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Fusarium Mycotoxins and Their Role in Plant–Pathogen Interactions

  • Gerhard Adam
  • Gerlinde Wiesenberger
  • Ulrich GüldenerEmail author
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Many plant pathogenic fungi produce secondary metabolites, which received scientific attention as mycotoxins due to their toxicity for humans and animals and their occurrence in infected plant material at relevant concentrations. According to the available fungal genome sequences, fungi seem to have the biosynthetic capacity to produce in planta a number of still largely unknown compounds in addition to the so far identified mycotoxins. In this review we summarize information about the role of known mycotoxins and other secondary metabolites in the virulence of Fusarium graminearum and other important mycotoxin producing Fusarium species. Only a few cases of functional testing by gene disruption resulted in clear-cut results about the role of mycotoxins in virulence, most experiments rather point to quantitative contributions. This is probably not only due to the functional redundancy of metabolites and other effectors but also due to largely neglected responses of plants. In this review an attempt is made to integrate fungal secondary metabolites, considered to be small molecule effectors, into the current picture of plant–pathogen interaction by adding another layer into the ZIG-ZAG model. Accordingly, secondary metabolites act as suppressors of effector (protein)-triggered immunity, but plants can regain resistance by antagonizing small molecule effectors. This response is dynamic and is caused by the multilayer action of proteins encoded by large gene families, explaining the quantitative nature of the resulting interaction.

Keywords

Mycotoxins Fusarium Fusarium graminearum Virulence Trichothecenes Deoxynivalenol T-2 toxin Eukaryotic protein synthesis Zearalenone Resorcylic acid lactones Fumonisins Ceramide biosynthesis Aggressiveness Nonribosomal peptide synthetase (NRPS) Pathogen-associated molecular pattern (PAMP) Siderophore 

References

  1. 1.
    Jorgensen K (2005) Occurrence of ochratoxin A in commodities and processed food—a review of EU occurrence data. Food Addit Contam 22(Suppl 1):26–30PubMedGoogle Scholar
  2. 2.
    EFSA Panel on Contaminants in the Food Chain (CONTAM) (2004) Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to deoxynivalenol (DON) as undesirable substance in animal feed. EFSA J 73:1–42Google Scholar
  3. 3.
    EFSA Panel on Contaminants in the Food Chain (CONTAM) (2005) Opinion of the scientific panel on contaminants in food chain on a request from the commission related to fumonisins as undesirable substances in animal feed. EFSA J 235:1–32Google Scholar
  4. 4.
    EFSA Panel on Contaminants in the Food Chain (CONTAM) (2011) Scientific opinion on the risks for public health related to the presence of zearalenone in food. EFSA J 9(6):1–124Google Scholar
  5. 5.
    Rohlfs M, Churchill AC (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48(1):23–34PubMedGoogle Scholar
  6. 6.
    Mobius N, Hertweck C (2009) Fungal phytotoxins as mediators of virulence. Curr Opin Plant Biol 12(4):390–398PubMedGoogle Scholar
  7. 7.
    Yoder O (1980) Toxins in pathogenesis. Annu Rev Phytopathol 18:103–129Google Scholar
  8. 8.
    Graniti A (1991) Phytotoxins and their involvement in plant diseases (Introduction). Experientia 47(8):751–755Google Scholar
  9. 9.
    Gilbert J, Abramson D, McCallum B, Clear R (2002) Comparison of canadian Fusarium graminearum isolates for aggressiveness, vegetative compatibility, and production of ergosterol and mycotoxins. Mycopathologia 153(4):209–215PubMedGoogle Scholar
  10. 10.
    Walton JD, Panaccione DG (1993) Host-selective toxins and disease specificity: perspectives and progress. Annu Rev Phytopathol 31:275–303PubMedGoogle Scholar
  11. 11.
    Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y et al (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37(1):44–66PubMedGoogle Scholar
  12. 12.
    Panaccione DG, Scott-Craig JS, Pocard JA, Walton JD (1992) A cyclic peptide synthetase gene required for pathogenicity of the fungus Cochliobolus carbonum on maize. Proc Natl Acad Sci U S A 89(14):6590–6594PubMedCentralPubMedGoogle Scholar
  13. 13.
    Johal GS, Briggs SP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science (New York NY) 258(5084):985–987PubMedGoogle Scholar
  14. 14.
    Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M’barek S, Gohari AM et al (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 35(3):542–554PubMedGoogle Scholar
  15. 15.
    Turgeon BG, Baker SE (2007) Genetic and genomic dissection of the Cochliobolus heterostrophus Tox1 locus controlling biosynthesis of the polyketide virulence factor T-toxin. Adv Genet 57:219–261PubMedGoogle Scholar
  16. 16.
    Multani DS, Meeley RB, Paterson AH, Gray J, Briggs SP, Johal GS (1998) Plant-pathogen microevolution: molecular basis for the origin of a fungal disease in maize. Proc Natl Acad Sci U S A 95(4):1686–1691PubMedCentralPubMedGoogle Scholar
  17. 17.
    Sindhu A, Chintamanani S, Brandt AS, Zanis M, Scofield SR, Johal GS (2008) A guardian of grasses: specific origin and conservation of a unique disease-resistance gene in the grass lineage. Proc Natl Acad Sci U S A 105(5):1762–1767PubMedCentralPubMedGoogle Scholar
  18. 18.
    Brar HK, Swaminathan S, Bhattacharyya MK (2011) The Fusarium virguliforme toxin FvTox1 causes foliar sudden death syndrome-like symptoms in soybean. Mol Plant Microbe Interact 24(10):1179–1188PubMedGoogle Scholar
  19. 19.
    Buerstmayr H, Ban T, Anderson JA (2009) Qtl mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breed 128(1):1–26Google Scholar
  20. 20.
    Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11(8):539–548. ([10.1038/nrg2812]. 2010 08//print)PubMedGoogle Scholar
  21. 21.
    Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406PubMedGoogle Scholar
  22. 22.
    Granado J, Felix G, Boller T (1995) Perception of fungal sterols in plants (subnanomolar concentrations of ergosterol elicit extracellular alkalinization in tomato cells). Plant Physiol 107(2):485–490PubMedCentralPubMedGoogle Scholar
  23. 23.
    Tugizimana F, Steenkamp PA, Piater LA, Dubery IA (2014) Multi-platform metabolomic analyses of ergosterol-induced dynamic changes in Nicotiana tabacum cells. PloS ONE 9(1):e87846PubMedCentralPubMedGoogle Scholar
  24. 24.
    Haas H, Eisendle M, Turgeon BG (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46:149–187PubMedGoogle Scholar
  25. 25.
    Haselwandter K, Winkelmann G (2007) Siderophores of symbiotic fungi. In: Varma A, Chincholkar S (eds) Microbial siderophores. Springer, Berlin, pp 91–104Google Scholar
  26. 26.
    Emery T (1980) Malonichrome, a new iron chelate from Fusarium roseum. Biochim Biophys Acta 629(2):382–390PubMedGoogle Scholar
  27. 27.
    Oide S, Berthiller F, Wiesenberger G, Adam G, Turgeon BG (2014) Individual and combined roles of malonichrome, ferricrocin, and TAFC siderophores in Fusarium graminearum pathogenic and sexual development. Front Microbiol 5:759. http://www.ncbi.nlm.nih.gov/pubmed/25628608.Google Scholar
  28. 28.
    Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, Martinez-Rocha AL et al (2013) Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat Commun 4:1996PubMedCentralPubMedGoogle Scholar
  29. 29.
    de Jonge R, Bolton MD, Thomma BP (2011) How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr Opin Plant Biol 14(4):400–406PubMedGoogle Scholar
  30. 30.
    Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A et al (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142(2):284–295PubMedGoogle Scholar
  31. 31.
    Wawra S, Djamei A, Albert I, Nurnberger T, Kahmann R, van West P (2013) In vitro translocation experiments with RxLR-reporter fusion proteins of Avr1b from Phytophthora sojae and AVR3a from Phytophthora infestans fail to demonstrate specific autonomous uptake in plant and animal cells. Mol Plant Microbe Interact 26(5):528–536PubMedGoogle Scholar
  32. 32.
    Tyler BM, Kale SD, Wang Q, Tao K, Clark HR, Drews K et al (2013) Microbe-independent entry of oomycete RxLR effectors and fungal RxLR-like effectors into plant and animal cells is specific and reproducible. Mol Plant Microbe Interact 26(6):611–616PubMedCentralPubMedGoogle Scholar
  33. 33.
    Nimchuk Z, Rohmer L, Chang JH, Dangl JL (2001) Knowing the dancer from the dance: R-gene products and their interactions with other proteins from host and pathogen. Curr Opin Plant Biol 4(4):288–294PubMedGoogle Scholar
  34. 34.
    Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61PubMedGoogle Scholar
  35. 35.
    Tan S, Wu S (2012) Genome wide analysis of nucleotide-binding site disease resistance genes in Brachypodium distachyon. Comp Funct Genomics 2012:418208PubMedCentralPubMedGoogle Scholar
  36. 36.
    van der Hoorn RA, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20(8):2009–2017PubMedCentralPubMedGoogle Scholar
  37. 37.
    Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I et al (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science (New York) 342(6154):118–123PubMedCentralPubMedGoogle Scholar
  38. 38.
    Stower H (2013) Small RNAs: RNAs attack! Nat Rev Genet 14(11):748–749PubMedGoogle Scholar
  39. 39.
    Geng X, Cheng J, Gangadharan A, Mackey D (2012) The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense. Plant Cell 24(11):4763–4774PubMedCentralPubMedGoogle Scholar
  40. 40.
    Dudler R (2013) Manipulation of host proteasomes as a virulence mechanism of plant pathogens. Annu Rev Phytopathol 51:521–542PubMedGoogle Scholar
  41. 41.
    Waspi U, Schweizer P, Dudler R (2001) Syringolin reprograms wheat to undergo hypersensitive cell death in a compatible interaction with powdery mildew. Plant Cell 13(1):153–161PubMedCentralPubMedGoogle Scholar
  42. 42.
    Atkinson MM, Midland SL, Sims JJ, Keen NT (1996) Syringolide 1 triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiol 112(1):297–302PubMedCentralPubMedGoogle Scholar
  43. 43.
    Bohnert HU, Fudal I, Dioh W, Tharreau D, Notteghem JL, Lebrun MH (2004) A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell 16(9):2499–2513PubMedCentralPubMedGoogle Scholar
  44. 44.
    Collemare J, Pianfetti M, Houlle AE, Morin D, Camborde L, Gagey MJ et al (2008) Magnaporthe grisea avirulence gene ACE1 belongs to an infection-specific gene cluster involved in secondary metabolism. New Phytol 179(1):196–208PubMedGoogle Scholar
  45. 45.
    Vergne E, Ballini E, Marques S, Sidi Mammar B, Droc G, Gaillard S et al (2007) Early and specific gene expression triggered by rice resistance gene Pi33 in response to infection by ACE1 avirulent blast fungus. New Phytol 174(1):159–171PubMedGoogle Scholar
  46. 46.
    Lorang JM, Sweat TA, Wolpert TJ (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci U S A 104(37):14861–14866PubMedCentralPubMedGoogle Scholar
  47. 47.
    Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, Tzeng SC et al (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science (New York) 338(6107):659–662PubMedCentralPubMedGoogle Scholar
  48. 48.
    Macko V, Stimmel MB, Wolpert TJ, Dunkle LD, Acklin W, Banteli R et al (1992) Structure of the host-specific toxins produced by the fungal pathogen Periconia circinata. Proc Natl Acad Sci U S A 89(20):9574–9578PubMedCentralPubMedGoogle Scholar
  49. 49.
    Nagy ED, Bennetzen JL (2008) Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res 18(12):1918–1923PubMedCentralPubMedGoogle Scholar
  50. 50.
    Serrano M, Hubert DA, Dangl JL, Schulze-Lefert P, Kombrink E (2010) A chemical screen for suppressors of the avrRpm1-RPM1-dependent hypersensitive cell death response in Arabidopsis thaliana. Planta 231(5):1013–1023PubMedCentralPubMedGoogle Scholar
  51. 51.
    Veening JW, Smits WK, Kuipers OP (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62:193–210PubMedGoogle Scholar
  52. 52.
    Connolly LR, Smith KM, Freitag M (2013) The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet 9(10):e1003916PubMedCentralPubMedGoogle Scholar
  53. 53.
    Lee H, Rustgi S, Kumar N, Burke I, Yenish JP, Gill KS et al (2011) Single nucleotide mutation in the barley acetohydroxy acid synthase (AHAS) gene confers resistance to imidazolinone herbicides. Proc Natl Acad Sci U S A 108(21):8909–8913PubMedCentralPubMedGoogle Scholar
  54. 54.
    Akamatsu H, Itoh Y, Kodama M, Otani H, Kohmoto K (1997) AAL-toxin-deficient mutants of alternaria alternata tomato pathotype by restriction enzyme-mediated integration. Phytopathology 87(9):967–972PubMedGoogle Scholar
  55. 55.
    Egusa M, Miwa T, Kaminaka H, Takano Y, Kodama M (2013) Nonhost resistance of Arabidopsis thaliana against Alternaria alternata involves both pre- and postinvasive defenses but is collapsed by AAL-toxin in the absence of LOH2. Phytopathology 103(7):733–740PubMedGoogle Scholar
  56. 56.
    Abbas HK, Duke SO, Shier WT, Riley RT, Kraus GA (1996) The chemistry and biological activities of the natural products AAL-toxin and the fumonisins. Adv Exp Med Biol 391:293–308PubMedGoogle Scholar
  57. 57.
    Desjardins AE, Proctor RH (2007) Molecular biology of Fusarium mycotoxins. Int J Food Microbiol 119(1–2):47–50PubMedGoogle Scholar
  58. 58.
    Yuan JS, Tranel PJ, Stewart CN Jr (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12(1):6–13PubMedGoogle Scholar
  59. 59.
    Remy E, Duque P (2014) Beyond cellular detoxification: a plethora of physiological roles for MDR transporter homologs in plants. Front Physiol 5:201PubMedCentralPubMedGoogle Scholar
  60. 60.
    Bowles D, Lim EK, Poppenberger B, Vaistij FE (2006) Glycosyltransferases of lipophilic small molecules. Annu Rev Plant Biol 57:567–597PubMedGoogle Scholar
  61. 61.
    Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3(3):Reviews 3004Google Scholar
  62. 62.
