The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Characterization of Nivalenol-Producing Fusarium asiaticum That Causes Cereal Head Blight in Korea

  • Jang, Ja Yeong (Microbial Safety Team, National Institute of Agricultural Sciences) ;
  • Baek, Seul Gi (Microbial Safety Team, National Institute of Agricultural Sciences) ;
  • Choi, Jung-Hye (Microbial Safety Team, National Institute of Agricultural Sciences) ;
  • Kim, Sosoo (Microbial Safety Team, National Institute of Agricultural Sciences) ;
  • Kim, Jeomsoon (Microbial Safety Team, National Institute of Agricultural Sciences) ;
  • Kim, Da-Woon (Department of Medical Biotechnology, Soonchunhyanag University) ;
  • Yun, Sung-Hwan (Department of Medical Biotechnology, Soonchunhyanag University) ;
  • Lee, Theresa (Microbial Safety Team, National Institute of Agricultural Sciences)
  • Received : 2019.06.18
  • Accepted : 2019.08.26
  • Published : 2019.12.01
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Abstract

Fusarium asiaticum of the F. graminearum species complex causes head blight in small-grain cereals. The nivalenol (NIV) chemotypes of F. asiaticum is more common than the deoxynivalenol (DON) chemotypes of F. asiaticum or F. graminearum in Korea. To understand the prevalence of F. asiaticum-NIV in Korean cereals, we characterized the biological traits of 80 cereal isolates of F. asiaticum producing NIV or 3-acetyl-deoxynivalenol (3-ADON), and 54 F. graminearum with 3-ADON or 15-acetyl-deoxynivalenol (15-ADON). There was no significant difference in mycelial growth between the chemotypes, but F. asiaticum isolates grew approximately 30% faster than F. graminearum isolates on potato dextrose agar. Sexual and asexual reproduction capacities differed markedly between the two species. Both chemotypes of F. graminearum (3-ADON and 15-ADON) produced significantly higher numbers of perithecia and conidia than F. asiaticum-NIV. The highest level of mycotoxins (sum of trichothecenes and zearalenone) was produced by F. graminearum-3-ADON on rice medium, followed by F. graminearum-15-ADON, F. asiaticum-3-ADON, and F. asiaticum-NIV. Zearalenone levels were correlated with DON levels in some chemotypes, but not with NIV levels. Disease assessment on barley, maize, rice, and wheat revealed that both F. asiaticum and F. graminearum isolates were virulent toward all crops tested. However, there is a tendency that virulence levels of F. asiaticum-NIV isolates on rice were higher than those of F. graminearum isolates. Taken together, the phenotypic traits found among the Korean F. asiaticum-NIV isolates suggest an association with their host adaptation to certain environments in Korea.

