A genome-wide survey of the secondary metabolite biosynthesis genes in the wheat pathogen Parastagonospora nodorum

References

• Awakawa T, Yokota K, Funa N, Doi F, Mori N, Watanabe H, Horinouchi S. 2009. Physically discrete β-lactamase-type thioesterase catalyzes product release in atrochrysone synthesis by iterative type I polyketide synthase. Chem Biol. 16:613–623. doi:10.1016/j.chembiol.2009.04.004
   PubMed Web of Science ®Google Scholar
• Balibar CJ, Howard-Jones AR, Walsh CT. 2007. Terrequinone A biosynthesis through L-tryptophan oxidation, dimerization and bisprenylation. Nat Chem Biol. 3:584–592. doi:10.1038/nchembio.2007.20
   Google Scholar
• Balibar CJ, Walsh CT. 2006. Glip, a multimodular nonribosomal peptide synthetase in Aspergillus fumigatus, makes the diketopiperazine scaffold of gliotoxin. Biochemistry. 45:15029–15038. doi:10.1021/bi061845b
   PubMed Web of Science ®Google Scholar
• Bathgate J, Loughman R. 2001. Ascospores are a source of inoculum of Phaeosphaeria nodorum, P. avenaria f. sp. avenaria and Mycosphaerella graminicola in Western Australia. Australas Plant Pathol. 30:317–322. doi:10.1071/AP01043
   Web of Science ®Google Scholar
• Berestetskiy A, Dmitriev A, Mitina G, Lisker I, Andolfi A, Evidente A. 2008. Nonenolides and cytochalasins with phytotoxic activity against Cirsium arvense and Sonchus arvensis: a structure-activity relationships study. Phytochemistry. 69:953–960. doi:10.1016/j.phytochem.2007.11.003
   PubMed Web of Science ®Google Scholar
• Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T. 2013. Antismash 2.0 – a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 41:W204–W212.
   PubMed Web of Science ®Google Scholar
• Brakhage AA, Schroeckh V. 2011. Fungal secondary metabolites – strategies to activate silent gene clusters. Fungal Genet Biol. 48:15–22. doi:10.1016/j.fgb.2010.04.004
   PubMed Web of Science ®Google Scholar
• Brennan R, Fitt BD, Taylor G, Colhoun J. 1985. Dispersal of Septoria nodorum pycnidiospores by simulated raindrops in still air. J Phytopathol. 112:281–290. doi:10.1111/j.1439-0434.1985.tb00805.x
   Web of Science ®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 Web of Science ®Google Scholar
• Cabras A, Mannoni MA, Serra S, Andolfi A, Fiore M, Evidente A. 2006. Occurrence, isolation and biological activity of phytotoxic metabolites produced in vitro by Sphaeropsis sapinea, pathogenic fungus of Pinus radiata. Eur J Plant Pathol. 115:187–193. doi:10.1007/s10658-006-9006-7
   Web of Science ®Google Scholar
• Cacho RA, Chooi YH, Zhou H, Tang Y. 2013. Complexity generation in fungal polyketide biosynthesis: a spirocycle-forming P450 in the concise pathway to the antifungal drug griseofulvin. ACS Chem Biol. 8:2322–2330. doi:10.1021/cb400541z
   PubMed Web of Science ®Google Scholar
• Cacho RA, Jiang W, Chooi YH, Walsh CT, Tang Y. 2012. Identification and characterization of the echinocandin B biosynthetic gene cluster from Emericella rugulosa NRRL 11440. J Am Chem Soc. 134:16781–16790. doi:10.1021/ja307220z
   PubMed Web of Science ®Google Scholar
• Cane DE, Yang G, Xue Q, Shim JH. 1995. Trichodiene synthase. Substrate specificity and inhibition. Biochemistry. 34:2471–2479. doi:10.1021/bi00008a010
   PubMed Web of Science ®Google Scholar
• Chen HQ, Lee MH, Daub ME, Chung KR. 2007. Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae. Mol Microbiol. 64:755–770. doi:10.1111/j.1365-2958.2007.05689.x
   PubMed Web of Science ®Google Scholar
• Chen L, Yue Q, Zhang X, Xiang M, Wang C, Li S, Che Y, Ortiz-Lopez FJ, Bills GF, Liu X, et al. 2013. Genomics-driven discovery of the pneumocandin biosynthetic gene cluster in the fungus Glarea lozoyensis. BMC Genomics. 14:339.
