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Antagonistic and Plant Growth-Promoting Effects of Bacillus velezensis BS1 Isolated from Rhizosphere Soil in a Pepper Field

  • Shin, Jong-Hwan (Division of Bio-Resource Sciences, BioHerb Research Institute, and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Park, Byung-Seoung (Division of Bio-Resource Sciences, BioHerb Research Institute, and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Kim, Hee-Yeong (Division of Bio-Resource Sciences, BioHerb Research Institute, and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Lee, Kwang-Ho (Division of Bio-Resource Sciences, BioHerb Research Institute, and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Kim, Kyoung Su (Division of Bio-Resource Sciences, BioHerb Research Institute, and Interdisciplinary Program in Smart Agriculture, Kangwon National University)
  • 투고 : 2021.03.29
  • 심사 : 2021.04.14
  • 발행 : 2021.06.01

초록

Pepper (Capsicum annuum L.) is an important agricultural crop worldwide. Recently, Colletotrichum scovillei, a member of the C. acutatum species complex, was reported to be the dominant pathogen causing pepper anthracnose disease in South Korea. In the present study, we isolated bacterial strains from rhizosphere soil in a pepper field in Gangwon Province, Korea, and assessed their antifungal ability against C. scovillei strain KC05. Among these strains, a strain named BS1 significantly inhibited mycelial growth, appressorium formation, and disease development of C. scovillei. By combined sequence analysis using 16S rRNA and partial gyrA sequences, strain BS1 was identified as Bacillus velezensis, a member of the B. subtilis species complex. BS1 produced hydrolytic enzymes (cellulase and protease) and iron-chelating siderophores. It also promoted chili pepper (cv. Nockwang) seedling growth compared with untreated plants. The study concluded that B. velezensis BS1 has good potential as a biocontrol agent of anthracnose disease in chili pepper caused by C. scovillei.

키워드

과제정보

This study was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, and Forestry through the Agri-Food Export Business Model Development Program (319088-3) and the Strategic Initiative for Microbiomes in Agriculture and Food (918019-4), funded by the Ministry of Agriculture, Food and Rural Affairs.

