The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Diffusible and Volatile Antifungal Compounds Produced by an Antagonistic Bacillus velezensis G341 against Various Phytopathogenic Fungi

  • Lim, Seong Mi (Division of Applied Bioscience and Biotechnology, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Sciences, Chonnam National University) ;
  • Yoon, Mi-Young (Eco-friendly New Material Research Group, Korea Research Institute of Chemical Technology) ;
  • Choi, Gyung Ja (Eco-friendly New Material Research Group, Korea Research Institute of Chemical Technology) ;
  • Choi, Yong Ho (Eco-friendly New Material Research Group, Korea Research Institute of Chemical Technology) ;
  • Jang, Kyoung Soo (Eco-friendly New Material Research Group, Korea Research Institute of Chemical Technology) ;
  • Shin, Teak Soo (Crop Protection Research Center, Farm Hannong Company, Ltd.) ;
  • Park, Hae Woong (R&D Division, World Institute of Kimchi) ;
  • Yu, Nan Hee (Division of Applied Bioscience and Biotechnology, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Sciences, Chonnam National University) ;
  • Kim, Young Ho (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Jin-Cheol (Division of Applied Bioscience and Biotechnology, Institute of Environmentally Friendly Agriculture, College of Agriculture and Life Sciences, Chonnam National University)
  • Received : 2017.04.03
  • Accepted : 2017.06.14
  • Published : 2017.10.01
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Abstract

The aim of this study was to identify volatile and agardiffusible antifungal metabolites produced by Bacillus sp. G341 with strong antifungal activity against various phytopathogenic fungi. Strain G341 isolated from four-year-old roots of Korean ginseng with rot symptoms was identified as Bacillus velezensis based on 16S rDNA and gyrA sequences. Strain G341 inhibited mycelial growth of all phytopathogenic fungi tested. In vivo experiment results revealed that n-butanol extract of fermentation broth effectively controlled the development of rice sheath blight, tomato gray mold, tomato late blight, wheat leaf rust, barley powdery mildew, and red pepper anthracnose. Two antifungal compounds were isolated from strain G341 and identified as bacillomycin L and fengycin A by MS/MS analysis. Moreover, volatile compounds emitted from strain G341 were found to be able to inhibit mycelial growth of various phytopathogenic fungi. Based on volatile compound profiles of strain G341 obtained through headspace collection and analysis on GC-MS, dimethylsulfoxide, 1-butanol, and 3-hydroxy-2-butanone (acetoin) were identified. Taken together, these results suggest that B. valezensis G341 can be used as a biocontrol agent for various plant diseases caused by phytopathogenic fungi.

Keywords

References

  1. Almenar, E., Valle, V. D., Catala, R. and Gavara, R. 2007. Active package for wild strawberry fruit (Fragaria vesca L.). J. Agric. Food Chem. 55:2240-2245. https://doi.org/10.1021/jf062809m
  2. Archibold, D. D., Hamilton-Kemp, T. R., Barth, M. M. and Langlois, B. E. 1997. Identifying natural volatile compounds that control gray mold (Botrytis cinerea) during postharvest storage of strawberry, blackberry, and grape. J. Agric. Food Chem. 45:4032-4037. https://doi.org/10.1021/jf970332w
  3. Arrebola, E., Sivakumar, D. and Korsten, L. 2010. Effect of volatile compounds produced by Bacillus strains on postharvest decay in citrus. Biol. Control 53:122-128. https://doi.org/10.1016/j.biocontrol.2009.11.010
  4. Asaka, O. and Shoda, M. 1996. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl. Environ. Microbiol. 62:4081-4085.
