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Biological Control of Gom-chwi (Ligularia fischeri) Phytophthora Root Rot with Enterobacter asburiae ObRS-5 to Suppress Zoosporangia Formation and Zoospores Germination

  • Kim, Dayeon (Division of Agricultural Microbiology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Lee, Sang Yeob (Division of Agricultural Microbiology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Ahn, Seong Ho (Division of Agricultural Microbiology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Han, Ji Hee (Division of Agricultural Microbiology, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Park, Jin Woo (Division of Agricultural Microbiology, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2019.11.29
  • Accepted : 2020.04.28
  • Published : 2020.06.01

Abstract

Gom-chwi (Ligularia fischeri) is severely infected with Phytophthora drechsleri, the causal organism of Phytophthora root rot, an economically important crop disease that needs management throughout the cultivation period. In the present study, Phytophthora root rot was controlled by using bacterial isolates from rhizosphere soils collected from various plants and screened for antagonistic activity against P. drechsleri. A total of 172 bacterial strains were isolated, of which, 49 strains showed antagonistic activities by dual culture assay. In the seedling assay, six out of the 49 strains showed a predominant effect on suppressing P. drechsleri. Among the six strains, the ObRS-5 strain showed remarkable against P. drechsleri when treated with seed dipping or soil drenching. The ObRS-5 strain was identified as Enterobacter asburiae based on 16S ribosomal RNA gene sequences analysis. The bacterial cells of E. asburiae ObRS-5 significantly suppressed sporangium formation and zoospore germination in P. drechsleri by 87.4% and 66.7%, respectively. In addition, culture filtrate of E. asburiae ObRS-5 also significantly inhibited sporangium formation and zoospore germination by 97.0% and 67.6%, respectively. Soil drenched bacterial cells, filtrate, and culture solution of E. asburiae ObRS-5 effectively suppressed Phytophthora root rot by 63.2%, 57.9%, and 81.1%, respectively. Thus, E. asburiae ObRS-5 could be used as a potential agent for the biological control of Phytophthora root rot infecting gom-chwi.

Keywords

References

  1. Bae, S.-J., Mohanta, T. K., Chung, J. Y., Ryu, M., Park, G., Shim, S., Hong, S.-B., Seo, H., Bae, D.-W., Bae, I., Kim, J.-J. and Bae, H. 2016. Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biol. Control 92:128-138. https://doi.org/10.1016/j.biocontrol.2015.10.005
  2. Bakker, P. A. H. M., Ran, L. X., Pieterse, C. M. J. and van Loon, L. C. 2003. Understanding the involvement of rhizobacteriamediated induction of systemic resistance in biocontrol of plant diseases. Can. J. Plant Pathol. 25:5-9. https://doi.org/10.1080/07060660309507043
  3. Barash, I., Klisiewicz, J. M. and Kosuge, T. 1965. Utilization of carbon compounds by zoospores of Phytophthora drechsleri and their effect on motility and germination. Phytopathology 55:1257-1261.
  4. Berner, I., Konetschny-Rapp, S., Jung, G. and Winkelmann, G. 1988. Characterization of ferrioxamine E as the principal siderophore of Erwinia herbicola (Enterobacter agglomerans). Biol. Met. 1:51-56. https://doi.org/10.1007/BF01128017
  5. Bhardwaj, D., Ansari, M. W., Sahoo, R. K. and Tuteja, N. 2014. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb. Cell Fact. 13:66. https://doi.org/10.1186/1475-2859-13-66
  6. Biles, C. L., Bruton, B. D., Wall, M. M. and Rivas, M. 1995. Phytophthora capsici zoospore infection of pepper fruit in various physical environments. Proc. Okla. Acad. Sci. 75:1-5.
  7. Borriss, R. 2015. Bacillus, a plant-beneficial bacterium. In: Principles of plant-microbe interactions: microbes for sustainable agriculture, ed. by B. Lugtenberg, pp. 379-391. Springer, Cham, Switzerland.
  8. Chernin, L., Ismailov, Z., Haran, S. and Chet, I. 1995. Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl. Environ. Microbiol. 61:1720-1726. https://doi.org/10.1128/aem.61.5.1720-1726.1995
  9. Cho, S.-D. and Kim, G.-H. 2005. Food product development and quality characteristics of Ligularia fischeri for food resources. Korean J. Food Preserv. 12:43-47 (in Korean).