   PubMed Web of Science ®Google Scholar
• Chiang YM, Szewczyk E, Nayak T, Davidson AD, Sanchez JF, Lo HC, Ho WY, Simityan H, Kuo E, Praseuth A, et al. 2008. Molecular genetic mining of the Aspergillus secondary metabolome: discovery of the emericellamide biosynthetic pathway. Chem Biol. 15:527–532. doi:10.1016/j.chembiol.2008.05.010
   PubMedGoogle Scholar
• Chooi YH, Cacho R, Tang Y. 2010. Identification of the viridicatumtoxin and griseofulvin gene clusters from Penicillium aethiopicum. Chem Biol. 17:483–494. doi:10.1016/j.chembiol.2010.03.015
   PubMed Web of Science ®Google Scholar
• Chooi YH, Tang Y. 2010. Adding the lipo to lipopeptides: do more with less. Chem Biol. 17:791–793. doi:10.1016/j.chembiol.2010.08.001
   PubMed Web of Science ®Google Scholar
• Chooi YH, Tang Y. 2012. Navigating the fungal polyketide chemical space: from genes to molecules. J Org Chem. 77:9933–9953. doi:10.1021/jo301592k
   PubMed Web of Science ®Google Scholar
• Chooi YH, Wang P, Fang J, Li Y, Wu K, Wang P, Tang Y. 2012. Discovery and characterization of a group of fungal polycyclic polyketide prenyltransferases. J Am Chem Soc. 134:9428–9437. doi:10.1021/ja3028636
   PubMed Web of Science ®Google Scholar
• Choquer M, Dekkers KL, Chen HQ, Cao L, Ueng PP, Daub ME, Chung KR. 2005. The CTB1 gene encoding a fungal polyketide synthase is required for cercosporin biosynthesis and fungal virulence of Cercospora nicotianae. Mol Plant Microbe Interact. 18:468–476. doi:10.1094/MPMI-18-0468
   PubMed Web of Science ®Google Scholar
• Christianson DW. 2008. Unearthing the roots of the terpenome. Curr Opin Chem Biol. 12:141–150. doi:10.1016/j.cbpa.2007.12.008
   PubMed Web of Science ®Google Scholar
• Cox RJ. 2007. Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org Biomol Chem. 5:2010–2026. doi:10.1039/b704420h
   PubMed Web of Science ®Google Scholar
• Cramer Jr. RA, Gamcsik MP, Brooking RM, Najvar LK, Kirkpatrick WR, Patterson TF, Balibar CJ, Graybill JR, Perfect JR, Abraham SN, et al. 2006. Disruption of a nonribosomal peptide synthetase in Aspergillus fumigatus eliminates gliotoxin production. Eukaryot Cell. 5:972–980. doi:10.1128/EC.00049-06
   PubMed Web of Science ®Google Scholar
• Crawford JM, Dancy BC, Hill EA, Udwary DW, Townsend CA. 2006. Identification of a starter unit acyl-carrier protein transacylase domain in an iterative type I polyketide synthase. Proc Natl Acad Sci USA. 103:16728–16733. doi:10.1073/pnas.0604112103
   PubMed Web of Science ®Google Scholar
• Crawford JM, Thomas PM, Scheerer JR, Vagstad AL, Kelleher NL, Townsend CA. 2008. Deconstruction of iterative multidomain polyketide synthase function. Science. 320:243–246. doi:10.1126/science.1154711
   PubMed Web of Science ®Google Scholar
• Crawford JM, Townsend CA. 2010. New insights into the formation of fungal aromatic polyketides. Nat Rev Microbiol. 8:879–889. doi:10.1038/nrmicro2465
   PubMed Web of Science ®Google Scholar
• Crook AD, Friesen TL, Liu ZH, Ojiambo PS, Cowger C. 2012. Novel necrotrophic effectors from Stagonospora nodorum and corresponding host sensitivities in winter wheat germplasm in the southeastern United States. Phytopathology. 102:498–505. doi:10.1094/PHYTO-08-11-0238
   PubMed Web of Science ®Google Scholar
• Dalmais B, Schumacher J, Moraga J, LEP P, Tudzynski B, Collado IG, Viaud M. 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. 12:564–579. doi:10.1111/j.1364-3703.2010.00692.x
   PubMed Web of Science ®Google Scholar
• Daub ME. 1982. Cercosporin, a photosensitizing toxin from Cercospora species. Phytopathology. 72:370–374. doi:10.1094/Phyto-72-370
   Web of Science ®Google Scholar
• Daub ME, Herrero S, Chung KR. 2005. Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiol Lett. 252:197–206. doi:10.1016/j.femsle.2005.08.033
   PubMed Web of Science ®Google Scholar
• Devys M, Barbier M, Bousquet JF, Kollmann A. 1994. Isolation of the (-)-(3r)-5-hydroxymellein from the fungus septoria nodorum. Phytochemistry. 35:825–826. doi:10.1016/S0031-9422(00)90617-4
   Web of Science ®Google Scholar
• Devys M, Barbier M, Kollmann A, Bousquet JF. 1982. Septorine and n-methoxy septorine, substituted pyrazines from the fungus Septoria nodorum berk. Tetrahedron Lett. 23: 5409–5412.
