The Plant Pathology Journal

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

DOI QR Code

Potentiality of Beneficial Microbe Bacillus siamensis GP-P8 for the Suppression of Anthracnose Pathogens and Pepper Plant Growth Promotion

  • Ji Min Woo (Division of Biological Resource Sciences, Department of Applied Plant Sciences, Kangwon National University) ;
  • Hyun Seung Kim (Division of Biological Resources Sciences, Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • In Kyu Lee (Department of Life Sciences, Pohang University of Science and Technology) ;
  • Eun Jeong Byeon (Division of Biological Resource Sciences, Department of Applied Plant Sciences, Kangwon National University) ;
  • Won Jun Chang (Division of Biological Resources Sciences, Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Youn Su Lee (Division of Biological Resource Sciences, Department of Applied Plant Sciences, Kangwon National University)
  • Received : 2024.01.31
  • Accepted : 2024.07.01
  • Published : 2024.08.01
Download PDF
⟨ Previous Next ⟩

Abstract

This study was carried out to screen the antifungal activity against Colletotrichum acutatum, Colletotrichum dematium, and Colletotrichum coccodes. Bacterial isolate GP-P8 from pepper soil was found to be effective against the tested pathogens with an average inhibition rate of 70.7% in in vitro dual culture assays. 16S rRNA gene sequencing analysis result showed that the effective bacterial isolate as Bacillus siamensis. Biochemical characterization of GP-P8 was also performed. According to the results, protease and cellulose, siderophore production, phosphate solubilization, starch hydrolysis, and indole-3-acetic acid production were shown by the GP-P8. Using specific primers, genes involved in the production of antibiotics, such as iturin, fengycin, difficidin, bacilysin, bacillibactin, surfactin, macrolactin, and bacillaene were also detected in B. siamensis GP-P8. Identification and analysis of volatile organic compounds through solid phase microextraction/gas chromatography-mass spectrometry (SPME/GC-MS) revealed that acetoin and 2,3-butanediol were produced by isolate GP-P8. In vivo tests showed that GP-P8 significantly reduced the anthracnose disease caused by C. acutatum, and enhanced the growth of pepper plant. Reverse transcription polymerase chain reaction analysis of pepper fruits revealed that GP-P8 treated pepper plants showed increased expression of immune genes such as CaPR1, CaPR4, CaNPR1, CaMAPK4, CaJA2, and CaERF53. These results strongly suggest that GP-P8 could be a promising biocontrol agent against pepper anthracnose disease and possibly a pepper plant growth-promoting agent.