    Taguchi G, Ubukata T, Nozue H, Kobayashi Y, Takahi M, Yamamoto H et al (2010) Malonylation is a key reaction in the metabolism of xenobiotic phenolic glucosides in Arabidopsis and tobacco. Plant J 63(6):1031–1041PubMedGoogle Scholar
  63. 63.
    Brazier-Hicks M, Evans KM, Cunningham OD, Hodgson DR, Steel PG, Edwards R (2008) Catabolism of glutathione conjugates in Arabidopsis thaliana. Role in metabolic reactivation of the herbicide safener fenclorim. J Biol Chem 283(30):21102–21112PubMedCentralPubMedGoogle Scholar
  64. 64.
    Gaffoor I, Brown DW, Plattner R, Proctor RH, Qi W, Trail F (2005) Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 4(11):1926–1933PubMedCentralPubMedGoogle Scholar
  65. 65.
    Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, Yoshioka K et al (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18(10):2836–2853PubMedCentralPubMedGoogle Scholar
  66. 66.
    Dalmais B, Schumacher J, Moraga J, LE Pechêur P, Tudzynski B, Collado IG et al (2011) The Botrytis cinerea phytotoxin botcinic acid requires two polyketide synthases for production and has a redundant role in virulence with botrydial. Mol Plant Pathol 12(6):564–579PubMedGoogle Scholar
  67. 67.
    Tobiasen C, Aahman J, Ravnholt KS, Bjerrum MJ, Grell MN, Giese H (2007) Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet 51(1):43–58PubMedGoogle Scholar
  68. 68.
    Lysoe E, Seong KY, Kistler HC (2011) The transcriptome of Fusarium graminearum during the infection of wheat. Mol Plant Microbe Interact 24(9):995–1000PubMedGoogle Scholar
  69. 69.
    Woloshuk CP, Shim WB (2013) Aflatoxins, fumonisins, and trichothecenes: a convergence of knowledge. FEMS Microbiol Rev 37(1):94–109PubMedGoogle Scholar
  70. 70.
    Hertweck C (2009) The biosynthetic logic of polyketide diversity. Angew Chem 48(26):4688–4716. (International ed in English)Google Scholar
  71. 71.
    Hur GH, Vickery CR, Burkart MD (2012) Explorations of catalytic domains in non-ribosomal peptide synthetase enzymology. Nat Prod Rep 29(10):1074–1098PubMedGoogle Scholar
  72. 72.
    Boettger D, Hertweck C (2013) Molecular diversity sculpted by fungal PKS-NRPS hybrids. Chembiochem Eur J Chem Biol 14(1):28–42Google Scholar
  73. 73.
    Wawrzyn GT, Bloch SE, Schmidt-Dannert C (2012) Discovery and characterization of terpenoid biosynthetic pathways of fungi. Methods Enzymol 515:83–105PubMedGoogle Scholar
  74. 74.
    Steffan N, Grundmann A, Yin WB, Kremer A, Li SM (2009) Indole prenyltransferases from fungi: a new enzyme group with high potential for the production of prenylated indole derivatives. Curr Med Chem 16(2):218–231PubMedGoogle Scholar
  75. 75.
    Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH et al (2010) SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol 47(9):736–741PubMedCentralPubMedGoogle Scholar
  76. 76.
    Dionisio PM, Gurudu SR, Leighton JA, Leontiadis GI, Fleischer DE, Hara AK et al (2010) Capsule endoscopy has a significantly higher diagnostic yield in patients with suspected and established small-bowel Crohn’s disease: a meta-analysis. Am J Gastroenterol 105(6):1240–1248 (quiz 1249)PubMedGoogle Scholar
  77. 77.
    Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E et al (2013) Antismash 2.0—a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 41(Web Server issue):W204–212PubMedCentralPubMedGoogle Scholar
  78. 78.
    Fedorova ND, Moktali V, Medema MH (2012) Bioinformatics approaches and software for detection of secondary metabolic gene clusters. Methods Mol Biol 944:23–45PubMedGoogle Scholar
  79. 79.
    Wiemann P, Sieber CM, von Bargen KW, Studt L, Niehaus EM, Espino JJ et al (2013) Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog 9(6):e1003475PubMedCentralPubMedGoogle Scholar
  80. 80.
    Harris LJ, Alexander NJ, Saparno A, Blackwell B, McCormick SP, Desjardins AE et al (2007) A novel gene cluster in Fusarium graminearum contains a gene that contributes to butenolide synthesis. Fungal Genet Biol 44(4):293–306PubMedGoogle Scholar
  81. 81.
    Sieber CMK, Wong P, Münsterkötter M, Mewes H-W, Schmeitzl C, Varga E, Berthiller F, Adam G, Güldener U (2014) The Fusarium graminearum genome reveals more secondary metabolite gene clusters and hints of horizontal gene transfer. PloS ONE 9:e110311Google Scholar
  82. 82.
    Proctor RH, Butchko RA, Brown DW, Moretti A (2007) Functional characterization, sequence comparisons and distribution of a polyketide synthase gene required for perithecial pigmentation in some Fusarium species. Food Addit Contam 24(10):1076–1087PubMedGoogle Scholar
  83. 83.
    Hansen FT, Droce A, Sorensen JL, Fojan P, Giese H, Sondergaard TE (2012) Overexpression of NRPS4 leads to increased surface hydrophobicity in Fusarium graminearum. Fungal Biol 116(8):855–862PubMedGoogle Scholar
  84. 84.
    Pestka JJ (2010) Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84(9):663–679PubMedGoogle Scholar
  85. 85.
    Desmond OJ, Manners JM, Stephens AE, Maclean DJ, Schenk PM, Gardiner DM et al (2008) The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Mol Plant Pathol 9(4):435–445PubMedGoogle Scholar
  86. 86.
    Arunachalam C, Doohan FM (2013) Trichothecene toxicity in eukaryotes: cellular and molecular mechanisms in plants and animals. Toxicol Lett 217(2):149–158PubMedGoogle Scholar
  87. 87.
    Diamond M, Reape TJ, Rocha O, Doyle SM, Kacprzyk J, Doohan FM et al (2013) The Fusarium mycotoxin deoxynivalenol can inhibit plant apoptosis-like programmed cell death. PloS ONE 8(7):e69542PubMedCentralPubMedGoogle Scholar
  88. 88.
    McCormick S (2003) The role of don in pathogenicity. In: Leonhard KJ, Bushnell WR (eds) Fusarium head blight of wheat and barley. American Phytopathological Society, St. Paul, pp 165–183Google Scholar
  89. 89.
    McCormick SP, Stanley AM, Stover NA, Alexander NJ (2011) Trichothecenes: from simple to complex mycotoxins. Toxins 3(7):802–814PubMedCentralPubMedGoogle Scholar
  90. 90.
    Proctor RH, Hohn TM, McCormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8(4):593–601PubMedGoogle Scholar
  91. 91.
    Bai GH, Desjardins AE, Plattner RD (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153(2):91–98PubMedGoogle Scholar
  92. 92.
    Jansen C, von Wettstein D, Schafer W, Kogel KH, Felk A, Maier FJ (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(46):16892–16897PubMedCentralPubMedGoogle Scholar
  93. 93.