  10. Cother, E. J. and Griffin, D. M. 1973. The role of alternative hosts in survival of Phytophthora drechsleri. Aust. J. Biol. Sci. 26:1109-1113. https://doi.org/10.1071/bi9731109
  11. De Bruijn, I., de Kock, M. J. D., Yang, M., de Waard, P., van Beek, T. A. and Raaijmakers, J. M. 2007. Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol. Microbiol. 63:417-428. https://doi.org/10.1111/j.1365-2958.2006.05525.x
  12. De Cock, A. W. A. M. and Levesque, C. A. 2004. ew species of Pythium and Phytophthora. Stud. Mycol. 50:481-487.
  13. Doran, J. W. and Zeiss, M. R. 2000. Soil health and sustainability: managing the biotic component of soil quality. Appl. Soil Ecol. 15:3-11. https://doi.org/10.1016/S0929-1393(00)00067-6
  14. Elliott, M., Shamoun, S. F., Sumampong, G., James, D., Masri, S. and Varga, A. 2009. Evaluation of several commercial biocontrol products on European and North American populations of Phytophthora ramorum. Biocontrol Sci. Technol. 19:1007-1021. https://doi.org/10.1080/09583150903243870
  15. Erwin, D. C. and Ribeiro, O. K. 1996. Phytophthora diseases worldwide. American Phytopathological Society, St. Paul, MN, USA. 562 pp.
  16. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791. https://doi.org/10.2307/2408678
  17. Fravel, D. R. 2005. Commercialization and implementation of biocontrol. Annu. Rev. Phytopathol. 43:337-359. https://doi.org/10.1146/annurev.phyto.43.032904.092924
  18. Gupta, G., Parihar, S. S., Ahirwar, N. K., Snehi, S. K. and Singh, V. 2015. Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J. Microb. Biochem. Technol. 7:96-102.
  19. Haggag, W. M. and Timmusk, S. 2008. Colonization of peanut roots by biofilm-forming Paenibacillus polymyxa initiates biocontrol against crown rot disease. J. Appl. Microbiol. 104:961-969. https://doi.org/10.1111/j.1365-2672.2007.03611.x
  20. Idris, H. A., Labuschagne, N. and Korsten, L. 2007. Screening rhizobacteria for biological control of Fusarium root and crown rot of sorghum in Ethiopia. Biol. Control 40:97-106. https://doi.org/10.1016/j.biocontrol.2006.07.017
  21. Irabor, A. and Mmbaga, M. T. 2017. Evaluation of selected bacterial endophytes for biocontrol potential against phytophthora blight of bell pepper (Capsicum annuum L.). J. Plant Pathol. Microbiol. 8:424.
  22. Jetiyanon, K. 2015. Multiple mechanisms of Enterobacter asburiae strain RS83 for plant growth enhancement. Songklanakarin J. Sci. Technol. 37:29-36.
  23. Jetiyanon, K. and Plianbangchang, P. 2013. Lipopolysaccharide of Enterobacter asburiae strain RS83: a bacterial determinant for induction of early defensive enzymes in Lactuca sativa against soft rot disease. Biol. Control 67:301-307. https://doi.org/10.1016/j.biocontrol.2013.09.014
  24. Kim, D., Lee, S. Y., Ahn, S. H., Han, J. H. and Park, J. W. 2019. Biocontrol effect on Phytophthora root rot and changes in rhizosphere bacterial communities in Ligularia fischeri by Enterobacter asburiae ObRS-5. Korean J. Pestic. Sci. 23:348-357 (in Korean). https://doi.org/10.7585/kjps.2019.23.4.348
  25. Kim, J.-S., Kwon, S.-W., Lee, S.-J., Jung, B.-G., Song, J.-K., Go, S.-J. and Ryu, J.-C. 1999. Analysis of microbial community structure in soil and crop root system: I. Analysis of bacterial community structure in the soil and root system of red pepper and tomato. J. Korean Soc. Soil Sci. Fert. 32:319-325 (in Korean).
  26. Kim, Y., Choi, B., Kim, S., Moon, Y., Kim, K., Shin, D., Kim, D. and Hong, D. 2016. Investigation of the injury cause by the continuous cropping of Ligularia fischeri Turcz in Gangwon area. Korean J. Hortic. Sci. Technol. 34 Suppl. I:128.
  27. Kim, Y.-K., Hong, S.-J., Shim, C.-K., Kim, M.-J., Park, J.-H., Han, E.-J., Park, J.-W., Park, S.-H., Jee, H.-J. and Kim, S.-C. 2015. Effect of extract and bacteria from Korean fermented foods on the control of sesame seed-borne fungal disease. Res. Plant Dis. 21:297-308 (in Korean). https://doi.org/10.5423/RPD.2015.21.4.297
  28. Kloepper, J. W. and Schroth, M. N. 1981. Relationship of in vitro antibiosis of plant growth-promoting rhizobacteria to plant growth and the displacement of root microflora. Phytopathology 71:1020-1024. https://doi.org/10.1094/Phyto-71-1020
  29. Korean Society of Plant Pathology. 2009. List of plant diseases in Korea. 5th ed. The Korean Society of Plant Pathology, Suwon, Korea. 853 pp. (in Korean).
