Skip to main content

4 Fungal Toxins of Agricultural Importance

  • Chapter
  • First Online:
Agricultural Applications

Abstract

Fungi produce a diverse array of toxins that contribute both positively and negatively to agriculture. We describe phytotoxins which have defined roles in plant disease, as well as mycotoxins which generally have no direct role in disease but have significant impacts on animals that feed on infected host plants. We have included examples of host-specific phytotoxins which act upon a very narrow range of susceptible host genotypes, and non-specific phytotoxins which can affect a wide range of plants. We also describe fungal secondary metabolites that underpin certain mutualistic symbioses. Toxins are described based on their core biosynthesis, and include agriculturally important examples of non-ribosomally synthesised peptides, polyketide-based peptides, proteinaceous phytotoxins, sesquiterpenoid-containing compounds and miscellaneaous toxins of herbivores. The role of each toxin in the plant–fungus interaction, as well as the biochemistry and molecular basis of toxin biosynthesis, will be described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe K, Iwanami H, Kotoda N, Moriya S, Takahashi S (2010) Evaluation of apple genotypes and Malus species for resistance to Alternaria blotch caused by Alternaria alternata apple pathotype using detached-leaf method. Plant Breed 129:208–218

    CAS  Google Scholar 

  • Abeysekara NS, Friesen TL, Keller B, Faris JD (2009) Identification and characterization of a novel host-toxin interaction in the wheat-Stagonospora nodorum pathosystem. Theor Appl Genet 120:117–126

    PubMed  CAS  Google Scholar 

  • Aboukhaddour R, Kim YM, Strelkov SE (2012) RNA-mediated gene silencing of ToxB in Pyrenophora tritici-repentis. Mol Plant Pathol 13:318–326

    PubMed  CAS  Google Scholar 

  • Ahn J-H, Walton JD (1996) Chromosomal organization of TOX2, a complex locus required for host-selective toxin biosynthesis in Cochliobolus carbonum. Plant Cell 8:887–897

    PubMed  CAS  Google Scholar 

  • Ahn J-H, Walton JD (1997) A fatty acid synthase gene in Cochliobolus carbonum required for production of HC-toxin, cyclo(D-prolyl-L-alanyl-D-alanyl-L-2-amino-9,10-epoxi-8-oxodecanoyl). Mol Plant Microbe Interact 10:207–214

    PubMed  CAS  Google Scholar 

  • Ahuja M, Chiang YM, Chang SL, Praseuth MB, Entwistle R et al (2012) Illuminating the diversity of aromatic polyketide synthases in Aspergillus nidulans. J Am Chem Soc 134(19):8212–8221

    PubMed  CAS  Google Scholar 

  • Akagi Y, Akamatsu H, Otani H, Kodama M (2009a) Horizontal chromosome transfer: a mechanism for the evolution and differentiation of a plant pathogenic fungus. Eukaryot Cell 8:1732–1738

    PubMed  CAS  Google Scholar 

  • Akagi Y, Taga M, Yamamoto M, Tsuge T, Fukumasa-Nakai Y, Otani H, Kodama M (2009b) Chromosome constitution of hybrid strains constructed by protoplast fusion between the tomato and strawberry pathotypes of Alternaria alternata. J Genet Plant Pathol 75:101–109

    Google Scholar 

  • 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 87:967–972

    PubMed  CAS  Google Scholar 

  • Akamatsu H, Taga M, Kodama M, Johnson R, Otani H, Kohmoto K (1999) Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxins. Curr Genet 35:647–656

    PubMed  CAS  Google Scholar 

  • Akamatsu H, Otani H, Kodama M (2003) Characterization of a gene cluster for host-specific AAL-toxin biosynthesis in the tomato pathotype of Alternaria alternata. Fungal Genet Newsl 50:355

    Google Scholar 

  • Amaike S, Ozga JA, Basu U, Strelkov SE (2008) Quantification of ToxB gene expression and formation of appressoria by isolates of Pyrenophora triticirepentis differing in pathogenicity. Plant Pathol 57:623–633

    CAS  Google Scholar 

  • Andrie RM, Ciuffetti LM (2011) Pyrenophora bromi, causal agent of brownspot of bromegrass, expresses a gene encoding a protein with homology and similar activity to Ptr ToxB, a host-selective toxin of wheat. Mol Plant Microbe Interact 24:359–367

    PubMed  CAS  Google Scholar 

  • Andrie RM, Schoch CL, Hedges R, Spatafora JW, Ciuffetti LM (2008) Homologs of ToxB, a host-selective toxin gene from Pyrenophora tritici-repentis, are present in the genome of sister-species Pyrenophora bromi and other members of the Ascomycota. Fungal Genet Biol 45:363–377

    PubMed  CAS  Google Scholar 

  • Anonymous (2005) Commission Regulation (EC) No 856/2005 of 6 June 2005 amending Regulation (EC) No 466/2001 as regards Fusarium toxins. Off J Eur Union L143:3–8

    Google Scholar 

  • Bacetty A, Snook M, Glenn A, Noe J, Hill N, Culbreath A, Timper P, Nagabhyru P, Bacon C (2009) Toxicity of endophyte-infected tall fescue alkaloids and grass metabolites on Pratylenchus scribneri. Phytopathology 99:1336–1345

    PubMed  CAS  Google Scholar 

  • Bacon CW (1988) Procedure for isolating the endophyte from tall fescue and screening the isolates for ergot alkaloids. Appl Environ Microbiol 54:2615–2618

    PubMed  CAS  Google Scholar 

  • Bacon CW (1995) Toxic endophyte-infected tall fescue and range grasses: historic perspectives. J Anim Sci 73:861–870

    PubMed  CAS  Google Scholar 

  • Bacon CW, Lyons PC, Porter JK, Robbins JD (1986) Ergot toxicity from endophyte-infected grasses: a review. Agron J 78:106–116

    CAS  Google Scholar 

  • Bai GH, Desjardins AE, Plattner RD (2002) Deoxynivalenol non-producing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91–98

    PubMed  CAS  Google Scholar 

  • Bailey AM, Kershaw MJ, Hunt BA, Paterson IC, Charnley K, Reynolds SE, Clarkson JM (1996) Cloning and sequence analysis of an intron-containing domain from a peptide synthetase-encoding gene of the entomopathogenic fungus Metarhizium anisopliae. Gene 173:195–197

    PubMed  CAS  Google Scholar 

  • Baker SE, Kroken S, Inderbitzin P, Asvarak T, Li B-Y et al (2006) Two polyketide synthase-encoding genes are required for biosynthesis of the polyketide virulence factor, T-toxin, by Cochliobolus heterostrophus. Mol Plant Microbe Interact 19(2):139–149

    PubMed  CAS  Google Scholar 

  • Ball OJ, Tapper BA (1999) The production of loline alkaloids in artificial and natural grass/endophyte associations. In: Proceedings of the 52nd New Zealand plant protection conference, Auckland, pp 264–269

    Google Scholar 

  • Ball OJP, Coudron TA, Tapper BA, Davies E, Trently D, Bush LP, Gwinn KD, Popay AJ (2006) Importance of host plant species, Neotyphodium endophyte isolate, and alkaloids on feeding by Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. J Econ Entomol 99:1462–1473

    PubMed  CAS  Google Scholar 

  • Ball OJP, Gwinn KD, Pless CD, Popay AJ (2011) Endophyte isolate and host grass effects on Chaetocnema pulicaria (Coleoptera: Chrysomelidae) feeding. J Econ Entomol 104:665–672

    PubMed  Google Scholar 

  • Baltriukiene D, Kalvelyte A, Bukelskiene V (2007) Induction of apoptosis and activation of JNK and p38 MAPK pathways in deoxynivalenol-treated cell lines. Altern Lab Anim 35:53–59

    PubMed  CAS  Google Scholar 

  • Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16(3):497–516

    PubMed  CAS  Google Scholar 

  • Berestetskiy A (2008) A review of fungal phytotoxins: from basic studies to practical use. Appl Biochem Microbiol 44(5):453–465

    CAS  Google Scholar 

  • Bezuidenhout SC, Gelderblom WCA, Gorst-Allman CP, Horak RM, Marasas WFO, Spiteller G, Vleggaar R (1988) Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme. J Chem Soc Chem Commun 11:743–745

    Google Scholar 

  • Blankenship JD, Spiering MJ, Wilkinson HH, Fannin FF, Bush LP, Schardl CL (2001) Production of loline alkaloids by the grass endophyte, Neotyphodium uncinatum, in defined media. Phytochemistry 58:395–401

    PubMed  CAS  Google Scholar 

  • Blankenship JD, Houseknecht JB, Pal S, Bush LP, Grossman RB, Schardl CL (2005) Biosynthetic precursors of fungal pyrrolizidines, the loline alkaloids. Chembiochem 6:1016–1022

    PubMed  CAS  Google Scholar 

  • Böhnert 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 16:2499–2513

    PubMed  Google Scholar 

  • Bojja RS, Cerny RL, Proctor RH, Du L (2004) Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J Agric Food Chem 52:2855–2860

    PubMed  CAS  Google Scholar 

  • Bottini AT, Bowen JR, Gilchrist DG (1981) Phytotoxins II. Characterization of a phytotoxic fraction from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22:2723–2726

    CAS  Google Scholar 

  • Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA, Watson RH, Parish JA, Hawkins LL, Thompson FN (2002) Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron J 94:567–574

    Google Scholar 

  • Brandwagt BF, Mesbah LA, Takken FLW, Laurent PL, Kneppers TJA, Hille J, Nijkamp HJJ (2000) A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 97:4961–4966

    PubMed  CAS  Google Scholar 

  • Braun CJ, Siedow JN, Williams ME, Levings CS III (1989) Mutations in the maize mitochondrial T-urf13 gene eliminate sensitivity to a fungal pathotoxin. Proc Natl Acad Sci USA 86:4435–4439

    PubMed  CAS  Google Scholar 

  • Braun CJ, Siedow JN, Levings CS III (1990) Fungal toxins bind to the URF13 protein in maize mitochondria and Escherichia coli. Plant Cell 2:153–161

    PubMed  CAS  Google Scholar 

  • Brosch G, Ransom R, Lechner T, Walton JD, Loidl P (1995) Inhibition of maize histone deacetylases by HC-toxin, the host-selective toxin of Cochliobolus carbonum. Plant Cell 7:1941–1950