    Eudes F, Comeau A, Rioux S, Collin J (2001) Impact of trichothecenes on fusarium head blight [Fusarium graminearum] development in spring wheat (Triticum aestivum). Can J Plant Pathol 23(3):318–322Google Scholar
  94. 94.
    Langevin F, Eudes F, Comeau A (2004) Effect of trichothecenes produced by Fusarium graminearum during fusarium head blight development in six cereal species. Eur J Plant Pathol 110(7):735–746Google Scholar
  95. 95.
    Liu S, Anderson JA (2003) Targeted molecular mapping of a major wheat QTL for Fusarium head blight resistance using wheat ESTs and synteny with rice. Genome 46(5):817–823PubMedGoogle Scholar
  96. 96.
    Buerstmayr H, Steiner B, Hartl L, Griesser M, Angerer N, Lengauer D et al (2003) Molecular mapping of QTLs for fusarium head blight resistance in spring wheat. II. Resistance to fungal penetration and spread. TAG Theor Appl Genet (Theoretische und angewandte Genetik) 107(3):503–508Google Scholar
  97. 97.
    Lemmens M, Scholz U, Berthiller F, Dall’Asta C, Koutnik A, Schuhmacher R et al (2005) The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for fusarium head blight resistance in wheat. Mol Plant Microbe Interact 18(12):1318–1324PubMedGoogle Scholar
  98. 98.
    Horevaj P, Brown-Guedira G, Milus EA (2012) Resistance in winter wheat lines to deoxynivalenol applied into florets at flowering stage and tolerance to phytotoxic effects on yield. Plant Pathol 61(5):925–933Google Scholar
  99. 99.
    Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R et al (2003) Detoxification of the Fusarium mycotoxin deoxynivalenol by a udp-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278(48):47905–47914PubMedGoogle Scholar
  100. 100.
    Gardiner SA, Boddu J, Berthiller F, Hametner C, Stupar RM, Adam G et al (2010) Transcriptome analysis of the barley-deoxynivalenol interaction: evidence for a role of glutathione in deoxynivalenol detoxification. Mol Plant Microbe Interact 23(7):962–976PubMedGoogle Scholar
  101. 101.
    Schweiger W, Boddu J, Shin S, Poppenberger B, Berthiller F, Lemmens M et al (2010) Validation of a candidate deoxynivalenol-inactivating UDP-glucosyltransferase from barley by heterologous expression in yeast. Mol Plant Microbe Interact 23(7):977–986PubMedGoogle Scholar
  102. 102.
    Muehlbauer GJ, Shin S, Li X, Boddu J, Heinen S, Torres Acosta JA et al (2012) Developing Fusarium head blight resistant wheat. In: Canty S, Clark A, Anderson-Scully A, Van Sanford D (eds) Proceedings of the national Fusarium head blight forum, 2012 December 4–6, Orlando, Florida, USA. East Lansing, MI/Lexington, KY, USA: U.S. Wheat & Barley Scab Initiative, p 144Google Scholar
  103. 103.
    Boenisch MJ, Schafer W (2011) Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol 11:110PubMedCentralPubMedGoogle Scholar
  104. 104.
    Hallen-Adams HE, Wenner N, Kuldau GA, Trail F (2011) Deoxynivalenol biosynthesis-related gene expression during wheat kernel colonization by Fusarium graminearum. Phytopathology 101(9):1091–1096PubMedGoogle Scholar
  105. 105.
    Fruhmann P, Weigl-Pollack T, Mikula H, Wiesenberger G, Adam G, Varga E et al (2014) Methylthiodeoxynivalenol (MTD): insight into the chemistry, structure and toxicity of thia-michael adducts of trichothecenes. Org Biomol Chem 12(28):5144–5150PubMedGoogle Scholar
  106. 106.
    Savard ME, Sinha RC, Lloyd Seaman W, Fedak G (2000) Sequential distribution of the mycotoxin deoxynivalenol in wheat spikes after inoculation with fusarium graminearum. Can J Plant Pathol 22(3):280–285Google Scholar
  107. 107.
    Gunnaiah R, Kushalappa AC, Duggavathi R, Fox S, Somers DJ (2012) Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PloS ONE 7(7):e40695PubMedCentralPubMedGoogle Scholar
  108. 108.
    Grove JF (2007) The trichothecenes and their biosynthesis. Fortschr Chem Org Naturst 88:63–130PubMedGoogle Scholar
  109. 109.
    Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics and biology. (Chapter 1: Trichothecenes). American Phytopathological Society, St. PaulGoogle Scholar
  110. 110.
    Lee T, Han YK, Kim KH, Yun SH, Lee YW (2002) Tri13 and Tri7 determine deoxynivalenol- and nivalenol-producing chemotypes of Gibberella zeae. Appl Environ Microbiol 68(5):2148–2154PubMedCentralPubMedGoogle Scholar
  111. 111.
    Alexander NJ, McCormick SP, Waalwijk C, van der Lee T, Proctor RH (2011) The genetic basis for 3-ADON and 15-ADON trichothecene chemotypes in Fusarium. Fungal Genet Biol 48(5):485–495PubMedGoogle Scholar
  112. 112.
    Kimura M, Kaneko I, Komiyama M, Takatsuki A, Koshino H, Yoneyama K et al (1998) Trichothecene 3-O-acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins. Cloning and characterization of Tri101. J Biol Chem 273(3):1654–1661PubMedGoogle Scholar
  113. 113.
    Alexander NJ, McCormick SP, Ziegenhorn SL (1999) Phytotoxicity of selected trichothecenes using Chlamydomonas reinhardtii as a model systemt. Nat Toxins 7(6):265–269PubMedGoogle Scholar
  114. 114.
    Ward TJ, Clear RM, Rooney AP, O’Donnell K, Gaba D, Patrick S et al (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(4):473–484PubMedGoogle Scholar
  115. 115.
    McMullen M, Jones R, Gallenberg D (1997) Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 81(12):1340–1348Google Scholar
  116. 116.
    Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O’Donnell K (2002) Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proc Natl Acad Sci U S A 99(14):9278–9283PubMedCentralPubMedGoogle Scholar
  117. 117.
    Desjardins AE, McCormick SP, Appell M (2007) Structure-activity relationships of trichothecene toxins in an Arabidopsis thaliana leaf assay. J Agric Food Chem 55(16):6487–6492PubMedGoogle Scholar
  118. 118.
    Hedman R, Pettersson H, Lindberg JE (1997) Absorption and metabolism of nivalenol in pigs. Arch Tierernahr 50(1):13–24PubMedGoogle Scholar
  119. 119.
    Schweiger W, Pasquet JC, Nussbaumer T, Paris MP, Wiesenberger G, Macadre C et al (2013) Functional characterization of two clusters of Brachypodium distachyon UDP-glycosyltransferases encoding putative deoxynivalenol detoxification genes. Mol Plant Microbe Interact 26(7):781–792PubMedGoogle Scholar
  120. 120.
    Caputi L, Malnoy M, Goremykin V, Nikiforova S, Martens S (2012) A genome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J 69(6):1030–1042PubMedGoogle Scholar
  121. 121.
    Kluger B, Bueschl C, Lemmens M, Berthiller F, Haubl G, Jaunecker G et al (2013) Stable isotopic labelling-assisted untargeted metabolic profiling reveals novel conjugates of the mycotoxin deoxynivalenol in wheat. Anal Bioanal Chem 405(15):5031–5036PubMedCentralPubMedGoogle Scholar
  122. 122.