   Web of Science ®Google Scholar
• Devys M, Barbier M, Kollmann A, Bousquet JF. 1992. N-methoxy septorinol, a substituted pyrazine from the fungus Septoria nodorum. Phytochemistry. 31:4393–4394. doi:10.1016/0031-9422(92)80492-W
   Web of Science ®Google Scholar
• Devys M, Bousquet JF, Kollmann A, Barbier M. 1978. Isolation of a new pyrazine, septorine, from culture medium of phyto-pathogen fungus Septoria nodorum berk. C R Acad Sci. 286:457–458.
   Google Scholar
• Devys M, Bousquet JF, Kollmann A, Barbier M. 1980. Dihydroisocoumarins and mycophenolic-acid of culture-medium of a phytopathogenic fungus, Septoria nodorum. Phytochemistry. 19:2221–2222. doi:10.1016/S0031-9422(00)82234-7
   Web of Science ®Google Scholar
• Eisenman HC, Casadevall A. 2012. Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol. 93:931–940. doi:10.1007/s00253-011-3777-2
   PubMed Web of Science ®Google Scholar
• Elliott CE, Callahan DL, Schwenk D, Nett M, Hoffmeister D, Howlett BJ. 2013. A gene cluster responsible for biosynthesis of phomenoic acid in the plant pathogenic fungus, Leptosphaeria maculans. Fung Genet Biol. 53:50–58. doi:10.1016/j.fgb.2013.01.008
   PubMed Web of Science ®Google Scholar
• Elsebai MF, Kehraus S, Gutschow M, Konig GM. 2010. Spartinoxide, a new enantiomer of A82775C with inhibitory activity toward HLE from the marine-derived fungus Phaeosphaeria spartinae. Nat Prod Commun. 5: 1071–1076.
   PubMed Web of Science ®Google Scholar
• Evidente A, Andolfi A, Vurro M, Zonno MC, Motta A. 2002. Cytochalasins Z1, Z2 and Z3, three 24-oxa[14]cytochalasans produced by Pyrenophora semeniperda. Phytochemistry. 60:45–53. doi:10.1016/S0031-9422(02)00071-7
   PubMed Web of Science ®Google Scholar
• Evidente A, Cimmino A, Berestetskiy A, Andolfi A, Motta A. 2008. Stagonolides G-I and modiolide A, nonenolides produced by Stagonospora cirsii, a potential mycoherbicide for Cirsium arvense. J Nat Prod. 71:1897–1901. doi:10.1021/np800415w
   PubMed Web of Science ®Google Scholar
• Evidente A, Cimmino A, Berestetskiy A, Mitina G, Andolfi A, Motta A. 2008. Stagonolides B-F, nonenolides produced by Stagonospora cirsii, a potential mycoherbicide of Cirsium arvense. J Nat Prod. 71:31–34. doi:10.1021/np0703038
   PubMed Web of Science ®Google Scholar
• Finking R, Marahiel MA. 2004. Biosynthesis of nonribosomal peptides. Annu Rev Microbiol. 58:453–488. doi:10.1146/annurev.micro.58.030603.123615
   PubMed Web of Science ®Google Scholar
• Francki MG, Shankar M, Walker E, Loughman R, Golzar H, Ohm H. 2011. New quantitative trait loci in wheat for flag leaf resistance to Stagonospora nodorum blotch. Phytopathology. 101:1278–1284. doi:10.1094/PHYTO-02-11-0054
   PubMed Web of Science ®Google Scholar
• Friesen TL, Chu C, Xu SS, Faris JD. 2012. Sntox5-snn5: a novel Stagonospora nodorum effector-wheat gene interaction and its relationship with the SnToxA-Tsn1 and SnTox3-Snn3-B1 interactions. Mol Plant Pathol. 13:1101–1109. doi:10.1111/j.1364-3703.2012.00819.x
   PubMed Web of Science ®Google Scholar
• Fujii I, Watanabe A, Sankawa U, Ebizuka Y. 2001. Identification of claisen cyclase domain in fungal polyketide synthase WA, a naphthopyrone synthase of Aspergillus nidulans. Chem Biol. 8:189–197. doi:10.1016/S1074-5521(00)90068-1
   PubMed Web of Science ®Google Scholar
• Fujii I, Yasuoka Y, Tsai HF, Chang YC, Kwon-Chung KJ, Ebizuka Y. 2004. Hydrolytic polyketide shortening by ayg1p, a novel enzyme involved in fungal melanin biosynthesis. J Biol Chem. 279:44613–44620. doi:10.1074/jbc.M406758200
   PubMed Web of Science ®Google Scholar
• Fujii I, Yoshida N, Shimomaki S, Oikawa H, Ebizuka Y. 2005. An iterative type I polyketide synthase PKSN catalyzes synthesis of the decaketide alternapyrone with regio-specific octa-methylation. Chem Biol. 12:1301–1309. doi:10.1016/j.chembiol.2005.09.015