    PubMed  CAS  Google Scholar 

  • Brown DW, Butchko RAE, Busman M, Proctor RH (2007) The Fusarium verticillioides FUM gene cluster encodes a Zn(II)2cys6 protein that affects FUM gene expression and fumonisin production. Eukaryot Cell 6:1210–1218

    PubMed  CAS  Google Scholar 

  • Brown DW, Butchko RAE, Baker SE, Proctor RH (2012) Phylogenomic and functional domain analysis of polyketide synthases in Fusarium. Fungal Biol 116(2):318–331

    PubMed  CAS  Google Scholar 

  • Bultman T, Pulas C, Grant L, Bell G, Sullivan T (2006) Effects of fungal endophyte isolate on performance and preference of bird cherry-oat aphid. Environ Entomol 35:1690–1695

    Google Scholar 

  • Bushley KE, Turgeon BG (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10:26

    PubMed  Google Scholar 

  • Butchko RAE, Plattner RD, Proctor RH (2003) FUM13 encodes a short chain dehydrogenase/reductase required for C-3 carbonyl reduction during fumonisin biosynthesis in Gibberella moniliformis. J Agric Food Chem 51:3000–3006

    PubMed  CAS  Google Scholar 

  • Butchko RAE, Plattner RD, Proctor RH (2006) Deletion analysis of FUM genes involved in tricarballylic ester formation during fumonisin biosynthesis. J Agric Food Chem 54:9398–9404

    PubMed  CAS  Google Scholar 

  • Caldas ED, Jones AD, Winter CK, Ward B, Gilchrist DG (1995) Electrospray ionization mass spectrometry of sphinganine analog mycotoxins. Anal Chem 67:196–207

    CAS  Google Scholar 

  • Caporael LR (1976) Ergotism: the satan loosed in Salem? Science 192:21–26

    PubMed  CAS  Google Scholar 

  • Cardoza RE, Malmierca MG, Hermosa MR, Alexander NJ, McCormick SP et al (2011) Identification of loci and functional dharacterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl Environ Microbiol 77:4867–4877

    PubMed  CAS  Google Scholar 

  • Carrasco L, Barbacid M, Vazquez D (1973) The trichodermin group of antibiotics, inhibitors of peptide bond formation by eukaryotic ribosomes. Biochim et Biophys Acta (BBA) Nucleic Acids Protein Synth 312:368–376

    CAS  Google Scholar 

  • Challis GL, Ravel J, Townsend CA (2000) Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 7:211–224

    PubMed  CAS  Google Scholar 

  • Chang HR, Bronson CR (1996) A reciprocal translocation and possible insertion(s) tightly associated with host-specific virulence in Cochliobolus heterostrophus. Genome 39:549–557

    PubMed  CAS  Google Scholar 

  • Chen H, Lee M-H, Daub ME, Chung K-R (2007) Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae. Mol Microbiol 64(3):755–770

    PubMed  CAS  Google Scholar 

  • Cheng Y-Q, Walton JD (2000) A eukaryotic alanine racemase gene involved in cyclic peptide biosynthesis. J Biol Chem 275:4906–5008

    PubMed  CAS  Google Scholar 

  • Cheng Y-Q, Ahn J-H, Walton JD (1999) A putative branched-chain amino acid aminotransferase gene required for HC-toxin biosynthesis and pathogenicity in Cochliobolus carbonum. Microbiology 145:3539–3546

    PubMed  CAS  Google Scholar 

  • Choquer M, Dekkers KL, Chen H-Q, Cao L, Ueng PP et al (2005) The CTB1 gene encoding a fungal polyketide synthase is required for cercosporin biosynthesis and fungal virulence of Cercospora nicotianae. Mol Plant Microbe Interact 18(5):468–476

    PubMed  CAS  Google Scholar 

  • Chung KR, Jenns AE, Ehrenshaft M, Daub ME (1999) A novel gene required for cercosporin toxin resistance in the fungus Cercospora nicotianae. Mol Gen Genet 262:382–389

    PubMed  CAS  Google Scholar 

  • Ciuffetti LM, Pope MR, Dunkle LD, Daly JM, Knoche HW (1983) Isolation and structure of an inactive product from the host-specific toxin produced by Helminthosporium carbonum. Biochemistry 22:3507–3510

    CAS  Google Scholar 

  • Ciuffetti LM, Francl LJ, Ballance GM, Bockus WW, Lamari L, Meinhardt SW, Rasmussen JB (1998) Standardization of toxin nomenclature in the Pyrenophora tritici-repentis/wheat interaction. Can J Plant Pathol 20:421–424

    Google Scholar 

  • Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP (2010) Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187:911–919

    PubMed  CAS  Google Scholar 

  • Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127

    PubMed  Google Scholar 

  • Cole RJ, Dorner JW, Lansden JA, Cox RH, Pape C, Cunfer BM, Nicholson SS, Bendell DM (1977) Paspalum staggers: isolation and identification of tremorgenic metabolites from sclerotia of Claviceps paspali. J Agric Food Chem 25:1197–1201

    PubMed  CAS  Google Scholar 

  • Comstock JC, Scheffer RP (1973) Role of host-selective toxin in colonization of corn leaves by Helminthosporium carbonum. Phytopathology 63:24–29

    CAS  Google Scholar 

  • Coppock RW, Mostrom MS, Sparling CG, Jacobsen B, Ross SC (1990) Apparent zearalenone intoxication in a dairy herd from feeding spoiled acid-treated corn. Vet Hum Toxicol 32(3):246–248

    PubMed  CAS  Google Scholar 

  • Covert SF (1998) Supernumerary chromosomes in filamentous fungi. Curr Genet 33:311–319

    PubMed  CAS  Google Scholar 

  • Cox RJ (2007) Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org Biomol Chem 5(13):2010–2026

    PubMed  CAS  Google Scholar 

  • Craig AM (2009) Toxic effects of the endophyte in seed straw. In: Fribourg HA, Hannaway DB, West CP (eds) Tall fescue for the twenty-first century, vol 53, Agronomy monograph. ASA/CSSA/SSSA, Madison, pp 327–335

    Google Scholar 

  • Cross DL (2009) Toxic effects of the endophyte in horses. In: Fribourg HA, Hannaway DB, West CP (eds) Tall fescue for the twenty-first century, vol 53, Agronomy monograph. ASA/SSA/SSSA, Madison, pp 311–326

    Google Scholar 

  • Curtis MJ, Wolpert TJ (2002) The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J 29:295–312

    PubMed  Google Scholar 

  • Curtis MJ, Wolpert TJ (2004) The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J 38:244–259

    PubMed  CAS  Google Scholar 

  • Danko SJ, Kono Y, Daly JM, Suzuki Y, Takeuchi S, McCrery DA (1984) Structural and biological activity of a host-specific toxin produced by the fungal corn pathogen Phyllosticta maydis. Biochemistry 23:759–766

    CAS  Google Scholar 

  • Daub ME (1982) Peroxidation of tobacco membrane lipids by the photosensitizing toxin, cercosporin. Plant Physiol 69:1361–1364

    PubMed  CAS  Google Scholar 

  • Daub ME, Hangarter RP (1983) Production of singlet oxygen and superoxide by the fungal toxin, cercosporin. Plant Physiol 73:855–857

    PubMed  CAS  Google Scholar 

  • Daub ME, Herrero S, Chung K-R (2005) Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiol Lett 252(2):197–206

    PubMed  CAS  Google Scholar 

  • De Costa C (2002) St Anthony’s fire and living ligatures: a short history of ergometrine. Lancet 359:1768–1770

    PubMed  Google Scholar 

  • de Zélicourt A, Montiel G, Pouvreau J-B, Thoiron S, Delgrange S, Simier P, Delavault P (2009) Susceptibility of Phelipanche and Orobanche species to AAL-toxin. Planta 230:1047–1055

    PubMed  Google Scholar 

  • Desjardins AE (2006) Fusarium mycotoxins: chemistry, genetics, and biology. The American Phytopathological Society, Minnesota

    Google Scholar 

  • Desjardins AE, Spencer GF, Plattner RD, Beremand MN (1989) Furanocoumarin phytoalexins, trichothecene toxins, and infection of Pastinaca sativa by Fusarium sprorotrichioides. Phytopathology 79:170–175

    CAS  Google Scholar 

  • Desjardins AE, Hohn TM, McCormick SP (1992) The effect of gene disruption of trichodiene synthase (Tox5) on the virulence of Gibberella pulicaris. Mol Plant Microbe Interact 5:214–222

    CAS  Google Scholar 

  • 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 61:79–86

    PubMed  CAS  Google Scholar 

  • Desmond OJ, Manners JM, Stephens AE, Maclean DJ, Schenk PM et al (2008) The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Mol Plant Pathol 9:435–445

    PubMed  CAS  Google Scholar 

  • Dewey RE, Timothy DH, Levings CS III (1987) A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci USA 84:5374–5378

    PubMed  CAS  Google Scholar 

  • Dewey RE, Siedow JN, Timothy DH, Levings CS III (1988) A 13-kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science 239:293–295

    PubMed  CAS  Google Scholar 

  • Di R, Blechl A, Dill-Macky R, Tortora A, Tumer NE (2010) Expression of a truncated form of yeast ribosomal protein L3 in transgenic wheat improves resistance to Fusarium head blight. Plant Sci 178:374–380

    CAS  Google Scholar 

  • Diekman MA, Green ML (1992) Mycotoxins and reproduction in domestic livestock. J Anim Sci 70(5):1615–1627

    PubMed  CAS  Google Scholar 

  • Diez B, Gutierrez S, Barredo JL, van Solingen P, van der Voort LH, Martin JF (1990) The cluster of penicillin biosynthetic genes. Identification and characterization of the pcbAB gene encoding the alpha-aminoadipyl-cysteinyl-valine synthetase and linkage to pcbC and penDE genes. J Biol Chem 265:16358–16365

    PubMed  CAS  Google Scholar 

  • DiMenna ME, Lauren DR, Poole PR, Mortimer PH, Hill RA et al (1987) Zearalenone in New Zealand pasture herbage and the mycotoxin-producing potential of Fusarium species from pasture. N Z J Agric Res 30(4):499–504

    Google Scholar 

  • DiMenna ME, Mortimer PH, Prestidge RA, Hawkes AD, Sprosen JM (1992) Lolitrem B concentrations, counts of Acremonium lolii hyphae, and the incidence of ryegrass staggers in lambs on plots of A. lolii-infected perennial ryegrass. N Z J Agric Res 35:211–217