    Varga E, Wiesenberger G, Hametner C, Ward TJ, Dong Y, Schofbeck D, McCormick S, Broz K, Stuckler R, Schuhmacher R, et al (2014) New tricks of an old enemy: isolates of Fusarium graminearum produce a type A trichothecene mycotoxin. Environmental microbiology. http://www.ncbi.nlm.nih.gov/pubmed/25403493Google Scholar
  123. 123.
    Edwards SG (2011) Zearalenone risk in European wheat. World Mycotoxin J 4(4):433–438Google Scholar
  124. 124.
    Kuiper-Goodman T, Scott PM, Watanabe H (1987) Risk assessment of the mycotoxin zearalenone. Regul Toxicol Pharmacol 7(3):253–306PubMedGoogle Scholar
  125. 125.
    Commission regulation (ec) no 1881/2006 (2012) Setting maximum levels for certain contaminants in foodstuff—consolidated version 03.12.2012. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2006R1881:20121203:EN:PDF. Accessed 15 April 2015
  126. 126.
    Kim YT, Lee YR, Jin J, Han KH, Kim H, Kim JC et al (2005) Two different polyketide synthase genes are required for synthesis of zearalenone in Gibberella zeae. Mol Microbiol 58(4):1102–1113PubMedGoogle Scholar
  127. 127.
    Gaffoor I, Trail F (2006) Characterization of two polyketide synthase genes involved in zearalenone biosynthesis in Gibberella zeae. Appl Environ Microbiol 72(3):1793–1799PubMedCentralPubMedGoogle Scholar
  128. 128.
    Lysoe E, Klemsdal SS, Bone KR, Frandsen RJ, Johansen T, Thrane U et al (2006) The PKS4 gene of Fusarium graminearum is essential for zearalenone production. Appl Environ Microbiol 72(6):3924–3932PubMedCentralPubMedGoogle Scholar
  129. 129.
    Werner U (2005) Characterisation of the effect of the Fusarium mycotoxin zearalenone in Arabidopsis thaliana. Ph.D. thesis, BOKU-Universität für BodenkulturGoogle Scholar
  130. 130.
    Berthiller F, Werner U, Sulyok M, Krska R, Hauser MT, Schuhmacher R (2006) Liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) determination of phase II metabolites of the mycotoxin zearalenone in the model plant Arabidopsis thaliana. Food Addit Contam 23(11):1194–1200PubMedCentralPubMedGoogle Scholar
  131. 131.
    Metzler M (2011) Proposal for a uniform designation of zearalenone and its metabolites. Mycotoxin Res 27(1):1–3PubMedGoogle Scholar
  132. 132.
    Kovalsky Paris MP, Schweiger W, Hametner C, Stuckler R, Muehlbauer GJ, Varga E et al (2014) Zearalenone-16-O-glucoside: a new masked mycotoxin. J Agric Food Chem 62(5):1181–1189PubMedGoogle Scholar
  133. 133.
    Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164PubMedGoogle Scholar
  134. 134.
    Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochim Biophys Acta 1823(3):689–697PubMedGoogle Scholar
  135. 135.
    de la Fuente van Benten S, Vossen JH, de Vries KJ, van Wees S, Tameling WI, Dekker HL et al (2005) Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant J 43(2):284–298Google Scholar
  136. 136.
    Utermark J, Karlovsky P (2007) Role of zearalenone lactonase in protection of Gliocladium roseum from fungitoxic effects of the mycotoxin zearalenone. Appl Environ Microbiol 73(2):637–642PubMedCentralPubMedGoogle Scholar
  137. 137.
    Malz S, Grell MN, Thrane C, Maier FJ, Rosager P, Felk A et al (2005) Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet Biol 42(5):420–433PubMedGoogle Scholar
  138. 138.
    Frandsen RJ, Nielsen NJ, Maolanon N, Sorensen JC, Olsson S, Nielsen J et al (2006) The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol Microbiol 61(4):1069–1080PubMedGoogle Scholar
  139. 139.
    Frandsen RJ, Schutt C, Lund BW, Staerk D, Nielsen J, Olsson S et al (2011) Two novel classes of enzymes are required for the biosynthesis of aurofusarin in Fusarium graminearum. J Biol Chem 286(12):10419–10428PubMedCentralPubMedGoogle Scholar
  140. 140.
    Rugbjerg P, Naesby M, Mortensen UH, Frandsen RJ (2013) Reconstruction of the biosynthetic pathway for the core fungal polyketide scaffold rubrofusarin in Saccharomyces cerevisiae. Microbe Cell Fact 12(1):31Google Scholar
  141. 141.
    Frandsen RJ, Albertsen KS, Stougaard P, Sorensen JL, Nielsen KF, Olsson S et al (2010) Methylenetetrahydrofolate reductase activity is involved in the plasma membrane redox system required for pigment biosynthesis in filamentous fungi. Eukaryot Cell 9(8):1225–1235PubMedCentralPubMedGoogle Scholar
  142. 142.
    Dvorska JE, Surai PF, Speake BK, Sparks NH (2001) Effect of the mycotoxin aurofusarin on the antioxidant composition and fatty acid profile of quail eggs. Br Poult Sci 42(5):643–649PubMedGoogle Scholar
  143. 143.
    Dvorska JE, Surai PF, Speake BK, Sparks NH (2002) Antioxidant systems of the developing quail embryo are compromised by mycotoxin aurofusarin. Comp Biochem Physiol C Toxicol Pharmacol 131(2):197–205PubMedGoogle Scholar
  144. 144.
    Streit E, Naehrer K, Rodrigues I, Schatzmayr G (2013) Mycotoxin occurrence in feed and feed raw materials worldwide: long-term analysis with special focus on Europe and Asia. J Sci Food Agric 93(12):2892–2899PubMedGoogle Scholar
  145. 145.
    Macias M, Ulloa M, Gamboa A, Mata R (2000) Phytotoxic compounds from the new coprophilous fungus Guanomyces polythrix. J Nat Prod 63(6):757–761PubMedGoogle Scholar
  146. 146.
    Grundlinger M, Yasmin S, Lechner BE, Geley S, Schrettl M, Hynes M et al (2013) Fungal siderophore biosynthesis is partially localized in peroxisomes. Mol Microbiol 88(5):862–875PubMedCentralPubMedGoogle Scholar
  147. 147.
    Min K, Son H, Lee J, Choi GJ, Kim JC, Lee YW (2012) Peroxisome function is required for virulence and survival of Fusarium graminearum. Mol Plant Microbe Interact 25(12):1617–1627PubMedGoogle Scholar
  148. 148.
    Condon BJ, Oide S, Gibson DM, Krasnoff SB, Turgeon BG (2014) Reductive iron assimilation and intracellular siderophores assist extracellular siderophore-driven iron homeostasis and virulence. Mol Plant Microbe Interact 27(8):793–808PubMedGoogle Scholar
  149. 149.
    Hof C, Eisfeld K, Welzel K, Antelo L, Foster AJ, Anke H (2007) Ferricrocin synthesis in Magnaporthe grisea and its role in pathogenicity in rice. Mol Plant Pathol 8(2):163–172PubMedGoogle Scholar
  150. 150.
