DOI QR코드

DOI QR Code

Biological Control Potential of Penicillium brasilianum against Fire Blight Disease

  • Kim, Yeong Seok (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Ngo, Men Thi (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Kim, Bomin (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Han, Jae Woo (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Song, Jaekyeong (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Park, Myung Soo (Department of School of Biological Sciences, Seoul National University) ;
  • Choi, Gyung Ja (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology) ;
  • Kim, Hun (Center for Eco-friendly New Materials, Korea Research Institute of Chemical Technology)
  • Received : 2022.06.09
  • Accepted : 2022.07.19
  • Published : 2022.10.01

Abstract

Erwinia amylovora is a causative pathogen of fire blight disease, affecting apple, pear, and other rosaceous plants. Currently, management of fire blight relies on cultural and chemical practices, whereas it has been known that few biological resources exhibit disease control efficacy against the fire blight. In the current study, we found that an SFC20201208-M01 fungal isolate exhibits antibacterial activity against E. amylovora TS3128, and the isolate was identified as a Penicillium brasilianum based on the 𝛽-tubulin (BenA) gene sequence. To identify active compounds from the P. brasilianum culture, the culture filtrate was partitioned with ethyl acetate and n-butanol sequentially. From the ethyl acetate layer, we identified two new compounds (compounds 3-4) and two known compounds (compounds 1-2) based on spectroscopic analyses and comparison with literature data. Of these active compounds, penicillic acid (1) exhibited promising antibacterial activity against E. amylovora TS3128 with a minimal inhibitory concentration value of 25 ㎍/ml. When culture filtrate and penicillic acid (125 ㎍/ml) were applied onto Chinese pearleaf crab apple seedlings prior to inoculation of E. amylovora TS3128, the development of fire blight disease was effectively suppressed in the treated plants. Our results provide new insight into the biocontrol potential of P. brasilianum SFC20201208-M01 with an active ingredient to control fire blight.

Keywords

Acknowledgement

This research was supported by the Cooperative Research Program for Agricultural Science and Technology Development (Project PJ01529603), Rural Development Administration, Republic of Korea.

