1887

Abstract

, which causes the globally important head blight disease of wheat, is responsible for the production of the harmful mycotoxin deoxynivalenol (DON) in infected grain. The production of DON by occurs at much higher levels during infection than during axenic growth, and it is therefore important to understand how DON production is regulated in the fungus. Recently, we have identified amines as potent inducers of DON production in . Although amines strongly induced expression of the key DON biosynthesis gene and DON production to levels equivalent to those observed during infection, the timing of this induction suggested that other factors are also likely to be important for the regulation of DON biosynthesis. Here we demonstrate that low extracellular pH both promotes and is required for DON production in . A combination of low pH and amines results in significantly enhanced expression of the gene and increased DON production during axenic growth. A better understanding of DON production in would have implications in developing future toxin management strategies.

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2009-09-01
2024-03-28
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References

  1. Aleandri M. P., Magro P., Chilosi G. 2007; Modulation of host pH during the wheat– Fusarium culmorum interaction and its influence on the production and activity of pectolytic enzymes. Plant Pathol 56:517–525
    [Google Scholar]
  2. Alkan N., Fluhr R., Sherman A., Prusky D. 2008; Role of ammonia secretion and pH modulation on pathogenicity of Colletotrichum coccodes on tomato fruit. Mol Plant Microbe Interact 21:1058–1066
    [Google Scholar]
  3. Anonymous. 2005; Commission Regulation (EC) no. 856/2005 of 6 June 2005 amending Regulation (EC) no. 466/2001 as regards Fusarium toxins. Official Journal of the European Union L143:3–8
    [Google Scholar]
  4. Bagar T., Altenbach K., Read N. D., Bencina M. 2009; Live-cell imaging and measurement of intracellular pH in filamentous fungi using a genetically encoded ratiometric probe. Eukaryot Cell 8:703–712
    [Google Scholar]
  5. Bai G. H., Desjardins A. E., Plattner R. D. 2002; Deoxynivalenol non-producing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91–98
    [Google Scholar]
  6. Bluhm B. H., Woloshuk C. P. 2005; Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels. Mol Plant Microbe Interact 18:1333–1339
    [Google Scholar]
  7. Boddu J., Cho S., Kruger W. M., Muehlbauer G. J. 2006; Transcriptome analysis of the barley– Fusarium graminearum interaction. Mol Plant Microbe Interact 19:407–417
    [Google Scholar]
  8. Boutigny A.-L., Richard-Forget F., Barreau C. 2008; Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. Eur J Plant Pathol 121:411–423
    [Google Scholar]
  9. Espeso E. A., Arst H. N. Jr 2000; On the mechanism by which alkaline pH prevents expression of an acid-expressed gene. Mol Cell Biol 20:3355–3363
    [Google Scholar]
  10. Flaherty J. E., Pirttila A. M., Bluhm B. H., Woloshuk C. P. 2003; PAC1, a pH-regulatory gene from Fusarium verticillioides . Appl Environ Microbiol 69:5222–5227
    [Google Scholar]
  11. Gardiner D. M., Kazan K., Manners J. M. 2009; Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum . Fungal Genet Biol 46:604–613
    [Google Scholar]
  12. Goswami R. S., Kistler H. C. 2004; Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525
    [Google Scholar]
  13. Hadas Y., Goldberg I., Pines O., Prusky D. 2007; Involvement of gluconic acid and glucose oxidase in the pathogenicity of Penicillium expansum in apples. Phytopathology 97:384–390
    [Google Scholar]
  14. Jansen C., von Wettstein D., Schafer W., Kogel K.-H., Felk A., Maier F. J. 2005; Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum . Proc Natl Acad Sci U S A 102:16892–16897
    [Google Scholar]
  15. Jernejc K., Legiša M. 2001; Activation of plasma membrane H+-ATPase by ammonium ions in Aspergillus niger . Appl Microbiol Biotechnol 57:368–373
