DOI QR코드

DOI QR Code

Enhanced Biological Control of Phytophthora Blight of Pepper by Biosurfactant-Producing Pseudomonas

  • Ozyilmaz, Umit (Adnan Menderes University, Faculty of Agriculture, Plant Protection Dept.) ;
  • Benlioglu, Kemal (Adnan Menderes University, Faculty of Agriculture, Plant Protection Dept.)
  • Received : 2013.02.20
  • Accepted : 2013.05.20
  • Published : 2013.12.01

Abstract

Pseudomonas isolates from different crop plants were screened for in vitro growth inhibition of Phytophthora capsici and production of biosurfactant. Two in vivo experiments were performed to determine the efficacy of selected Pseudomonas strains against Phytophthora blight of pepper by comparing two fungicide treatments [acibenzolar-S-methyl (ASM) and ASM + mefenoxam]. Bacterial isolates were applied by soil drenching ($1{\times}10^9$ cells/ml), ASM ($0.1{\mu}g$ a.i./ml) and ASM + mefenoxam (0.2 mg product/ml) were applied by foliar spraying, and P. capsici inoculum was incorporated into the pot soil three days after treatments. In the first experiment, four Pseudomonas strains resulted in significant reduction from 48.4 to 61.3% in Phytophthora blight severity. In the second experiment, bacterial treatments combining with olive oil (5 mL per plant) significantly enhanced biological control activity, resulting in a reduction of disease level ranging from 56.8 to 81.1%. ASM + mefenoxam was the most effective treatment while ASM alone was less effective in both bioassays. These results indicate that our Pseudomonas fluorescens strains (6L10, 6ba6 and 3ss9) that have biosurfactant-producing abilities are effective against P. capsici on pepper, and enhanced disease suppression could be achieved when they were used in combination with olive oil.