   PubMed Web of Science ®Google Scholar
• Funa N, Awakawa T, Horinouchi S. 2007. Pentaketide resorcylic acid synthesis by type III polyketide synthase from Neurospora crassa. J Biol Chem. 282:14476–14481. doi:10.1074/jbc.M701239200
   PubMed Web of Science ®Google Scholar
• Gao X, Haynes SW, Ames BD, Wang P, Vien LP, Walsh CT, Tang Y. 2012. Cyclization of fungal nonribosomal peptides by a terminal condensation-like domain. Nat Chem Biol. 8:823–830. doi:10.1038/nchembio.1047
   PubMed Web of Science ®Google Scholar
• Gao Y, Honzatko RB, Peters RJ. 2012. Terpenoid synthase structures: a so far incomplete view of complex catalysis. Nat Prod Rep. 29:1153–1175. doi:10.1039/c2np20059g
   PubMed Web of Science ®Google Scholar
• Gardiner DM, Cozijnsen AJ, Wilson LM, Pedras MS, Howlett BJ. 2004. The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol Microbiol. 53:1307–1318. doi:10.1111/j.1365-2958.2004.04215.x
   PubMed Web of Science ®Google Scholar
• Goudet C, Milat ML, Sentenac H, Thibaud JB. 2000. Beticolins, nonpeptidic, polycyclic molecules produced by the phytopathogenic fungus Cercospora beticola, as a new family of ion channel-forming toxins. Mol Plant Microbe Interact. 13:203–209. doi:10.1094/MPMI.2000.13.2.203
   PubMed Web of Science ®Google Scholar
• Graziani S, Vasnier C, Daboussi MJ. 2004. Novel polyketide synthase from Nectria haematococca. Appl Environ Microbiol. 70:2984–2988. doi:10.1128/AEM.70.5.2984-2988.2004
   PubMed Web of Science ®Google Scholar
• Griffiths E, Ao HC. 1976. Dispersal of Septoria nodorum spores and spread of glume blotch of wheat in the field. Trans Br Mycol Soc. 67:413–418. doi:10.1016/S0007-1536(76)80166-0
   Web of Science ®Google Scholar
• Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, et al. 2007. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell. 19:3347–3368. doi:10.1105/tpc.107.052829
   PubMed Web of Science ®Google Scholar
• Hansen BG, Mnich E, Nielsen KF, Nielsen JB, Nielsen MT, Mortensen UH, Larsen TO, Patil KR. 2012. Involvement of a natural fusion of a cytochrome P450 and a hydrolase in mycophenolic acid biosynthesis. Appl Environ Microbiol. 78:4908–4913. doi:10.1128/AEM.07955-11
   PubMed Web of Science ®Google Scholar
• Hansen BG, Salomonsen B, Nielsen MT, Nielsen JB, Hansen NB, Nielsen KF, Regueira TB, Nielsen J, Patil KR, Mortensen UH. 2011. Versatile enzyme expression and characterization system for Aspergillus nidulans, with the Penicillium brevicompactum polyketide synthase gene from the mycophenolic acid gene cluster as a test case. Appl Environ Microbiol. 77:3044–3051. doi:10.1128/AEM.01768-10
   PubMed Web of Science ®Google Scholar
• Hissen AH, Wan AN, Warwas ML, Pinto LJ, Moore MM. 2005. The Aspergillus fumigatus siderophore biosynthetic gene sida, encoding l-ornithine n5-oxygenase, is required for virulence. Infect Immun. 73:5493–5503. doi:10.1128/IAI.73.9.5493-5503.2005
   PubMed Web of Science ®Google Scholar
• Hoffmeister D, Keller NP. 2007. Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep. 24:393–416. doi:10.1039/b603084j
   PubMed Web of Science ®Google Scholar
• Itoh T, Tokunaga K, Matsuda Y, Fujii I, Abe I, Ebizuka Y, Kushiro T. 2010. Reconstitution of a fungal meroterpenoid biosynthesis reveals the involvement of a novel family of terpene cyclases. Nat Chem. 2:858–864. doi:10.1038/nchem.764
   PubMed Web of Science ®Google Scholar
• Itoh T, Tokunaga K, Radhakrishnan EK, Fujii I, Abe I, Ebizuka Y, Kushiro T. 2012. Identification of a key prenyltransferase involved in biosynthesis of the most abundant fungal meroterpenoids derived from 3,5-dimethylorsellinic acid. Chembiochem. 13:1132–1135. doi:10.1002/cbic.201200124
   PubMed Web of Science ®Google Scholar
• Johnson L. 2008. Iron and siderophores in fungal-host interactions. Mycol Res. 112:170–183.