  5. Baehler, E., de Werra, P., Wick, L. Y., Pechy-Tarr, M., Mathys, S., Maurhofer, M. and Keel, C. 2006. Two novel Mvat-like global regulators control exoproduct formation and biocontrol activity in root-associated Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 19:313-329. https://doi.org/10.1094/MPMI-19-0313
  6. Barnard, M., Padgitt, M. and Uri, N. D. 1997. Pesticide use and its measurement. Int. Pest Control 39:161-164.
  7. Besson, F., Peypoux, F., Michel, G. and Delcambe, L. 1978. Identification of antibiotics of iturin group in various strains of Bacillus subtilis. J. Antibiot. (Tokyo) 31:284-288. https://doi.org/10.7164/antibiotics.31.284
  8. Cai, X.-C., Liu, C.-H., Wang, B.-T. and Xue, Y.-R. 2017. Genomic and metabolic traits endow Bacillus velezensis CC09 with a potential biocontrol agent in control of wheat powdery mildew disease. Microbiol. Res. 196:89-94. https://doi.org/10.1016/j.micres.2016.12.007
  9. Cazorla, F. M., Dukett, S. B., Derström, E. T., Noreen, S., Odijk, R., Lugtenberg, B. J. J., Thomas-Oates, J. E. and Bloemberg, G. V. 2006. Biocontrol of avocado dematophora root rot by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl-5-propyl resorcinol. Mol. Plant-Microbe Interact. 19:418-428. https://doi.org/10.1094/MPMI-19-0418
  10. Cazorla, F. M., Romero, D., Perez-Garcia, A., Lugtenberg, B. J., Vicente, A. and Bloemberg, G. 2007. Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J. Appl. Microbiol. 103:1950-1959. https://doi.org/10.1111/j.1365-2672.2007.03433.x
  11. Chun, J. 2001. PHYDIT version 3.1. URL http://plaza.snu.ac.kr/-jchun/phydit/.
  12. Chun, J. S. 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
  13. Compant, S., Duffy, B., Nowak, J., Clement, C. and Barka, E. A. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 71:4951-4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005
  14. DeMilo, A. B., Lee, C. J., Moreno, D. S. and Martinez, A. J. 1996. Identification of volatiles derived from Citrobacter freundii fermentation of a trypticase soy broth. J. Agric. Food Chem. 44:607-612. https://doi.org/10.1021/jf950525o
  15. Farag, M. A., Ryu, C.-M., Sumner, L. W. and Pare, P. W. 2006. GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262-2268. https://doi.org/10.1016/j.phytochem.2006.07.021
  16. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  17. Fernando, W. G. D., Ramarathnam, R., Krishnamoorthy, A. S. and Savchuk, S. C. 2005. Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol. Biochem. 37:955-964. https://doi.org/10.1016/j.soilbio.2004.10.021
  18. Fletcher, J., Bender, C., Budowle, B., Cobb, W. T., Gold, S. E., Ishimaru, C. A., Luster, D., Melcher, U., Murch, R., Scherm, H., Seem, R. C., Sherwood, J. L., Sobral, B. W. and Tolin, S. A. 2006. Plant pathogen forensics: capabilities, needs, and recommendations. Microbiol. Mol. Biol. Rev. 70:450-471. https://doi.org/10.1128/MMBR.00022-05
  19. Fogliano, V., Ballio, A., Gallo, M., Woo, S., Scala, F. and Lorito, M. 2002. Pseudomonas lipodepsipeptides and fungal cell wall-degrading enzymes act synergistically in biological control. Mol. Plant-Microbe Interact. 15:323-333. https://doi.org/10.1094/MPMI.2002.15.4.323
  20. Gao, Z., Zhang, B., Liu, H., Han, J. and Zhang, Y. 2017. Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biol. Control 105:27-39. https://doi.org/10.1016/j.biocontrol.2016.11.007
  21. Han, J. S., Cheng, J. H., Yoon, T. M., Song, J., Rajkarnikar, A., Kim, W. G., Yoo, I. D., Yang, Y. Y. and Suh, J. W. 2005. Biological control agent of common scab disease by antagonistic strain Bacillus sp. sunhua. J. Appl. Microbiol. 99:213-221. https://doi.org/10.1111/j.1365-2672.2005.02614.x
  22. Hossain, M. T., Khan, A., Chung, E. J., Rashid, M. H. O. and Chung, Y. R. 2016. Biological control of rice bakanae by an endophytic Bacillus oryzicola YC7007. Plant Pathol. J. 32:228-241. https://doi.org/10.5423/PPJ.OA.10.2015.0218
  23. Huang, H., Huang, J. W., Saidon, G. and Erickson, R. 1997. Effect of allyl alcohol and fermented agricultural wastes on carpogenic germination of sclerotia of Sclerotinia sclerotiorum and colonization by Trichoderma spp. Can. J. Plant Pathol. 9:43-46.
