1998. Synthesizing research: a guide for literature reviews. 3rd ed. Sage Publications, Thousand Oaks, CA, USA. 216 pp.
  39. Copas, J. and Shi, J. Q. 2000. Meta-analysis, funnel plots and sensitivity analysis. Biostatistics 1:247-262.
  40. Dalla Lana, F., Ziegelmann, P. K., de H. N. Maia, A., Godoy, C. V. and Del Ponte, E. M. 2015. Meta-analysis of the relationship between crop yield and soybean rust severity. Phytopathology 105:307-315.
  41. Dey, R., Pal, K. K. and Tilak, K. V. B. R. 2014. Plant growth promoting rhizobacteria in crop protection and challenges. In: Future challenges in crop protection against fungal pathogens, fungal biology, eds. by A. Goyal and C. Manoharachary, pp. 31-58. Springer, New York, NY, USA.
  42. Figueiredo, M. V. B., Seldin, L., Araujo, F. F. and Mariano, R. L. R. 2010. Plant growth promoting rhizobacteria: fundamentals and applications. In: Plant growth and health promoting bacteria. Microbiology monographs 18, ed. by D. K. Maheshwari, pp. 21-43. Springer, Berlin, Germany.
  43. Guo, J.-H., Qi, H.-Y., Guo, Y.-H., Ge, H.-L., Gong, L.-Y., Zhang, L.-X. and Sun, P.-H. 2004. Biocontrol of tomato wilt by plant growth promoting rhizobacteria. Biol. Control 29:66-72.
  44. Gurevitch, J. and Hedges, L. V. 1999. Statistical issues in ecological meta-analysis. Ecology 80:1142-1149.[1142:SIIEMA]2.0.CO;2
  45. Hayward, A. C. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65-87.
  46. Huang, C., Sun, Z., Wang, H., Luo, Y. and Ma, Z. 2012. Effects of wheat cultivar mixtures on stripe rust: a meta-analysis of field trials. Crop Prot. 33:52-58.
  47. Huet, G. 2014. Breeding for resistances to Ralstonia solanacearum. Front. Plant Sci. 5:715.
  48. Ji, X., Lu, G., Gai, Y., Zheng, C. and Mu, Z. 2008. Biological control against bacterial wilt and colonization of mulberry by an endophytic Bacillus subtilis strain. FEMS Microbiol. Ecol. 65:565-573.
  49. Kiaer, L. P., Skovgaard, I. M. and Ostergard, H. 2009. Grain yield increase in cereal variety mixtures: a meta-analysis of field trials. Field Crops Res. 114:361-373.
  50. Koricheva, J. and Gurevitch, J. 2014. Uses and misuses of metaanalysis in plant ecology. J. Ecol. 102:828-844.
  51. Kurabachew, H. and Wydra, K. 2013. Characterization of plant growth promoting rhizobacteria and their potential as bioprotectant against tomato bacterial wilt caused by Ralstonia solancearum. Biol. Control 67:75-83.
  52. Lajeunesse, M. J. 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92:2049-2055.

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