The Plant Pathology Journal

한국식물병리학회 (The Korean Society of Plant Pathology)
권호 표지
DOI QR코드

DOI QR Code

Anti-Oomycete Activity and Pepper Root Colonization of Pseudomonas plecoglossicida YJR13 and Pseudomonas putida YJR92 against Phytophthora capsici

  • Elena, Volynchikova (Laboratory of Plant Disease and Biocontrol, Department of Plant Biotechnology, Korea University) ;
  • Ki Deok, Kim (Laboratory of Plant Disease and Biocontrol, Department of Plant Biotechnology, Korea University)
  • 투고 : 2023.01.03
  • 심사 : 2023.01.17
  • 발행 : 2023.02.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Previously, Pseudomonas plecoglossicida YJR13 and Pseudomonas putida YJR92 from a sequential screening procedure were proven to effectively control Phytophthora blight caused by Phytophthora capsici. In this study, we further investigated the anti-oomycete activities of these strains against mycelial growth, zoospore germination, and germ tube elongation of P. capsici. We also investigated root colonization ability of the bacterial strains in square dishes, including cell motility (swimming and swarming motilities) and biofilm formation. Both strains significantly inhibited mycelial growth in liquid and solid V8 juice media and M9 minimal media, zoospore germination, and germ tube elongation compared with Bacillus vallismortis EXTN-1 (positive biocontrol strain), Sphingomonas aquatilis KU408 (negative biocontrol strain), and MgSO4 solution (untreated control). In diluted (nutrient-deficient) V8 juice broth, the tested strain populations were maintained at >108 cells/ml, simultaneously providing mycelial inhibitory activity. Additionally, these strains colonized pepper roots at a 106 cells/ml concentration for 7 days. The root colonization of the strains was supported by strong swimming and swarming activities, biofilm formation, and chemotactic activity towards exudate components (amino acids, organic acids, and sugars) of pepper roots. Collectively, these results suggest that strains YJR13 and YJR92 can effectively suppress Phytophthora blight of pepper through direct anti-oomycete activities against mycelial growth, zoospore germination and germ tube elongation. Bacterial colonization of pepper roots may be mediated by cell motility and biofilm formation together with chemotaxis to root exudates.

키워드

과제정보

Elena Volynchikova was supported by the Korean Government Scholarship Program (KGSP) during her PhD study at the Korea University, Seoul, Korea.