Keywords

References

  1. Abouseoud, M., Maachi, R., Amrane, A., Boudergua, A. and Nabi, A. 2008. Evaluation of different carbon and nitrogen sources in production of biosurfactant by Pseudomonas fluorescens. Desalination 223:143-151. https://doi.org/10.1016/j.desal.2007.01.198
  2. Akgul, S. D. and Mirik, M. 2008. Biocontrol of Phytophthora capsici on pepper plants by Bacillus megaterium strains. J. Plant Pathol. 90:29-34.
  3. Alegbejo, M. D., Lawal, A. B. and Chindo, P. S. 2006. Outbreak of basal stem rot and wilt disease of pepper in Katsina, Nigeria. Arch. Phytopathol. PFL 39:93-98. https://doi.org/10.1080/03235400500180834
  4. Aravind, R., Kumar, A., Eapen, S. J. and Ramana, K. V. 2009. Endophytic bacterial ora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identication and evaluation against Phytophthora capsici. Lett. Appl. Microbiol. 48:58-64. https://doi.org/10.1111/j.1472-765X.2008.02486.x
  5. Bakker, A. W. and Schippers, B. 1987. Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp-mediated plant growth-stimulation. Soil Biol. Biochem. 19:451-457. https://doi.org/10.1016/0038-0717(87)90037-X
  6. Baris, M., Gulsoy, E., Guncu, M., Maden, S., Sagir, A., Senyurek, M., Ulukus, ., Yalcin, O. and Zengin, H. 1986. Investigations on the primary inoculum source and control measurements of the crown blight disease (Phytophthora capsici Leon.) of peppers. Plant Prot. Bull. 26:59-95 (in Turkish).
  7. Berg, G., Frankowski, J. and Bahl, H. 2000. Interactions between Serratia plymuthica and the soil borne pathogen Verticillium longisporum. In Advances in Verticillium Research and Disease Management, eds. by E. C. Tjamos, C. Rowe, J. B. Heale, D. R. Fravel, pp. 269-273. St Paul, MN, USA: American Phytopathological Society Press.
  8. Boz, O, Dogan, M. N. and Albay, F. 2003. Olive processing waste as a method of weed control. Weed Res. 43:439-443. https://doi.org/10.1046/j.0043-1737.2003.00360.x
  9. Castric, P. A. 1975. Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can. J. Microbiol. 21:613-618. https://doi.org/10.1139/m75-088
  10. Chae, D. H., Jin, R. D., Hwangbo, H., Kim, Y. W., Kim, Y. C., Park, R. D., Krishnan, H. B. and Kim, K. Y. 2006. Control of late blight (Phytophthora capsici) in pepper plant with a compost containing multitude of chitinase-producing bacteria. Biocontrol 51:339-351. https://doi.org/10.1007/s10526-005-2934-x
  11. Chung, S., Kong, H., Buyer, J. S., Lakshman, D. K., Lydon, J., Kim, S. D. and Roberts, D. 2008. Isolation and partial characterization of Bacillus subtilis ME488 for suppression of soilborne pathogen of cucumber and pepper. Appl. Microbiol Biot. 80:115-123. https://doi.org/10.1007/s00253-008-1520-4
  12. Cui, X. and Harling, R. 2006. Evaluation of bacterial antagonists for biological control of broccoli head rot caused by Pseudomonas fluorescens. Phytopathology 96:408-416. https://doi.org/10.1094/PHYTO-96-0408
  13. D'aes, J., De Maeyer, K., Pauwelyn, E. and Hofte, M. 2010. Biosurfactants in plant-Pseudomonas interactions and their importance to biocontrol. Environ. Microbiol. Rep. 2:359-372.
  14. Dai, X. Y. and Guan, G. L. 1999. Study on two strains of antagonistic bacteria producing antagonistic proteins to Phytophthora capsici. Chinese J. Biol. Control 15:81-84. https://doi.org/10.1006/bcon.1999.0702
  15. De Freitas, J. R., Banerjee, M. R. and Germida, J. J. 1997. Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol. Fert. Soils 24:358-364. https://doi.org/10.1007/s003740050258
  16. De Souza, J. T., Arnould, C., Deulvot, C., Lemanceau, P., Gianinazzi-Pearson, V. and Raaijmakers, J. M. 2003. Effect of 2,4-diacetylphloroglucinol on Pythium: Cellular responses and variation in sensitivity among propagules and species. Phytopathology 93:966-975. https://doi.org/10.1094/PHYTO.2003.93.8.966
  17. Dworkin, M. and Foster, J. W. 1958. Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 75:592-603.
  18. Ezziyyani, M., Perez, S. C., Requena, M. E., Sid, A. A. and Candela, M. E. 2004. Evaluacion del biocontrol de Phytophthora capsici en pimiento (Capsicum annuum L.) por tratamiento con Burkholderia cepacia. An. Biol. 26:61-68.