   PubMedGoogle Scholar
• Johnson LJ, Koulman A, Christensen M, Lane GA, Fraser K, Forester N, Johnson RD, Bryan GT, Rasmussen S. 2013. An extracellular siderophore is required to maintain the mutualistic interaction of epichloë festucae with lolium perenne. Plos Pathog. 9:e1003332. doi:10.1371/journal.ppat.1003332
   Google Scholar
• Kawaide H, Imai R, Sassa T, Kamiya Y. 1997. Ent-kaurene synthase from the fungus Phaeosphaeria sp. L487. cDNA isolation, characterization, and bacterial expression of a bifunctional diterpene cyclase in fungal gibberellin biosynthesis. J Biol Chem. 272:21706–21712. doi:10.1074/jbc.272.35.21706
   PubMed Web of Science ®Google Scholar
• Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND. 2010. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol. 47:736–741. doi:10.1016/j.fgb.2010.06.003
   PubMed Web of Science ®Google Scholar
• Kimura N, Tsuge T. 1993. Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol. 175:4427–4435.
   PubMed Web of Science ®Google Scholar
• Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kunoh H. 1997. Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J. 11:525–537. doi:10.1046/j.1365-313X.1997.11030525.x
   Web of Science ®Google Scholar
• Kobayashi Y, Yamada M, Kobayashi I, Kunoh H. 1997. Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant Cell Physiol. 38:725–733. doi:10.1093/oxfordjournals.pcp.a029226
   Web of Science ®Google Scholar
• Kraas FI, Giessen TW, Marahiel MA. 2012. Exploring the mechanism of lipid transfer during biosynthesis of the acidic lipopeptide antibiotic CDA. FEBS Lett. 586:283–288. doi:10.1016/j.febslet.2012.01.003
   PubMed Web of Science ®Google Scholar
• Kraas FI, Helmetag V, Wittmann M, Strieker M, Marahiel MA. 2010. Functional dissection of surfactin synthetase initiation module reveals insights into the mechanism of lipoinitiation. Chem Biol. 17:872–880. doi:10.1016/j.chembiol.2010.06.015
   PubMed Web of Science ®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. doi:10.1074/jbc.M109.071324
   PubMed Web of Science ®Google Scholar
• Li G, Wang H, Zhu R, Sun L, Wang L, Li M, Li Y, Liu Y, Zhao Z, Lou H. 2012. Phaeosphaerins A-F, cytotoxic perylenequinones from an endolichenic fungus, Phaeosphaeria sp. J Nat Prod. 75:142–147. doi:10.1021/np200614h
   PubMed Web of Science ®Google Scholar
• Li SM. 2009. Evolution of aromatic prenyltransferases in the biosynthesis of indole derivatives. Phytochemistry. 70:1746–1757.
   PubMed Web of Science ®Google Scholar
• Li Y, Chooi YH, Sheng Y, Valentine JS, Tang Y. 2011. Comparative characterization of fungal anthracenone and naphthacenedione biosynthetic pathways reveals an α-hydroxylation-dependent claisen-like cyclization catalyzed by a dimanganese thioesterase. J Am Chem Soc. 133:15773–15785. doi:10.1021/ja206906d
   PubMed Web of Science ®Google Scholar
• Lin HC, Chooi YH, Dhingra S, Xu W, Calvo AM, Tang Y. 2013. The fumagillin biosynthetic gene cluster in Aspergillus fumigatus encodes a cryptic terpene cyclase involved in the formation of beta-trans-bergamotene. J Am Chem Soc. 135:4616–4619. doi:10.1021/ja312503y
   PubMed Web of Science ®Google Scholar
• Lo HC, Entwistle R, Guo CJ, Ahuja M, Szewczyk E, Hung JH, Chiang YM, Oakley BR, Wang CC. 2012. Two separate gene clusters encode the biosynthetic pathway for the meroterpenoids austinol and dehydroaustinol in aspergillus nidulans. J Am Chem Soc. 134:4709–4720. doi:10.1021/ja209809t
   PubMed Web of Science ®Google Scholar
• Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, Tzeng SC, Maier CS, Wolpert TJ. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science. 338:659–662. doi:10.1126/science.1226743