    Eichhorn H, Lessing F, Winterberg B, Schirawski J, Kamper J, Muller P et al (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18(11):3332–3345PubMedCentralPubMedGoogle Scholar
  151. 151.
    Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics and biology. (Chapter 5: Other selected metabolites). American Phytopathological Society, St. PaulGoogle Scholar
  152. 152.
    Burmeister HR, Grove MD, Kwolek WF (1980) Moniliformin and butenolide: effect on mice of high-level, long-term oral intake. Appl Environ Microbiol 40(6):1142–1144PubMedCentralPubMedGoogle Scholar
  153. 153.
    Tookey HL, Yates SG, Ellis JJ, Grove MD, Nichols RE (1972) Toxic effects of a butenolide mycotoxin and of Fusarium tricinctum cultures in cattle. J Am Vet Med Assoc 160(11):1522–1526PubMedGoogle Scholar
  154. 154.
    Burmeister HR, Hesseltine CW (1970) Biological assays for two mycotoxins produced by Fusarium tricinctum. Appl Microbiol 20(3):437–440PubMedCentralPubMedGoogle Scholar
  155. 155.
    Wang YZ, Miller JD (1988) Effects of Fusarium graminearum metabolites on wheat tissue in relation to Fusarium head blight resistance. J Phytopathol 122(2):118–125Google Scholar
  156. 156.
    Streit E, Schwab C, Sulyok M, Naehrer K, Krska R, Schatzmayr G (2013) Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins 5(3):504–523PubMedCentralPubMedGoogle Scholar
  157. 157.
    Wang YM, Peng SQ, Zhou Q, Wang MW, Yan CH, Yang HY et al (2006) Depletion of intracellular glutathione mediates butenolide-induced cytotoxicity in HepG2 cells. Toxicology Lett 164(3):231–238Google Scholar
  158. 158.
    Liu JB, Wang YM, Peng SQ, Han G, Dong YS, Yang HY et al (2007) Toxic effects of Fusarium mycotoxin butenolide on rat myocardium and primary culture of cardiac myocytes. Toxicon 50(3):357–364PubMedGoogle Scholar
  159. 159.
    Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics and biology. (Chapter 4: Other selected mycotoxins). American Phytopathological Society, St. PaulGoogle Scholar
  160. 160.
    Kleigrewe K, Aydin F, Hogrefe K, Piecuch P, Bergander K, Wurthwein EU et al (2012) Structure elucidation of new fusarins revealing insights in the rearrangement mechanisms of the Fusarium mycotoxin fusarin C. J Agric Food Chem 60(21):5497–5505PubMedGoogle Scholar
  161. 161.
    Niehaus EM, Kleigrewe K, Wiemann P, Studt L, Sieber CM, Connolly LR et al (2013) Genetic manipulation of the Fusarium fujikuroi fusarin gene cluster yields insight into the complex regulation and fusarin biosynthetic pathway. Chem Biol 20(8):1055–1066PubMedGoogle Scholar
  162. 162.
    Kleigrewe K, Sohnel AC, Humpf HU (2011) A new high-performance liquid chromatography-tandem mass spectrometry method based on dispersive solid phase extraction for the determination of the mycotoxin fusarin C in corn ears and processed corn samples. J Agric Food Chem 59(19):10470–10476PubMedGoogle Scholar
  163. 163.
    Kleigrewe K, Niehaus EM, Wiemann P, Tudzynski B, Humpf HU (2012) New approach via gene knockout and single-step chemical reaction for the synthesis of isotopically labeled Fusarin C as an internal standard for the analysis of this Fusarium mycotoxin in food and feed samples. J Agric Food Chem 60(34):8350–8355PubMedGoogle Scholar
  164. 164.
    Zhu B, Jeffrey AM (1992) Stability of Fusarin C: effects of the normal cooking procedure used in China and pH. Nutr Cancer 18(1):53–58PubMedGoogle Scholar
  165. 165.
    Sondergaard TE, Hansen FT, Purup S, Nielsen AK, Bonefeld-Jorgensen EC, Giese H et al (2011) Fusarin C acts like an estrogenic agonist and stimulates breast cancer cells in vitro. Toxicol Lett 205(2):116–121PubMedGoogle Scholar
  166. 166.
    Shier WT, Shier AC, Xie W, Mirocha CJ (2001) Structure-activity relationships for human estrogenic activity in zearalenone mycotoxins. Toxicon 39(9):1435–1438PubMedGoogle Scholar
  167. 167.
    Gelderblom WC, Thiel PG, van der Merwe KJ (1988) The chemical and enzymatic interaction of glutathione with the fungal metabolite, Fusarin C. Mutat Res 199(1):207–214PubMedGoogle Scholar
  168. 168.
    Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49(1):159–172PubMedGoogle Scholar
  169. 169.
    Dubreuil-Maurizi C, Poinssot B (2012) Role of glutathione in plant signaling under biotic stress. Plant Signal Behav 7(2):210–212PubMedCentralPubMedGoogle Scholar
  170. 170.
    McCormick SP, Alexander NJ, Harris LJ (2010) CLM1 of Fusarium graminearum encodes a longiborneol synthase required for culmorin production. Appl Environ Microbiol 76(1):136–141PubMedCentralPubMedGoogle Scholar
  171. 171.
    Ghebremeskel M, Langseth W (2001) The occurrence of culmorin and hydroxy-culmorins in cereals. Mycopathologia 152(2):103–108PubMedGoogle Scholar
  172. 172.
    Pedersen PB, Miller JD (1999) The fungal metabolite culmorin and related compounds. Nat Toxins 7(6):305–309PubMedGoogle Scholar
  173. 173.
    Sorensen JL, Hansen FT, Sondergaard TE, Staerk D, Lee TV, Wimmer R et al (2012) Production of novel fusarielins by ectopic activation of the polyketide synthase 9 cluster in Fusarium graminearum. Environ Microbiol 14(5):1159–1170PubMedGoogle Scholar
  174. 174.
    Sorensen JL, Akk E, Thrane U, Giese H, Sondergaard TE (2013) Production of fusarielins by Fusarium. Int J Food Microbiol 160(3):206–211PubMedGoogle Scholar
  175. 175.
    Sondergaard TE, Klitgaard LG, Purup S, Kobayashi H, Giese H, Sorensen JL (2012) Estrogenic effects of fusarielins in human breast cancer cell lines. Toxicol Lett 214(3):259–262PubMedGoogle Scholar
  176. 176.
    Kobayashi H, Sunaga R, Furihata K, Morisaki N, Iwasaki S (1995 Jan) Isolation and structures of an antifungal antibiotic, fusarielin A, and related compounds produced by a Fusarium sp. J Antibiot 48(1):42–52PubMedGoogle Scholar
  177. 177.
    Sirtori CR (2014) The pharmacology of statins. Pharmacol Res 88:3–11Google Scholar
  178. 178.
    Noguchi-Yachide T, Dodo K, Aoyama H, Fujimoto H, Hori M, Hashimoto Y et al (2010) Identification of binding proteins of fusarielin A as actin and tubulin. Chem Pharm Bull 58(1):129–134PubMedGoogle Scholar
  179. 179.
    Vershinin A (1999) Biological functions of carotenoids—diversity and evolution. Biofactors (Oxford, England) 10(2–3):99–104PubMedGoogle Scholar
  180. 180.