  30. Kwon, S. B., Jee, H. J., Bang, S. B., Lee, K. K. and Hong, C. K. 1999. Phytophthora root rot of Ligularia fishcheri caused by P. drechsleri. Plant Dis. Agric. 5:58-60 (in Korean).
  31. Lee, Y.-H., Jee, H.-J., Cha, K.-H., Ko, S.-J. and Park, K.-B. 2001. Occurrence of Phytophthora root rot on kiwifruit in Korea. Plant Pathol. J. 17:154-158.
  32. Liu, C., Sheng, J., Chen, L., Zheng, Y., Lee, D. Y., Yang, Y., Xu, M. and Shen, L. 2015. Biocontrol activity of Bacillus subtilis isolated from agaricus bisporus mushroom compost against pathogenic fungi. J. Agric. Food Chem. 63:6009-6018. https://doi.org/10.1021/acs.jafc.5b02218
  33. Macias-Rodriguez, L., Guzman-Gomez, A., Garcia-Juarez, P. and Contreras-Cornejo, H. A. 2018. Trichoderma atroviride promotes tomato development and alters the root exudation of carbohydrates, which stimulates fungal growth and the biocontrol of the phytopathogen Phytophthora cinnamomi in a tripartite interaction system. FEMS Microbiol. Ecol. 94:fiy137.
  34. Mahaffee, W. F. and Backman, P. A. 1993. Effects of seed factors on spermosphere and rhizosphere colonization of cotton by Bacillus subtilis GB03. Phytopathology 83:1120-1125. https://doi.org/10.1094/Phyto-83-1120
  35. Mahmood, A., Turgay, O. C., Farooq, M. and Hayat, R. 2016. Seed biopriming with plant growth promoting rhizobacteria: a review. FEMS Microbiol. Ecol. 92:fiw112. https://doi.org/10.1093/femsec/fiw112
  36. Mansoori, B. and Banihashemi, Z. 1982. Evaluating cucurbit seedling resistance to Phytophthora drechsleri. Plant Dis. 66:373-376. https://doi.org/10.1094/PD-66-373
  37. Maleki M., Mokhtarnejad, L. and Mostafaee, S. 2011. Screening of rhizobacteria for biological control of cucumber root and crown rot caused by Phytophthora drechsleri. Plant Pathol. J. 27:78-84. https://doi.org/10.5423/PPJ.2011.27.1.078
  38. Mehrotra, R. S. 1970. Techniques for demonstrating accumulation of zoospores of Phytophthora species on roots in soil. Can. J. Bot. 48:879-882. https://doi.org/10.1139/b70-122
  39. Meszka, B. and Michalecka, M. 2016.Identification of Phytophthora spp. isolated from plants and soil samples on strawberry plantations in Poland. J. Plant Dis. Prot. 123:29-36. https://doi.org/10.1007/s41348-016-0007-2
  40. Moon, Y.-G., Kim, S.-W., Choi, J.-K., Kwon, S.-B., Shim, H.-S., Ju, H.-J. and Choi, I.-Y. 2015. Stem rot on Ligularia fischeri caused by Sclerotium rolfsii in Korea. Res. Plant Dis. 21:36-39 (in Korean). https://doi.org/10.5423/RPD.2015.21.1.036
  41. Nam, K. U. 2001. Development of control measures and ecology against main plants disease in greenhouse. Prot. Hortic. 14:23-29 (in Korean).
  42. Nelson, E. B. 2018. The seed microbiome: origins, interactions, and impacts. Plant Soil. 422:7-34. https://doi.org/10.1007/s11104-017-3289-7
  43. Nelson, E. B., Chao, W.-L., Norton, J. M., Nash, G. T. and Harman, G. E. 1986. Attachment of Enterobacter cloacae to hyphae of Pythium ultimum: possible role in the biological control of Pythium preemergenee damping-off. Phytopatholgy 76:327-335. https://doi.org/10.1094/Phyto-76-327
  44. Pang, Y., Liu, X., Ma, Y., Chernin, L., Berg, G. and Gao, K. 2009. Induction of systemic resistance, root colonisation and biocontrol activities of the rhizospheric strain of Serratia plymuthica are dependent on N-acyl homoserine lactones. Eur. J. Plant Pathol. 124:261-268. https://doi.org/10.1007/s10658-008-9411-1
  45. Park, J.-W., Jahaggirdar, S., Cho, Y.-E., Park, K.-S., Lee, S.-H. and Park, K.-S. 2010. Evaluation of Bacillus subtilis native strains for plant growth promotion and induced systemic resistance in tomato and red-pepper. Korean J. Pestic. Sci. 14:407-414.