  19. Ezziyyani, M., Requena, M. E., Egea-Gilabert, C. and Candela, M. E. 2007. Biological control of Phytophthora root rot of pepper using Trichoderma harzianum and Streptomyces rochei in combination. J. Phytopathol. 155:342-349. https://doi.org/10.1111/j.1439-0434.2007.01237.x
  20. FAO, 2010. Statistical Databases (FAOSTAT). Food and Agriculture Organization of the United Nations. http://faostat3.fao.org/home/index.html (Accessed March 1, 2012).
  21. Foster, J. M. and Hausbeck, M. K. 2010. Managing phytophthora crown and root rot in bell pepper using fungicides and host resistance. Plant Dis. 94:697-702. https://doi.org/10.1094/PDIS-94-6-0697
  22. Gordon, S. A. and Weber, R. P. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol. 26:192-195. https://doi.org/10.1104/pp.26.1.192
  23. Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., Oostendorp, S., Staub, T., Ward, E., Kessmann, H. and Ryals, J. 1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629-643. https://doi.org/10.1105/tpc.8.4.629
  24. Guillen-Cruz, R., Hernandez-Castillo, F. D., Gallegos-Morales, G., Rodriguez-Herrera, R., Aguilar-Gonzalez, C. N., Padron-Corral, E. and Reyes-Valdes, M. H. 2006. Bacillus spp. como biocontrol en un suelo infestado con Fusarium spp., Rhizoctonia solani Kühn y Phytophthora capsici Leonina y su efecto en el desarrollo y rendimiento del cultivo de chile (Capsicum annuum L.). Rev. Mex. Fitopatol. 24:105-114.
  25. Haas, D. and Keel, C. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 4:117-153.
  26. Hausbeck, M. K. and Lamour, K. H. 2004. Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Dis. 88:1292-1303. https://doi.org/10.1094/PDIS.2004.88.12.1292
  27. Jiang, Z., Guo, Y., Li, S., Qi, H. and Guo, J. 2006. Evaluation of biocontrol efciency of different Bacillus preparations and eld application methods against Phytophthora blight of bell pepper. Biol. Control 36:216-223. https://doi.org/10.1016/j.biocontrol.2005.10.012
  28. Jung, H. K. and Kim, S. D. 2003. Purication and characteriztion of an antifungal antibiotic from Bacillus megaterium KL 39, a biocontrol agent of red-papper Phytophtora blight disease. Kor. J. Microbiol. Biotechnol. 31:235-241.
  29. Jung, H. K. and Kim, S. D. 2004. Selection and antagonistic mechanism of Pseudomonas uorescens 4059 against phytophthora blight disease. Kor. J. Microbiol. Biotechnol. 32:312-316.
  30. Jung, H. K. and Kim, S. D. 2005. An antifungal antibiotic puried from Bacillus megaterium KL39, a biocontrol agent of redpepper Phytophthora-blight disease. J. Microbiol. Biotechnol. 15:1001-1010.
  31. Kasana, R., C., Salwan, R., Dhar, H., Dutt, S. and Gulati, A. 2008. A rapid and easy method for the detection of microbial cellulases on agar plates using Gram's iodine, Curr. Microbiol. 57:503-507. https://doi.org/10.1007/s00284-008-9276-8
  32. Kim, B. S., Lee, J. Y. and Hwang, B. K. 2000. In vivo control and in vitro antifungal activity of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. Pest Manag. Sci. 56:1029-1035. https://doi.org/10.1002/1526-4998(200012)56:12<1029::AID-PS238>3.0.CO;2-Q
  33. Kim, S. G., Jang, Y., Kim, H. Y., Koh, Y. J. and Kim, Y. H. 2010. Comparison of microbial fungicides in antagonistic activities related to the biological control of phytophthora blight in chili pepper caused by Phytophthora capsici. Plant Pathol. J. 26:340−345. https://doi.org/10.5423/PPJ.2010.26.4.340
  34. Kim, Y. C., Jung, H., Kim, K. Y. and Park, S. K. 2008a. An effective biocontrol bioformulation against Phytophthora blight of pepper using growth mixtures of combined chitinolytic bacteria under different field conditions. Eur. J. Plant Pathol. 120:373-382. https://doi.org/10.1007/s10658-007-9227-4
  35. Kim, Y. S., Jang, B., Chung, I. M., Sang, M. K., Ku, H. M., Kim, K. D. and Chun, S. C. 2008b. Enhancement of biocontrol activity of antagonistic Chryseobacterium strain KJ1R5 by adding carbon sources against Phytophthora capsici. Plant Pathol. J. 24:164-170. https://doi.org/10.5423/PPJ.2008.24.2.164
  36. King, E. O., Ward, M. K. and Raney, D. E. 1954. Two simple media for the demonstration of pyocyanin and uorescin. J. Lab. Clin. Med. 44:301-307.
  37. Kloepper, J. W., Leong, J., Teintze, M. and Schroth, M. N. 1980. Pseudomonas siderophores: A mechanism explaining disease suppression in soils. Curr. Microbiol. 4:317-320. https://doi.org/10.1007/BF02602840