  24. Isman, M. B. 2000. Plant essential oils for pest and disease management. Crop Prot. 19:603-608. https://doi.org/10.1016/S0261-2194(00)00079-X
  25. Kim, J.-C., Choi, G. J., Lee, S.-W., Kim, J.-S., Chung, K. Y. and Cho, K. Y. 2004. Screening extracts of Achyranthes japonica and Rumex crispus for activity against various plant pathogenic fungi and control of powdery mildew. Pest Manag. Sci. 60:803-808. https://doi.org/10.1002/ps.811
  26. Kim, J.-C., Choi, G. J., Park, J.-H., Kim, H. T. and Cho, K. Y. 2001. Activity against plant pathogenic fungi of phomalactone isolated from Nigrospora sphaerica. Pest Manag. Sci. 57:554-559. https://doi.org/10.1002/ps.318
  27. Kim, J. S., Lee, J., Lee, C. H., Woo, S. Y., Kang, H., Seo, S. G. and Kim, S. H. 2015. Activation of pathogenesis-related genes by the rhizobacterium, Bacillus sp. JS, which induces systemic resistance in tobacco plants. Plant Pathol. J. 31:195-201. https://doi.org/10.5423/PPJ.NT.11.2014.0122
  28. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120. https://doi.org/10.1007/BF01731581
  29. Kordali, S., Cakir, A., Ozer, H., Cakmakci, R., Kesdek, M. and Mete, E. 2008. Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresour. Technol. 99:8788-8795. https://doi.org/10.1016/j.biortech.2008.04.048
  30. Kulimushi, P. Z., Arias, A. A., Franzil, L., Steels, A. and Ongena, M. 2017. Stimulation of fengycin-type antifungal lipopeptides in Bacillus amyloliquefaciens in the presence of the maize fungal pathogen Rhizomucor variabilis. Front. Microbiol. 8:850. https://doi.org/10.3389/fmicb.2017.00850
  31. Liu, C. H., Chen, X., Liu, T. T., Lian, B., Gu, Y., Caer, V., Xue, Y. R. and Wang, B. T. 2007. Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Appl. Microbiol. Biotechnol. 76:459-466. https://doi.org/10.1007/s00253-007-1010-0
  32. Loeffler, W., Tschen, J., Vanittanakom, N., Kugler, M., Knorpp, E., Hsieh, T. F. and Wu, T. G. 1986. Antifungal effects of bacilysin and fengymycin from Bacillus subtilis F-29-3: a comparison with activities of other Bacillus antibiotics. J. Phytopathol. 115:204-213. https://doi.org/10.1111/j.1439-0434.1986.tb00878.x
  33. Mhammedi, A., Peypoux, F., Besson, F. and Michel, G. 1982. Bacillomycin F, a new antibiotic of iturin group: isolation and characterization. J. Antibiot. (Tokyo) 35:306-311. https://doi.org/10.7164/antibiotics.35.306
  34. Misra, G. and Pavlostathis, S. G. 1997. Biodegradation kinetics of monoterpenes in liquid and soil-slurry systems. Appl. Microbiol. Biotechnol. 47:572-577. https://doi.org/10.1007/s002530050975
  35. Moyne, A. L., Shelby, R., Cleveland, T. E. and Tuzun, S. 2001. Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J. Appl. Microbiol. 90:622-629. https://doi.org/10.1046/j.1365-2672.2001.01290.x
  36. Nam, H. S., Yang, H.-J., Oh, B. J., Anderson, A. J. and Kim, Y. C. 2016. Biological control potential of Bacillus amyloliquefaciens KB3 isolated from the feces of Allomyrina dichotoma larvae. Plant Pathol. J. 32:273-280. https://doi.org/10.5423/PPJ.NT.12.2015.0274
  37. Nam, M. H., Park, M. S., Kim, H. G. and Yoo, S. J. 2009. Biological control of strawberry Fusarium wilt caused by Fusarium oxysporum f. sp. fragariae using Bacillus velezensis BS87 and RK1 formulation. J. Mcirobiol. Biotechnol. 19:520-524. https://doi.org/10.4014/jmb.0805.333
  38. Ongena, M. and Jacques, P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16:115-125. https://doi.org/10.1016/j.tim.2007.12.009
  39. 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. https://doi.org/10.1016/j.micres.2016.06.002
  40. 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.
