DOI QR코드

DOI QR Code

Inhibition of Fusarium oxysporum f. sp. nicotianae Growth by Phenylpropanoid Pathway Intermediates

  • Shull, Timothy E. (Department of Plant and Soil Sciences, University of Kentucky) ;
  • Kurepa, Jasmina (Department of Plant and Soil Sciences, University of Kentucky) ;
  • Miller, Robert D. (Department of Plant and Soil Sciences, University of Kentucky) ;
  • Martinez-Ochoa, Natalia (Department of Plant and Soil Sciences, University of Kentucky) ;
  • Smalle, Jan A. (Department of Plant and Soil Sciences, University of Kentucky)
  • Received : 2020.08.24
  • Accepted : 2020.09.14
  • Published : 2020.12.01

Abstract

Fusarium wilt in tobacco caused by the fungus Fusarium oxysporum f. sp. nicotianae is a disease-management challenge worldwide, as there are few effective and environmentally benign chemical agents for its control. This challenge results in substantial losses in both the quality and yield of tobacco products. Based on an in vitro analysis of the effects of different phenylpropanoid intermediates, we found that the early intermediates trans-cinnamic acid and para-coumaric acid effectively inhibit the mycelial growth of F. oxysporum f. sp. nicotianae strain FW316F, whereas the downstream intermediates quercetin and caffeic acid exhibit no fungicidal properties. Therefore, our in vitro screen suggests that trans-cinnamic acid and para-coumaric acid are promising chemical agents and natural lead compounds for the suppression of F. oxysporum f. sp. nicotianae growth.