Keywords

References

  1. Ali, O., Ramsubhag, A. and Jayaraman, J. 2021. Biostimulant properties of seaweed extracts in plants: implications towards sustainable crop production. Plants 10:531.
  2. Arora, N. K. and Verma, M. 2017. Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech 7:381.
  3. Asari, S., Matzen, S., Petersen, M. A., Bejai, S. and Meijer, J. 2016. Multiple effects of Bacillus amyloliquefaciens volatile compounds: plant growth promotion and growth inhibition of phytopathogens. FEMS Microbiol. Ecol. 92:fiw070.
  4. Barchenger, D. W. and Khoury, C. K. 2022. A global strategy for the conservation and use of Capsicum genetic resources. Global Crop Diversity Trust, Bonn, Germany. 77 pp.
  5. Borad, V. and Sriram, S. 2008. Pathogenesis-related proteins for the plant protection. Asian J. Exp. Sci. 22:189-196.
  6. Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C. and Mahillon, J. 2019. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front. Microbiol. 10:302.
  7. Chaves-Lopez, C., Serio, A., Gianotti, A., Sacchetti, G., Ndagijimana, M., Ciccarone, C., Stellarini, A., Corsetti, A. and Paparella, A. 2015. Diversity of food-borne Bacillus volatile compounds and influence on fungal growth. J. Appl. Microbiol. 119:487-499.
  8. Cherif-Silini, H., Silini, A., Yahiaoui, B., Ouzari, I. and Boudabous, A. 2016. Phylogenetic and plant-growth-promoting characteristics of Bacillus isolated from the wheat rhizosphere. Ann. Microbiol. 66:1087-1097.
  9. Clemente, M., Corigliano, M. G., Pariani, S. A., Sanchez-Lopez, E. F., Sander, V. A. and Ramos-Duarte, V. A. 2019. Plant serine protease inhibitors: biotechnology application in agriculture and molecular farming. Int. J. Mol. Sci. 20:1345.
  10. Connolly, M. A., Clausen, P. A. and Lazar, J. G. 2006. Preparation of RNA from plant tissue using TRIzol. CSH Protoc. 2006:pdb.prot4105.
  11. Du Jardin, P. 2015. Plant biostimulants: definition, concept, main categories and regulation. Sci. Hortic. 196:3-14.
  12. Fei, H., Crouse, M., Papadopoulos, Y. and Vessey, J. K. 2017. Enhancing the productivity of hybrid poplar (Populus × hybrid) and switchgrass (Panicum virgatum L.) by the application of beneficial soil microbes and a seaweed extract. Biomass Bioenergy 107:122-134.
  13. Fincher, G. B. 1989. Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu. Rev. Plant Biol. 40:305-346.
  14. Franche, C., Lindstrom, K. and Elmerich, C. 2009. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35-59.
  15. Goswami, D., Dhandhukia, P., Patel, P. and Thakker, J. N. 2014. Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiol. Res. 169:66-75.
  16. Haidar, R., Roudet, J., Bonnard, O., Dufour, M. C., Corio-Costet, M. F., Fert, M., Gautier, T., Deschamps, A. and Fermaud, M. 2016. Screening and modes of action of antagonistic bacteria to control the fungal pathogen Phaeomoniella chlamydospora involved in grapevine trunk diseases. Microbiol. Res. 192:172-184.
  17. Han, J.-H., Kim, M.-J. and Kim, K. S. 2015a. Control of Colletotrichum acutatum and plant growth promotion of pepper by antagonistic microorganisms. Korean J. Mycol. 43:253-259.
  18. Han, J.-H., Shim, H., Shin, J.-H. and Kim, K. S. 2015b. Antagonistic activities of Bacillus spp. strains isolated from tidal flat sediment towards anthracnose pathogens Colletotrichum acutatum and C. gloeosporioides in South Korea. Plant Pathol. J. 31:165-175.
  19. Hazarika, D. J., Goswami, G., Gautom, T., Parveen, A., Das, P., Barooah, M. and Boro, R. C. 2019. Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiol. 19:71.
  20. Hong, J. K., Yang, H. J., Jung, H., Yoon, D. J., Sang, M. K. and Jeun, Y.-C. 2015. Application of volatile antifungal plant essential oils for controlling pepper fruit anthracnose by Colletotrichum gloeosporioides. Plant Pathol. J. 31:269-277.
  21. Khan, W., Rayirath, U. P., Subramanian, S., Jithesh, M. N., Rayorath, P., Hodges, D. M., Critchley, A. T., Craigie, J. S., Norrie, J. and Prithiviraj, B. 2009. Seaweed extracts as biostimulants of plant growth and development. J. Plant Growth Regul. 28:386-399.
  22. Kloepper, J. W., Reddy, M. S., Rodriguez-Kabana, R., Kenney, D. S., Kokalis-Burelle, N. and Martinez-Ochoa, N. 2004. Application for rhizobacteria in transplant production and yield enhancement. Acta Hortic. 631:219-229.
  23. Kwon, H.-T., Lee, Y., Kim, J., Balaraju, K., Kim, H. T. and Jeon, Y. 2022. Identification and characterization of Bacillus tequilensis GYUN-300: an antagonistic bacterium against red pepper anthracnose caused by Colletotrichum acutatum in Korea. Front. Microbiol. 13:826827.