  38. Krechel, A., Faupel, A., Hallmann, J., Ulrich, A. and Berg, G. 2002. Potato associated bacteria and their antagonistic potantial towards plant-pathogenic fungi and the plant-parasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Can. J. Microbiol. 48:772-786. https://doi.org/10.1139/w02-071
  39. Kurze, S., Bahl, H., Dahl, R. and Berg, G. 2001. Biological control of fungal strawberry disease by Serratia plymuthica HRA-C48. Plant Dis. 85:529-534. https://doi.org/10.1094/PDIS.2001.85.5.529
  40. Lamour, K. H. and Hausbeck, M. K. 2001. The dynamics of mefenoxam insensitivity in a recombining population of Phytophthora capsici characterized with amplified fragment length polymorphism markers. Phytopathology 91:553-557. https://doi.org/10.1094/PHYTO.2001.91.6.553
  41. Lee, E. T., Lim, S. K., Nam, D. H., Khang, Y. H. and Kim, S. D. 2003a. Pyoverdin 2112 of Pseudomonas uorescens 2112 inhibits Phytophthora capsici, a red-pepper blight-causing fungus. J. Microbiol. Biotechnol. 13:415-421.
  42. Lee, J. Y. and Hwang, B. K. 2002. Diversity of antifungal actinomycetes in various vegetative soils of Korea. Can. J. Microbiol. 48:407-417. https://doi.org/10.1139/w02-025
  43. Lee, J. Y., Kim, B. S., Lim, S. W., Lee, B. K., Kim, C. H. and Hwang, B. K. 1999. Field control of phytophthora blight of pepper plants with antagonistic rhizobacteria and DL-$\beta$-aminon-butyric acid. Plant Pathol. J. 15:217-222.
  44. Lee, J. Y., Moon, S. S. and Hwang, B. K. 2003b. Isolation and antifungal and antiomycete activities of aerugine produced by Pseudomonas uorescens strain MM-B16. Appl. Environ. Microb. 69:2023-2031. https://doi.org/10.1128/AEM.69.4.2023-2031.2003
  45. Lee, J. Y., Moon, S. S. and Hwang, B. K. 2003c. Isolation and in vitro and in vivo activity against Phytophthora capsici and Volletoteichum orbiculare of phenazine-1-carboxylic acid from Pseudomonas aeruginosa strain GC-B26. Pest Manag. Sci. 59:872-882. https://doi.org/10.1002/ps.688
  46. Leeman, M., Denouden, E. M., van Pelt, J. A., Dirkx, F., Steijl, H., Bakker, P. and Schippers, B. 1996. Iron availability affects induction of systemic resistance to fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149-155. https://doi.org/10.1094/Phyto-86-149
  47. Ma, Y., Chang, Z., Zhao, J. and Zhou, M. 2008. Antifungal activity of Penicillium striatisporum Pst10 and its biocontrol effect on Phytophthora root rot of chilli pepper. Biol. Control 44:24-31. https://doi.org/10.1016/j.biocontrol.2007.10.005
  48. Matheron, M. E. and Porchas, M. 2000. Comparison of five fungicides on development of root, crown, and fruit rot of chile pepper and recovery of Phytophthora capsici from soil. Plant Dis. 84:1038-1043. https://doi.org/10.1094/PDIS.2000.84.9.1038
  49. Matheron, M. E. and Porchas, M. 2002. Suppression of Phytophthora root and crown rot on pepper plants treated with acibenzolar-S-methyl. Plant Dis. 86:292-297. https://doi.org/10.1094/PDIS.2002.86.3.292
  50. McSpadden Gardener, B. B., Mavrodi, D. V., Thomashow, L. S. and Weller, D. M. 2001. A rapid polymerase chain reactionbased assay characterizing rhizosphere populations of 2,4-diacetylphloroglucinolproducing bacteria. Phytopathology 91:44-54. https://doi.org/10.1094/PHYTO.2001.91.1.44
  51. Mercade, M. E. and Manresa, M. A. 1994. The use of agroindustrial by-products for biosurfactant production. J. Am. Oil Chem. Soc. 71:61-64. https://doi.org/10.1007/BF02541473
  52. Mercade, M. E., Manresa, M. A., Robert, M., Espuny, M. J., Andres, C. and Guinea, J. 1993. Olive oil mill effluent (OOME): new substrate for biosurfactant production. Bioresource Technol. 43:1-6. https://doi.org/10.1016/0960-8524(93)90074-L
  53. Nam, C. G., Jee, H. J. and Kim, C. H. 1988. Studies on biological control of Phytophthora blight of Red-pepper II. Enhancement of antagonistic activity by soil amendment with organic materials. Kor. J. Plant Pathol. 4:313-318.
  54. Nielsen, C. J., Ferrin, D. M. and Stanghellini, M. E. 2006. Efficacy of biosurfactants in the management of Phytophthora capsici on pepper in recirculating hydroponic systems. Can. J. Plant Pathol. 28:450-460. https://doi.org/10.1080/07060660609507319