  46. Pascale, A., Proietti, S., Pantelides, I. S. and Stringlis, I. A. 2020. Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Front. Plant Sci. 10:1741. https://doi.org/10.3389/fpls.2019.01741
  47. Pieterse, C. M., van Wees, S. C., Hoffland, E., van Pelt, J. A. and van Loon, L. C. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225-1237. https://doi.org/10.1105/tpc.8.8.1225
  48. Pliego, C., Ramos, C., de Vicente, A. and Cazorla, F. M. 2011. Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant Soil. 340:505-520. https://doi.org/10.1007/s11104-010-0615-8
  49. Rural Development Administration. 2018. Assistant agricultural technology 60. Wild vegetable. 4th ed. Rural Development Administration, Jeonju, Korea. 441 pp. (in Korean).
  50. Rural Development Administration, Agricultural Sciences Institute. 1991. Compendium of medicinal plant diseases with colour plates. Rural Development Administration, Suwon, Korea. 210 pp. (in Korean).
  51. Rural Development Administration, National Institute of Agricultural Science and Technology, Plant Pathology Division. 2000. Phytophthora diseases in Korea. Rural Development Administration, Suwon, Korea. 226 pp. (in Korean).
  52. Ryan, R. P., Germaine, K., Franks, A., Ryan, D. J. and Dowling, D. N. 2008. Bacterial endophytes: recent developments and applications. FEMS Microbiol. Lett. 278:1-9. https://doi.org/10.1111/j.1574-6968.2007.00918.x
  53. Schroth, M. N. and Hancock, J. G. 1982. Disease-suppressive soil and root-colonizing bacteria. Science 216:1376-1381. https://doi.org/10.1126/science.216.4553.1376
  54. Shahidi Bonjar, G. H., Barkhordar, B., Pakgohar, N., Aghighi, S., Biglary, S., Rashid Farrokhi, P., Aminaii, M., Mahdavi, M. J. and Aghelizadeh, A. 2006. Biological control of Phytophthora drechsleri Tucker, the causal agent of pistachio gummosis, under greenhouse conditions by use of Actinomycetes. Plant Pathol. J. 5:20-23. https://doi.org/10.3923/ppj.2006.20.23
  55. Shirzad, A., Fallahzadeh-Mamaghani, V. and Pazhouhandeh, M. 2012. antagonistic potential of fluorescent Pseudomonads and control of crown and root rot of cucumber caused by Phythophtora drechsleri. Plant Pathol. J. 28:1-9. https://doi.org/10.5423/PPJ.OA.05.2011.0100
  56. Singh, U. P., Chauhan, V. B., Wagner, K. G. and Kumar, A. 1992. Effect of ajoene, a compound derived from garlic (Allium sativum), on Phytophthora drechsleri f. sp. Cajani. Mycologia 84:105-108. https://doi.org/10.2307/3760408
  57. Syed-Ab-Rahman, S. F., Carvalhais, L. C., Chua, E., Xiao, Y., Wass, T. J. and Schenk, P. M. 2018. Identification of soil bacterial isolates suppressing different Phytophthora spp. and promoting plant growth. Front. Plant Sci. 9:1052. https://doi.org/10.3389/fpls.2018.01052
  58. Szczech, M. and Shoda, M. 2006. The effect of mode of application of Bacillus subtilis RB14-C on its efficacy as a biocontrol agent against Rhizoctonia solani. J. Phytopathol. 154:370-377. https://doi.org/10.1111/j.1439-0434.2006.01107.x
  59. Tjamos, E. C., Tsitsigiannis, D. I., Tjamos, S. E., Antoniou, P. P. and Katinakis, P. 2004. Selection and screening of endorhizosphere bacteria from solarized soils as biocontrol agents against Verticillium dahliae of solanaceous hosts. Eur. J. Plant Pathol. 110:35-44. https://doi.org/10.1023/b:ejpp.0000010132.91241.cb
  60. Tsuda, K., Tsuji, G., Higashiyama, M., Ogiyama, H., Umemura, K., Mitomi, M., Kubo, Y. and Kosaka, Y. 2016. Biological control of bacterial soft rot in Chinese cabbage by Lactobacillus plantarum strain BY under field conditions. Biol. Control 100:63-69. https://doi.org/10.1016/j.biocontrol.2016.05.010
  61. Utkhede, R. S. 1986. Biology and control of apple crown rot caused by Phytophthora cactorum: a review. Phytoprotection 67:1-13.