References

  1. Acimovic, S. G., Zeng, Q., McGhee, G. C., Sundin, G. W. and Wise, J. C. 2015. Control of fire blight (Erwinia amylovora) on apple trees with trunk-injected plant resistance inducers and antibiotics and assessment of induction of pathogenesis-related protein genes. Front. Plant Sci. 6:16.
  2. Alsberg, C. L. and Black, O. F. 1913. Contributions to the study of maize deterioration: biochemical and toxicological investigations of Penicillium puberulum and Penicillium stoloniferum. U.S. Department of Agriculture, Washington, DC, USA. 47 pp.
  3. Auffray, Y., Boutibonnes, P. and Lemarinier, S. 1984. Filamentous forms of Bacillus thuringiensis (Berliner) formed in the presence of genotoxic mycotoxins. Microbiol. Alim. Nutr. 2:59-67.
  4. Bazioli, J. M., Amaral, L. D. S., Fill, T. P. and Rodrigues-Filho, E. 2017. Insights into Penicillium brasilianum secondary metabolism and its biotechnological potential. Molecules 22:858.
  5. Bonaterra, A., Cabrefiga, J., Camps, J. and Montesinos, E. 2007. Increasing survival and efficacy of a bacterial biocontrol agent of fire blight of rosaceous plants by means of osmoadaptation. FEMS Microbiol. Ecol. 61:185-195. https://doi.org/10.1111/j.1574-6941.2007.00313.x
  6. Broggini, G. A. L., Duffy, B., Holliger, E., Scharer, H.-J., Gessler, C. and Patocchi, A. 2005. Detection of the fire blight biocontrol agent Bacillus subtilis BD170 (Biopro®) in a Swiss apple orchard. Eur. J. Plant Pathol. 111:93-100. https://doi.org/10.1007/s10658-004-1423-x
  7. Coyier, D. L. and Covey, R. P. 1975. Tolerance of Erwinia amylovora to streptomycin sulfate in Oregon and Washington. Plant Dis. Rep. 59:849-852.
  8. Dagher, F., Olishevska, S., Philion, V., Zheng, J. and Deziel, E. 2020. Development of a novel biological control agent targeting the phytopathogen Erwinia amylovora. Heliyon 6:e05222.
  9. De Leon Door, A. P., Romo Chacon, A. and Acosta Muniz, C. 2013. Detection of streptomycin resistance in Erwinia amylovora strains isolated from apple orchards in Chihuahua, Mexico. Eur. J. Plant Pathol. 137:223-229. https://doi.org/10.1007/s10658-013-0241-4
  10. Dong, H. and Cohen, Y. 2001. Extracts of killed Penicillium chrysogenum induce resistance against Fusarium wilt of melon. Phytoparasitica 29:421.
  11. Erfani, J., Abdollahi, H., Ebadi, A., Moghaddam, M. R. F. and Arzani, K. 2013. Evaluation of fire blight resistance and the related markers in some European and Asian pear cultivars. Seed Plant Improv. J. 29:659-672.
  12. Espinel-Ingroff, A., Fothergill, A., Ghannoum, M., Manavathu, E., Ostrosky-Zeichner, L., Pfaller, M., Rinaldi, M., Schell, W. and Walsh, T. 2005. Quality control and reference guidelines for CLSI broth microdilution susceptibility method (M 38-A document) for amphotericin B, itraconazole, posaconazole, and voriconazole. J. Clin. Microbiol. 43:5243-5246. https://doi.org/10.1128/JCM.43.10.5243-5246.2005
  13. Ezzat, S. M., El-Sayed, E. A., Abou El-Hawa, M. I. and Ismaiel, A. A. 2007. Morphological and ultrastructural studies for the biological action of penicillic acid on some bacterial species. Res. J. Microbiol. 2:303-314. https://doi.org/10.3923/jm.2007.303.314
  14. Glass, N. L. and Donaldson, G. C. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
  15. Hamed, I., Ozogul, F., Ozogul, Y. and Regenstein, J. M. 2015. Marine bioactive compounds and their health benefits: a review. Compr. Rev. Food Sci. Food Saf. 14:446-465. https://doi.org/10.1111/1541-4337.12136
  16. Hauben, L. and Swings, J. 2005. Genus XIII. Erwinia. In: Bergey's manual of systematic bacteriology, Vol. 2. The proteobacteria, 2nd ed., eds. by D. J. Brenner, N. R. Krieg, J. T. Staley and G. M. Garrity, pp. 670-679. Springer, New York, NY, USA.
  17. Kang, S. W. and Kim, S. W. 2004. New antifungal activity of penicillic acid against Phytophthora species. Biotechnol. Lett. 26:695-698. https://doi.org/10.1023/B:BILE.0000024090.96693.a4
  18. Kirk, P. M., Cannon, P. F., Minter, D. W. and Stalpers, J. A. 2008. Ainsworth & Bisby's dictionary of the fungi. 10th ed. CABI Publishing, Wallingford, UK. 771 pp.
  19. Kong, H. G., Ham, H., Lee, M.-H., Park, D. S. and Lee, Y. H. 2021. Microbial community dysbiosis and functional gene content changes in apple flowers due to fire blight. Plant Pathol. J. 37:404-412. https://doi.org/10.5423/PPJ.NT.05.2021.0072
  20. Li, Y., Jiao, M., Li, Y., Zhong, Y., Li, X., Chen, Z., Chen, S. and Wang, J. 2021. Penicillium chrysogenum polypeptide extract protects tobacco plants from tobacco mosaic virus infection through modulation of ABA biosynthesis and callose priming. J. Exp. Bot. 72:3526-3539. https://doi.org/10.1093/jxb/erab102
  21. Malnoy, M., Martens, S., Norelli, J. L., Barny, M.-A., Sundin, G. W., Smits, T. H. M. and Duffy, B. 2012. Fire blight: applied genomic insights of the pathogen and host. Annu. Rev. Phytopathol. 50:475-494. https://doi.org/10.1146/annurev-phyto-081211-172931