  24. Meena, R. S., Kumar, S., Datta, R., Lal, R., Vijayakumar, V., Brtnicky, M., Sharma, M. P., Yadav, G. S., Jhariya, M. K., Jangir, C. K., Pathan, S. I., Dokulilova, T., Pecina, V. and Marfo, T. D. 2020. Impact of agrochemicals on soil microbiota and management: a review. Land 9:34.
  25. Ngalimat, M. S., Yahaya, R. S. R., Baharudin, M. M. A.-A., Yaminudin, S. M., Karim, M., Ahmad, S. A. and Sabri, S. 2021. A review on the biotechnological applications of the operational group Bacillus amyloliquefaciens. Microorganisms 9:614.
  26. Ons, L., Bylemans, D., Thevissen, K. and Cammue, B. P. A. 2020. Combining biocontrol agents with chemical fungicides for integrated plant fungal disease control. Microorganisms 8:1930.
  27. Pal, A. K., Mandal, S. and Sengupta, C. 2019. Exploitation of IAA producing PGPR on mustard (Brassica nigra L.) seedling growth under cadmium stress condition in comparison with exogenous IAA application. Plant Sci. Today 6:22-30.
  28. Palazzini, J. M., Dunlap, C. A., Bowman, M. J. and Chulze, S. N. 2016. Bacillus velezensis RC 218 as a biocontrol agent to reduce Fusarium head blight and deoxynivalenol accumulation: genome sequencing and secondary metabolite cluster profiles. Microbiol. Res. 192:30-36.
  29. Park, K. S. and Kim, C. H. 1992. Identification, distribution and etiological characteristics of anthracnose fungi of red pepper in Korea. Korean J. Plant Pathol. 8:61-69.
  30. Raaijmakers, J. M. and Mazzola, M. 2012. Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopathol. 50:403-424.
  31. Rao, X., Huang, X., Zhou, Z. and Lin, X. 2013. An improvement of the 2-∆∆CT method for quantitative real-time polymerase chain reaction data analysis. Biostat. Bioinforma Biomath. 3:71-85.
  32. Ribeiro, C. M. and Cardoso, E. J. B. N. 2012. Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol. Res. 167:69-78.
  33. Ro, N., Haile, M., Hur, O., Ko, H.-C., Yi, J.-Y., Woo, H.-J., Choi, Y.-M., Rhee, J., Lee, Y.-J., Kim, D.-A., Do, J.-W., Kim, G. W., Kwon, J.-K. and Kang, B.-C. 2023. Genome-wide association study of resistance to anthracnose in pepper (Capsicum chinense) germplasm. BMC Plant Biol. 23:389.
  34. Ro, N.-Y., Sebastin, R., Hur, O.-S., Cho, G.-T., Geum, B., Lee, Y.-J. and Kang, B.-C. 2021. Evaluation of anthracnose resistance in pepper (Capsicum spp.) genetic resources. Horticulturae 7:460.
  35. Schwyn, B. and Neilands, J. B. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
  36. Shin, J.-H., Park, B.-S., Kim, H.-Y., Lee, K.-H. and Kim, K. S. 2021. Antagonistic and plant growth-promoting effects of Bacillus velezensis BS1 isolated from rhizosphere soil in a pepper field. Plant Pathol. J. 37:307-314.
  37. Singh, D., Ghosh, P., Kumar, J. and Kumar, A. 2019. Plant growth-promoting rhizobacteria (PGPRs): functions and benefits. In: Microbial interventions in agriculture and environment. Vol. 2. Rhizosphere, microbiome and agro-ecology, eds. by D. P. Singh, V. K. Gupta and R. Prabha, pp. 205-227. Springer, Singapore.
  38. Son, J.-S., Sumayo, M., Hwang, Y.-J., Kim, B.-S. and Ghim, S.-Y. 2014. Screening of plant growth-promoting rhizobacteria as elicitor of systemic resistance against gray leaf spot disease in pepper. Appl. Soil Ecol. 73:1-8.
  39. Suprapta, D. N. 2022. Biocontrol of anthracnose disease on chili pepper using a formulation containing Paenibacillus polymyxa C1. Front. Sustain. Food Syst. 5:782425.
  40. Van Loon, L. C. 2007. Plant responses to plant growth-promoting rhizobacteria. Eur. J. Plant Pathol. 119:243-254.
  41. Van Loon, L. C., Bakker, P. A. and Pieterse, C. M. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483.
  42. Yashaswini, M. S., Nysanth, N. S. and Anith, K. N. 2021. Endospore-forming bacterial endophytes from Amaranthus spp. improve plant growth and suppress leaf blight (Rhizoctonia solani Kuhn) disease of Amaranthus tricolor L. Rhizosphere 19:100387.
  43. Yazdani, M., Bahmanyar, M. A., Pirdashti, H. and Esmaili, M. A. 2009. Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). World Acad. Sci. Eng. Technol. 3:50-52.
  44. Zaidi, A., Khan, M. S., Ahemad, M. and Oves, M. 2009. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung. 56:263-284.
  45. Zhou, D., Huang, X.-F., Chaparro, J. M., Badri, D. V., Manter, D. K., Vivanco, J. M. and Guo, J. 2016. Root and bacterial secretions regulate the interaction between plants and PGPR leading to distinct plant growth promotion effects. Plant Soil 401:259-272.
  46. Vessey, J. K. 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571-586.