Keywords

References

  1. Aoki, T., Ward, T. J., Kistler, H. C. and O'Donnell, K. 2012. Systematics, phylogeny and trichothecene mycotoxin potential of Fusarium head blight cereal pathogens. Mycotoxins 62:91-102. https://doi.org/10.2520/myco.62.91
  2. Bowden, R. L. and Leslie, J. F. 1999. Sexual recombination in Gibberella zeae. Phytopathology 89:182-188. https://doi.org/10.1094/PHYTO.1999.89.2.182
  3. Chun, J. H. 1963. Epidemiological survey of human mycotoxicosis caused by scabby cereals. In: Research report on wheat and barley scab, ed. by Republic of Korea, pp. 385-507. Ministry of Agriculture and Forestry, Seoul, Korea (in Korean).
  4. Chung, H. S. 1975. Cereal scab causing mycotoxicoses in Korea and present status of mycotoxin researches. Korean. J. Mycol. 3:31-36.
  5. Del Ponte, E. M., Spolti, P., Ward, T. J., Gomes, L. B., Nicolli, C. P., Kuhnem, P. R., Silva, C. N. and Tessmann, D. J. 2015. Regional and field-specific factors affect the composition of fusarium head blight pathogens in subtropical no-till wheat agroecosystem of Brazil. Phytopathology 105:246-254. https://doi.org/10.1094/PHYTO-04-14-0102-R
  6. Desjardins, A. E. 2006. Fusarium mycotoxins: chemistry, genetics and biology. American Phytopathological Society, St. Paul, MN, USA. 268 pp.
  7. Desjardins, A. E. and Proctor, R. H. 2011. Genetic diversity and trichothecene chemotypes of the Fusarium graminearum clade isolated from maize in Nepal and identification of a putative new lineage. Fungal Biol. 115:38-48. https://doi.org/10.1016/j.funbio.2010.10.002
  8. Gale, L. R., Harrison, S. A., Ward, T. J., O'Donnell, K., Milus, E. A., Gale, S. W. and Kistler, H. C. 2011. Nivalenol-type populations of Fusarium graminearum and F. asiaticum are prevalent on wheat in southern Louisiana. Phytopathology 101:124-134. https://doi.org/10.1094/PHYTO-03-10-0067
  9. Gomes, L. B., Ward, T. J., Badiale-Furlong, E. and Del Ponte, E. M. 2015. Species composition, toxigenic potential and pathogenicity of Fusarium graminearum species complex isolates from southern Brazilian rice. Plant Pathol. 64:980-987. https://doi.org/10.1111/ppa.12332
  10. Goswami, R. S. and Kistler, H. C. 2004. Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5:515-525. https://doi.org/10.1111/j.1364-3703.2004.00252.x
  11. Groth, J. V., Ozmon, E. A. and Busch, R. H. 1999. Repeatability and relationship of incidence and severity measures of scab of wheat caused by Fusarium graminearum in inoculated nurseries. Plant Dis. 83:1033-1038. https://doi.org/10.1094/PDIS.1999.83.11.1033
  12. Joo, H. J., Kim, H.-Y., Kim, L.-H., Lee, S., Ryu, J.-G. and Lee, T. 2015. A Brevibacillus sp. antagonistic to mycotoxigenic Fusarium spp. Biol. Control 87:64-70. https://doi.org/10.1016/j.biocontrol.2015.04.010
  13. Karugia, G. W., Suga, H., Gale, L. R., Nakajima, T., Tomimura, K. and Hyakumachi, M. 2009. Population structure of the Fusarium graminearum species complex from a single Japanese wheat field sampled in two consecutive years. Plant Dis. 93:170-174. https://doi.org/10.1094/PDIS-93-2-0170
  14. Lee, J., Chang, I. Y., Kim, H., Yun, S. H., Leslie, J. F. and Lee, Y. W. 2009. Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. Appl. Environ. Microbiol. 75:3289-3295. https://doi.org/10.1128/AEM.02287-08
  15. Lee, S.-H., Lee, J.-K., Nam, Y.-J., Lee, S.-H., Ryu, J.-G. and Lee, T. 2010. Population structure of Fusarium graminearum from maize and rice in 2009 in Korea. Plant Pathol. J. 26:321-327. https://doi.org/10.5423/PPJ.2010.26.4.321
  16. Lee, S., Lee, T., Kim, M., Yu, O., Im, H. and Ryu, J.-G. 2013. Survey on contamination of Fusarium mycotoxins in 2011-harvested rice and its by-products from rice processing complexes in Korea. Res. Plant Dis. 19:259-264 (in Korean). https://doi.org/10.5423/RPD.2013.19.4.259
  17. Lee, T., Han, Y.-K., Kim, K.-H., Yun, S.-H. and Lee, Y.-W. 2002. Tri13 and Tri7 determine deoxynivalenol- and nivalenolproducing chemotypes of Gibberella zeae. Appl. Environ. Microbiol. 68:2148-2154. https://doi.org/10.1128/AEM.68.5.2148-2154.2002
  18. Lee, T., Paek, J.-S., Lee, K. A., Lee, S., Choi, J.-H., Ham, H., Hong, S. K. and Ryu, J.-G. 2016. Occurrence of toxigenic Fusarium vorosii among small grain cereals in Korea. Plant Pathol. J. 32:407-413. https://doi.org/10.5423/PPJ.OA.05.2016.0123