    Arrach N, Schmidhauser TJ, Avalos J (2002) Mutants of the carotene cyclase domain of al-2 from Neurospora crassa. Mol Genet Genomics 266(6):914–921PubMedGoogle Scholar
  181. 181.
    Linnemannstons P, Prado MM, Fernandez-Martin R, Tudzynski B, Avalos J (2002) A carotenoid biosynthesis gene cluster in Fusarium fujikuroi: the genes carb and carra. Mol Genet Genomics 267(5):593–602PubMedGoogle Scholar
  182. 182.
    Jin JM, Lee J, Lee YW (2010) Characterization of carotenoid biosynthetic genes in the ascomycete Gibberella zeae. FEMS Microbiol Lett 302(2):197–202PubMedGoogle Scholar
  183. 183.
    Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28(4):663–692PubMedGoogle Scholar
  184. 184.
    Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant-pathogen interactions. J Plant Res 124(4):489–499PubMedGoogle Scholar
  185. 185.
    Torres-Vera R, Garcia JM, Pozo MJ, Lopez-Raez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15(2):211–216PubMedGoogle Scholar
  186. 186.
    Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97(6):925–931PubMedCentralPubMedGoogle Scholar
  187. 187.
    Dor E, Joel DM, Kapulnik Y, Koltai H, Hershenhorn J (2011) The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi. Planta 234(2):419–427PubMedGoogle Scholar
  188. 188.
    Siewers V, Kokkelink L, Smedsgaard J, Tudzynski P (2006) Identification of an abscisic acid gene cluster in the grey mold Botrytis cinerea. Appl Environ Microbiol 72(7):4619–4626PubMedCentralPubMedGoogle Scholar
  189. 189.
    Jorgensen SH, Frandsen RJ, Nielsen KF, Lysoe E, Sondergaard TE, Wimmer R et al (2014) Fusarium graminearum PKS14 is involved in orsellinic acid and orcinol synthesis. Fungal Genet Biol 70c:24–31Google Scholar
  190. 190.
    Bacon CW, Porter JK, Norred WP, Leslie JF (1996) Production of fusaric acid by Fusarium species. Appl Environ Microbiol 62(11):4039–4043PubMedCentralPubMedGoogle Scholar
  191. 191.
    Smith TK, Sousadias MG (1993) Fusaric acid content of swine feedstuffs. J Agric Food Chem 41(12):2296–2298Google Scholar
  192. 192.
    Mogensen JM, Sorensen SM, Sulyok M, van der Westhuizen L, Shephard GS, Frisvad JC et al (2011) Single-kernel analysis of fumonisins and other fungal metabolites in maize from South African subsistence farmers. Food Addit Contam Part A. Chem Anal Control Expo Risk Assess 28(12):1724–1734PubMedGoogle Scholar
  193. 193.
    Wang H, Ng TB (1999) Pharmacological activities of fusaric acid (5-butylpicolinic acid). Life Sci 65(9):849–856PubMedGoogle Scholar
  194. 194.
    Rimando AM, Porter JK (1999) Effects of fusarium mycotoxins on levels of serotonin, melatonin, and 5-hydroxytryptophan in pineal cell cultures. Adv Exp Med Biol 467:425–431PubMedGoogle Scholar
  195. 195.
    Nagasaka A, Hara I, Imai Y, Uchikawa T, Yamauchi K, Suzuki S et al (1985) Effect of fusaric acid (a dopamine beta-hydroxylase inhibitor) on phaeochromocytoma. Clin Endocrinol (Oxf) 22(4):437–444Google Scholar
  196. 196.
    Yabuta T, Kambe K, Hayashi T (1937) Biochemistry of the bakanae fungus. I. Fusarinic acid, a new product of the bakanae fungus. J Agric Chem Soc Jpn 10:1059–1068Google Scholar
  197. 197.
    Venter SL, Steyn PJ (1998) Correlation between fusaric acid production and virulence of isolates of Fusarium oxysporum that causes potato dry rot in South Africa. Potato Res 41(3):289–294Google Scholar
  198. 198.
    Gapillout I, Milat ML, Blein JP (1996) Effects of fusaric acid on cells from tomato cultivars resistant or susceptible to Fusarium oxysporum f. sp. lycopersici. Eur J Plant Pathol 102(2):127–132Google Scholar
  199. 199.
    Kuo MS, Scheffer JM (1964) Evaluation of fusaric acid as a factor in development of Fusarium wilt. Phytopathology 54:1041–1044Google Scholar
  200. 200.
    Dong X, Ling N, Wang M, Shen Q, Guo S (2012) Fusaric acid is a crucial factor in the disturbance of leaf water imbalance in fusarium-infected banana plants. Plant Physiology Biochem 60:171–179Google Scholar
  201. 201.
    Bani M, Rispail N, Evidente A, Rubiales D, Cimmino A (2014) Identification of the main toxins isolated from Fusarium oxysporum f. sp. Pisi race 2 and their relation with isolates’ pathogenicity. J Agric Food Chem 62(12):2574–2580PubMedGoogle Scholar
  202. 202.
    Jiao J, Zhou B, Zhu X, Gao Z, Liang Y (2013) Fusaric acid induction of programmed cell death modulated through nitric oxide signalling in tobacco suspension cells. Planta 238(4):727–737PubMedGoogle Scholar
  203. 203.
    Wilson DM, Kays SJ, Etherton B (1978) The relationship between pathogenic fungal metabolities (fusaric and picolinic acid), endogenous ethylene evolution and the development of ethylene-like symptoms. Plant Soil 50(1–3):355–362 (1978/12/01)Google Scholar
  204. 204.
    Tamari K, Kaji J (1952) Studies on the mechanism of injurious action of fusarinic acid on plant-growth. J Agric Chem Soc Jpn 26(7):345–349Google Scholar
  205. 205.
    Malini S (1966) Heavy metal chelates of fusaric acid: in vitro spectrophotometry. J Phytopathol 57(3):221–231Google Scholar
  206. 206.
    Lakshminarayanan K, Subramanian D (1955) Is fusaric acid a vivotoxin? Nature 176(4484):697–698 (10/08/print, 10.1038/176697a0)Google Scholar
  207. 207.
    Pan JH, Lin YC, Tan N, Gu YC (2010) Cu(II): A “signaling molecule” of the mangrove endophyte Fusarium oxysporum ZZF51? Biometals 23(6):1053–1060PubMedGoogle Scholar
  208. 208.
    Gäumann E (1958) The mechanism of fusaric acid injury. Phytopathology 48:670–686Google Scholar
  209. 209.
    Brown DW, Butchko RA, Busman M, Proctor RH (2012) Identification of gene clusters associated with fusaric acid, fusarin, and perithecial pigment production in Fusarium verticillioides. Fungal Genet Biol 49(7):521–532PubMedGoogle Scholar
  210. 210.
    Brown DW, Lee SH, Kim LH, Ryu JG, Lee S, Seo Y, Kim YH, Busman M, Yun SH, Proctor RH, Lee T (2015) Identification of a 12-gene fusaric Acid biosynthetic gene cluster in fusarium species through comparative and functional genomics. Mol Plant Microbe Interact 28(3):319–332PubMedGoogle Scholar
  211. 211.