    CAS  Google Scholar 

  • Ding Y, Bojja RS, Du L (2004) Fum3p, a 2-ketoglutarate-dependent dioxygenase required for C-5 hydroxylation of fumonisins in Fusarium verticillioides. Appl Environ Microbiol 70:1931–1934

    PubMed  CAS  Google Scholar 

  • Easton HS (2007) Grasses and Neotyphodium endophytes: co-adaptation and adaptive breeding. Euphytica 154:295–306

    Google Scholar 

  • Evans BS, Robinson SJ, Kelleher NL (2011) Surveys of non-ribosomal peptide and polyketide assembly lines in fungi and prospects for their analysis in vitro and in vivo. Fungal Genet Biol 48(1):49–61

    PubMed  CAS  Google Scholar 

  • Faris JD, Friesen TL (2009) Reevaluation of a tetraploid wheat population indicates that the Tsnl-ToxA interaction is the only factor governing stagonospora nodorum blotch susceptibility. Phytopathology 99:906–912

    PubMed  CAS  Google Scholar 

  • Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS et al (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Nat Acad Sci USA 107:13544–13549

    PubMed  CAS  Google Scholar 

  • Faris JD, Zhang Z, Rasmussen JB, Friesen TL (2011) Variable expression of the Stagonospora nodorum effector SnToxA among isolates is correlated with levels of disease in wheat. Mol Plant Microbe Interact 24:1419–1426

    PubMed  CAS  Google Scholar 

  • Feng BN, Nakatsuka S, Goto T, Tsuge T, Nishimura S (1990) Biosynthesis of host-selective toxins produced by Alternaria alternata pathogens. I. (8R,9S)-9,10-epoxy-8-hydroxy-9-methyl-deca-(2E,4Z,6E)-trienoic acid as a biological precursor of AK-toxins. Agric Biol Chem 54:845–848

    CAS  Google Scholar 

  • Filajdic N, Sutton TB (1991) Identification and distribution of Alternaria mali on apples in North Carolina and susceptibility of different varieties of apples to Alternaria blotch. Plant Dis 75:1045–1048

    Google Scholar 

  • Fink-Gremmels J, Malekinejad H (2007) Clinical effects and biochemical mechanisms associated with exposure to the mycoestrogen zearalenone. Anim Feed Sci Technol 137(3–4):326–341

    CAS  Google Scholar 

  • Fleetwood DJ, Scott B, Lane GA, Tanaka A, Johnson RD (2007) A complex ergovaline gene cluster in Epichloë endophytes of grasses. Appl Environ Microbiol 73:2571–2579

    PubMed  CAS  Google Scholar 

  • Fletcher L (1986) Lolium endophyte and sheep performance on perennial ryegrass cultivars. Proc N Z Grassland Assoc 47:99–105

    Google Scholar 

  • Fletcher LR (1999) “Non-toxic” endophytes in ryegrass and their effect on livestock health and production. In: Woodfield DR, Matthew C (eds) Ryegrass endophyte: an essential New Zealand symbiosis. New Zealand Grassland Association, Napier, pp 133–139

    Google Scholar 

  • Fletcher LR, Harvey IC (1981) An association of a Lolium endophyte with ryegrass staggers. N Z Vet J 29:185–186

    PubMed  CAS  Google Scholar 

  • Foote CS (1976) Photosensitizing oxidation and singlet oxygen: consequences in biological systems. In: Pryor WA (ed) Free radicals in biology, vol II. Academic, New York, pp 85–133

    Google Scholar 

  • Fox EM, Howlett BJ (2008) Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol 11:481–487

    PubMed  CAS  Google Scholar 

  • Freeman GG, Morrison RI (1949) The isolation and chemical properties of trichothecin, an antifungal substance from Trichothecium roseum link. Biochem J 44:1–5

    PubMed  CAS  Google Scholar 

  • Fried HM, Warner JR (1981) Cloning of yeast gene for trichodermin resistance and ribosomal protein L3. Proc Natl Acad Sci 78:238–242

    PubMed  CAS  Google Scholar 

  • Friesen TL, Faris JD (2004) Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor Appl Genet 109:464–471

    PubMed  CAS  Google Scholar 

  • Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956

    PubMed  CAS  Google Scholar 

  • Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10:1421–1428

    PubMed  CAS  Google Scholar 

  • Gaffoor I, Trail F (2006) Characterization of two polyketide synthase genes involved in zearalenone biosynthesis in Gibberella zeae. Appl Environ Microbiol 72(3):1793–1799

    PubMed  CAS  Google Scholar 

  • Gallagher RT, Campbell AG, Hawkes AD, Holland PT, McGaveston DA, Pansier EA (1982) Ryegrass staggers: the presence of lolitrem neurotoxins in perennial ryegrass seed. N Z Vet J 30:183–184

    PubMed  CAS  Google Scholar 

  • Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R (1984) Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. J Chem Soc Chem Commun 9:614–616

    Google Scholar 

  • Gatenby WA, Munday-Finch SC, Wilkins AL, Miles CO (1999) Terpendole M, a novel indole-diterpenoid isolated from Lolium perenne infected with the endophytic fungus Neotyphodium lolii. J Agric Food Chem 47:1092–1097

    PubMed  CAS  Google Scholar 

  • Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185–1197

    PubMed  CAS  Google Scholar 

  • Gelderblom WCA, Jaskiewicz K, Marasas WFO, Thiel PG, Horak MJ, Vleggaar R, Kriek NPJ (1988) Fumonisins – novel mycotoxins with cancer promoting activity produced by Fusarium moniliforme. Appl Environ Microbiol 54:1806–1811

    PubMed  CAS  Google Scholar 

  • Gilchrist DG, Grogan RG (1976) Production and nature of a host-specific toxin from Alternaria alternata f. sp. lycopersici. Phytopathology 66(2):165–171

    Google Scholar 

  • Gilchrist DG, Wang H, Bostock RM (1995) Sphingosine-related mycotoxins in plant and animal disease. Can J Bot 73:S459–S467

    CAS  Google Scholar 

  • Glenn AE (2007) Mycotoxigenic Fusarium species in animal feed. Anim Feed Sci Technol 137(3–4):213–240

    CAS  Google Scholar 

  • 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 21:87–97

    PubMed  CAS  Google Scholar 

  • Grogan RG, Kimble KA, Misagi I (1975) A stem canker disease of tomato caused by Alternaria alternata f. sp. lycopersici. Phytopathology 65:880–886

    Google Scholar 

  • Gross ML, McCrery D, Crow F, Tomer KB, Pope MR, Ciuffetti LM, Knoche HW, Daly JM, Dunkle LD (1982) The structure of the toxin from Helminthosporium carbonum. Tet Lett 23:5381–5384

    CAS  Google Scholar 

  • Haarmann T, Machado C, Lubbe Y, Correia T, Schardl CL, Panaccione DG, Tudzynski P (2005) The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry 66:1312–1320

    PubMed  CAS  Google Scholar 

  • Hack E, Lin C, Yang H, Horner HT (1991) T-URF13 protein from mitochondria of Texas male-sterile maize (Zea mays L.): its purification and submitochondrial localization, and immunogold labeling in anther tapetum during microsporogenesis. Plant Physiol 95:861–870

    PubMed  CAS  Google Scholar 

  • Haese A, Schubert M, Herrmann M, Zocher R (1993) Molecular characterization of the enniatin synthetase gene encoding a multifunctional enzyme catalysing N-methyldepsipeptide formation in Fusarium scirpi. Mol Microbiol 7:905–914

    PubMed  CAS  Google Scholar 

  • Han F, Kleinhofs A, Kilian A, Ullrich SE (1997) Cloning and mapping of a putative barley NADP-dependent HC-toxin reductase. Mol Plant Microbe Interact 10:234–239

    PubMed  CAS  Google Scholar 

  • Han Y, Liu X, Benny U, Kistler HC, VanEtten HD (2001) Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J 25:305–314

    PubMed  CAS  Google Scholar 

  • Harimoto Y, Hatta R, Kodama M, Yamamoto M, Otani H, Tsuge T (2007) Expression profiles of genes encoded by the supernumerary chromosome controlling AM-toxin biosynthesis and pathogenicity in Alternaria alternata. Mol Plant Microbe Interact 20:1463–1476

    PubMed  CAS  Google Scholar 

  • Harris LJ, Gleddie SC (2001) A modified Rpl3 gene from rice confers tolerance of the Fusarium graminearum mycotoxin deoxynivalenol to transgenic tobacco. Physiol Mol Plant Pathol 58:173–181

    CAS  Google Scholar 

  • Hatta R, Ito K, Hosaki Y, Tanaka T, Tanaka A, Yamamoto M, Akimitsu K, Tsuge T (2002) A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59–70

    PubMed  CAS  Google Scholar 

  • Hoat TX, Nakayashiki H, Tosa Y, Mayama S (2006) Specific cleavage of ribosomal RNA and mRNA during victorin-induced apoptotic cell death in oat. Plant J 46:922–933

    PubMed  CAS  Google Scholar 

  • Hopkins AA, Young CA, Panaccione DG, Simpson WR, Mittal S, Bouton JH (2010) Agronomic performance and lamb health among several tall fescue novel endophyte combinations in the south-central USA. Crop Sci 50:1552–1561

    Google Scholar 

  • Hopkins AA, Young CA, Butler TJ, Bouton JH (2011) Registration of Texoma MaxQ II tall fescue. J Plant Registr 5:14–18

    Google Scholar 

  • Hopwood DA, Khosla C (1992) Genes for polyketide secondary metabolic pathways in microorganisms and plants. Ciba F Symp 171:88–106

    CAS  Google Scholar 

  • Hopwood DA, Sherman DH (1990) Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu Rev Genet 24:37–66

    PubMed  CAS  Google Scholar 

  • Huang J, Lee SH, Lin C, Medici R, Hack E, Myers AM (1990) Expression in yeast of the T-URF13 protein from Texas male-sterile maize mitochondria confers sensitivity to methomyl and to Texas-cytoplasm-specific fungal toxins. EMBO J 9:339–348

    PubMed  CAS  Google Scholar 

  • Hume D, Ryan D, Cooper B, Popay A (2007) Agronomic performance of AR37-infected ryegrass in northern New Zealand. Proc N Z Grassland Assoc 69:201–205

