l-Threonine and its analogue added to autoclaved solid medium suppress trichothecene production by Fusarium graminearum

Abstract

Fusarium graminearum produces trichothecene mycotoxins under certain nutritional conditions. When l-Thr and its analogue l-allo-threonine were added to brown rice flour solid medium before inoculation, trichothecene production after 4 days of incubation was suppressed. A time-course analysis of gene expression demonstrated that l-Thr suppressed transcription of Tri6, a trichothecene master regulator gene, and a terpene cyclase Tri5 gene. Regulation of trichothecene biosynthesis by altering major primary metabolic processes may open up the possibility to develop safe chemicals for the reduction of mycotoxin contamination might be developed.

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References

  1. Aristimuño Ficoseco ME, Vattuone MA, Audenaert K, Catalan CA, Sampietro DA (2014) Antifungal and antimycotoxigenic metabolites in Anacardiaceae species from northwest Argentina: isolation, identification and potential for control of Fusarium species. J Appl Microbiol 116:1262–1273. doi:10.1111/jam.12436

    Article  PubMed  Google Scholar 

  2. Bai GH, Desjardins AE, Plattner RD (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 91–98. doi:10.1023/A:1014419323550

    PubMed  Google Scholar 

  3. Boutigny AL, Barreau C, Atanasova-Penichon V, Verdal-Bonnin MN, Pinson-Gadais L, Richard-Forget F (2009) Ferulic acid, an efficient inhibitor of type B trichothecene biosynthesis and Tri gene expression in Fusarium liquid cultures. Mycol Res 113:746–753. doi:10.1016/j.mycres.2009.02.010

    CAS  Article  PubMed  Google Scholar 

  4. Boutigny AL, Atanasova-Penichon V, Benet M, Barreau C, Richard-Forget F (2010) Natural phenolic acids from wheat bran inhibit Fusarium culmorum trichothecene biosynthesis in vitro by repressing Tri gene expression. Eur J Plant Pathol 127:275–286. doi:10.1007/S10658-010-9592-2

    CAS  Article  Google Scholar 

  5. Desjardins AE (2009) From yellow rain to green wheat: 25 years of trichothecene biosynthesis research. J Agric Food Chem 57:4478–4484. doi:10.1021/jf9003847

    CAS  Article  PubMed  Google Scholar 

  6. Desjardins AE, Plattner RD, Beremand MN (1987) Ancymidol blocks trichothecene biosynthesis and leads to accumulation of trichodiene in Fusarium sporotrichioides and Gibberella pulicaris. Appl Environ Microbiol 53:1860–1865

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Desjardins AE, Plattner RD, Spencer GF (1988) Inhibition of trichothecene toxin biosynthesis by naturally occurring shikimate aromatics. Phytochemistry 27:767–771

    CAS  Article  Google Scholar 

  8. Edgar AJ (2005) Mice have a transcribed l-threonine aldolase/GLY1 gene, but the human GLY1 gene is a non-processed pseudogene. BMC Genomics 6:32. doi:10.1186/1471-2164-6-32

    Article  PubMed  PubMed Central  Google Scholar 

  9. Etzerodt T, Maeda K, Nakajima Y, Laursen B, Fomsgaard IS, Kimura M (2015) 2,4-Dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA) inhibits trichothecene production by Fusarium graminearum through suppression of Tri6 expression. Int J Food Microbiol 214:123–128. doi:10.1016/j.ijfoodmicro.2015.07.014

    CAS  Article  PubMed  Google Scholar 

  10. Faltusová Z, Chrpová J, Salačová L, Džuman Z, Pavel J, Zachariášová M, Hajšlová J, Ovesná J (2015) Effect of Fusarium culmorum Tri gene transcription on deoxynivalenol and D3G levels in two different barley cultivars. J Phytopathol 163:593–603. doi:10.1111/jph.12359

    Article  Google Scholar 

  11. Giese H, Sondergaard TE, Sorensen JL (2013) The AreA transcription factor in Fusarium graminearum regulates the use of some nonpreferred nitrogen sources and secondary metabolite production. Fungal Biol 117:814–821. doi:10.1016/j.funbio.2013.10.006