    Liu J, Bell A, Stipanovic R, Puckhaber L (2010) Fusaric acid production and pathogenicity of Fusarium oxysporum f. sp. vasinfectum [abstract]. Proceedings of Beltwide Cotton Conferences, January 4–7, 2010, New Orleans, Louisiana 2010 CDROMGoogle Scholar
  212. 212.
    Wu F, Groopman JD, Pestka JJ (2014) Public health impacts of foodborne mycotoxins. Annu Rev Food Sci Technol 5:351–372PubMedGoogle Scholar
  213. 213.
    Scott PM (2012) Recent research on fumonisins: a review. Food Addit Contam Part A. Chem Anal Control Expo Risk Assess 29(2):242–248PubMedGoogle Scholar
  214. 214.
    Rheeder JP, Marasas WF, Vismer HF (2002) Production of fumonisin analogs by Fusarium species. Appl Environ Microbiol 68(5):2101–2105PubMedCentralPubMedGoogle Scholar
  215. 215.
    Bartok T, Tolgyesi L, Mesterhazy A, Bartok M, Szecsi A (2010) Identification of the first fumonisin mycotoxins with three acyl groups by ESI-ITMS and ESI-TOFMS following RP-HPLC separation: Palmitoyl, linoleoyl and oleoyl EFB(1) fumonisin isomers from a solid culture of Fusarium verticillioides. Food Addit Contam Part A. Chem Anal Control Expo Risk Assess 27(12):1714–1723PubMedGoogle Scholar
  216. 216.
    Falavigna C, Lazzaro I, Galaverna G, Battilani P, Dall’Asta C (2013) Fatty acid esters of fumonisins: first evidence of their presence in maize. Food Addit Contam Part A. Chem Anal Control Expo Risk Assess 30(9):1606–1613PubMedGoogle Scholar
  217. 217.
    Musser SM, Gay ML, Mazzola EP, Plattner RD (1996) Identification of a new series of fumonisins containing 3-hydroxypyridine. J Nat Prod 59(10):970–972PubMedGoogle Scholar
  218. 218.
    Scientific Committee on Food (2003) Updated opinion of HTE scientific comettee on food on fumonisin B1, B2 and B3 (expressed on 4 April 2003). European Commission, BrusselsGoogle Scholar
  219. 219.
    Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics and biology. Chapter 3: Fumonisins. American Phytopathological Society, St. PaulGoogle Scholar
  220. 220.
    Nelson PE, Desjardins AE, Plattner RD (1993) Fumonisins, mycotoxins produced by Fusarium species: biology, chemistry, and significance. Annu Rev Phytopathol 31:233–252PubMedGoogle Scholar
  221. 221.
    World Health Organization (International Agancy for Research on Cancer) (2002) Some traditional herbal medicines, some mycotoxins, naphthalene and styreneGoogle Scholar
  222. 222.
    Riley RT, Enongene E, Voss KA, Norred WP, Meredith FI, Sharma RP et al (2001) Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis. Environ Health Perspect 109(Suppl 2):301–308PubMedCentralPubMedGoogle Scholar
  223. 223.
    Marasas WF, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J et al (2004) Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 134(4):711–716PubMedGoogle Scholar
  224. 224.
    Epstein S, Riezman H (2013) Sphingolipid signaling in yeast: potential implications for understanding disease. Front Biosci (Elite edition) 5:97–108Google Scholar
  225. 225.
    Stone JM, Heard JE, Asai T, Ausubel FM (2000) Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12(10):1811–1822PubMedCentralPubMedGoogle Scholar
  226. 226.
    Asai T, Stone JM, Heard JE, Kovtun Y, Yorgey P, Sheen J et al (2000) Fumonisin B1-induced cell death in arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12(10):1823–1836PubMedCentralPubMedGoogle Scholar
  227. 227.
    Lin SS, Martin R, Mongrand S, Vandenabeele S, Chen KC, Jang IC et al (2008) RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. Plant J 56(4):550–561PubMedGoogle Scholar
  228. 228.
    Chivasa S, Ndimba BK, Simon WJ, Lindsey K, Slabas AR (2005) Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability. Plant Cell 17(11):3019–3034PubMedCentralPubMedGoogle Scholar
  229. 229.
    Igarashi D, Bethke G, Xu Y, Tsuda K, Glazebrook J, Katagiri F (2013) Pattern-triggered immunity suppresses programmed cell death triggered by fumonisin B1. PloS ONE 8(4):e60769PubMedCentralPubMedGoogle Scholar
  230. 230.
    Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I (2005) Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J Biol Chem 280(38):32914–32920PubMedGoogle Scholar
  231. 231.
    Hara-Nishimura I, Hatsugai N, Nakaune S, Kuroyanagi M, Nishimura M (2005) Vacuolar processing enzyme: an executor of plant cell death. Curr Opin Plant Biol 8(4):404–408PubMedGoogle Scholar
  232. 232.
    Kimberlin AN, Majumder S, Han G, Chen M, Cahoon RE, Stone JM et al (2013) Arabidopsis 56-amino acid serine palmitoyltransferase-interacting proteins stimulate sphingolipid synthesis, are essential, and affect mycotoxin sensitivity. Plant Cell 25(11):4627–4639PubMedCentralPubMedGoogle Scholar
  233. 233.
    Desjardins AE, Plattner RD, Nelsen TC, Leslie JF (1995) Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Appl Environ Microbiol 61(1):79–86PubMedCentralPubMedGoogle Scholar
  234. 234.
    Desjardins AE, Plattner RD (2000) Fumonisin B(1)-nonproducing strains of Fusarium verticillioides cause maize (Zea mays) ear infection and ear rot. J Agric Food Chem 48(11):5773–5780PubMedGoogle Scholar
  235. 235.
    Desjardins AE, Munkvold GP, Plattner RD, Proctor RH (2002) FUM1—a gene required for fumonisin biosynthesis but not for maize ear rot and ear infection by Gibberella moniliformis in field tests. Mol Plant Microbe Interact 15(11):1157–1164PubMedGoogle Scholar
  236. 236.
    Glenn AE, Zitomer NC, Zimeri AM, Williams LD, Riley RT, Proctor RH (2008) Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings. Mol Plant Microbe Interact 21(1):87–97PubMedGoogle Scholar
  237. 237.
    Desjardins AE, Plattner RD, Stessman RJ, McCormick SP, Millard MJ (2005) Identification and heritability of fumonisin insensitivity in Zea mays. Phytochemistry 66(20):2474–2480PubMedGoogle Scholar
  238. 238.
    Dall’Asta C, Galaverna G, Mangia M, Sforza S, Dossena A, Marchelli R (2009) Free and bound fumonisins in gluten-free food products. Mol Nutr Food Res 53(4):492–499PubMedGoogle Scholar
  239. 239.
    Berthiller F, Crews C, Dall’Asta C, Saeger SD, Haesaert G, Karlovsky P et al (2013) Masked mycotoxins: a review. Mol Nutr Food Res 57(1):165–186PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Gerhard Adam
    • 1
  • Gerlinde Wiesenberger
    • 1
  • Ulrich Güldener
    • 2
    Email author
  1. 1.Department of Applied Genetics and Cell BiologyUniversity of Natural Resources and Life SciencesViennaAustria
  2. 2.Lehrstuhl für Genomorientierte BioinformatikTechnische Universität MünchenFreisingGermany

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