    Google Scholar 

  • Imazaki A, Tanaka A, Harimoto Y, Yamamoto M, Akimitsu K et al (2010) Contribution of peroxisomes to secondary metabolism and pathogenicity in the fungal plant pathogen Alternaria alternata. Eukaryot Cell 9(5):682–694

    PubMed  CAS  Google Scholar 

  • Inderbitzin P, Asvarak T, Turgeon BG (2010) Six new genes required for production of T-Toxin, a polyketide determinant of high virulence of Cochliobolus heterostrophus to maize. Molec Plant Microbe Interact 23(4):458–472

    CAS  Google Scholar 

  • Ito K, Tanaka T, Hatta R, Yamamoto M, Akimitsu K, Tsuge T (2004) Dissection of the host range of the fungal plant pathogen Alternaria alternata by modification of secondary metabolism. Mol Microbiol 52:399–411

    PubMed  CAS  Google Scholar 

  • Jansen C, von Wettstein D, Schafer W, Kogel K-H, Felk A et al (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci USA 102:16892–16897

    PubMed  CAS  Google Scholar 

  • Jenns AE, Daub ME, Upchurch RG (1989) Regulation of cercosporin accumulation in culture by medium and temperature manipulation. Phytopathology 79:213–219

    CAS  Google Scholar 

  • Jensen JG, Popay AJ (2004) Perennial ryegrass infected with AR37 endophyte reduces survival of porina larvae. N Z Plant Protect 57:323–328

    Google Scholar 

  • Jensen J, Popay A, Tapper B (2009) Argentine stem weevil adults are affected by meadow fescue endophyte and its loline alkaloids. N Z Plant Protect 62:12–18

    CAS  Google Scholar 

  • Johal GS, Briggs SP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258:985–987

    PubMed  CAS  Google Scholar 

  • Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K (2000a) Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact 13:742–753

    PubMed  CAS  Google Scholar 

  • Johnson RD, Johnson L, Kohmoto K, Otani H, Lane CR, Kodama M (2000b) A polymerase chain reaction-based method to specifically detect Alternaria alternata apple pathotype (A. mali), the causal agent of Alternaria blotch of apple. Phytopathology 90:973–976

    PubMed  CAS  Google Scholar 

  • Johnson L, Johnson RD, Akamatsu H, Salamiah A, Otani H, Kohmoto K, Kodama M (2001) Spontaneous loss of a conditionally dispensable chromosome from Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr Genet 40:65–72

    PubMed  CAS  Google Scholar 

  • Johnson R, Voisey C, Johnson L, Pratt J, Fleetwood D, Khan A, Bryan G (2007) Distribution of NRPS gene families within the Neotyphodium/Epichloë complex. Fungal Genet Biol 44:1180–1190

    PubMed  CAS  Google Scholar 

  • Kaspi CI, Siedow JN (1993) Cross-linking of the cms-T mitochondrial pore-forming protein URF13 by N, N’-dicyclohexylcarbodiimide and its effect on URF13 sensitivity to fungal toxins. J Biol Chem 268:5828–5833

    PubMed  CAS  Google Scholar 

  • Kawai M, Rich DH (1983) Total synthesis of the cyclic tetrapeptide, HC-toxin. Tet Lett 24:5309–5312

    CAS  Google Scholar 

  • Keller N (2011) The fungal treasure chest: spore origins? Fungal Biol Rev 25:73–77

    Google Scholar 

  • Kijima M, Yosida M, Sugita K, Horinouchi S, Beppu T (1993) Trapoxin, an antitumor cyclic tetrapeptide, is an irreversible inhibitor of mammalian histone deacetylase. J Biol Chem 268:553–560

    Google Scholar 

  • Kim S-D, Knoche HW, Dunkle LD (1987) Essentiality of the ketone function for toxicity of the host-selective toxin produced by Helminthosporium carbonum. Physiol Mol Plant Pathol 30:433–440

    CAS  Google Scholar 

  • Kim Y-T, Lee Y-R, Jin J, Han K-H, Kim H et al (2005) Two different polyketide synthase genes are required for synthesis of zearalenone in Gibberella zeae. Mol Microbiol 58(4):1102–1113

    PubMed  CAS  Google Scholar 

  • Kleinkauf H, von Döhren H (1990) Nonribosomal biosynthesis of peptide antibiotics. Eur J Biochem 236:335–351

    Google Scholar 

  • Knaus H, McManus OB, Lee SH, Schmalhofer WA, Garcia-Calvo M, Helms LMH, Sanchez M, Giangiacomo K, Reuben JP, Smith AB, Kaczorowski GJ, Garcia ML (1994) Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated channels. Biochemistry 33:5819–5828

    PubMed  CAS  Google Scholar 

  • Kodama M, Rose MS, Yang G, Yun SH, Yoder OC, Turgeon BG (1999) The translocation-associated Tox1 locus of Cochliobolus heterostrophus is two genetic elements on two different chromosomes. Genetics 151:585–596

    PubMed  CAS  Google Scholar 

  • Kohmoto K, Otani H (1991) Host recognition by toxigenic plant pathogens. Experientia 47:755–764

    PubMed  CAS  Google Scholar 

  • Kohmoto K, Taniguchi T, Nishimura S (1974) Correlation between the susceptibility of apple cultivars to Alternaria mali and their sensitivity to AM-toxin I. Ann Phytopathol Soc Jpn 43:65–66

    Google Scholar 

  • Kohmoto K, Khan ID, Renbutsu Y, Taniguchi T, Nishimura S (1976) Multiple host-specific toxins of Alternaria mali and their effect on the permeability of host cells. Physiol Plant Pathol 8:141–153

    CAS  Google Scholar 

  • Kohmoto K, Scheffer RP, Whiteside JO (1979) Host-selective toxins from Alternaria citri. Phytopathology 69:667–671

    CAS  Google Scholar 

  • Kohmoto K, Itoh Y, Shimomura N, Kondoh Y, Otani H, Kodama M, Nishimura S, Nakatsuka S (1993) Isolation and biological activities of two host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83:495–502

    CAS  Google Scholar 

  • Kono Y, Daly JM (1979) Characterization of the host-specific pathotoxin produced by Helminthosporium maydis race T affecting corn with Texas male sterile cytoplasm. Bioorg Chem 8:391–397

    CAS  Google Scholar 

  • Kono Y, Danko SJ, Suzuki Y, Takeuchi S, Daly JM (1983) Structure of the host-specific pathotoxins produced by Phyllosticta maydis. Tet Lett 24:3803–3806

    CAS  Google Scholar 

  • Korth KL, Kaspi CI, Siedow JN, Levings CS III (1991) URF13, a maize mitochondrial pore-forming protein, is oligomeric and has a mixed orientation in Escherichia coli plasma membranes. Proc Natl Acad Sci USA 88:10865–10869

    PubMed  CAS  Google Scholar 

  • Kościelniak J, Ostrowska A, Biesaga-Kościelniak J, Filek W, Janeczko A et al (2011) The effect of zearalenone on PSII photochemical activity and growth in wheat and soybean under salt (NaCl) stress. Acta Physiol Plant 33(6):2329–2338

    Google Scholar 

  • Koulman A, Lane GA, Christensen MJ, Fraser K, Tapper BA (2007) Peramine and other fungal alkaloids are exuded in the guttation fluid of endophyte-infected grasses. Phytochemistry 68:355–360

    PubMed  CAS  Google Scholar 

  • Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci USA 100(26):15670–15675

    PubMed  CAS  Google Scholar 

  • Kuo M-S, Scheffer RP (1970) Comparative effects of host-specific toxins and Helminthosporium infections on respiration and carboxylation by host tissue. Phytopathology 60:1391–1394

    CAS  Google Scholar 

  • Kutil BL, Greenwald C, Liu G, Spiering MJ, Schardl CL, Wilkinson HH (2007) Comparison of loline alkaloid gene clusters across fungal endophytes: predicting the co-regulatory sequence motifs and the evolutionary history. Fungal Genet Biol 44:1002–1010

    PubMed  CAS  Google Scholar 

  • Lamari L, Bernier CC (1989) Toxin of Pyrenophora tritici-repentis: host-specificity, significance in disease, and inheritance of host reaction. Phytopathology 79:740–744

    CAS  Google Scholar 

  • Lamari L, Bernier CC (1991) Genetics of tan necrosis and extensive chlorosis in tan spot of wheat caused by Pyrenophora tritici-repentis. Phytopathology 81:1092–1095

    Google Scholar 

  • Lamari L, Ballance GM, Orolaza NP, Kowatch R (1995) In planta production and antibody neutralization of the Ptr necrosis toxin from Pyrenophora tritici-repentis. Phytopathology 85:333–338

    CAS  Google Scholar 

  • Latch GCM, Christensen MJ (1985) Artificial infection of grasses with endophytes. Ann Appl Biol 107:17–24

    Google Scholar 

  • Leach J, Tegtmeier KJ, Daly JM, Yoder OC (1982) Dominance at the Tox1 locus controlling T-toxin production by Cochliobolus heterostrophus. Physiol Plant Pathol 21:327–333

    CAS  Google Scholar 

  • Lee BN, Kroken S, Chou DY, Robbertse B, Yoder OC, Turgeon BG (2005) Functional analysis of all nonribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryot Cell 4:545–555

    PubMed  CAS  Google Scholar 

  • Lee TV, Johnson LJ, Johnson RD, Koulman A, Lane GA, Lott JS, Arcus VL (2010) Structure of a eukaryotic nonribosomal peptide synthetase adenylation domain that activates a large hydroxamate amino acid in siderophore biosynthesis. J Biol Chem 285:2415–2427

    PubMed  CAS  Google Scholar 

  • Leisch JM, Sweeley CC, Staffeld GD, Anderson MS, Weber DJ, Scheffer RP (1982) Structure of HC-toxin, a cyclic tetrapeptide from Helminthosporium carbonum. Tetrahedron 38:45–48

    Google Scholar 

  • Levings CS III (1990) The Texas cytoplasm of maize: cytoplasmic male sterility and disease susceptibility. Science 250:942–947

    PubMed  CAS  Google Scholar 

  • Lim SM, Hooker AL (1971) Southern corn leaf blight: genetic control of toxin production in race T and race O of Cochliobolus heterostrophus. Genetics 69:115–117