    CAS  Article  PubMed  Google Scholar 

  12. Hohn TM, Beremand PD (1989) Isolation and nucleotide sequence of a sesquiterpene cyclase gene from the trichothecene-producing fungus Fusarium sporotrichioides. Gene 79:131–138

    CAS  Article  PubMed  Google Scholar 

  13. Kim HK, Yun SH (2011) Evaluation of potential reference genes for quantitative RT-PCR analysis in Fusarium graminearum under different culture conditions. Plant Pathol J 27:301–309. doi:10.5423/Ppj.2011.27.4.301

    CAS  Article  Google Scholar 

  14. Kimura M, Takahashi-Ando N, Nishiuchi T, Ohsato S, Tokai T, Ochial N, Fujimura M, Kudo T, Hamamoto H, Yamaguchi I (2006) Molecular biology and biotechnology for reduction of Fusarium mycotoxin contamination. Pestic Biochem Physiol 86:117–123. doi:10.1016/j.pestbp.2006.02.008

    CAS  Article  Google Scholar 

  15. Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M (2007) Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 71:2105–2123. doi:10.1271/bbb.70183

    CAS  Article  PubMed  Google Scholar 

  16. Kulik T, Busko M, Pszczolkowska A, Perkowski J, Okorski A (2014) Plant lignans inhibit growth and trichothecene biosynthesis in Fusarium graminearum. Lett Appl Microbiol 59:99–107. doi:10.1111/lam.12250

    CAS  Article  PubMed  Google Scholar 

  17. Maeda K, Nakajima Y, Motoyama T, Kitou Y, Kosaki T, Saito T, Nishiuchi T, Kanamaru K, Osada H, Kobayashi T, Kimura M (2014) Effects of acivicin on growth, mycotoxin production and virulence of phytopathogenic fungi. Lett Appl Microbiol 59:377–383. doi:10.1111/lam.12289

    CAS  Article  PubMed  Google Scholar 

  18. Maeda K, Nakajima Y, Tanahashi K, Kosaki T, Kitou Y, Kanamaru K, Kobayashi T, Nishiuchi T, Kimura M (2016) Characterization of the acivicin effects on trichothecene production by Fusarium graminearum species complex. J Gen Appl Microbiol 62:272-276. doi:10.2323/jgam.2016.04.002

    CAS  Article  PubMed  Google Scholar 

  19. McCormick SP, Stanley AM, Stover NA, Alexander NJ (2011) Trichothecenes: from simple to complex mycotoxins. Toxins 3:802–814. doi:10.3390/toxins3070802

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Merhej J, Richard-Forget F, Barreau C (2011) Regulation of trichothecene biosynthesis in Fusarium: recent advances and new insights. Appl Microbiol Biotechnol 91:519–528. doi:10.1007/s00253-011-3397-x

    CAS  Article  PubMed  Google Scholar 

  21. Min K, Shin Y, Son H, Lee J, Kim JC, Choi GJ, Lee YW (2012) Functional analyses of the nitrogen regulatory gene areA in Gibberella zeae. FEMS Microbiol Lett 334:66–73. doi:10.1111/j.1574-6968.2012.02620.x

    CAS  Article  PubMed  Google Scholar 

  22. Nakajima Y, Tokai T, Maeda K, Tanaka A, Takahashi-Ando N, Kanamaru K, Kobayashi T, Kimura M (2014) A set of heterologous promoters useful for investigating gene functions in Fusarium graminearum. JSM Mycotoxins 64:147–152. doi:10.2520/myco.64.147

    Article  Google Scholar 

  23. Nakajima Y, Maeda K, Jin Q, Takahashi-Ando N, Kanamaru K, Kobayashi T, Kimura M (2016) Oligosaccharides containing an α-(1→2) (glucosyl/xylosyl)-fructosyl linkage as inducer molecules of trichothecene biosynthesis for Fusarium graminearum. Int J Food Microbiol 238:215-221. doi:10.1016/j.ijfoodmicro.2016.09.011

