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Comparison of Trichothecene Biosynthetic Gene Expression between Fusarium graminearum and Fusarium asiaticum

  • Lee, Theresa (Microbial Safety Team, National Academy of Agricultural Science, Rural Development Administration (RDA)) ;
  • Lee, Seung-Ho (Ginseng Research Division, National Institute of Horticultural & Herbal Science, RDA) ;
  • Shin, Jean Young (Microbial Safety Team, National Academy of Agricultural Science, Rural Development Administration (RDA)) ;
  • Kim, Hee-Kyoung (Department of Medical Biotechnology, Soonchunhyang University) ;
  • Yun, Sung-Hwan (Department of Medical Biotechnology, Soonchunhyang University) ;
  • Kim, Hwang-Yong (Microbial Safety Team, National Academy of Agricultural Science, Rural Development Administration (RDA)) ;
  • Lee, Soohyung (Microbial Safety Team, National Academy of Agricultural Science, Rural Development Administration (RDA)) ;
  • Ryu, Jae-Gee (Microbial Safety Team, National Academy of Agricultural Science, Rural Development Administration (RDA))
  • Received : 2013.11.02
  • Accepted : 2013.11.25
  • Published : 2014.03.01

Abstract

Nivalenol (NIV) and deoxynivalenol (DON) are predominant Fusarium-producing mycotoxins found in grains, which are mainly produced by Fusarium asiaticum and F. graminearum. NIV is found in most of cereals grown in Korea, but the genetic basis for NIV production by F. asiaticum has not been extensively explored. In this study, 12 genes belonging to the trichothecene biosynthetic gene cluster were compared at the transcriptional level between two NIV-producing F. asiaticum and four DON-producing F. graminearum strains. Chemical analysis revealed that time-course toxin production patterns over 14 days did not differ between NIV and DON strains, excluding F. asiaticum R308, which was a low NIV producer. Both quantitative real-time polymerase chain reaction and Northern analysis revealed that the majority of TRI gene transcripts peaked at day 2 in both NIV and DON producers, which is 2 days earlier than trichothecene accumulation in liquid medium. Comparison of the gene expression profiles identified an NIV-specific pattern in two transcription factor-encoding TRI genes (TRI6 and TRI10) and TRI101, which showed two gene expression peaks during both the early and late incubation periods. In addition, the amount of trichothecenes produced by both DON and NIV producers were correlated with the expression levels of TRI genes, regardless of the trichothecene chemotypes. Therefore, the reduced production of NIV by R308 compared to NIV or DON by the other strains may be attributable to the significantly lower expression levels of the TRI genes, which showed early expression patterns.