참고문헌

  1. Adeniji, A. A., Aremu, O. S. and Babalola, O. O. 2019. Selecting lipopeptide-producing, Fusarium-suppressing Bacillus spp.: metabolomic and genomic probing of Bacillus velezensis NWUMFkBS10.5. MicrobiologyOpen 8:e00742.
  2. Ahmed, E. and Holmstrom, S. J. 2014. Siderophores in environmental research: roles and applications. Microb. Biotechnol. 7:196-208. https://doi.org/10.1111/1751-7915.12117
  3. Bandara, W. M. M., Seneviratne, G. and Kulasooriya, S. A. 2006. Interactions among endophytic bacteria and fungi: effects and potentials. J. Biosci. 31:645-650. https://doi.org/10.1007/BF02708417
  4. Barbero, G. F., Liazid, A., Azaroual, L., Palma, M. and Barroso, C. G. 2016. Capsaicinoid contents in peppers and pepper-related spicy foods. Int. J. Food Prop. 19:485-493. https://doi.org/10.1080/10942912.2014.968468
  5. Barbero, G. F., Ruiz, A. G., Liazid, A., Palma, M., Vera, J. C. and Barroso, C. G. 2014. Evolution of total and individual capsaicinoids in peppers during ripening of the Cayenne pepper plant (Capsicum annuum L.). Food Chem. 153:200-206. https://doi.org/10.1016/j.foodchem.2013.12.068
  6. Chen, L., Shi, H., Heng, J., Wang, D. and Bian, K. 2019. Antimicrobial, plant growth-promoting and genomic properties of the peanut endophyte Bacillus velezensis LDO2. Microbiol. Res. 218:41-48. https://doi.org/10.1016/j.micres.2018.10.002
  7. Chun, J. and Bae, K. S. 2000. Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie van Leeuwenhoek 78:123-127. https://doi.org/10.1023/A:1026555830014
  8. Cho, K. M., Hong, S. Y., Lee, S. M., Kim, Y. H., Kahng, G. G., Lim, Y. P., Kim, H. and Yun, H. D. 2007. Endophytic bacterial communities in ginseng and their antifungal activity against pathogens. Microb. Ecol. 54:341-351. https://doi.org/10.1007/s00248-007-9208-3
  9. de Souza, R., Ambrosini, A. and Passaglia, L. M. P. 2015. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet. Mol. Biol. 38:401-419. https://doi.org/10.1590/S1415-475738420150053
  10. Dias, J. S. 2012. Nutritional quality and health benefits of vegetables: a review. Food Nutr. Sci. 3:1354-1374. https://doi.org/10.4236/fns.2012.310179
  11. Fan, B., Blom, J., Klenk, H.-P. and Borriss, R. 2017. Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an "Operational group B. amyloliquefaciens" within the B. subtilis species complex. Front. Microbiol. 8:22.
  12. Fazle Rabbee, M. and Baek, K.-H. 2020. Antimicrobial activities of lipopeptides and polyketides of Bacillus velezensis for agricultural applications. Molecules 25:4973. https://doi.org/10.3390/molecules25214973
  13. Glick, B. R. 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:963401. https://doi.org/10.6064/2012/963401
  14. Grady, E. N., MacDonald, J., Ho, M. T., Weselowski, B., McDowell, T., Solomon, O., Renaud, J. and Yuan, Z.-C. 2019. Characterization and complete genome analysis of the surfactin-producing, plant-protecting bacterium Bacillus velezensis 9D-6. BMC Microbiol. 19:5. https://doi.org/10.1186/s12866-018-1380-8
  15. Han, J.-H., Park, G.-C. and Kim, K. S. 2017. Antagonistic evaluation of Chromobacterium sp. JH7 for biological control of ginseng root rot caused by Cylindrocarpon destructans. Mycobiology 45:370-378. https://doi.org/10.5941/MYCO.2017.45.4.370
  16. Han, J.-H., Shim, H., Shin, J.-H. and Kim, K. S. 2015. 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. https://doi.org/10.5423/PPJ.OA.03.2015.0036
  17. Jadhav, H. P. and Sayyed, R. Z. 2016. Hydrolytic enzymes of rhizospheric microbes in crop protection. MOJ Cell Sci. Rep. 3:135-136.
  18. Jiang, C.-H., Liao, M.-J., Wang, H.-K., Zheng, M.-Z., Xu, J.-J. and Guo, J.-H. 2018. Bacillus velezensis, a potential and efficient biocontrol agent in control of pepper gray mold caused by Botrytis cinerea. Biol. Control 126:147-157. https://doi.org/10.1016/j.biocontrol.2018.07.017