  19. Lee, U. S., Jang, H. S., Tanaka, T., Hasegawa, A., Oh, Y. J. and Ueno, Y. 1985. The coexistence of the Fusarium mycotoxins nivalenol, deoxynivalenol and zearalenone in Korean cereals harvested in 1983. Food Addit. Contam. 2:185-192. https://doi.org/10.1080/02652038509373542
  20. Leslie, J. F. and Summerell, B. A. 2006. The Fusarium laboratory manual. Blackwell Publishing, Ames, IA, USA. 388 pp.
  21. Liu, Y.-Y., Sun, H.-Y., Li, W., Xia, Y.-L., Deng, Y.-Y., Zhang, A.-X. and Chen, H.-G. 2017. Fitness of three chemotypes of Fusarium graminearum species complex in major winter wheatproducing areas of China. PLoS ONE 12:e0174040. https://doi.org/10.1371/journal.pone.0174040
  22. Maier, F. J., Miedaner, T., Hadeler, B., Felk, A., Salomon, S., Lemmens, M., Kassner, H. and Schafer, W. 2006. Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Mol. Plant Pathol. 7:449-461. https://doi.org/10.1111/j.1364-3703.2006.00351.x
  23. Nash, S. M. and Snyder, W. C. 1962. Quantitative estimations by plate counts of propagules of the Bean root rot Fusarium in field soils. Phytopathology 52:567-572.
  24. Nicolli, C. P., Machado, F. J., Spolti, P. and Del Ponte, E. M. 2018. Fitness traits of deoxynivalenol and nivalenol-producing Fusarium graminearum species complex strains from wheat. Plant Dis. 102:1341-1347. https://doi.org/10.1094/PDIS-12-17-1943-RE
  25. O'Donnell, K., Ward, T. J., Geiser, D. M., Kistler, H. C. and Aoki, T. 2004. Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet. Biol. 41:600-623. https://doi.org/10.1016/j.fgb.2004.03.003
  26. Proctor, R. H., Desjardins, A. E., McCormick, S. P., Plattner, R. D., Alexander, N. J. and Brown, D. W. 2002. Genetic analysis of the role of trichothecene and fumonisin mycotoxins in the virulence of Fusarium. Eur. J. Plant Pathol. 108:691-698. https://doi.org/10.1023/A:1020637832371
  27. Puri, K. D., Saucedo, E. S. and Zhong, S. 2012. Molecular characterization of Fusarium head blight pathogens sampled from a naturally infected disease nursery used for wheat breeding programs in China. Plant Dis. 96:1280-1285. https://doi.org/10.1094/PDIS-08-11-0713-RE
  28. Qui, J., Xu, J. and Shi, J. 2014. Molecular characterization of the Fusarium graminearum species complex in Eastern China. Eur. J. Plant Pathol. 139:811-823. https://doi.org/10.1007/s10658-014-0435-4
  29. Shin, S., Son, J.-H., Park, J.-C., Kim, K.-H., Yoon, Y., Cheong, Y.-K., Kim, K.-H., Hyun, J.-N., Park, C. S., Dill-Macky, R. and Kang, C.-S. 2018. Comparative pathogenicity of Fusarium graminearum isolates from wheat kernels in Korea. Plant Pathol. J. 34:347-355. https://doi.org/10.5423/PPJ.OA.01.2018.0013
  30. Starkey, D. E., Ward, T. J., Aoki, T., Gale, L. R., Kistler, H. C., Geiser, D. M., Suga, H., Toth, B., Varga, J. and O'Donnell, K. 2007. Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet. Biol. 44:1191-1204. https://doi.org/10.1016/j.fgb.2007.03.001
  31. Suga, H., Karugia, G. W., Ward, T., Gale, L. R., Tomimura, K., Nakajima, T., Miyasaka, A., Koizumi, S., Kageyama, K. and Hyakumachi, M. 2008. Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology 98:159-166. https://doi.org/10.1094/PHYTO-98-2-0159
  32. Tancic, S., Stankovic, S., Levic, J. and Krnjaja, V. 2015. Correlation of deoxynivalenol and zearalenone production by Fusarium species originating from wheat and maize grain. Pestic. Phytomed. 30:99-105. https://doi.org/10.2298/PIF1502099T
  33. van der Lee, T., Zhang, H., Diepeningen, A. and Waalwijk, C. 2015. Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 32:453-460. https://doi.org/10.1080/19440049.2014.984244
  34. Ward, T. J., Clear, R. M., Rooney, A. P., O'Donnell, K., Gaba, D., Patrick, S., Starkey, D. E., Gilbert, J., Geiser, D. M. and Nowicki, T. W. 2008. An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet. Biol. 45:473-484. https://doi.org/10.1016/j.fgb.2007.10.003
  35. Yli-Mattila, T. 2010. Ecology and evolution of toxigenic Fusarium species in cereals in northern Europe and Asia. J. Plant Pathol. 92:7-18.
  36. Zhang, H., van der Lee, T., Waalwijk, C., Chen, W., Xu, J., Xu, J., Zhang, Y. and Feng, J. 2012. Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. PLoS ONE 7:e31722. https://doi.org/10.1371/journal.pone.0031722
  37. Zhang, H., Zhang, Z., van der Lee, T., Chen, W. Q., Xu, J., Xu, J. S., Yang, L., Yu, D., Waalwijk, C. and Feng, J. 2010. Population genetic analyses of Fusarium asiaticum populations from barley suggest a recent shift favoring 3ADON producers in southern China. Phytopathology 100:328-336. https://doi.org/10.1094/PHYTO-100-4-0328