   PubMed Web of Science ®Google Scholar
• Maiya S, Grundmann A, Li SM, Turner G. 2006. The fumitremorgin gene cluster of Aspergillus fumigatus: identification of a gene encoding brevianamide F synthetase. Chembiochem. 7:1062–1069. doi:10.1002/cbic.200600003
   PubMed Web of Science ®Google Scholar
• Meiss E, Konno H, Groth G, Hisabori T. 2008. Molecular processes of inhibition and stimulation of ATP synthase caused by the phytotoxin tentoxin. J Biol Chem. 283:24594–24599. doi:10.1074/jbc.M802574200
   PubMed Web of Science ®Google Scholar
• Möbius N, Hertweck C. 2009. Fungal phytotoxins as mediators of virulence. Curr Opin Plant Biol. 12:390–398. doi:10.1016/j.pbi.2009.06.004
   PubMed Web of Science ®Google Scholar
• Murray GM, Brennan JP. 2009. Estimating disease losses to the Australian wheat industry. Australas Plant Pathol. 38:558–570. doi:10.1071/AP09053
   Web of Science ®Google Scholar
• Oliver RP, Friesen TL, Faris JD, Solomon PS. 2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annu Rev Phytopathol. 50:23–43. doi:10.1146/annurev-phyto-081211-173019
   PubMed Web of Science ®Google Scholar
• Oliver RP, Solomon PS. 2010. New developments in pathogenicity and virulence of necrotrophs. Curr Opin Plant Biol. 13:415–419. doi:10.1016/j.pbi.2010.05.003
   PubMed Web of Science ®Google Scholar
• Parisi A, Piattelli M, Tringali C, Di San Lio GM. 1993. Identification of the phytotoxin mellein in culture fluids of Phoma tracheiphila. Phytochemistry. 32:865–867. doi:10.1016/0031-9422(93)85221-C
   Web of Science ®Google Scholar
• Pinedo C, Wang CM, Pradier JM, Dalmais B, Choquer M, Le Pêcheur P, Morgant G, Collado IG, Cane DE, Viaud M. 2008. Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem Biol. 3:791–801. doi:10.1021/cb800225v
   PubMed Web of Science ®Google Scholar
• Qiao K, Chooi YH, Tang Y. 2011. Identification and engineering of the cytochalasin gene cluster from Aspergillus clavatus NRRL 1. Metab Eng. 13:723–732. doi:10.1016/j.ymben.2011.09.008
   PubMed Web of Science ®Google Scholar
• Qiao KJ, Zhou H, Xu W, Zhang WJ, Garg N, Tang Y. 2011. A fungal nonribosomal peptide synthetase module that can synthesize thiopyrazines. Org Lett. 13:1758–1761. doi:10.1021/ol200288w
   PubMed Web of Science ®Google Scholar
• Quaedvlieg W, Verkley GJ, Shin HD, Barreto RW, Alfenas AC, Swart WJ, Groenewald JZ, Crous PW. 2013. Sizing up septoria. Stud Mycol. 75:307–390. doi:10.3114/sim0017
   PubMed Web of Science ®Google Scholar
• Regueira TB, Kildegaard KR, Hansen BG, Mortensen UH, Hertweck C, Nielsen J. 2011. Molecular basis for mycophenolic acid biosynthesis in Penicillium brevicompactum. Appl Environ Microbiol. 77:3035–3043. doi:10.1128/AEM.03015-10
   PubMed Web of Science ®Google Scholar
• Rynkiewicz MJ, Cane DE, Christianson DW. 2002. X-ray crystal structures of D100E trichodiene synthase and its pyrophosphate complex reveal the basis for terpene product diversity. Biochemistry. 41:1732–1741. doi:10.1021/bi011960g
   PubMed Web of Science ®Google Scholar
• Sanchez JF, Entwistle R, Hung JH, Yaegashi J, Jain S, Chiang YM, Wang CC, Oakley BR. 2011. Genome-based deletion analysis reveals the prenyl xanthone biosynthesis pathway in Aspergillus nidulans. J Am Chem Soc. 133:4010–4017. doi:10.1021/ja1096682
   PubMed Web of Science ®Google Scholar
• Sanchez JF, Somoza AD, Keller NP, Wang CC. 2012. Advances in Aspergillus secondary metabolite research in the post-genomic era. Nat Prod Rep. 29:351–371. doi:10.1039/c2np00084a
   PubMed Web of Science ®Google Scholar
• Sanderson F, Hampton J. 1978. Role of the perfect states in the epidemiology of the common septoria diseases of wheat. New Zeal J Agr Res. 21:277–281. doi:10.1080/00288233.1978.10427411