Keywords

References

  1. Avenot, H. F. and Michailides, T. J. 2010. Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Prot. 29:643-651. https://doi.org/10.1016/j.cropro.2010.02.019
  2. Bock, C. H., Shapiro-Ilan, D. I., Wedge, D. E. and Cantrell, C. L. 2014. Identification of the antifungal compound, transcinnamic acid, produced by Photorhabdus luminescens, a potential biopesticide against pecan scab. J. Pest Sci. 87:155-162. https://doi.org/10.1007/s10340-013-0519-5
  3. Bubici, G., Kaushal, M., Prigigallo, M. I., Gomez-Lama Cabanas, C. and Mercado-Blanco, J. 2019. Biological control agents against Fusarium wilt of banana. Front. Microbiol. 10:616. https://doi.org/10.3389/fmicb.2019.00616
  4. Daoubi, M., Hernandez-Galan, R., Benharref, A. and Collado, I. G. 2005. Screening study of lead compounds for natural product-based fungicides:antifungal activity and biotransformation of 6α,7α-dihydroxy-β-himachalene by Botrytis cinerea. J. Agric. Food Chem. 53:6673-6677. https://doi.org/10.1021/jf050697d
  5. Duniway, J. M. 2002. Status of chemical alternatives to methyl bromide for pre-plant fumigation of soil. Phytopathology 92:1337-1343. https://doi.org/10.1094/PHYTO.2002.92.12.1337
  6. Fisher, C., Pearce, B. and Kinney, J. 2018. Chloropicrin fumigation to control fusarium wilt of burley tobacco in Kentucky. URL https://www.coresta.org/sites/default/files/abstracts/2018_TWC48_Fisher.pdf. [14 October 2020].
  7. Gordon, T. R. 2017. Fusarium oxysporum and the fusarium wilt syndrome. Annu. Rev. Phytopathol. 55:23-39. https://doi.org/10.1146/annurev-phyto-080615-095919
  8. Guzman, J. D. 2014. Natural cinnamic acids, synthetic derivatives and hybrids with antimicrobial activity. Molecules 19:19292-19349. https://doi.org/10.3390/molecules191219292
  9. Hao, W.-Y., Ren, L.-X., Ran, W. and Shen, Q.-R. 2010. Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.sp. niveum. Plant Soil 336:485-497. https://doi.org/10.1007/s11104-010-0505-0
  10. Hazir, S., Shapiro-Ilan, D. I., Bock, C. H. and Leite, L. G. 2017. Trans-cinnamic acid and Xenorhabdus szentirmaii metabolites synergize the potency of some commercial fungicides. J. Invertebr. Pathol. 145:1-8. https://doi.org/10.1016/j.jip.2017.03.007
  11. LaMondia, J. A. 1995. Influence of resistant tobacco and tobacco cyst nematodes on root infection and secondary inoculum of Fusarium oxysporum f. sp. nicotiana. Plant Dis. 79:337-340. https://doi.org/10.1094/PD-79-0337
  12. LaMondia, J. A. 2015. Fusarium wilt of tobacco. Crop Prot. 73:73-77. https://doi.org/10.1016/j.cropro.2015.03.003
  13. Leslie, J. F., Summerell, B. A. and Bullck, S. 2006. The Fusarium laboratory manual. Blackwell Publishing, Ames, IA, USA. 388 pp.
  14. Li, D., Luong, T. T. M., Dan, W.-J., Ren, Y., Nien, H. X., Zhang, A.-L. and Gao, J.-M. 2018. Natural products as sources of new fungicides (IV): synthesis and biological evaluation of isobutyrophenone analogs as potential inhibitors of classII fructose-1,6-bisphosphate aldolase. Bioorg. Med. Chem. 26:386-393. https://doi.org/10.1016/j.bmc.2017.10.046
  15. Lucas, J. A., Hawkins, N. J. and Fraaije, B. A. 2015. The evolution of fungicide resistance. Adv. Appl. Microbiol. 90:29-92. https://doi.org/10.1016/bs.aambs.2014.09.001
  16. Masiello, M., Somma, S., Ghionna, V., Logrieco, A. F. and Moretti, A. 2019. In vitro and in field response of different fungicides against Aspergillus flavus and Fusarium species causing ear rot disease of maize. Toxins (Basel) 11:11. https://doi.org/10.3390/toxins11010011
  17. Miller, N. F., Standish, J. R. and Quesada-Ocampo, L. M. 2020. Sensitivity of Fusarium oxysporum f. sp. niveum to prothioconazole and pydiflumetofen in vitro and efficacy for fusarium wilt management in watermelon. Plant Health Prog. 21:13-18. https://doi.org/10.1094/php-08-19-0056-rs
  18. Morales, J., Mendoza, L. and Cotoras, M. 2017. Alteration of oxidative phosphorylation as a possible mechanism of the antifungal action of p-coumaric acid against Botrytis cinerea. J. Appl. Microbiol. 123:969-976. https://doi.org/10.1111/jam.13540
  19. Mota, F. L., Queimada, A. J., Pinho, S. P. and Macedo, E. A. 2008. Aqueous solubility of some natural phenolic compounds. Ind. Eng. Chem. Res. 47:5182-5189. https://doi.org/10.1021/ie071452o
  20. Musso, L., Dallavalle, S., Farina, G. and Burrone, E. 2012. Natural products as sources of new fungicides: synthesis and antifungal activity of zopfiellin analogues. Chem. Biol. Drug. Des. 79:780-789. https://doi.org/10.1111/j.1747-0285.2012.01343.x
  21. Neelam, Khatkar, A. and Sharma, K. K. 2020. Phenylpropanoids and its derivatives: biological activities and its role in food, pharmaceutical and cosmetic industries. Crit. Rev. Food Sci. Nutr. 60:2655-2675. https://doi.org/10.1080/10408398.2019.1653822
  22. Nirmaladevi, D., Venkataramana, M., Srivastava, R. K., Uppalapati, S. R., Gupta, V. K., Yli-Mattila, T., Clement Tsui, K. M., Srinivas, C., Niranjana, S. R. and Chandra, N. S. 2016. Molecular phylogeny, pathogenicity and toxigenicity of Fusarium oxysporum f. sp. lycopersici. Sci. Rep. 6:21367. https://doi.org/10.1038/srep21367
  23. Schneider, S. M., Rosskopf, E. N., Leesch, J. G., Chellemi, D. O., Bull, C. T. and Mazzola, M. 2003. United States Department of Agriculture-Agricultural Research Service research on alternatives to methyl bromide: pre-plant and post-harvest. Pest Manag. Sci. 59:814-826. https://doi.org/10.1002/ps.728
  24. Steinkellner, S. and Mammerler, R. 2007. Effect of flavonoids on the development of Fusarium oxysporum f. sp. lycopersici. J. Plant Interact. 2:17-23. https://doi.org/10.1080/17429140701409352
  25. UNEP Ozone Secretariat. 2020. Handbook for the Montreal protocol on substances that deplete the ozone layer. 14th ed. United Nations Environment Programme, Nairobi, Kenya. 937 pp.
  26. Vogt, T. 2010. Phenylpropanoid biosynthesis. Mol. Plant 3:2-20. https://doi.org/10.1093/mp/ssp106
  27. Wu, H.-S., Raza, W., Fan, J.-Q., Sun, Y.-G., Bao, W. and Shen Q.-R. 2008. Cinnamic acid inhibits growth but stimulates production of pathogenesis factors by in vitro cultures of Fusarium oxysporum f.sp. niveum. J. Agric. Food Chem. 56:1316-1321. https://doi.org/10.1021/jf0726482
  28. Xie, H., Yan, D., Mao, L., Wang, Q., Li, Y., Ouyang, C., Guo, M. and Cao, A. 2015. Evaluation of methyl bromide alternatives efficacy against soil-borne pathogens, nematodes and soil microbial community. PLoS ONE 10:e0117980. https://doi.org/10.1371/journal.pone.0117980
  29. Xu, D., Hu, M.-J., Wang, Y.-Q. and Cui, Y.-L. 2019. Antioxidant activities of quercetin and its complexes for medicinal application. Molecules 24:1123. https://doi.org/10.3390/molecules24061123
  30. Ye, S. F., Yu, J. Q., Peng, Y. H., Zheng, J. H. and Zou, L. Y. 2004. Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant Soil 263:143-150. https://doi.org/10.1023/B:PLSO.0000047721.78555.dc
  31. Zhao, Q., Chen, L., Dong, K., Dong, Y. and Xiao, J. 2018. Cinnamic acid inhibited growth of faba bean and promoted the incidence of fusarium wilt. Plants (Basel) 7:84. https://doi.org/10.3390/plants7040084