    PubMed  CAS  Google Scholar 

  • Lipmann F (1971) Attempts to map a process evolution of peptide biosynthesis. Science 173:875–884

    PubMed  CAS  Google Scholar 

  • Liu Z, Faris JD, Oliver RP, Tan K-C, Solomon PS, McDonald MC, McDonald BA, Nunez A, Lu S, Rasmussen JB et al (2009) SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 Gene. PLoS Pathog 5:e1000581

    PubMed  Google Scholar 

  • Liu Z, Zhang Z, Faris JD, Oliver RP, Syme R, McDonald MC, McDonald BA, Solomon PS, Lu S, Shelver WL et al (2012) The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathog 8:e1002467

    PubMed  CAS  Google Scholar 

  • Lorang JM, Carkaci-Salli N, Wolpert TJ (2004) Identification and characterization of victorin sensitivity in Arabidopsis thaliana. Mol Plant Microbe Interact 17:577–582

    PubMed  CAS  Google Scholar 

  • Lorang JM, Sweat TA, Wolpert TJ (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci USA 104:14861–14866

    PubMed  CAS  Google Scholar 

  • Lorang J, Cuesta-Marcos A, Hayes PM, Wolpert TJ (2010) Identification and mapping of adult-onset sensitivity to victorin in barley. Mol Breed 26:545–550

    CAS  Google Scholar 

  • Lousberg RJJC, Weiss U, Salmink CA, Aronone A, Merlini L, Nasini G (1971) The structures of cercosporin, a naturally occurring quinone. Chem Commun 71:1463–1464

    Google Scholar 

  • Lu S, Lyngholm L, Yang G, Bronson C, Yoder OC, Turgeon BG (1994) Tagged mutations at the Tox1 locus of Cochliobolus heterostrophus by restriction enzyme-mediated integration. Proc Natl Acad Sci USA 91:12649–12653

    PubMed  CAS  Google Scholar 

  • Lysøe E, Bone KR, Klemsdal SS (2009) Real-time quantitative expression studies of the zearalenone biosynthetic gene cluster in Fusarium graminearum. Phytopathology 99(2):176–184

    PubMed  Google Scholar 

  • Ma LJ, van der Does HC, Borkovich KA et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373

    PubMed  CAS  Google Scholar 

  • Mackintosh CA, Lewis J, Radmer LE, Shin S, Heinen SJ et al (2006) Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight. Plant Cell Rep 26:479–488

    PubMed  Google Scholar 

  • Macri F, Vianello A (1979) Inhibition of K + uptake, H + extrusion and K + activated ATPase, and depolarization of transmembrane potential plant tissues treated with Cercospora beticola toxin. Physiol Plant Pathol 15:161–170

    CAS  Google Scholar 

  • Maier FJ, Miedaner T, Hadeler B, Felk A, Salomon S et al (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

    PubMed  CAS  Google Scholar 

  • Manning VA, Ciuffetti LM (2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17:3203–3212

    PubMed  CAS  Google Scholar 

  • Manning VA, Andrie RM, Trippe AF, Ciuffetti LM (2004) Ptr ToxA requires multiple motifs for complete activity. Mol Plant Microbe Interact 17:491–501

    PubMed  CAS  Google Scholar 

  • Manning VA, Hardison LK, Ciuffetti LM (2007) Ptr ToxA interacts with a chloroplast-localized protein. Mol Plant Microbe Interact 20:168–177

    PubMed  CAS  Google Scholar 

  • Manning VA, Hamilton SM, Karplus PA, Ciuffetti LM (2008) The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization. Mol Plant Microbe Interact 21:315–325

    PubMed  CAS  Google Scholar 

  • Marahiel MA, Stachelhaus T, Mootz HD (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97:2651–2673

    PubMed  CAS  Google Scholar 

  • McCormick SP, Stanley AM, Stover NA, Alexander NJ (2011) Trichothecenes: from simple to complex mycotoxins. Toxins 2011 3(7):802–814

    CAS  Google Scholar 

  • McLaughlin JE, Bin-Umer MA, Tortora A, Mendez N, McCormick S et al (2009) A genome-wide screen in Saccharomyces cerevisiae reveals a critical role for the mitochondria in the toxicity of a trichothecene mycotoxin. Proc Natl Acad Sci 106:21883–21888

    PubMed  CAS  Google Scholar 

  • Meehan F, Murphy HC (1946) A new Helminthosporium blight of oats. Science 104:412–413

    Google Scholar 

  • Meehan F, Murphy HC (1947) Differential toxicity of metabolic by-products of Helminthosporium victoriae. Science 106:270–271

    PubMed  CAS  Google Scholar 

  • Meeley RB, Walton JD (1991) Enzymatic detoxification of HC-toxin, the host-selective cyclic peptide from Cochliobolus carbonum. Plant Physiology 97(3):1080–1086

    PubMed  CAS  Google Scholar 

  • Meeley RB, Johal GS, Briggs SP, Walton JD (1992) A biochemical phenotype for a disease resistance gene of maize. Plant Cell 4(1):71–77

    PubMed  CAS  Google Scholar 

  • Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, M’Barek SB, Gohari AM, Jashni MK, Stergiopoulos I, Kema GHJ, de Wit PJGM (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 35:542–554

    PubMed  CAS  Google Scholar 

  • Merhoff GC, Porter JM (1974) Ergot intoxication: historical review and description of unusual clinical manifestations. Ann Surg 180:773

    PubMed  CAS  Google Scholar 

  • Miyazaki S, Ishizaki I, Ishizaka M, Kanbara T, Ishiguro-Takeda Y (2004) Lolitrem B residue in fat tissues of cattle consuming endophyte-infected perennial ryegrass straw. J Vet Diagn Invest 16:340

    PubMed  Google Scholar 

  • Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS, Kenerley CM (2012) Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 158:155–165

    PubMed  CAS  Google Scholar 

  • Mullen TD, Jenkins RW, Clarke CJ, Bielawski J, Hannun YA, Obeid LM (2011) Ceramide synthase-dependent ceramide generation and programmed cell death: involvement of salvage pathway in regulating postmitochondrial events. J Biol Chem 286:15929–15942

    PubMed  CAS  Google Scholar 

  • 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 USA 95:1686–1691

    PubMed  CAS  Google Scholar 

  • Musser SM, Plattner RD (1997) Fumonisin composition in cultures of Fusarium moniliforme, Fusarium proliferatum, and Fusarium nygami. J Agric Food Chem 45:1169–1173

    CAS  Google Scholar 

  • Nakashima T, Ueno T, Fukami H (1982) Structure elucidation of AK-toxins, host-specific phytotoxic metabolites produced by Alternaria kikuchiana Tanaka. Tet Lett 23:4469–4472

    CAS  Google Scholar 

  • Nakashima T, Ueno T, Fukami H, Taga T, Masuda H, Osaki K, Otani H, Kohomoto K, Hishimura S (1985) Isolation and structures of AK-toxin I and II, host-specific phytotoxic metabolites produced by Alternaria alternata Japanese pear pathotype. Agric Biol Chem 49:807–815

    CAS  Google Scholar 

  • Nakatsuka S, Feng B-N, Goto T, Tsuge T, Nishimura S (1990) Biosynthetic origin of (8R,9S)-9,10-epoxy-8-hydroxy-9-methyl-deca-(2E,4Z,6E)-trienoic acid, a precursor of AK-toxins produced by Alternaria alternata Japanese pear pathotype. Phytochemistry 29:1529–1531

    CAS  Google Scholar 

  • Namiki F, Okamoto H, Katou K, Yamamoto M, Nishimura S, Nakatsuka S, Goto T, Kohmoto K, Otani H, Novacky A (1986) Studies on host-specific AF-toxins produced by Alternaria alternata strawberry pathotype causing Alternaria black spot of strawberry. V. Effect of toxins on membrane potential of susceptible plants as assessed by electrophysiological method. Ann Phytopathol Soc Jpn 52:610–619

    Google Scholar 

  • Navarre DA, Wolpert TJ (1995) Inhibition of the glycine decarboxylase multienzyme complex by the host-selective toxin victorin. Plant Cell 7:463–471

    PubMed  CAS  Google Scholar 

  • Navarre DA, Wolpert TJ (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 11:237–249

    PubMed  CAS  Google Scholar 

  • Nelson RR, Ullstrup AJ (1961) The inheritance of pathogenicity in Cochliobolus carbonum. Phytopathology 51:1–2

    Google Scholar 

  • Nicholson MJ, Koulman A, Monahan BJ, Pritchard BL, Payne GA, Scott B (2009) Identification of two aflatrem biosynthesis gene loci in Aspergillus flavus and metabolic engineering of Penicillium paxilli to elucidate their function. Appl Environ Microbiol 75:7469–7481

    PubMed  CAS  Google Scholar 

  • Nikolskaya AN, Panaccione DG, Walton JD (1995) Identification of peptide synthetase-encoding genes from filamentous fungi producing host-selective phytotoxins or analogs. Gene 165:207–211

    PubMed  CAS  Google Scholar 

  • Nishiuchi T, Masuda D, Nakashita H, Ichimura K, Shinozaki K et al (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

    PubMed  CAS  Google Scholar 

  • Ohsato S, Ochiai-Fukuda T, Nishiuchi T, Takahashi-Ando N, Koizumi S et al (2007) Transgenic rice plants expressing trichothecene 3-O-acetyltransferase show resistance to the Fusarium phytotoxin deoxynivalenol. Plant Cell Rep 26:531–538

    PubMed  CAS  Google Scholar 

  • Okubara PA, Blechl AE, McCormick SP, Alexander NJ, Dill-Macky R et al (2002) Engineering deoxynivalenol metabolism in wheat through the expression of a fungal trichothecene acetyltransferase gene. Theor Appl Genet 106:74–83

    PubMed  CAS  Google Scholar 

  • Okuno T, Ishita Y, Sawai K, Matsumoto T (1974) Characterization of alternariolide, a host-specific toxin produced by Alternaria mali Roberts. Chem Lett 1974:635–638

    Google Scholar 

  • Otani H, Kohmoto K (1992) Host-specific toxins of Alternaria species. In: Chelkowski J, Visconti A (eds) Alternaria: biology, plant diseases and metabolites. Elsevier, Amsterdam, pp 123–156