참고문헌

  1. Alaux, P.-L., Cesar, V., Naveau, F., Cranenbrouck, S. and Declerck, S. 2018. Impact of Rhizophagus irregularis MUCL 41833 on disease symptoms caused by Phytophthora infestans in potato grown under field conditions. Crop Prot. 107:26-33. https://doi.org/10.1016/j.cropro.2018.01.003
  2. Aravind, R., Kumar, A., Eapen, S. J. and Ramana, K. V. 2009. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identification and evaluation against Phytophthora capsici. Lett. Appl. Microbiol. 48:58-64. https://doi.org/10.1111/j.1472-765X.2008.02486.x
  3. Arora, N. K., Kim, M. J., Kang, S. C. and Maheshwari, D. K. 2007. Role of chitinase and β-1,3-glucanase activities produced by a fluorescent pseudomonad and in vitro inhibition of Phytophthora capsici and Rhizoctonia solani. Can. J. Microbiol. 53:207-212. https://doi.org/10.1139/w06-119
  4. Barahona, E., Navazo, A., Martinez-Granero, F., Zea-Bonilla, T., Perez-Jimenez, R. M., Martin, M. and Rivilla, R. 2011. Pseudomonas fluorescens F113 mutant with enhanced competitive colonization ability and improved biocontrol activity against fungal root pathogens. Appl. Environ. Microbiol. 77:5412-5419. https://doi.org/10.1128/AEM.00320-11
  5. Barnhoorn, I. and van Dyk, C. 2020. The first report of selected herbicides and fungicides in water and fish from a highly utilized and polluted freshwater urban impoundment. Environ. Sci. Pollut. Res. 27:33393-33398. https://doi.org/10.1007/s11356-020-09930-7
  6. Barratt, B. I. P., Moran, V. C., Bigler, F. and van Lenteren, J. C. 2018. The status of biological control and recommendations for improving uptake for the future. BioControl 63:155-167. https://doi.org/10.1007/s10526-017-9831-y
  7. Chemeltorit, P. P., Mutaqin, K. H. and Widodo, W. 2017. Combining Trichoderma hamatum THSW13 and Pseudomonas aeruginosa BJ10-86: a synergistic chili pepper seed treatment for Phytophthora capsici infested soil. Eur. J. Plant Pathol. 147:157-166. https://doi.org/10.1007/s10658-016-0988-5
  8. Chowdhury, S. P., Khanna, S., Verma, S. C. and Tripathi, A. K. 2004. Molecular diversity of tannic acid degrading bacteria isolated from tannery soil. J. Appl. Microbiol. 97:1210-1219. https://doi.org/10.1111/j.1365-2672.2004.02426.x
  9. De Vrieze, M., Germanier, F., Vuille, N. and Weisskopf, L. 2018. Combining different potato-associated Pseudomonas strains for improved biocontrol of Phytophthora infestans. Front. Microbiol. 9:2573.
  10. Dietz, S., Herz, K., Gorzolka, K., Jandt, U., Bruelheide, H. and Scheel, D. 2020. Root exudate composition of grass and forb species in natural grasslands. Sci. Rep. 10:10691.
  11. Dutta, S. and Lee, Y. H. 2022. High-throughput identification of genes influencing the competitive ability to obtain nutrients and performance of biocontrol in Pseudomonas putida JBC17. Sci. Rep. 12:872.
  12. Faramarzi, M. A. and Brandl, H. 2006. Formation of water-soluble metal cyanide complexes from solid minerals by Pseudomonas plecoglossicida. FEMS Microbiol. Lett. 259:47-52. https://doi.org/10.1111/j.1574-6968.2006.00245.x
  13. Gao, S., Wu, H., Yu, X., Qian, L. and Gao, X. 2016. Swarming motility plays the major role in migration during tomato root colonization by Bacillus subtilis SWR01. Biol. Control 98:11-17. https://doi.org/10.1016/j.biocontrol.2016.03.011
  14. Guyer, A., De Vrieze, M., Bonisch, D., Gloor, R., Musa, T., Bodenhausen, N., Bailly, A. and Weisskopf, L. 2015. The anti-Phytophthora effect of selected potato-associated Pseudomonas strains: from the laboratory to the field. Front. Microbiol. 6:1309.
  15. Hamon, M. A. and Lazazzera, B. A. 2001. The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42:1199-1209. https://doi.org/10.1046/j.1365-2958.2001.02709.x
  16. 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
  17. Herrera, H., Fuentes, A., Soto, J., Valadares, R. and Arriagada, C. 2020. Orchid-associated bacteria and their plant growth promotion capabilities. In: Orchids phytochemistry, biology and horticulture: fundamentals and applications, eds. by J.-M. Merillon and H. Kodja, pp. 175-200. Springer, Cham, Switzerland.
