AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Mycology Article
Article Link
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Invited Article | Open Access

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

Yit-Heng Chooi( ), Mariano Jordi Muria-Gonzalez, Peter S. Solomon
Plant Sciences Division, Research School of Biology, The Australian National University, Canberra, 0200, Australia
Show Author Information

Abstract

The model pathogen Parastagonospora nodorum is a necrotroph and the causal agent of the wheat disease Septoria nodorum blotch (SNB). The sequenced P. nodorum genome has revealed that the fungus harbours a large number of secondary metabolite genes. Secondary metabolites are known to play important roles in the virulence of plant pathogens, but limited knowledge is available about the SM repertoire of this wheat pathogen. Here, we review the secondary metabolites that have been isolated from P. nodorum and related species of the same genus and provide an in-depth genome-wide overview of the secondary metabolite gene clusters encoded in the P. nodorum genome. The secondary metabolite gene survey reveals that P. nodorum is capable of producing a diverse range of small molecules and exciting prospects exist for discovery of novel virulence factors and bioactive molecules.

Keywords

Parastagonospora nodorumsecondary metabolitesterpene synthaseplant pathogenpolyketide synthasenonribosomal peptide synthetase

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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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.
Crossref 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
Crossref 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
Crossref Google Scholar
 

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

Daub ME. 1982. Cercosporin, a photosensitizing toxin from Cercospora species. Phytopathology. 72:370–374. doi:10.1094/Phyto-72-370
Crossref 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
Crossref 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
Crossref 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.
Crossref 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
Crossref 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.
Crossref 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
Crossref 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
Crossref 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
Crossref 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.
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref Google Scholar
 

Johnson L. 2008. Iron and siderophores in fungal-host interactions. Mycol Res. 112:170–183.
Crossref Google 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
Crossref 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
Crossref 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
Crossref Google Scholar
 

Kimura N, Tsuge T. 1993. Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol. 175:4427–4435.
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref Google Scholar
 

Li SM. 2009. Evolution of aromatic prenyltransferases in the biosynthesis of indole derivatives. Phytochemistry. 70:1746–1757.
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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: 10.1071/CP13443
Crossref 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.
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref Google Scholar
 

Venkatasubbaiah P, Chilton WS. 1990. Phytotoxins of Botryosphaeria obtusa. J Nat Prod. 53:1628–1630. doi:10.1021/np50072a044
Crossref 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
Crossref 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
Crossref 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
Crossref Google Scholar
 

Walton JD. 2006. Hc-toxin. Phytochemistry. 67:1406–1413. doi:10.1016/j.phytochem.2006.05.033
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref 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
Crossref Google Scholar
Mycology
Volume 5 Issue 3,
September 2014
Pages 192-206
DOI: 10.1080/21501203.2014.928386
Cite this article:
Chooi Y-H, Muria-Gonzalez MJ, Solomon PS. A genome-wide survey of the secondary metabolite biosynthesis genes in the wheat pathogen Parastagonospora nodorum. Mycology, 2014, 5(3): 192-206. https://doi.org/10.1080/21501203.2014.928386

122

Views

25

Crossref

N/A

Web of Science

21

Scopus

Altmetrics
Received: 02 April 2014
Accepted: 22 May 2014
Published: 22 July 2014
© 2014 The Author(s).

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The moral rights of the named author(s) have been asserted.
Return