  55. Okomoto, H., Sato, M., Sato, Z. and Isaka, M. 1998. Biological control of Phytopthora capsici by Serratia marcescence F-1-1 and analysis of biocontrol mechanisms using transposon insertion mutants. Ann. Phytopathol. Soc. Japan 64:287-293. https://doi.org/10.3186/jjphytopath.64.287
  56. Ölmez, F. 2006. Determination of The Effect of Organic Matter and Pumice Usage to Pepper Root and Crown Rot (Phytophthora capsici Leon). MsC Thesis, University of Cukurova, Adana, Turkey (in Turkish).
  57. Park, H. J., Lee, J. Y., Hwang, I. S., Yun, B. S., Kim, B. S. and Hwang, B. K. 2006. Isolation and antifungal and antioomycete activities of staurosporine from Streptomyces roseoavus strain LS-A24. J. Agr. Food Chem. 54:3041-3046. https://doi.org/10.1021/jf0532617
  58. Patten, C. L. and Glick, B. R. 2002. Role of Pseudomonas putida Indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol. 68:3795-3801. https://doi.org/10.1128/AEM.68.8.3795-3801.2002
  59. Qiu, S. X., He, H., Ruan, H. C., Guan, X. and Hu, F. P. 2004. Biological control of pepper Phytophthora blight by endophytic TB2 (Bacillus sp.). Acta Phytopathol. Sin. 34:173-179.
  60. Robles-Yerena, L., Rodriguez-Villarreal, R. A., Ortega-Amaro, M. A., Fraire-Velazquez, S., Simpson, J., Rodriguez-Guerra, R. and Jimenez-Bremont, J. F. 2010. Characterization of a new fungal antagonist of Phytophthora capsici. Sci. Hortic-Amsterdam 125:248-255. https://doi.org/10.1016/j.scienta.2010.03.016
  61. Sang, M. K., Chun, S. C. and Kim, K. D. 2008. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol. Control 46:424-433. https://doi.org/10.1016/j.biocontrol.2008.03.017
  62. Schwyn, B. and Neilands, J. B. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56. https://doi.org/10.1016/0003-2697(87)90612-9
  63. Shen, S. S., Choi, O. H., Park, S. H., Kim, C. G. and Park, C. S. 2005. Root colonizing and biocontrol competency of Serratia plymuthica A21-4 against Phytophthora blight of pepper. Plant Pathol. J. 21:64-67. https://doi.org/10.5423/PPJ.2005.21.1.064
  64. Sid, A., Ezziyyani, M., Egea-Gilabert, C. and Candela, M. E. 2003. Selecting bacterial strains for use in the biocontrol of diseases caused by Phytophthora capsici and Alternaria alternata in sweet pepper plants. Biol. Plant. 47:569-574.
  65. Siegmund, I. and Wagner, F. 1991. New method for detecting rhamnolipid excreted by Pseudomonas species during growth on mineral agar. Biotechnol. Tech. 5:265-268. https://doi.org/10.1007/BF02438660
  66. Silvar, C., Merino, F. and Diaz, J. 2006. Diversity of Phytophthora capsici in northwest Spain: Analysis of virulence, metalaxyl response, and molecular characterization. Plant Dis. 90:1135-1142. https://doi.org/10.1094/PD-90-1135
  67. Stanghellini, M. E. and Miller, R. M. 1997. Biosurfactants, their identity and potential efficacy in the biological control of zoosporic plant pathogens. Plant Dis. 81:4-12. https://doi.org/10.1094/PDIS.1997.81.1.4
  68. Van Loon, L. C., Bakker, P. A. H. M. and Pieterse, C. M. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483. https://doi.org/10.1146/annurev.phyto.36.1.453
  69. Zhang, S., White, T. L., Martinez, M. C., McInroy, J. A., Kloepper, J. W. and Klassen, W. 2010. Evaluation of plant growthpromoting rhizobacteria for control of Phytophthora blight on squash under greenhouse conditions. Biol. Control 53:129-135. https://doi.org/10.1016/j.biocontrol.2009.10.015

Cited by

  1. Identification of endophytic Bacillus mojavensis with highly specialized broad spectrum antibacterial activity vol.6, pp.2, 2016, https://doi.org/10.1007/s13205-016-0508-5
  2. Efficacy of indigenous Trichoderma harzianum in controlling Phytophthora leaf fall (Phytophthora palmivora) in Thai rubber trees vol.124, pp.1, 2017, https://doi.org/10.1007/s41348-016-0051-y
  3. Impact of a Recombinant Biocontrol Bacterium, Pseudomonas fluorescens pc78, on Microbial Community in Tomato Rhizosphere vol.32, pp.2, 2016, https://doi.org/10.5423/PPJ.OA.08.2015.0172
  4. Isolation and characterization of Bacillus altitudinis JSCX-1 as a new potential biocontrol agent against Phytophthora sojae in soybean [Glycine max (L.) Merr.] vol.416, pp.1-2, 2017, https://doi.org/10.1007/s11104-017-3195-z