Keywords

References

  1. Boddu, J., Cho, S., Kruger, W. M. and Muehlbauer, G. J. 2005. Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol. Plant Microbe Interact. 19:407-417.
  2. Brown, D. W., McCormick, S. P., Alexander, N. J., Proctor, R. H. and Desjardins, A. E. 2001. A genetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genet. Biol. 32:121-133. https://doi.org/10.1006/fgbi.2001.1256
  3. Desjardins, A. E. 2006. Fusarium mycotoxins: chemistry, genetics, and biology. The American Phytopathological Society, St. Paul, Minnesota, USA. 260 pp.
  4. Doohan, F. M., Weston, G., Rezanoor, H. N., Parry, D. W. and Nicholson, P. 1999. Development and use of a reverse transcription- PCR assay to study expression of Tri5 by Fusarium species in vitro and in planta. Appl. Environ. Microbiol. 65:3850-3854.
  5. Dyer, R. B., Plattner, R. D., Kendra, D. F. and Brown, D. W. 2005. Fusarium graminearum TRI14 is required for high virulence and DON production on wheat but not for DON synthesis in vitro. J. Agric. Food Chem. 53:9281-9287. https://doi.org/10.1021/jf051441a
  6. Eriksen, G. S., Pettersson, H. and Lundh, T. 2004. Comparative cytotoxicity of deoxynivalenol, nivalenol, their acetylated derivatives and de-epoxy metabolites. Food Chem. Toxicol. 42:619-624. https://doi.org/10.1016/j.fct.2003.11.006
  7. Gale, L. R., Harrision, 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
  8. Gardiner, D. M., Kazan, K. and Manners, J. M. 2009. Mutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet. Biol. 46:604-613. https://doi.org/10.1016/j.fgb.2009.04.004
  9. Hallen-Adams, H. E., Wenner, N., Kuldau, G. A. and Trail, F. 2011. Deoxynivalenol biosynthesis-related gene expression during wheat kernel colonization by Fusarium graminearum. Phytopathology 101:1091-1096. https://doi.org/10.1094/PHYTO-01-11-0023
  10. Jiao, F., Kawakami, A. and Nakajima, T. 2008. Effects of different carbon sources on trichothecene production and Tri gene expression by Fusarium graminearum in liquid culture. FEMS Microbiol. Lett. 285:212-219. https://doi.org/10.1111/j.1574-6968.2008.01235.x
  11. Karugia, G. W., Suga, H., Gale, L. R., Nakajima, T., Ueda, A. and Hyakumachi, M. 2009. Population structure of Fusarium asiaticum from two Japanese regions and eastern China. J. Gen. Plant Pathol. 75:110-118. https://doi.org/10.1007/s10327-009-0153-5
  12. Kim, H.-K., Cho, E. J., Lee, S., Lee, Y.-S. and Yun, S.-H. 2012. Functional analyses of individual mating-type transcripts at MAT loci in Fusarium graminearum and Fusarium asiaticum. FEMS Microbiol Lett. 337:89-96. https://doi.org/10.1111/1574-6968.12012
  13. Kim, J. E., Han, K. H., Jin, J., Kim, H., Kim, J. C., Yun, S.-H. and Lee, Y.-W. 2005. Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl. Environ. Microbiol. 71:1701-1708. https://doi.org/10.1128/AEM.71.4.1701-1708.2005
  14. Kim, H.-K. and Yun, S.-H. 2011. Evaluation of potential reference genes for quantitative RT-PCR analysis in Fusarium graminearum under different culture conditions. Plant Pathol. J. 27: 301-309. https://doi.org/10.5423/PPJ.2011.27.4.301
  15. Kimura, M., Tokai, T., O'Donnell, K., Ward, T. J., Fujimura, M., Hamamoto, H., Shibata, T. and Yamaguchi, I. 2003. The trichothecene biosynthesis gene cluster of Fusarium greminearum F15 contains a limited number of essential pathway genes and expressed non-essential genes. FEBS Lett. 539:105-110. https://doi.org/10.1016/S0014-5793(03)00208-4
  16. Kimura, M., Tokai, Takahashi-Ando, N., Ohsato, S. and Fujimura, M. 2007. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci. Biotechnol. Biochem. 71:2105-2123. https://doi.org/10.1271/bbb.70183
  17. Lee, J., Chang, I. Y., 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
  18. 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
  19. Lee, T., Lee, S.-H., Lee, S.-H., Shin, J. Y., Yun, J.-C., Lee, Y.-W. and Ryu, J.-G. 2011. Occurrence of Fusarium mycotoxins in rice and its milling by-products in Korea. J. Food Prot. 74:1169-1174. https://doi.org/10.4315/0362-028X.JFP-10-564
  20. Lee, T., Oh, D.-W., Kim, H.-S., Lee, J., Kim, Y.-H., Yun, S.-H. and Lee, Y.-W. 2001. Identification of deoxynivalenol- and nivalenol-producing chemotypes of Gibberella zeae by using PCR. Appl. Environ. Microbiol. 67:2966-2972. https://doi.org/10.1128/AEM.67.7.2966-2972.2001
  21. Leslie, J. F. and Summerell, B. A. 2006. The Fusarium laboratory manual. Blackwell Publishing Professional, Ames, Iowa, U.S.A. 388 pp.
  22. Merhej, J., Boutigny, A. L., Pinson-Gadais, L., Richard-Forget, F. and Barreau, C. 2010. Acidic pH as a determinant of TRI gene expression and trichothecene B biosynthesis in Fusarium graminearum. Food Addit. Contam. 27:710-717. https://doi.org/10.1080/19440040903514531
  23. Mule, G., Logrieco, A., Stea, G. and Bottalico, A. 1997. Clustering of trichothecene-producing strains determined from 28S ribosomal DNA sequences. Appl. Environ. Microbiol. 63:1843-1846.
  24. O'Donnell, K., Kistler, H. C., Tacke, B. K. and Casper, H. H. 2000. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc. Natl. Acad. Sci. USA 97:7905-7910. https://doi.org/10.1073/pnas.130193297
  25. Pasquali, M., Giraud, F., Brochot, C., Cocco, E., Hoffmann, L. and Bohn, T. 2010. Genetic Fusarium chemotyping as a useful tool for predicting nivalenol contamination in winter wheat. Int. J. Food Microbiol. 137:246-253. https://doi.org/10.1016/j.ijfoodmicro.2009.11.009
  26. Peplow, A. W., Tag, A. G., Garifullina, G. F. and Beremand, M. N. 2003. Identification of new genes positively regulated by Tri10 and a regulatory network for trichothecene mycotoxin production. App. Environ. Microbiol. 69: 2731-2736. https://doi.org/10.1128/AEM.69.5.2731-2736.2003
  27. Sambrook, J. and Russell, D. W. 2001. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York.
  28. Sobrova, P., Adam, V., Vasatkova, A., Beklova, M., Zeman, L. and Kizek, R. 2010. Deoxynivalenol and its toxicity. Interdisciplinary Toxicol. 3:94-99.
  29. Trail, F. and Common, R. 2000. Perithecial development by Gibberella zeae: a light microscopy study. Mycologia 92:130-138. https://doi.org/10.2307/3761457
  30. Wang, J.-H., Ndoye, M., Zhang, J.-B., Li, H.-P. and Liao, Y.-C. 2011. Population structure and genetic diversity of the Fusarium graminearum species complex. Toxins 3:1020-1037. https://doi.org/10.3390/toxins3081020
  31. Yli-Mattila, T. 2011. Detection of trichothecene-producing Fusarium species in cereals in Northern Europe and Asia. Agron. Res. 9:521-526.
  32. Zhang, J.-B., Li, H.-P., Dang, F.-J., Qu, B., Xu, Y.-B., Zhao, C.- S. and Liao, Y.-C. 2007. Determination of the trichothecene mycotoxin chemotypes and associated geographical distribution and phylogenetic species of the Fusarium graminearum clade from China. Mycol. Res. 111:967-975. https://doi.org/10.1016/j.mycres.2007.06.008

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