DOI QR코드

DOI QR Code

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 (Department of Bioresource and Food Science, College of Life and Environmental Science, Konkuk University) ;
  • Subramanian, Dharaneedharan (Department of Marine Biomedical Sciences, College of Ocean Sciences, Jeju National University) ;
  • Yoon, Ee (Department of Bioresource and Food Science, College of Life and Environmental Science, Konkuk University) ;
  • Kwon, Taehoon (Department of Bioresource and Food Science, College of Life and Environmental Science, Konkuk University) ;
  • Chun, Se-Chul (Department of Bioresource and Food Science, College of Life and Environmental Science, Konkuk University)
  • Received : 2015.11.02
  • Accepted : 2016.02.02
  • Published : 2016.06.01

Abstract

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.

Keywords

References

  1. 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. https://doi.org/10.1111/j.1439-0434.2012.01915.x
  2. 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. https://doi.org/10.1007/s13199-014-0288-9
  3. 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. https://doi.org/10.1080/07060669709500530
  4. 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. https://doi.org/10.1007/s00572-014-0582-7
  5. 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. https://doi.org/10.1016/j.jenvman.2014.01.043
  6. Coll, N. S. and Valls, M. 2013. Current knowledge on the Ralstonia solanacearum type III secretion system. Microb. Biotechnol. 6:614-620.
  7. Cook, R. J. 1993. Making greater use of introduced microorganisms for biological control of plant pathogens. Annu. Rev. Phytopathol. 31:53-80. https://doi.org/10.1146/annurev.py.31.090193.000413
  8. Cooper, H. 1998. Synthesizing research: a guide for literature reviews. 3rd ed. Sage Publications, Thousand Oaks, CA, USA. 216 pp.
  9. Copas, J. and Shi, J. Q. 2000. Meta-analysis, funnel plots and sensitivity analysis. Biostatistics 1:247-262. https://doi.org/10.1093/biostatistics/1.3.247
  10. 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. https://doi.org/10.1094/PHYTO-06-14-0157-R
  11. 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.
  12. 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.
  13. 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. https://doi.org/10.1016/S1049-9644(03)00124-5
  14. Gurevitch, J. and Hedges, L. V. 1999. Statistical issues in ecological meta-analysis. Ecology 80:1142-1149. https://doi.org/10.1890/0012-9658(1999)080[1142:SIIEMA]2.0.CO;2
  15. Hayward, A. C. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65-87. https://doi.org/10.1146/annurev.py.29.090191.000433
  16. 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. https://doi.org/10.1016/j.cropro.2011.11.020
  17. Huet, G. 2014. Breeding for resistances to Ralstonia solanacearum. Front. Plant Sci. 5:715.
  18. 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. https://doi.org/10.1111/j.1574-6941.2008.00543.x
  19. 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. https://doi.org/10.1016/j.fcr.2009.09.006
  20. Koricheva, J. and Gurevitch, J. 2014. Uses and misuses of metaanalysis in plant ecology. J. Ecol. 102:828-844. https://doi.org/10.1111/1365-2745.12224
  21. 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. https://doi.org/10.1016/j.biocontrol.2013.07.004
  22. Lajeunesse, M. J. 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92:2049-2055. https://doi.org/10.1890/11-0423.1
  23. 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. https://doi.org/10.1016/j.soilbio.2014.11.013
  24. 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. https://doi.org/10.1016/j.soilbio.2013.11.001
  25. 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. https://doi.org/10.1016/j.biocontrol.2009.02.007
  26. Lugtenberg, B. J. J., Dekkers, L. and Bloemberg, G. V. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39:461-490. https://doi.org/10.1146/annurev.phyto.39.1.461
  27. 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.
  28. 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. https://doi.org/10.1111/j.1364-3703.2012.00804.x
  29. 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. https://doi.org/10.1094/PDIS-04-14-0396-RE
  30. 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. https://doi.org/10.1094/PHYTO-03-10-0068
  31. 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. https://doi.org/10.1094/PHYTO-12-09-0348
  32. 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. https://doi.org/10.1094/PHYTO-96-1168
  33. 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. https://doi.org/10.1094/PHYTO-03-11-0091
  34. Paulitz, T. C. and Belanger, R. R. 2001. Biological control in greenhouse systems. Annu. Rev. Phytopathol. 39:103-133. https://doi.org/10.1146/annurev.phyto.39.1.103
  35. 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. https://doi.org/10.1111/mpp.12038
  36. 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. https://doi.org/10.1094/MPMI-19-0699
  37. 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. https://doi.org/10.1016/j.cropro.2012.02.008
  38. 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. https://doi.org/10.1111/j.0014-3820.2005.tb01004.x
  39. 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. https://doi.org/10.1094/PHYTO.2004.94.9.1013
  40. 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.
  41. 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. https://doi.org/10.1007/s12571-013-0255-y
  42. 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.
  43. 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. https://doi.org/10.3923/ppj.2011.146.153
  44. 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. https://doi.org/10.1016/j.cropro.2012.10.012
  45. 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. https://doi.org/10.1007/s12600-014-0427-0
  46. 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. https://doi.org/10.1016/j.biocontrol.2005.02.017
  47. 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. https://doi.org/10.1094/PHYTO-98-2-0187
  48. 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. https://doi.org/10.1007/s10526-009-9217-x
  49. 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. https://doi.org/10.1016/j.apsoil.2011.03.013
  50. 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.
  51. 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. https://doi.org/10.1016/j.apsoil.2013.11.004
  52. 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. https://doi.org/10.1016/j.biocontrol.2014.07.006

Cited by

  1. Expression of β-1,3-glucanase (GLU) and phenylalanine ammonia-lyase (PAL) genes and their enzymes in tomato plants induced after treatment with Bacillus subtilis CBR05 against Xanthomonas campestris pv. vesicatoria vol.83, pp.1, 2017, https://doi.org/10.1007/s10327-016-0692-5
  2. Root-mediated signal transmission of systemic acquired resistance against above-ground and below-ground pathogens vol.118, pp.4, 2016, https://doi.org/10.1093/aob/mcw152
  3. Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum vol.6, pp.2296-701X, 2018, https://doi.org/10.3389/fevo.2018.00090