  18. Huang, L., Liu, W., Jiang, Q., Zuo, Y., Su, Y., Zhao, L., Qin, Y. and Yan, Q. 2018. Integration of transcriptomic and proteomic approaches reveals the temperature-dependent virulence of Pseudomonas plecoglossicida. Front. Cell. Infect. Microbiol. 8:207.
  19. Hunziker, L., Bonisch, D., Groenhagen, U., Bailly, A., Schulz, S. and Weisskopf, L. 2015. Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl. Environ. Microbiol. 81:821-830. https://doi.org/10.1128/AEM.02999-14
  20. Hyder, S., Gondal, A. S., Rizvi, Z. F., Ahmad, R., Alam, M. M., Hannan, A., Ahmed, W., Fatima, N. and Inam-ul-Haq, M. 2020. Characterization of native plant growth promoting rhizobacteria and their anti-oomycete potential against Phytophthora capsici affecting chilli pepper (Capsicum annuum L.). Sci. Rep. 10:13859.
  21. Jeong, J.-J., Park, B. H., Park, H., Choi, I.-G. and Kim, K. D. 2016. Draft genome sequence of Chryseobacterium sp. strain GSE06, a biocontrol endophytic bacterium isolated from cucumber (Cucumis sativus). Genome Announc. 4:e00577-16.
  22. Kamilova, F., Kravchenko, L. V., Shaposhnikov, A. I., Azarova, T., Makarova, N. and Lugtenberg, B. 2006. Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol. Plant-Microbe Interact. 19:250-256. https://doi.org/10.1094/MPMI-19-0250
  23. Kim, H. S., Sang, M. K., Jeun, Y.-C., Hwang, B. K. and Kim, K. D. 2008. Sequential selection and efficacy of antagonistic rhizobacteria for controlling Phytophthora blight of pepper. Crop Prot. 27:436-443. https://doi.org/10.1016/j.cropro.2007.07.013
  24. Kim, Y. J., Hwang, B. K. and Park, K. W. 1989. Expression of age-related resistance in pepper plants infected with Phytophthora capsici. Plant Dis. 73:745-747. https://doi.org/10.1094/PD-73-0745
  25. Kohl, J., Kolnaar, R. and Ravensberg, W. J. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front. Plant Sci. 10:845.
  26. Levene, H. 1960. Contributions to probability and statistics: essays in honor of harold hotelling. Stanford University Press, Stanford, CA, USA. 517 pp.
  27. Li, S., Zhang, N., Zhang, Z., Luo, J., Shen, B., Zhang, R. and Shen, Q. 2013. Antagonist Bacillus subtilis HJ5 controls Verticillium wilt of cotton by root colonization and biofilm formation. Biol. Fertil. Soils 49:295-303. https://doi.org/10.1007/s00374-012-0718-x
  28. Li, Y., Feng, X., Wang, X., Zheng, L. and Liu, H. 2020. Inhibitory effects of Bacillus licheniformis BL06 on Phytophthora capsici in pepper by multiple modes of action. Biol. Control 144:104210.
  29. Lim, J.-H. and Kim, S.-D. 2010. Biocontrol of Phytophthora blight of red pepper caused by Phytophthora capsici using Bacillus subtilis AH18 and B. licheniformis K11 formulations. J. Korean Soc. Appl. Biol. Chem. 53:766-773. https://doi.org/10.3839/jksabc.2010.116
  30. Ma, L., Zheng, S. C., Zhang, T. K., Liu, Z. Y., Wang, X. J., Zhou, X. K., Yang, C. G., Duo, J. L. and Mo, M. H. 2018. Effect of nicotine from tobacco root exudates on chemotaxis, growth, biocontrol efficiency, and colonization by Pseudomonas aeruginosa NXHG29. Antonie Van Leeuwenhoek 111:1237-1257. https://doi.org/10.1007/s10482-018-1035-7
  31. Mannaa, M., Oh, J. Y. and Kim, K. D. 2017. Biocontrol activity of volatile-producing Bacillus megaterium and Pseudomonas protegens against Aspergillus flavus and aflatoxin production on stored rice grains. Mycobiology 45:213-219. https://doi.org/10.5941/MYCO.2017.45.3.213
  32. Marley, J., Lu, M. and Bracken, C. 2001. A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20:71-75. https://doi.org/10.1023/A:1011254402785
  33. Meyer, J.-M., Geoffroy, V. A., Baida, N., Gardan, L., Izard, D., Lemanceau, P., Achouak, W. and Palleroni, N. J. 2002. Siderophore typing, a powerful tool for the identification of fluorescent and nonfluorescent pseudomonads. Appl. Environ. Microbiol. 68:2745-2753. https://doi.org/10.1128/AEM.68.6.2745-2753.2002
  34. Ngo, V. A., Wang, S.-L., Nguyen, V. B., Doan, C. T., Tran, T. N., Tran, D. M., Tran, T. D. and Nguyen, A. D. 2020. Phytophthora antagonism of endophytic bacteria isolated from roots of black pepper (Piper nigrum L.). Agronomy 10:286.