    Google Scholar 

  • Otani H, Nishimura S, Kohmoto K (1972) Nature of specific susceptibility to Alternaria kikuchiana in Nijisseiki cultivars among Japanese pears (I). J Fac Agric Tottori Univ 7:5–12

    Google Scholar 

  • Otani J, Kohmoto K, Nishimura S, Nakashima T, Ueno T, Fukami H (1985) Biological activities of AK-toxins I and II, host-specific toxins from Alternaria alternata Japanese pear pathotype. Ann Phytopathol Soc Jpn 51:285–293

    CAS  Google Scholar 

  • Otani H, Tomiyama K, Okamoto H, Nishimura S, Kohmoto K (1989) Effect of AK-toxin produced by Alternaria alternata Japanese pear pathotype on membrane potential of pear cells. Ann Phytopathol Soc Jpn 55:466–468

    Google Scholar 

  • Panaccione DG (1996) Multiple families of peptide synthetase genes from ergopeptine-producing fungi. Mycol Res 100:429–436

    CAS  Google Scholar 

  • 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 USA 89:6590–6594

    PubMed  CAS  Google Scholar 

  • Panaccione DG, Johnson RD, Wang J, Young CA, Damrongkool P, Scott B, Schardl CL (2001) Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc Natl Acad Sci USA 98:12820–12825

    PubMed  CAS  Google Scholar 

  • Parent-Massin D (2004) Haematotoxicity of trichothecenes. Toxicol Lett 153:75–81

    PubMed  CAS  Google Scholar 

  • Park P, Tsuda M, Hayashi Y, Ueno T (1977) Effect of a host-specific toxin (AM-toxin I) produced by Alternaria mali, an apple pathogen, on the ultrastructure of plasma membrane of cells in apple and Japanese pear leaves. Can J Bot 55:2383–2393

    CAS  Google Scholar 

  • Park P, Nishimura S, Kohmoto K, Otani H, Tsujimoto K (1981) Two action sites of AM-toxin I produced by apple pathotype of Alternaria alternata in host cells: an ultrastructural study. Can J Bot 59:301–310

    Google Scholar 

  • Park P, Ohno T, Nishimura S, Kohmoto K, Otani H (1987) Leakage of sodium ions from plasma membrane modification, associated with permeability change, in host cells treated with a host-specific toxin from a Japanese pear pathotype of Alternaria alternata. Can J Bot 65:330–339

    CAS  Google Scholar 

  • Park P, Lee SS, Ohno T, Tsuge T, Nishimura S (1992) Slightly damaged type of plasma membrane modification in strawberry leaves treated with AF-toxin I produced by Alternaria alternata strawberry pathotype. Ann Phytopathol Soc Jpn 58:431–445

    CAS  Google Scholar 

  • Patchett B, Chapman R, Fletcher L, Gooneratne S (2008) Root loline concentration in endophyte-infected meadow fescue (festuca pratensis) is increased by grass grub (Costelytra zealandica) attack. N Z Plant Protect 61:210–214

    CAS  Google Scholar 

  • Pedley KF, Walton JD (2001) Regulation of cyclic peptide biosynthesis in a plant pathogenic fungus by a novel transcription factor. Proc Natl Acad Sci USA 98:14174–14179

    PubMed  CAS  Google Scholar 

  • Pestka JJ (2007) Deoxynivalenol: toxicity, mechanisms and animal health risks. Anim Feed Sci Technol 137:283–298

    CAS  Google Scholar 

  • Pitkin JW, Panaccione DG, Walton JD (1996) A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant pathogenic fungus Cochliobolus carbonum. Microbiology 142:1557–1565

    PubMed  CAS  Google Scholar 

  • Pope MR, Ciuffetti LM, Knoche HW, McCrery D, Daly JM, Dunkle LD (1983) Structure of the host-specific toxin produced by Helminthosporium carbonum. Biochemistry 22:3502–3506

    CAS  Google Scholar 

  • Porter JK, Bacon CW, Robbins JD, Betowski D (1981) Ergot alkaloid identification in Clavicipitaceae systemic fungi of pasture grasses. J Agric Food Chem 29:653–657

    CAS  Google Scholar 

  • 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 8:593–601

    PubMed  CAS  Google Scholar 

  • Proctor RH, Desjardins AE, Plattner RD, Hohn TM (1999) A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet Biol 27:100–112

    PubMed  CAS  Google Scholar 

  • Proctor RH, Brown DW, Plattner RD, Desjardins AE (2003) Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet Biol 38:237–249

    PubMed  CAS  Google Scholar 

  • Proctor RH, Plattner RD, Desjardins AE, Busman M, Butchko RAE (2006) Fumonisin production in the maize pathogen Fusarium verticillioides: genetic basis of naturally occurring chemical variation. J Agric Food Chem 54:2424–2430

    PubMed  CAS  Google Scholar 

  • Proctor RH, McCormick SP, Alexander NJ, Desjardins AE (2009) Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol Microbiol 74:1128–1142

    PubMed  CAS  Google Scholar 

  • Ransom R, Walton JD (1997) Histone hyperacetylation in maize in response to treatment with HC-toxin or infection by the filamentous fungus Cochliobolus carbonum. Plant Physiol 115:1021–1027

    PubMed  CAS  Google Scholar 

  • Rasmussen JB, Scheffer RP (1988) Isolation and biological activities of four selective toxins from Helminthosporium carbonum. Plant Physiol 86:187–191

    PubMed  CAS  Google Scholar 

  • Rausch C, Weber T, Kohlbacher O, Wohlleben W, Huson DH (2005) Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res 33:5799–5808

    PubMed  CAS  Google Scholar 

  • Reed KFM, Walsh JR, Sprague M (2004) Zearalenone and its presence in pasture. Anim Prod Aust 25:140–143

    Google Scholar 

  • Rhoads DM, Burnner-Neuenschwander B, Levings CS III (1998) Characterization of the interaction between fungal pathotoxins and URF13, the cms-T maize mitochondrial T-toxin receptor. In: Yoder OC, Kohmoto K (eds) Molecular genetics of host specific toxins in plant disease. Kluwer, The Netherlands, pp 355–365

    Google Scholar 

  • Rocha O, Ansari K, Doohan FM (2005) Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Addit Contam 22:369–378

    PubMed  CAS  Google Scholar 

  • Rose MS, Yun S-H, Asvarak T, Lu S-W, Yoder OC et al (2002) A decarboxylase encoded at the Cochliobolus heterostrophus translocation-associated Tox1B locus is required for polyketide (T-toxin) biosynthesis and high virulence on T-cytoplasm maize. Molec Plant Microbe Interact 15(9):883–893

    CAS  Google Scholar 

  • Rotter BA, Thompson BK, Lessard M, Trenholm HL, Tryphonas H (1994) Influence of low-level exposure to Fusarium mycotoxins on selected immunological and hematological parameters in young swine. Toxicol Sci 23:117–124

    CAS  Google Scholar 

  • Saikia S, Scott B (2009) Functional analysis and subcellular localization of two geranylgeranyl diphosphate synthases from Penicillium paxilli. Molec Genet Genom 282:257–271

    CAS  Google Scholar 

  • Saito K, Niizeki K (1988) Fundamental studies on breeding of the apple. IX. Genetic analysis of resistance to Alternaria blotch in the interspecific crosses. Bull Fac Agric Hirosaki Univ 50:27–34

    Google Scholar 

  • Sarma GN, Manning VA, Ciuffetti LM, Karplus PA (2005) Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell 17:3190–3202

    PubMed  CAS  Google Scholar 

  • Sawamura K (1966) Studies on spotted disease of apples. VI. On the host-specific toxin of Alternaria mali Roberts. Bull Hortic Res Stn Japan Ser C 4:43–59

    Google Scholar 

  • Sawamura K (1990) Alternaria blotch. In: Jones AL, Aldwinckle H (eds) Compendium of apple and pear diseases. APS Press, St. Paul, pp 24–25

    Google Scholar 

  • Schardl CL (1996) Epichloë species: fungal symbionts of grasses. Annu Rev Phytopathol 34:109–130

    PubMed  CAS  Google Scholar 

  • Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340

    PubMed  CAS  Google Scholar 

  • Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007) Loline alkaloids: currencies of mutualism. Phytochemistry 68:980–996

    PubMed  CAS  Google Scholar 

  • Schardl CL, Young CA, Faulkner JR, Florea S, Pan J (2012) Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol 5:331–344

    Google Scholar 

  • Scheffer RP, Ullstrup AJ (1965) A host-specific toxic metabolite from Helminthosporium carbonum. Phytopathology 55:1037–1038

    CAS  Google Scholar 

  • Scheffer RP, Nelson RR, Ullstrup AJ (1967) Inheritance of toxin production and pathogenicity in Cochliobolus carbonum and Cochliobolus victoriae. Phytopathology 57:1288–1291

    Google Scholar 

  • Scherm B, OrrÙ M, Balmas V, Spanu F, Azara E et al (2011) Altered trichothecene biosynthesis in TRI6-silenced transformants of Fusarium culmorum influences the severity of crown and foot rot on durum wheat seedlings. Mol Plant Pathol 12:759–771

    PubMed  CAS  Google Scholar 

  • Schoevers EJ, Santos RR, Colenbrander B, Fink-Gremmels J, Roelen BAJ (2012) Transgenerational toxicity of Zearalenone in pigs. Reprod Toxicol 34(1):110–119

    PubMed  CAS  Google Scholar 

  • Schwarzer D, Finking R, Marahiel MA (2003) Nonribosomal peptides: from genes to products. Nat Prod Rep 20:275–287

    PubMed  CAS  Google Scholar 

  • Scott-Craig JS, Panaccione DG, Pocard JA, Walton JD (1992) The multifunctional cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungus Cochliobolus carbonum is encoded by a 15.7-kb open reading frame. J Biol Chem 67:26044–26049

    Google Scholar 

  • Seshime Y, Juvvadi PR, Fujii I, Kitamoto K (2005) Discovery of a novel superfamily of type III polyketide synthases in Aspergillus oryzae. Biochem Biophys Res Commun 331(1):253–260

    PubMed  CAS  Google Scholar 

  • Shabeer A, Bockus WW (1988) Tan spot effects on yield and yield components relative to growth stage in winter wheat. Plant Disease 72:599–602

    Google Scholar 

  • Shiba T, Sugawara K (2009) Fungal loline alkaloids in grass–endophyte associations confer resistance to the rice leaf bug, Trigonotylus caelestialium. Entomol Exp Appl 130:55–62