   Web of Science ®Google Scholar
• Scherlach K, Boettger D, Remme N, Hertweck C. 2010. The chemistry and biology of cytochalasans. Nat Prod Rep. 27:869–886. doi:10.1039/b903913a
   PubMed Web of Science ®Google Scholar
• Schneider P, Bouhired S, Hoffmeister D. 2008. Characterization of the atromentin biosynthesis genes and enzymes in the homobasidiomycete Tapinella panuoides. Fungal Genet Biol. 45:1487–1496. doi:10.1016/j.fgb.2008.08.009
   PubMed Web of Science ®Google Scholar
• Schneider P, Weber M, Rosenberger K, Hoffmeister D. 2007. A one-pot chemoenzymatic synthesis for the universal precursor of antidiabetes and antiviral bis-indolylquinones. Chem Biol. 14:635–644. doi:10.1016/j.chembiol.2007.05.005
   PubMed Web of Science ®Google Scholar
• Schwartz RE, Helms GL, Bolessa EA, Wilson KE, Giacobbe RA, Tkacz JS, Bills GF, Liesch JM, Zink DL, Curotto JE, et al. 1994. Pramanicin, a novel antimicrobial agent from a fungal fermentation. Tetrahedron. 50:1675–1686. doi:10.1016/S0040-4020(01)80843-7
   Web of Science ®Google Scholar
• Schwecke T, Göttling K, Durek P, Dueñas I, Käufer NF, Zock-Emmenthal S, Staub E, Neuhof T, Dieckmann R, von Döhren H. 2006. Nonribosomal peptide synthesis in schizosaccharomyces pombe and the architectures of ferrichrome-type siderophore synthetases in fungi. Chembiochem. 7:612–622. doi:10.1002/cbic.200500301
   PubMed Web of Science ®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. 331:253–260. doi:10.1016/j.bbrc.2005.03.160
   PubMed Web of Science ®Google Scholar
• Shaner G. 1981. Effect of environment on fungal leaf blights of small grains. Annu Rev Phytopathol. 19:273–296. doi:10.1146/annurev.py.19.090181.001421
   Web of Science ®Google Scholar
• Solomon PS, Lowe RG, Tan KC, Waters OD, Oliver RP. 2006. Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Mol Plant Pathol. 7:147–156. doi:10.1111/j.1364-3703.2006.00326.x
   PubMed Web of Science ®Google Scholar
• Solomon PS, Tan KC, Sanchez P, Cooper RM, Oliver RP. 2004. The disruption of a galpha subunit sheds new light on the pathogenicity of Stagonospora nodorum on wheat. Mol Plant Microbe Interact. 17:456–466. doi:10.1094/MPMI.2004.17.5.456
   PubMed Web of Science ®Google Scholar
• Stergiopoulos I, Collemare J, Mehrabi R, De Wit PJ. 2013. Phytotoxic secondary metabolites and peptides produced by plant pathogenic dothideomycete fungi. FEMS Microbiol Rev. 37:67–93. doi:10.1111/j.1574-6976.2012.00349.x
   PubMed Web of Science ®Google Scholar
• Sun H, Ho CL, Ding F, Soehano I, Liu XW, Liang ZX. 2012. Synthesis of (r)-mellein by a partially reducing iterative polyketide synthase. J Am Chem Soc. 134:11924–11927. doi:10.1021/ja304905e
   PubMed Web of Science ®Google Scholar
• Syme RA, Hane JK, Friesen TL, Oliver RP. 2013. Resequencing and comparative genomics of Stagonospora nodorum: sectional gene absence and effector discovery. G3 (Bethesda). 3:959–969. doi:10.1534/g3.112.004994
   Web of Science ®Google Scholar
• Tan K-C, Trengove RD, Maker GL, Oliver RP, Solomon PS. 2009. Metabolite profiling identifies the mycotoxin alternariol in the pathogen Stagonospora nodorum. Metabolomics. 5:330–335. doi:10.1007/s11306-009-0158-2
   Web of Science ®Google Scholar
• Tan K-C, Waters O, Rybak K, Antoni E, Furuki E, Oliver R. 2013. Sensitivity to three Parastagonospora nodorum necrotrophic effectors in current Australian wheat cultivars and the presence of further fungal effectors. Crop Pasture Sci. 65:150–158. doi: http://dx.doi.org/10.1071/CP13443
   Web of Science ®Google Scholar
• Thomas R. 1961. Studies in the biosynthesis of fungal metabolites. 2. The biosynthesis of alternariol and its relation to other fungal phenols. Biochem J. 78:748–758.