  35. Nishimori, E., Kita-Tsukamoto, K. and Wakabayashi, H. 2000. Pseudomonas plecoglossicida sp. nov., the causative agent of bacterial haemorrhagic ascites of ayu, Plecoglossus altivelis. Int. J. Syst. Evol. Microbiol. 50:83-89. https://doi.org/10.1099/00207713-50-1-83
  36. Oliver, C., Hernandez, I., Caminal, M., Lara, J. M. and Fernandez, C. 2019. Pseudomonas putida strain B2017 produced as technical grade active ingredient controls fungal and bacterial crop diseases. Biocontrol Sci. Technol. 29:1053-1068. https://doi.org/10.1080/09583157.2019.1645304
  37. O'Toole, G. A., Pratt, L. A., Watnick, P. I., Newman, D. K., Weaver, V. B. and Kolter, R. 1999. Genetic approaches to study of biofilms. Methods Enzymol. 310:91-109. https://doi.org/10.1016/S0076-6879(99)10008-9
  38. Park, M. S., Jung, S. R., Lee, M. S., Kim, K. O., Do J. O., Lee, K. H., Kim, S. B. and Bae, K. S. 2005. Isolation and characterization of bacteria associated with two sand dune plant species, Calystegia soldanella and Elymus mollis. J. Microbiol. 43:219-227.
  39. Parra, G. and Ristaino, J. B. 2001. Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phytophthora blight of bell pepper. Plant Dis. 85:1069-1075. https://doi.org/10.1094/pdis.2001.85.10.1069
  40. Raio, A., Brilli, F., Baraldi, R., Neri, L. and Puopolo, G. 2020. Impact of spontaneous mutations on physiological traits and biocontrol activity of Pseudomonas chlororaphis M71. Microbiol. Res. 239:126517.
  41. Sang, M. K. and Kim, K. D. 2014. Biocontrol activity and root colonization by Pseudomonas corrugata strains CCR04 and CCR80 against Phytophthora blight of pepper. BioControl 59:437-448. https://doi.org/10.1007/s10526-014-9584-9
  42. Sang, M. K., Shrestha, A., Kim, D.-Y., Park, K., Pak, C. H. and Kim, K. D. 2013. Biocontrol of Phytophthora blight and anthracnose in pepper by sequentially selected antagonistic rhizobacteria against Phytophthora capsici. Plant Pathol. J. 29:154-167. https://doi.org/10.5423/PPJ.OA.07.2012.0104
  43. Sheoran, N., Nadakkakath, A. V., Munjal, V., Kundu, A., Subaharan, K., Venugopal, V., Rajamma, S., Eapen, S. J. and Kumar, A. 2015. Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol. Res. 173:66-78. https://doi.org/10.1016/j.micres.2015.02.001
  44. Singh, M., Mersie, W. and Brlansky, R. H. 2003. Phytotoxicity of the fungicide metalaxyl and its optical isomers. Plant Dis. 87:1144-1147. https://doi.org/10.1094/pdis.2003.87.9.1144
  45. Sun, D., Zhuo, T., Hu, X., Fan, X. and Zou, H. 2017. Identification of a Pseudomonas putida as biocontrol agent for tomato bacterial wilt disease. Biol. Control 114:45-50. https://doi.org/10.1016/j.biocontrol.2017.07.015
  46. Thind, T. S. and Hollomon, D. W. 2018. Thiocarbamate fungicides: reliable tools in resistance management and future outlook. Pest Manag. Sci. 74:1547-1551. https://doi.org/10.1002/ps.4844
  47. Van de Broek, A., Lambrecht, M. and Vanderleyden, J. 1998. Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599-2606. https://doi.org/10.1099/00221287-144-9-2599
  48. Vancura, V. and Hovadik, A. 1965. Root exudates of plants: II. Composition of root exudates of some vegetables. Plant Soil 22:21-32. https://doi.org/10.1007/BF01377686
  49. Vogel, G., Gore, M. A. and Smart, C. D. 2021. Genome-wide association study in New York Phytophthora capsici isolates reveals loci involved in mating type and mefenoxam sensitivity. Phytopathology 111:204-216. https://doi.org/10.1094/PHYTO-04-20-0112-FI
  50. Volynchikova, E. and Kim, K. D. 2022. Biological control of oomycete soilborne diseases caused by Phytophthora capsici, Phytophthora infestans, and Phytophthora nicotianae in solanaceous crops. Mycobiology 50:269-293. https://doi.org/10.1080/12298093.2022.2136333
  51. Zhai, Y., Shao, Z., Cai, M., Zheng, L., Li, G., Huang, D., Cheng, W., Thomashow, L. S., Weller, D. M., Yu, Z. and Zhang, J. 2018. Multiple modes of nematode control by volatiles of Pseudomonas putida 1A00316 from Antarctic soil against Meloidogyne incognita. Front. Microbiol. 9:253.