  22. McManus, P. S., Stockwell, V. O., Sundin, G. W. and Jones, A. L. 2002. Antibiotic use in plant agriculture. Anuu. Rev. Phytopathol. 40:443-465. https://doi.org/10.1146/annurev.phyto.40.120301.093927
  23. Naglot, A., Goswami, S., Rahman, I., Shrimali, D. D., Yadav, K. K., Gupta, V. K., Rabha, A. J., Gogoi, H. K. and Veer, V. 2015. Antagonistic potential of native Trichoderma viride strain against potent tea fungal pathogens in North East India. Plant Pathol. J. 31:278-289. https://doi.org/10.5423/PPJ.OA.01.2015.0004
  24. Nguyen, H. T., Yu, N. H., Jeon, S. J., Lee, H. W., Bae, C.-H., Yeo, J. H., Lee, H. B., Kim, I.-S., Park, H. W. and Kim, J.-C. 2016. Antibacterial activities of penicillic acid isolated from Aspergillus persii against various plant pathogenic bacteria. Lett. Appl. Microbiol. 62:488-493. https://doi.org/10.1111/lam.12578
  25. Norelli, J. L., Jones, A. L. and Aldwinckle, H. S. 2003. Fire blight management in the twenty-first century: using new technologies that enhance host resistance in apple. Plant Dis. 87:756-765. https://doi.org/10.1094/PDIS.2003.87.7.756
  26. Oh, M., Son, H., Choi, G. J., Lee, C., Kim, J.-C., Kim, H. and Lee, Y.-W. 2016. Transcription factor ART1 mediates starch hydrolysis and mycotoxin production in Fusarium graminearum and F.verticillioides. Mol. Plant Pathol. 17:755-768. https://doi.org/10.1111/mpp.12328
  27. Park, D. H., Yu, J.-G., Oh, E.-J., Han, K.-S., Yea, M. C., Lee, S. J., Myung, I.-S., Shim, H. S. and Oh, C.-S. 2016. First report of fire blight disease on Asian pear caused by Erwinia amylovora in Korea. Plant Dis. 100:1946.
  28. Pusey, P. L., Stockwell, V. O., Reardon, C. L., Smits, T. H. M. and Duffy, B. 2011. Antibiosis activity of Pantoea agglomerans biocontrol strain E325 against Erwinia amylovora on apple flower stigmas. Phytopathology 101:1234-1241 https://doi.org/10.1094/PHYTO-09-10-0253
  29. Rasmussen, T. B., Skindersoe, M. E., Bjarnsholt, T., Phipps, R. K., Christensen, K. B., Jensen, P. O., Andersen, J. B., Koch, B., Larsen, T. O., Hentzer, M., Eberl, L., Hoiby, N. and Givskov, M. 2005. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325-1340. https://doi.org/10.1099/mic.0.27715-0
  30. Rosello, G., Bonaterra, A., Frances, J., Montesinos, L., Badosa, E. and Montesinos, E. 2013. Biological control of fire blight of apple and pear with antagonistic Lactobacillus plantarum. Eur. J. Plant Pathol. 137:621-633. https://doi.org/10.1007/s10658-013-0275-7
  31. Russo, N. L., Burr, T. J., Breth, D. I. and Aldwinckle, H. S. 2008. Isolation of streptomycin-resistant isolates of Erwinia amylovora in New York. Plant Dis. 92:714-718. https://doi.org/10.1094/PDIS-92-5-0714
  32. Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
  33. Schaad, N. W., Wang, Z. K., Di, M., McBeath, J., Peterson, G. L. and Bonde, M. R. 1996. An improved infiltration technique to test the pathogenicity of Xanthomonas oryzae pv. oryzae in rice seedlings. Seed Sci. Technol. 24:449-456.
  34. Schroth, M. N., Thomson, S. V., Hildebrand, D. C. and Moller, W. J. 1974. Epidemiology and control of fire blight. Anuu. Rev. Phytopathol. 12:389-412. https://doi.org/10.1146/annurev.py.12.090174.002133
  35. Sholberg, P. L., Bedford, K. E., Haag, P. and Randal, P. 2001. Survey of Erwinia amylovora isolates from British Columbia for resistance to bactericides and virulence on apple. Can. J. Plant Pathol. 23:60-67. https://doi.org/10.1080/07060660109506910
  36. Sobiczewski, P., Peil, A., Mikicinski, A., Richter, K., Lewandowski, M., Zurawicz, E. and Kellerhals, M. 2015. Susceptibility of apple genotypes from European genetic resources to fire blight (Erwinia amylovora). Eur. J. Plant Pathol. 141:51-62. https://doi.org/10.1007/s10658-014-0521-7
  37. Thomson, S. V., Gouk, S. C., Vanneste, J. L., Hale, C. N. and Clark, R. G. 1993. The presence of streptomycin resistant isolates of Erwinia amylovora in New Zealand. Acta. Hortic. 338:223-230.
  38. Vanneste, J. L. 2000. Fire blight: the disease and its causative agent, Erwinia amylovora. CABI publishing, Wallingford, UK. 370 pp.
  39. Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S.-B., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Varga, J., Yaguchi, T. and Samson, R. A. 2014. Identification and nomenclature of the genus Penicillium. Stud. Mycol. 78:343-371. https://doi.org/10.1016/j.simyco.2014.09.001
  40. Vrancken, K., Holtappels, M., Schoofs, H., Deckers, T. and Valcke, R. 2013. Pathogenicity and infection strategies of the fire blight pathogen Erwinia amylovora in Rosaceae: state of the art. Microbiology 159:823-832. https://doi.org/10.1099/mic.0.064881-0
  41. Wang, D., Korban, S. S. and Zhao, Y. 2010. Molecular signature of differential virulence in natural isolates of Erwinia amylovora. Phytopathology 100:192-198. https://doi.org/10.1094/PHYTO-100-2-0192
  42. Zhao, X., Ni, Y., Zhao, H., Liu, X., He, B., Shi, B., Ma, Q. and Liu, H. 2021. Plant growth-promoting ability and control efficacy of Penicillium aurantiogriseum 44M-3 against sesame Fusarium wilt disease. Biocontrol Sci. Technol. 31:1314-1329. https://doi.org/10.1080/09583157.2021.1946011