  19. Kang, X., Zhang, W., Cai, X., Zhu, T., Xue, Y. and Liu, C. 2018. Bacillus velezensis CC09: a potential 'Vaccine' for controlling wheat diseases. Mol. Plant-Microbe Interact. 31:623-632. https://doi.org/10.1094/MPMI-09-17-0227-R
  20. Khan, A., Singh, P. and Srivastava, A. 2018. Synthesis, nature and utility of universal iron chelator - Siderophore: a review. Microbiol. Res. 212-213:103-111. https://doi.org/10.1016/j.micres.2017.10.012
  21. Khan, M. S., Gao, J., Chen, X., Zhang, M., Yang, F., Du, Y., Moe, T. S., Munir, I., Xue, J. and Zhang, X. 2020. The endophytic bacteria Bacillus velezensis Lle-9, isolated from Lilium leucanthum, harbors antifungal activity and plant growthpromoting effects. J. Microbiol. Biotechnol. 30:668-680. https://doi.org/10.4014/jmb.1910.10021
  22. Kim, J.-O., Shin, J.-H., Gumilang, A., Chung, K., Choi, K. Y. and Kim, K. S. 2016. Effectiveness of different classes of fungicides on Botrytis cinerea causing gray mold on fruit and vegetables. Plant Pathol. J. 32:570-574. https://doi.org/10.5423/PPJ.NT.05.2016.0114
  23. Kim, J.-T., Park, S.-Y., Choi, W.-B., Lee, Y.-H. and Kim, H.-T. 2008. Characterization of Colletotrichum isolates causing anthracnose of pepper in Korea. Plant Pathol. J. 24:17-23. https://doi.org/10.5423/PPJ.2008.24.1.017
  24. Kim, W. G. and Cho, W. D. 2003. Occurrence of sclerotinia rot in solanaceous crops caused by Sclerotinia spp. Mycobiology 31:113-118. https://doi.org/10.4489/MYCO.2003.31.2.113
  25. Kraft, K. H., Brown, C. H., Nabhan, G. P., Luedeling, E., Luna Ruiz, J. J., Coppens d'Eeckenbrugge, G., Hijmans, R. J. and Gepts, P. 2014. Multiple lines of evidence for the origin of domesticated chili pepper, Capsicum annuum, in Mexico. Proc. Natl. Acad. Sci. U. S. A. 111:6165-6170. https://doi.org/10.1073/pnas.1308933111
  26. Kwon, D. Y., Jang, D.-J., Yang, H. J. and Chung, K. R. 2014. History of Korean gochu, gochujang, and kimchi. J. Ethn. Foods 1:3-7. https://doi.org/10.1016/j.jef.2014.11.003
  27. Laskaridou-Monnerville, A. 1999. Determination of capsaicin and dihydrocapsaicin by micellar electrokinetic capillary chromatography and its application to various species of Capsicum, Solanaceae. J. Chromatogr. A 838:293-302. https://doi.org/10.1016/S0021-9673(98)00969-8
  28. Li, F.-Z., Zeng, Y.-J., Zong, M.-H., Yang, J.-G. and Lou, W.-Y. 2020. Bioprospecting of a novel endophytic Bacillus velezensis FZ06 from leaves of Camellia assamica: production of three groups of lipopeptides and the inhibition against food spoilage microorganisms. J. Biotechnol. 323:42-53. https://doi.org/10.1016/j.jbiotec.2020.07.021
  29. Li, X., Geng, X., Xie, R., Fu, L., Jiang, J., Gao, L. and Sun, J. 2016. The endophytic bacteria isolated from elephant grass (Pennisetum purpureum Schumach) promote plant growth and enhance salt tolerance of Hybrid Pennisetum. Biotechnol. Biofuels 9:190. https://doi.org/10.1186/s13068-016-0592-0
  30. Luna-Bulbarela, A., Tinoco-Valencia, R., Corzo, G., Kazuma, K., Konno, K., Galindo, E. and Serrano-Carreon, L. 2018. Effects of bacillomycin D homologues produced by Bacillus amyloliquefaciens 83 on growth and viability of Colletotrichum gloeosporioides at different physiological stages. Biol. Control 127:145-154. https://doi.org/10.1016/j.biocontrol.2018.08.004
  31. Mesnage, R., Defarge, N., Spiroux de Vendomois, J. S. and Seralini, G.-E. 2014. Major pesticides are more toxic to human cells than their declared active principles. Biomed. Res. Int. 2014:179691.
  32. Oo, M. M., Lim, G., Jang, H. A. and Oh, S.-K. 2017. Characterization and pathogenicity of new record of anthracnose on various chili varieties caused by Colletotrichum scovillei in Korea. Mycobiology 45:184-191. https://doi.org/10.5941/MYCO.2017.45.3.184
  33. Park, H.-K., Shim, S.-S., Kim, S.-Y., Park, J.-H., Park, S.-E., Kim, H.-J., Kang, B.-C. and Kim, C.-M. 2005. Molecular analysis of colonized bacteria in a human newborn infant gut. J. Microbiol. 43:345-353.