    Google Scholar 

  • Shimizu N, Hosogi N, Hyon GS, Jiang S, Inoue K et al (2006) Reactive oxygen species (ROS) generation and ROS-induced lipid peroxidation are associated with plasma membrane modifications in host cells in response to AK-toxin I from Alternaria alternata Japanese pear pathotype. J Gen Plant Pathol 72(1):6–15

    CAS  Google Scholar 

  • Shimomura N, Otani H, Kodama M, Kohmoto K (1991) Two primary action sites for AM-toxin produced by Alternaria alternata apple pathotype and their pathological significance. Ann Phytopathol Soc Jpn 57:47–255

    Google Scholar 

  • Shin S, Mackintosh CA, Lewis J, Heinen SJ, Radmer L et al (2008) Transgenic wheat expressing a barley class II chitinase gene has enhanced resistance against Fusarium graminearum. J Exp Bot 59:2371–2378

    PubMed  CAS  Google Scholar 

  • Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC (1990) Fungal endophyte-infected grasses: alkaloid accumulation and aphid response. J Chem Ecol 16:3301–3315

    CAS  Google Scholar 

  • Slot JC, Rokas A (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21:134–139

    PubMed  CAS  Google Scholar 

  • Smith JF, Morris CA (2006) Review of zearalenone studies with sheep in New Zealand. Proc New Zeal Soc An 66:306–310

    Google Scholar 

  • Solomon PS, Lowe RGT, Tan K-C, Waters ODC, Oliver RP (2006) Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Molec Plant Pathol 7:147–156

    Google Scholar 

  • Spassieva SD, Markham JE, Hille J (2002) The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 32:561–572

    PubMed  CAS  Google Scholar 

  • Spiering MJ, Wilkinson HH, Blankenship JD, Schardl CL (2002) Expressed sequence tags and genes associated with loline alkaloid expression by the fungal endophyte Neotyphodium uncinatum. Fungal Genet Biol 36:242–254

    PubMed  CAS  Google Scholar 

  • Spiering MJ, Moon CD, Wilkinson HH, Schardl CL (2005) Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 169:1403–1414

    PubMed  CAS  Google Scholar 

  • Spiering MJ, Faulkner JR, Zhang DX, Machado C, Grossman RB, Schardl CL (2008) Role of the LolP cytochrome P450 monooxygenase in loline alkaloid biosynthesis. Fungal Genet Biol 45:1307–1314

    PubMed  CAS  Google Scholar 

  • Stachelhaus T, Mootz HD, Marahiel MA (1999) The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 6:493–505

    PubMed  CAS  Google Scholar 

  • Stadler P, Stütz P (1975) The ergot alkaloids. Alkaloids Chem Physiol 15:1–40

    CAS  Google Scholar 

  • Stein T, Vater J, Kruft V, Wittmann-Liebold B, Franke P, Panico M, McDowell R, Morris HR (1994) Detection of 4¢-phosphopantetheine as the thioester binding site for L-valine of gramicidin S synthetase 2. FEBS Lett 340:39–44

    PubMed  CAS  Google Scholar 

  • Strelkov SE, Lamari L, Ballance GM (1998) Induced chlorophyll degradation by a chlorosis toxin from Pyrenophora tritici-repentis. Can J Plant Pathol 20:428–435

    CAS  Google Scholar 

  • Strickland JR, Aiken GE, Spiers DE, Fletcher LR, Oliver JW (2009) Physiological basis of fescue toxicosis. In: Fribourg HA, Hannaway DB, West CP (eds) Tall fescue for the twenty-first century, vol 53, Agronomy monograph. ASA/CSSA/SSSA, Madison, pp 203–228

    Google Scholar 

  • Stukenbrock EH, McDonald BA (2007) Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Molec Plant Pathol 8:321–332

    CAS  Google Scholar 

  • Sweat TA, Wolpert TJ (2007) Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell 19:673–687

    PubMed  CAS  Google Scholar 

  • Sweat TA, Lorang JM, Bakker EG, Wolpert TJ (2008) Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis. Mol Plant Microbe Interact 21:7–19

    PubMed  CAS  Google Scholar 

  • Tada Y, Hata S, Takata Y, Nakayashiki H, Tosa Y, Mayama S (2001) Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol Plant Microbe Interact 14:477–486

    PubMed  CAS  Google Scholar 

  • Tada Y, Kusaka K, Betsuyaku S, Shinogi T, Sakamoto M, Ohura Y, Hata S, Mori T, Tosa Y, Mayama S (2005) Victorin triggers programmed cell death and the defense response via interaction with a cell surface mediator. Plant Cell Physiol 46:1787–1798

    PubMed  CAS  Google Scholar 

  • Tan K-C, Oliver RP, Solomon PS, Moffat CS (2010) Proteinaceous necrotrophic effectors in fungal virulence. Funct Plant Biol 37:907–912

    CAS  Google Scholar 

  • Tanaka S (1933) Studies on black spot disease of Japanese pear (Pyrus serotina Rehd). Mem Coll Agric Kyoto Imp Univ 28:1–31

    Google Scholar 

  • Tanaka A, Tsuge T (2000) Structural and functional complexity of the genomic region controlling AK-toxin biosynthesis and pathogenicity in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 13:975–986

    PubMed  CAS  Google Scholar 

  • Tanaka A, Shiotani H, Yamamoto M, Tsuge T (1999) Insertional mutagenesis and cloning of the genes required for biosynthesis of the host-specific AK-toxin in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 12:691–702

    PubMed  CAS  Google Scholar 

  • Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050

    PubMed  CAS  Google Scholar 

  • Tatsuno T, Saito M, Enomoto M, Tsunoda H (1968) Nivalenol, a toxic principle of Fusarium nivale. Chem Pharm Bull(Tokyo) 16:2519–2520

    CAS  Google Scholar 

  • Timper P, Gates RN, Bouton JH (2005) Response of Pratylenchus spp. in tall fescue infected with different strains of the fungal endophyte Neotyphodium coenophialum. Nematology 7:105–110

    Google Scholar 

  • Tkacz JS (2000) Polyketide and peptide products of endophytic fungi: variations on two biosynthetic themes of secondary metabolism. In: Bacon CW, White JF (eds) Microbial endophytes. Dekker Inc., New York, pp 263–294

    Google Scholar 

  • Tomás A, Bockus WW (1987) Cultivar specific toxicity of culture filtrate of Pyrenophora tritici-repentis. Phytopathology 77:1337–1366

    Google Scholar 

  • Towers NR, Sprosen JM (1993) Zearalenone-induced infertility in sheep and cattle in New Zealand. N Z Vet J 41:223–224

    Google Scholar 

  • Tsai H, Wang H, Gebler JC, Poulter CD, Schardl CL (1995) The Claviceps purpurea gene encoding dimethylallyltryptophan synthase, the committed step for ergot alkaloid biosynthesis. Biochem Biophys Res Commun 216:119–125

    PubMed  CAS  Google Scholar 

  • Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37(1):44–66

    Google Scholar 

  • Tudzynski B, Hölter K (1998) Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet Biol 25:157–170

    PubMed  CAS  Google Scholar 

  • Tudzynski P, Holter K, Correia T, Arntz C, Grammel N, Keller U (1999) Evidence for an ergot alkaloid gene cluster in Claviceps purpurea. Mol Gen Genet 261:133–141

    PubMed  CAS  Google Scholar 

  • Turgay K, Marahiel MA (1994) A general approach for identifying and cloning peptide synthetase genes. Peptide Res 7:238–241

    CAS  Google Scholar 

  • Turgeon BG, Baker SE (2007) Genetic and genomic dissection of the Cochliobolus heterostrophus Tox1 locus controlling biosynthesis of the polyketide virulence factor T-toxin. In: Dunlap JC (ed) Fungal genomics. San Diego, pp 219–261

    Google Scholar 

  • Tzeng TH, Lyngholm LK, Ford CF, Bronson CR (1992) A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Genetics 130:81–96

    PubMed  CAS  Google Scholar 

  • Ueno T, Nakashima T, Hayashi Y, Fukami H (1975) Structures of Am-toxin I and II, host-specific phytotoxic metabolites produced by Alternaria mali. Agric Biol Chem 39:1115–1122

    CAS  Google Scholar 

  • Ueno T, Nakashima T, Uemoto M, Fukami H, Lee SN, Izumiya N (1977) Mass spectrometry of Alternaria mali toxins and related cyclodepsipeptides. Biomed Mass Spectr 4:134–142

    CAS  Google Scholar 

  • Uhlig S, Botha CJ, Vrålstad T, Rolén E, Miles CO (2009) Indole−diterpenes and ergot alkaloids in Cynodon dactylon (Bermuda Grass) Infected with Claviceps cynodontis from an outbreak of tremors in Cattle. J Agric Food Chem 57:11112–11119

    PubMed  CAS  Google Scholar 

  • Ullstrup AJ (1941) Two physiologic races of Helminthosporium maydis in the corn belt. Phytopathology 31:508–521

    Google Scholar 

  • Ullstrup AJ, Brunson AM (1947) Linkage relationships of a gene in corn determining susceptibility to a Helminthosporium leaf spot. J Am Soc Agron 39:606–609

    Google Scholar 

  • Upchurch RG, Walker DC, Rollins JA, Ehrenshaft M, Daub ME (1991) Mutants of Cercospora kikuchii altered in cercosporin synthesis and pathogenicity. Appl Environ Microbiol 57:2940–2945

    PubMed  CAS  Google Scholar 

  • van Egmond H, Schothorst R, Jonker M (2007) Regulations relating to mycotoxins in food. Anal Bioanal Chem 389:147–157

    PubMed  CAS  Google Scholar 

  • Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ (2011) A plant alternative to animal caspases: Subtilisin-like proteases. Cell Death Differ 18:1289–1297

    PubMed  CAS  Google Scholar 

  • Verdin E, Dequiedt F, Kasler HG (2003) Class II histone deacetylases: versatile regulators. Trends Genet 19:286–293

    PubMed  CAS  Google Scholar 

  • von Allmen JM, Rottmann WH, Gengenbach BG, Ahrvey AJ, Lonsdale DM (1991) Transfer of methomyl and HmT-toxin sensitivity from T-cytoplasm maize to tobacco. Mol Gen Genet 229:405–412

    Google Scholar 

  • von Döhren H, Keller U, Vater J, Zocher R (1997) Multifunctional peptide synthetases. Chem Rev 97:2675–2705