    CAS  Article  PubMed  Google Scholar 

  24. Nelson DL, Cox MN (2008) Lehninger principles of biochemistry, 5 edn. Freeman, New York, NY, USA

    Google Scholar 

  25. Nishiuchi T, Masuda D, Nakashita H, Ichimura K, Shinozaki K, Yoshida S, Kimura M, Yamaguchi I, Yamaguchi K (2006) Fusarium phytotoxin trichothecenes have an elicitor-like activity in Arabidopsis thaliana, but the activity differed significantly among their molecular species. Mol Plant Microbe Interact 19:512–520. doi:10.1094/MPMI-19-0512

    CAS  Article  PubMed  Google Scholar 

  26. Ochiai N, Tokai T, Takahashi-Ando N, Fujimura M, Kimura M (2007) Genetically engineered Fusarium as a tool to evaluate the effects of environmental factors on initiation of trichothecene biosynthesis. FEMS Microbiol Lett 275:53–61. doi:10.1111/j.1574-6968.2007.00869.x

    CAS  Article  PubMed  Google Scholar 

  27. Ohno M, Tsuda K, Sakaguchi M, Sugahara Y, Oyama F (2012) Chitinase mRNA levels by quantitative PCR using the single standard DNA: acidic mammalian chitinase is a major transcript in the mouse stomach. PLoS One 7:e50381. doi:10.1371/journal.pone.0050381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Pagnussatt FA, Del Ponte EM, Garda-Buffon J, Badiale-Furlong E (2014) Inhibition of Fusarium graminearum growth and mycotoxin production by phenolic extract from Spirulina sp. Pestic Biochem Physiol 108:21–26. doi:10.1016/j.pestbp.2013.11.002

    CAS  Article  Google Scholar 

  29. Pani G, Scherm B, Azara E, Balmas V, Jahanshiri Z, Carta P, Fabbri D, Dettori MA, Fadda A, Dessi A, Dallocchio R, Migheli Q, Delogu G (2014) Natural and natural-like phenolic inhibitors of type B trichothecene in vitro production by the wheat (Triticum sp.) pathogen Fusarium culmorum. J Agric Food Chem 62:4969–4978. doi:10.1021/jf500647h

    CAS  Article  PubMed  Google Scholar 

  30. Pinson-Gadais L, Richard-Forget F, Frasse P, Barreau C, Cahagnier B, Richard-Molard D, Bakan B (2008) Magnesium represses trichothecene biosynthesis and modulates Tri5, Tri6, and Tri12 genes expression in Fusarium graminearum. Mycopathologia 165:51–59. doi:10.1007/s11046-007-9076-x

    CAS  Article  PubMed  Google Scholar 

  31. Ponts N, Pinson-Gadais L, Verdal-Bonnin MN, Barreau C, Richard-Forget F (2006) Accumulation of deoxynivalenol and its 15-acetylated form is significantly modulated by oxidative stress in liquid cultures of Fusarium graminearum. FEMS Microbiol Lett 258:102–107. doi:10.1111/j.1574-6968.2006.00200.x

    CAS  Article  PubMed  Google Scholar 

  32. Ponts N, Pinson-Gadais L, Boutigny AL, Barreau C, Richard-Forget F (2011) Cinnamic-derived acids significantly affect Fusarium graminearum growth and in vitro synthesis of type B trichothecenes. Phytopathology 101:929–934. doi:10.1094/Phyto-09-10-0230

    CAS  Article  PubMed  Google Scholar 

  33. Proctor RH, Hohn TM, McCormick SP, Desjardins AE (1995) Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl Environ Microbiol 61:1923–1930

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Ravagnani A, Gorfinkiel L, Langdon T, Diallinas G, Adjadj E, Demais S, Gorton D, Arst HN Jr, Scazzocchio C (1997) Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter-specific recognition by the Aspergillus nidulans GATA factor AreA. EMBO J 16:3974–3986. doi:10.1093/emboj/16.13.3974

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Sakuda S, Yoshinari T, Furukawa T, Jermnak U, Takagi K, Iimura K, Yamamoto T, Suzuki M, Nagasawa H (2016) Search for aflatoxin and trichothecene production inhibitors and analysis of their modes of action. Biosci Biotechnol Biochem 80:43–54. doi:10.1080/09168451.2015.1086261