   PubMed Web of Science ®Google Scholar
• Tietjen KG, Matern U. 1984. Induction and suppression of phytoalexin biosynthesis in cultured cells of safflower, Carthamus tinctorius L., by metabolites of Alternaria carthami chowdhury. Arch Biochem Biophys. 229:136–144. doi:10.1016/0003-9861(84)90138-3
   PubMed Web of Science ®Google Scholar
• Tsai HF, Fujii I, Watanabe A, Wheeler MH, Chang YC, Yasuoka Y, Ebizuka Y, Kwon-Chung KJ. 2001. Pentaketide melanin biosynthesis in Aspergillus fumigatus requires chain-length shortening of a heptaketide precursor. J Biol Chem. 276:29292–29298. doi:10.1074/jbc.M101998200
   PubMed Web of Science ®Google Scholar
• Tudzynski B, Kawaide H, Kamiya Y. 1998. Gibberellin biosynthesis in Gibberella fujikuroi: cloning and characterization of the copalyl diphosphate synthase gene. Curr Genet. 34:234–240. doi:10.1007/s002940050392
   PubMed Web of Science ®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. Adv Genet. 57:219–261. doi:10.1016/S0065-2660(06)57006-3
   PubMed Web of Science ®Google Scholar
• Vagstad AL, Hill EA, Labonte JW, Townsend CA. 2012. Characterization of a fungal thioesterase having claisen cyclase and deacetylase activities in melanin biosynthesis. Chem Biol. 19:1525–1534. doi:10.1016/j.chembiol.2012.10.002
   PubMed Web of Science ®Google Scholar
• Venkatasubbaiah P, Chilton WS. 1990. Phytotoxins of Botryosphaeria obtusa. J Nat Prod. 53:1628–1630. doi:10.1021/np50072a044
   Web of Science ®Google Scholar
• Wackler B, Lackner G, Chooi YH, Hoffmeister D. 2012. Characterization of the Suillus grevillei quinone synthetase GreA supports a nonribosomal code for aromatic α-keto acids. Chembiochem. 13:1798–1804. doi:10.1002/cbic.201200187
   PubMed Web of Science ®Google Scholar
• Wada M, Kato H, Malik K, Sriprasertsak P, Ichinose Y, Shiraishi T, Yamada T. 1995. A supprescin from a phytopathogenic fungus deactivates transcription of a plant defense gene encoding phenylalanine ammonia-lyase. J Mol Biol. 249:513–519. doi:10.1006/jmbi.1995.0313
   PubMed Web of Science ®Google Scholar
• Wallwey C, Li SM. 2011. Ergot alkaloids: structure diversity, biosynthetic gene clusters and functional proof of biosynthetic genes. Nat Prod Rep. 28:496–510. doi:10.1039/c0np00060d
   PubMed Web of Science ®Google Scholar
• Walton JD. 2006. Hc-toxin. Phytochemistry. 67:1406–1413. doi:10.1016/j.phytochem.2006.05.033
   PubMed Web of Science ®Google Scholar
• Wheeler MH, Abramczyk D, Puckhaber LS, Naruse M, Ebizuka Y, Fujii I, Szaniszlo PJ. 2008. New biosynthetic step in the melanin pathway of Wangiella (Exophiala) dermatitidis: evidence for 2-acetyl-1,3,6,8-tetrahydroxynaphthalene as a novel precursor. Eukaryot Cell. 7:1699–1711. doi:10.1128/EC.00179-08
   PubMed Web of Science ®Google Scholar
• Wight WD, Kim KH, Lawrence CB, Walton JD. 2009. Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. Mol Plant Microbe Interact. 22:1258–1267. doi:10.1094/MPMI-22-10-1258
   PubMed Web of Science ®Google Scholar
• Yang XL, Awakawa T, Wakimoto T, Abe I. 2013. Induced biosyntheses of a novel butyrophenone and two aromatic polyketides in the plant pathogen Stagonospora nodorum. Nat Prod Bioprosp. 3:141–144. doi:10.1007/s13659-013-0055-2
   Google Scholar
• Yeh HH, Chiang YM, Entwistle R, Ahuja M, Lee KH, Bruno KS, Wu TK, Oakley BR, Wang CC. 2012. Molecular genetic analysis reveals that a nonribosomal peptide synthetase-like (NRPS-like) gene in Aspergillus nidulans is responsible for microperfuranone biosynthesis. Appl Microbiol Biotechnol. 96:739–748. doi:10.1007/s00253-012-4098-9
   PubMed Web of Science ®Google Scholar
• Yin WB, Baccile JA, Bok JW, Chen Y, Keller NP, Schroeder FC. 2013. A nonribosomal peptide synthetase-derived iron(iii) complex from the pathogenic fungus Aspergillus fumigatus. J Am Chem Soc. 135:2064–2067. doi:10.1021/ja311145n
   PubMed Web of Science ®Google Scholar
• Zabala AO, Xu W, Chooi YH, Tang Y. 2012. Characterization of a silent azaphilone gene cluster from Aspergillus niger ATCC 1015 reveals a hydroxylation-mediated pyran-ring formation. Chem Biol. 19:1049–1059. doi:10.1016/j.chembiol.2012.07.004
   PubMed Web of Science ®Google Scholar