  41. Peypoux, F., Bonmatin, J. M. and Wallach, J. 1999. Recent trends in the biochemistry of surfactin. Appl. Microbiol. Biotechnol. 51:553-563. https://doi.org/10.1007/s002530051432
  42. Qian, S., Lu, H., Sun, J., Zhang, C., Zhao, H., Lu, F., Bie, X. and Lu, Z. 2016. Antifungal activity mode of Aspergillus ochraceus by bacillomycin D and its inhibition of ochratoxin A (OTA) production in food samples. Food Control 60:281-288. https://doi.org/10.1016/j.foodcont.2015.08.006
  43. Razafindralambo, H., Popineau, Y., Deleu, M., Hbid, C., Jacques, P., Thonart, P. and Paquot, M. 1998. Foaming properties of lipopeptides produced by Bacillus subtilis: effect of lipid and peptide structural attributes. J. Agric. Food Chem. 46:911-916. https://doi.org/10.1021/jf970592d
  44. Robinson, P. M., McKee, N. D., Thompson, L. A. A., Harper, D. B. and Hamilton, J. T. G. 1989. Autoinhibition of germination and growth in Geotrichum candidum. Mycol. Res. 93:214-222. https://doi.org/10.1016/S0953-7562(89)80120-0
  45. Ruiz-Garcia, C., Bejar, V., Martinex-Checa, F., Llamas, I. and Quesada, E. 2005. Bacillus velezensis sp. nov., a surfactant-producing bacterium isolated from the river Velez in Malaga, southern Spain. Int. J. Syst. Evol. Microbiol. 55:191-195. https://doi.org/10.1099/ijs.0.63310-0
  46. Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Wei, H. X., Pare, P. W. and Kloepper, J. W. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100:4927-4932. https://doi.org/10.1073/pnas.0730845100
  47. Schneider, J., Taraz, K., Budzikiewicz, H., Deleu, M., Thonart, P. and Jacques, P. 1999. The structure of two fengycins from Bacillus subtilis S499. Z. Naturforsch. C 54:859-865.
  48. Sharifi, T. A. and Ramezani, M. 2003. Biological control of Fusarium oxysporum, the causal agent of onion wilt by antagonistic bacteria. Commun. Agric. Appl. Biol. Sci. 68:543-547.
  49. Shoda, M. 2000. Bacterial control of plant disease. J. Biosci. Bioeng. 89:515-521. https://doi.org/10.1016/S1389-1723(00)80049-3
  50. Son, S. H., Khan, Z., Kim, S. G. and Kim, Y. H. 2009. Plant growth-promoting rhizobacteria, Paenibacillus polymyxa and Paenibacillus lentimorbus suppress disease complex caused by root-knot nematode and fusarium wilt fungus. J. Appl. Microbiol. 107:524-532. https://doi.org/10.1111/j.1365-2672.2009.04238.x
  51. 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
  52. Vanittanakom, N., Loeffler, W., Koch, U. and Jung, G. 1986. Fengycin--a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J. Antibiot. (Tokyo) 39:888-901. https://doi.org/10.7164/antibiotics.39.888
  53. Voisard, C., Keel, D., Haas, D. and Defago, G. 1989. Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J. 8:351-358.
  54. Williams, B. H., Hathout, Y. and Fenselau, C. 2002. Structural characterization of lipopeptide biomarkers isolated from Bacillus globigii. J. Mass Spectrom. 37:259-264. https://doi.org/10.1002/jms.279
  55. Yoon, M.-Y., Choi, G. J., Choi, Y. H., Jang, K. S., Park, M. S., Cha, B. and Kim, J.-C. 2010. Effect of polyacetylenic acids from Prunella vulgaris on various plant pathogens. Lett. Appl. Microbiol. 51:511-517. https://doi.org/10.1111/j.1472-765X.2010.02922.x
  56. Yu, G. Y., Sinclair, J. B., Hartman, G. L. and Bertagnolli, B. L. 2002. Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol. Biochem. 34:955-963. https://doi.org/10.1016/S0038-0717(02)00027-5

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