    Google Scholar 

  • Wakil SJ (1989) Fatty acid synthase, a proficient multifunctional enzyme. Biochemistry 28:4523–4530

    PubMed  CAS  Google Scholar 

  • Walton JD (1987) Two enzymes involved in biosynthesis of the host-selective phytotoxin HC-toxin. Proc Nat Acad Sci USA 84:8444–8447

    PubMed  CAS  Google Scholar 

  • Walton JD (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30:167–171

    PubMed  CAS  Google Scholar 

  • Walton JD (2006) HC-toxin. Phytochemistry 67:1406–1413

    PubMed  CAS  Google Scholar 

  • Walton JD, Earle ED (1983) The epoxide in HC-toxin is required for activity against susceptible maize. Physiol Plant Pathol 22:371–376

    CAS  Google Scholar 

  • Walton JD, Holden FR (1988) Properties of two enzymes involved in the biosynthesis of the fungal pathogenicity factor HC-toxin. Mol Plant Microbe Interact 1:128–134

    Google Scholar 

  • Walton JD, Earle ED, Gibson BW (1982) Purification and structure of the host-specific toxin from Helminthosporium carbonum race 1. Biochem Biophys Res Comm 107:785–794

    PubMed  CAS  Google Scholar 

  • Walton JD, Ahn JH, Pitkin JW, Cheng YQ, Nikolskaya AN, Ransom R, Wegener S (1998) Enzymology, molecular genetics, and regulation of biosynthesis of the host-selective toxin HC-toxin. In: Kohomoto K, Yoder OC (eds) Molecular genetics of host-specific toxins in plant disease. Kluwer, The Netherlands, pp 25–34

    Google Scholar 

  • Wang W, Jones C, Ciacci-Zanella J, Holt T, Gilchrist DG, Dickman MB (1996) Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc Natl Acad Sci USA 93:3461–3465

    PubMed  CAS  Google Scholar 

  • Wang J, Machado C, Panaccione DG, Tsai H, Schardl CL (2004) The determinant step in ergot alkaloid biosynthesis by an endophyte of perennial ryegrass. Fungal Genet Biol 41:189–198

    PubMed  CAS  Google Scholar 

  • Wang M, Zhou H, Wirz M, Tang Y, Boddy CN (2009) A thioesterase from an iterative fungal polyketide synthase shows macrocyclization and cross coupling activity and may play a role in controlling iterative cycling through product offloading. Biochemistry 48(27):6288–6290

    PubMed  CAS  Google Scholar 

  • Weber G, Schmörgendorfer K, Schneider-Scherzer E, Leitner E (1994) The peptide synthetase catalyzing cyclosporine production in Tolypocladium niveum is encoded by a giant 45.8 kilobase open reading frame. Curr Genet 26:120–125

    PubMed  CAS  Google Scholar 

  • Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL (2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol PlantMicrobe Interact 13:1027–1033

    CAS  Google Scholar 

  • Williams LD, Glenn AE, Bacon CW, Smith MA, Riley RT (2006) Fumonisin production and bioavailability to maize seedlings grown from seeds inoculated with Fusarium verticillioides and grown in natural soils. J Agric Food Chem 54:5694–5700

    PubMed  CAS  Google Scholar 

  • Wise RP, Fliss AE, Pring DR, Gengenbach BG (1987) urf13-T of T cytoplasm maize mitochondria encodes a 13 kD polypeptide. Plant Mol Biol 9:121–126

    CAS  Google Scholar 

  • Wolf SJ, Earle ED (1991) Effects of Helminthosporium carbonum race 1 toxin on host and non-host cereal protoplasts. Plant Sci 70:127–137

    Google Scholar 

  • Wolpert TJ, Macko V, Acklin W, Juan B, Seibl J, Meili J, Arigoni D (1985) Structure of victorin C, the major host-selective toxin from Cochliobolus victoriae. Experientia 41:1524–1529

    CAS  Google Scholar 

  • Wolpert TJ, Macko V, Acklin W, Juan B, Arigoni D (1986) Structure of minor host-selective toxins from Cochliobolus victoriae. Experientia 42:1296–1301

    CAS  Google Scholar 

  • Wolpert TJ, Navarre DA, Moore DL, Macko V (1994) Identification of the 100 kD victorin binding protein from oats. Plant Cell 6:1145–1155

    PubMed  CAS  Google Scholar 

  • Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285

    PubMed  CAS  Google Scholar 

  • Yamagishi D, Akamatsu H, Otani H, Kodama M (2006) Pathological evaluation of host-specific AAL-toxins and fumonisin mycotoxins produced by Alternaria and Fusarium species. J Gen Plant Pathol 72:323–326

    CAS  Google Scholar 

  • Yamazaki S, Ogawa T (1972) The chemistry and stereochemistry of cercosporin. Agric Biol Chem 36:1707–1718

    CAS  Google Scholar 

  • Yang G, Rose MS, Turgeon BG, Yoder OC (1996) A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Cell 8:2139–2150

    PubMed  CAS  Google Scholar 

  • Yao N, Tada Y, Park P, Nakayashiki H, Tosa Y, Mayama S (2001) Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. Plant J 28:13–26

    PubMed  CAS  Google Scholar 

  • Yates SG, Tookey HL, Ellis JJ, Burkhardt HJ (1968) Mycotoxins produced by Fusarium nivale isolated from tall fescue (Festuca arundinacea schreb.). Phytochemistry 7:139–146

    CAS  Google Scholar 

  • Yi H, Bojja RS, Fu J, Du L (2005) Direct evidence for the function of FUM13 in 3-ketoreduction of mycotoxin fumonisins in Fusarium verticillioides. J Agric Food Chem 53:5456–5460

    PubMed  CAS  Google Scholar 

  • Yoder OC (1998) A mechanistic view of the fungal/plant interaction based on host-specific toxin studies. In: Kohmoto K, Yoder OC (eds) Molecular genetics of host-specific toxins in plant disease. Kluwer, The Netherlands, pp 3–15

    Google Scholar 

  • Yoder OC, Scheffer RP (1973a) Effects of Helminthosporium carbonum toxin on nitrate uptake and reduction by corn tissues. Plant Physiol 52:513–517

    PubMed  CAS  Google Scholar 

  • Yoder OC, Scheffer RP (1973b) Effects of Helminthosporium carbonum toxin on absorption of solutes by corn roots. Plant Physiol 52:518–523

    PubMed  CAS  Google Scholar 

  • Yoshida H, Sugita K (1992) A novel tetracyclic peptide, trapoxin, induces phenotypic change from transformed to normal in sis-oncogene-transformed NIH3T3 cells. Jpn J Cancer Res 83:324–328

    PubMed  CAS  Google Scholar 

  • Yoshida M, Kijima M, Akita M, Beppu T (1990) Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem 265:17174–17179

    PubMed  CAS  Google Scholar 

  • Yoshizawa T, Morooka N (1973) Deoxynivalenol and its monacetate: new mycotoxins from Fusarium roseum and moldy barley. Agric Biol Chem 37:2933–2934

    CAS  Google Scholar 

  • You B-J, Lee M-H, Chung K-R (2008) Production of cercosporin toxin by the phytopathogenic Cercospora fungi is affected by diverse environmental signals. Can J Microbiol 54(4):259–269

    PubMed  CAS  Google Scholar 

  • Young CA, McMillan L, Telfer E, Scott B (2001) Molecular cloning and genetic analysis of an indole-diterpene gene cluster from Penicillium paxilli. Mol Microbiol 39:754–764

    PubMed  CAS  Google Scholar 

  • Young CA, Bryant MK, Christensen MJ, Tapper BA, Bryan GT, Scott B (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol Genet Genomics 274:13–29

    PubMed  CAS  Google Scholar 

  • Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, Bryan GT, Saikia S, Scott B (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43:679–693

    PubMed  CAS  Google Scholar 

  • Young CA, Tapper BA, May K, Moon CD, Schardl CL, Scott B (2009) Indole-diterpene biosynthetic capability of epichloë endophytes as predicted by ltm gene analysis. Appl Environ Microbiol 75:2200–2211

    PubMed  CAS  Google Scholar 

  • Yun SH, Turgeon BG, Yoder OC (1998) REMI-induced mutants of Mycosphaerella zeae-maydis lacking the polyketide PM-toxin are deficient in pathogenesis to corn. Physiol Mol Plant Pathol 52:53–66

    CAS  Google Scholar 

  • Zaleta-Rivera K, Xu C, Yu F, Butchko RAE, Proctor RH, Hidalgo-Lara ME, Raza A, Dussault PH, Du L (2006) A bidomain nonribosomal peptide synthetase encoded by FUM14 catalyzes the formation of tricarballylic esters in the biosynthesis of fumonisins. Biochemistry 45:2561–2569

    PubMed  CAS  Google Scholar 

  • Zhang S, Monahan BJ, Tkacz JS, Scott B (2004) Molecular cloning and genetic analysis of an indole-diterpene gene cluster from Aspergillus flavus. Appl Environ Microbiol 70:6875–6883

    PubMed  CAS  Google Scholar 

  • Zhou H, Zhan J, Watanabe K, Xie X, Tang Y (2008) A polyketide macrolactone synthase from the filamentous fungus Gibberella zeae. Proc Natl Acad Sci USA 105(17):6249–6254

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank the authors of the previous edition, D. G. Panaccione (West Virginia University, Morgantown, WV, USA), T. L. Friesen, and J.B. Rasmussen (both of North Dakota State University, Fargo, ND, USA) who provided some of the framework and text for the current work. We thank C. L. Schardl (University of Kentucky, Lexington, KY, USA) for providing the chemical structures of epichloae secondary metabolites, and Joy Dick and Rosemary van Essen (AgResearch, New Zealand) for searching the literature for relevant articles. We would like to acknowledge funding from the New Zealand Foundation for Research Science and Technology (C10X0815), Grants-in-Aid for Scientific Research (23380025) from the Japanese Society for Promotion of Sciences (JSPS), and the Global COE Program, MEXT, Japan, and funding from the Samuel Roberts Noble Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard D. Johnson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Johnson, R.D. et al. (2013). 4 Fungal Toxins of Agricultural Importance. In: Kempken, F. (eds) Agricultural Applications. The Mycota, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36821-9_4

Download citation

Publish with us

Policies and ethics