    CAS  Google Scholar 

  36. Shyh-Chang N, Locasale JW, Lyssiotis CA, Zheng Y, Teo RY, Ratanasirintrawoot S, Zhang J, Onder T, Unternaehrer JJ, Zhu H, Asara JM, Daley GQ, Cantley LC (2013) Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 339:222–226. doi:10.1126/science.1226603

    Article  PubMed  Google Scholar 

  37. Son H, Lee Y-W (2012) Fusarium graminearum mycotoxins and their biosynthetic genes. Mycotoxins 62:29–40. doi:10.2520/myco.62.29

    CAS  Article  Google Scholar 

  38. Sugita-Konishi Y (2008) Toxicity and control of trichothecene mycotoxins. Mycotoxins 58:23–28. doi:10.2520/myco.58.23

    CAS  Article  Google Scholar 

  39. Takahashi-Ando N, Ochiai N, Tokai T, Ohsato S, Nishiuchi T, Yoshida M, Fujimura M, Kimura M (2008a) A screening system for inhibitors of trichothecene biosynthesis: hydroxylation of trichodiene as a target. Biotechnol Lett 30:1055–1059. doi:10.1007/s10529-008-9649-x

    CAS  Article  PubMed  Google Scholar 

  40. Takahashi-Ando N, Tokai T, Yoshida M, Fujimura M, Kimura M (2008b) An easy method to identify 8-keto-15-hydroxytrichothecenes by thin-layer chromatography. Mycotoxins 58:115–117. doi:10.2520/myco.58.115

    CAS  Article  Google Scholar 

  41. Todd RB, Fraser JA, Wong KH, Davis MA, Hynes MJ (2005) Nuclear accumulation of the GATA factor AreA in response to complete nitrogen starvation by regulation of nuclear export. Eukaryot Cell 4:1646–1653. doi:10.1128/EC.4.10.1646-1653.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Wang J, Alexander P, Wu L, Hammer R, Cleaver O, McKnight SL (2009) Dependence of mouse embryonic stem cells on threonine catabolism. Science 325:435–439. doi:10.1126/science.1173288

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Whittaker MM, Whittaker JW (2001) Catalytic reaction profile for alcohol oxidation by galactose oxidase. Biochemistry 40:7140–7148

    CAS  Article  PubMed  Google Scholar 

  44. Yaguchi A, Yoshinari T, Tsuyuki R, Takahashi H, Nakajima T, Sugita-Konishi Y, Nagasawa H, Sakuda S (2009) Isolation and identification of precocenes and piperitone from essential oils as specific inhibitors of trichothecene production by Fusarium graminearum. J Agric Food Chem 57:846–851. doi:10.1021/jf802813h

    CAS  Article  PubMed  Google Scholar 

  45. Yin DT, Urresti S, Lafond M, Johnston EM, Derikvand F, Ciano L, Berrin JG, Henrissat B, Walton PH, Davies GJ, Brumer H (2015) Structure-function characterization reveals new catalytic diversity in the galactose oxidase and glyoxal oxidase family. Nat Commun 6:10197. doi:10.1038/ncomms10197

    CAS  Article  PubMed  Google Scholar 

  46. Yoshizawa T (2013) Thirty-five years of research on deoxynivalenol, a trichothecene mycotoxin: with special reference to its discovery and co-occurrence with nivalenol in Japan. Food Saf 1. doi:10.14252/foodsafetyfscj.2013002

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Acknowledgements

This work was supported by Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry.

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Correspondence to Makoto Kimura.

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Kazuyuki Maeda and Yuichi Nakajima contributed equally to this work.

Communicated by Erko Stackebrandt.

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Maeda, K., Nakajima, Y., Tanahashi, Y. et al. l-Threonine and its analogue added to autoclaved solid medium suppress trichothecene production by Fusarium graminearum . Arch Microbiol 199, 945–952 (2017). https://doi.org/10.1007/s00203-017-1364-3

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Keywords

  • Amino acids
  • Fusarium graminearum
  • Mycotoxin production inhibitor
  • Nitrogen source
  • Tri gene expression