    [Google Scholar]
  16. Jiao F., Kawakami A., 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
    [Google Scholar]
  17. Kachholz T., Demain A. L. 1983; Nitrate repression of averufin and aflatoxin biosynthesis. J Nat Prod 46:499–506
    [Google Scholar]
  18. Keller N. P., Nesbitt C., Sarr B., Phillips T. D., Burow G. B. 1997a; pH regulation of sterigmatocystin and aflatoxin biosynthesis in Aspergillus spp. Phytopathology 87:643–648
    [Google Scholar]
  19. Keller S. E., Sullivan T. M., Chirtel S. 1997b; Factors affecting the growth of Fusarium proliferatum and the production of fumonisin B1: oxygen and pH. J Ind Microbiol Biotechnol 19:305–309
    [Google Scholar]
  20. Kim K. S., Min J.-Y., Dickman M. B. 2008; Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant Microbe Interact 21:605–612
    [Google Scholar]
  21. Marcé M., Brown D. S., Capell T., Figueras X., Tiburcio A. F. 1995; Rapid high-performance liquid chromatographic method for the quantitation of polyamines as their dansyl derivatives: application to plant and animal tissues. J Chromatogr B Biomed Appl 666:329–335
    [Google Scholar]
  22. Miller J. D., Taylor A., Greenhalgh R. 1983; Production of deoxynivalenol and related compounds in liquid culture by Fusarium graminearum . Can J Microbiol 29:1171–1178
    [Google Scholar]
  23. Morton A. G., Macmillan A. 1954; The assimilation of nitrogen from ammonium salts and nitrate by fungi. J Exp Bot 5:232–252
    [Google Scholar]
  24. Mudge A. M., Dill-Macky R., Dong Y., Gardiner D. M., White R. G., Manners J. M. 2006; A role for the mycotoxin deoxynivalenol in stem colonisation during crown rot disease of wheat caused by Fusarium graminearum and Fusarium pseudograminearum . Physiol Mol Plant Pathol 69:73–85
    [Google Scholar]
  25. O'Callaghan J., Stapleton P. C., Dobson A. D. W. 2006; Ochratoxin A biosynthetic genes in Aspergillus ochraceus are differentially regulated by pH and nutritional stimuli. Fungal Genet Biol 43:213–221
    [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
    [Google Scholar]
  27. Peñalva M. A., Tilburn J., Bignell E., Arst H. N. Jr 2008; Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16:291–300
    [Google Scholar]
  28. 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
    [Google Scholar]
  29. Ponts N., Pinson-Gadais L., Verdal-Bonnin M. N., 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
    [Google Scholar]
  30. Proctor R. H., Hohn T. M., McCormick S. P. 1995; Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8:593–601
    [Google Scholar]
  31. Shah A. J., Tilburn J., Adlard M. W., Arst H. N. Jr 1991; pH regulation of penicillin production in Aspergillus nidulans . FEMS Microbiol Lett 61:209–212
    [Google Scholar]
  32. Tilburn J., Sarkar S., Widdick D. A., Espeso E. A., Orejas M., Mungroo J., Penalva M. A., Arst H. N. Jr 1995; The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J 14:779–790
    [Google Scholar]
  33. Tsitsigiannis D. I., Keller N. P. 2006; Oxylipins act as determinants of natural product biosynthesis and seed colonization in Aspergillus nidulans . Mol Microbiol 59:882–892
    [Google Scholar]
  34. Williamson B., Tudzynski B., Tudzynski P., Van Kan J. A. L. 2007; Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580
    [Google Scholar]
  35. Woloshuk C. P., Cavaletto J. R., Cleveland T. E. 1997; Inducers of aflatoxin biosynthesis from colonized maize kernels are generated by an amylase activity from Aspergillus flavus . Phytopathology 87:164–169
    [Google Scholar]
  36. Yu J. H., Keller N. 2005; Regulation of secondary metabolism in filamentous fungi. Annu Rev Phytopathol 43:437–458
    [Google Scholar]
  37. Yu Q., Tang C., Kuo J. 2000; A critical review on methods to measure apoplastic pH in plants. Plant Soil 219:29–40
    [Google Scholar]
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