  34. Perfect, S. E., Hughes, H. B., O'Connell, R. J. and Green, J. R. 1999. Colletotrichum: a model genus for studies on pathology and fungal-plant interactions. Fungal Genet. Biol. 27:186-198. https://doi.org/10.1006/fgbi.1999.1143
  35. Rabbee, M. F., Ali, M. S., Choi, J., Hwang, B. S., Jeong, S. C. and Baek, K.-H. 2019. Bacillus velezensis: a valuable mem-ber of bioactive molecules within plant microbiomes. Molecules 24:1046. https://doi.org/10.3390/molecules24061046
  36. Rajkumar, M., Lee, K. J. and Freitas, H. 2008. Effects of chitin and salicylic acid on biological control activity of Pseudomonas spp. against damping off of pepper. S. Afr. J. Bot. 74:268-273. https://doi.org/10.1016/j.sajb.2007.11.014
  37. Rooney, A. P., Price, N. P., Ehrhardt, C., Swezey, J. L. and Bannan, J. D. 2009. Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov. Int. J. Syst. Evol. Microbiol. 59:2429-2436. https://doi.org/10.1099/ijs.0.009126-0
  38. Sanatombi, K. and Sharma, G. J. 2008. Capsaicin content and pungency of different Capsicum spp. cultivars. Not. Bot. Hort. Agrobot. Cluj. 36:89-90.
  39. Saxena, A., Raghuwanshi, R., Gupta, V. K. and Singh, H. B. 2016. Chilli anthracnose: the epidemiology and management. Front. Microbiol. 7:1527. https://doi.org/10.3389/fmicb.2016.01527
  40. Shahid, I., Han, J., Hanooq, S., Malik, K. A., Borchers, C. H. and Mehnaz, S. 2021. Profiling of metabolites of Bacillus spp. and their application in sustainable plant growth promotion and biocontrol. Front. Sustain. Food Syst. 5:605195. https://doi.org/10.3389/fsufs.2021.605195
  41. Shin, J.-H., Han, J.-H., Park, H.-H., Fu, T. and Kim, K. S. 2019. Optimization of polyethylene glycol-mediated transformation of the pepper anthracnose pathogen Colletotrichum scovillei to develop an applied genomics approach. Plant Pathol. J. 35:575-584. https://doi.org/10.5423/PPJ.OA.06.2019.0171
  42. Sokol, P. A., Ohman, D. E. and Iglewski, B. H. 1979. A more sensitive plate assay for detection of protease production by Pseudomanas aeruginosa. J. Clin. Microbiol. 9:538-540. https://doi.org/10.1128/jcm.9.4.538-540.1979
  43. Stenberg, J. A., Heil, M., Ahman, I. and Bjorkman, C. 2015. Optimizing crops for biocontrol of pests and disease. Trends Plant Sci. 20:698-712. https://doi.org/10.1016/j.tplants.2015.08.007
  44. Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56:845-857. https://doi.org/10.1111/j.1365-2958.2005.04587.x
  45. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. https://doi.org/10.1093/molbev/msr121
  46. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882. https://doi.org/10.1093/nar/25.24.4876
  47. Ullah, A., Nisar, M., Ali, H., Hazrat, A., Hayat, K., Keerio, A. A., Ihsan, M., Laiq, M., Ullah, S., Fahad, S., Khan, A., Khan, A. H., Akbar, A. and Yang, X. 2019. Drought tolerance improvement in plants: an endophytic bacterial approach. Appl. Microbiol. Biotechnol. 103:7385-7397. https://doi.org/10.1007/s00253-019-10045-4
  48. Vagelas, I., Papachatzis, A., Kalorizou, H. and Wogiatzi, E. 2009. Biological control of Botrytis fruit rot (Gray Mold) on strawberry and red pepper fruits by olive oil mill wastewater. Biotechnol. Biotechnol. Equip. 23:1489-1491. https://doi.org/10.2478/V10133-009-0017-3
  49. Wang, C., Zhao, D., Qi, G., Mao, Z., Hu, X., Du, B., Liu, K. and Ding, Y. 2020. Effects of Bacillus velezensis FKM10 for promoting the growth of Malus hupehensis Rehd. and inhibiting Fusarium verticillioides. Front. Microbiol. 10:2889. https://doi.org/10.3389/fmicb.2019.02889
  50. Wellman, R. H. 1977. Problems in development, registration, and use of fungicides. Annu. Rev. Phytopathol. 15:153-163. https://doi.org/10.1146/annurev.py.15.090177.001101
  51. Wisniewski, M., Droby, S., Norelli, J., Liu, J. and Schena, L. 2016. Alternative management technologies for postharvest disease control: the journey from simplicity to complexity. Postharvest Biol. Technol. 122:3-10. https://doi.org/10.1016/j.postharvbio.2016.05.012