An In planta-expressed polyketide synthase produces (R)-mellein in the wheat pathogen Parastagonospora nodorum

Applied and Environmental Microbiology

Volumn 81, Issue 1, 2015, Pages 177-186

  Chooi, Yit Heng ^a   Krill, Christian ^b   Barrow, Russell A ^c   Chen, Shasha ^c   Trengove, Robert ^b   Oliver, Richard P ^d   Solomon, Peter S ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b MURDOCH UNIVERSITY   (Australia)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d CURTIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; KETONES; YEAST;

COMPARATIVE SEQUENCE ANALYSIS; HETEROLOGOUS EXPRESSION; MEDICAGO TRUNCATULA; PHYLOGENETIC ANALYSIS; POLYKETIDE SYNTHASES; SACCHAROMYCES CEREVISIAE YEAST; TRANSCRIPTIONAL ANALYSIS; TRITICUM AESTIVUM;

SEED;

COLOR; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; FUNGUS; GENETIC VARIATION; PATHOGEN; PHYLOGENETICS; WHEAT; YEAST;

BACTERIA (MICROORGANISMS); DOTHIDEOMYCETES; FUNGI; MEDICAGO TRUNCATULA; SACCHAROMYCES CEREVISIAE; TRITICUM AESTIVUM;

FUNGAL DNA; OCHRACIN; OCHRATOXIN; POLYKETIDE SYNTHASE;

ASCOMYCETES; CHEMISTRY; DNA SEQUENCE; FUNGAL GENE; GENE EXPRESSION; GENE INACTIVATION; GENETICS; MEDICAGO; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PLANT DEVELOPMENT; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; WHEAT;

ASCOMYCOTA; CLONING, MOLECULAR; DNA, FUNGAL; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; GENES, FUNGAL; MEDICAGO; MOLECULAR SEQUENCE DATA; OCHRATOXINS; PHYLOGENY; PLANT DEVELOPMENT; POLYKETIDE SYNTHASES; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRITICUM;

EID: 84917729581     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02745-14     Document Type: Article

References (68)

1. Muria-Gonzalez MJ, Chooi YH, Breen S, Solomon PS. 29 May 2014. The past, present and future of secondary metabolite research in the Dothideomycetes. Mol Plant Pathol http://dx.doi.org/10.1111/mpp.12162.
2. Mobius N, Hertweck C. 2009. Fungal phytotoxins as mediators of virulence. Curr Opin Plant Biol 12:390-398. http://dx.doi.org/10.1016/j.pbi.2009.06.004.
3. Collemare J, Lebrun M-H. 2011. Fungal secondary metabolites: ancient toxins and novel effectors in plant-microbe interactions, p 379-402. In Martin F, Kamoun S (ed), Effectors in plant-microbe interactions. Wiley-Blackwell, Oxford, United Kingdom.
4. Bohnert M, Wackler B, Hoffmeister D. 2010. Spotlights on advances in mycotoxin research. Appl Microbiol Biotechnol 87:1-7. http://dx.doi.org/10.1007/s00253-010-2565-8.
5. Oliver RP, Friesen TL, Faris JD, Solomon PS. 2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annu Rev Phytopathol 50: 23-43. http://dx.doi.org/10.1146/annurev-phyto-081211-173019.
6. Hane JK, Lowe RG, Solomon PS, Tan KC, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SF, McDonald BA, Oliver RP. 2007. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19:3347-3368. http://dx.doi.org/10.1105/tpc.107.052829.
7. Chooi YH, Muria-Gonzalez MJ, Solomon PS. 2014. A genome-wide survey of the secondary metabolite biosynthesis genes in the wheat pathogen Parastagonospora nodorum. Mycology 5:192-206. http://dx.doi.org/10.1080/21501203.2014.928386.
8. 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. http://dx.doi.org/10.1016/S0031-9422(00)82234-7.
9. Devys M, Barbier M, Bousquet JF, Kollmann A. 1992. Isolation of the new (-)-(3R,4S)-4-hydroxymellein from the fungus Septoria nodorum Berk. Z Naturforsch C 47:779-781.
10. 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. http://dx.doi.org/10.1016/0040-4039(82)80143-3.
11. Devys M, Bousquet JF, Kollmann A, Barbier M. 1978. Isolation of a new pyrazine, septorine, from culture medium of phytopathogen fungus Septoria nodorum Berk. C R Hebd Seances Acad Sci C 286:457-458.
12. 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. http://dx.doi.org/10.1007/s11306-009-0158-2.
13. 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 Bioprospect 3:141-144. http://dx.doi.org/10.1007/s13659-013-0055-2.
14. Huffman J, Gerber R, Du L. 2010. Recent advancements in the biosynthetic mechanisms for polyketide-derived mycotoxins. Biopolymers 93: 764-776. http://dx.doi.org/10.1002/bip.21483.
15. Ipcho SV, Hane JK, Antoni EA, Ahren D, Henrissat B, Friesen TL, Solomon PS, Oliver RP. 2012. Transcriptome analysis of Stagonospora nodorum: gene models, effectors, metabolism and pantothenate dispensability. Mol Plant Pathol 13:531-545. http://dx.doi.org/10.1111/j.1364-3703.2011.00770.x.
16. Bousquet JF, Skajennikoff M. 1974. Isolement et mode d'action d'une phytotoxine produite en culture par Septoria nodorum Berk. J Phytopathol 80:355-360. http://dx.doi.org/10.1111/j.1439-0434.1974.tb02768.x.
17. Benedikz PW, Mappledoram CJ, Scott PR. 1981. A laboratory technique for screening cereals for resistance to Septoria nodorum using detached seedling leaves. Trans Br Mycol Soc 77:667-669. http://dx.doi.org/10.1016/S0007-1536(81)80126-X.
18. Solomon PS, Waters ODC, Simmonds J, Cooper RM, Oliver RP. 2005. The Mak2 MAP kinase signal transduction pathway is required for pathogenicity in Stagonospora nodorum. Curr Genet 48:60-68. http://dx.doi.org/10.1007/s00294-005-0588-y.
19. Solomon PS, Rybak K, Trengove RD, Oliver RP. 2006. Investigating the role of calcium/calmodulin-dependent protein kinases in Stagonospora nodorum. Mol Microbiol 62:367-381. http://dx.doi.org/10.1111/j.1365-2958.2006.05380.x.
20. Mattern I, Punt P, Van den Hondel C. 1988. A vector of Aspergillus transformation conferring phleomycin resistance. Fungal Genet Newsl 35:25.
21. 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. http://dx.doi.org/10.1094/MPMI.2004.17.5.456.
22. Solomon PS, Ipcho SV, Hane JK, Tan KC, Oliver RP. 2008. A quantitative PCR approach to determine gene copy number. Fungal Genet Rep 55:5-8.
23. Lee KM, DaSilva NA. 2005. Evaluation of the Saccharomyces cerevisiae ADH2 promoter for protein synthesis. Yeast 22:431-440. http://dx.doi.org/10.1002/yea.1221.
24. Lee KK, Da Silva NA, Kealey JT. 2009. Determination of the extent of phosphopantetheinylation of polyketide synthases expressed in Escherichia coli and Saccharomyces cerevisiae. Anal Biochem 394:75-80. http://dx.doi.org/10.1016/j.ab.2009.07.010.
25. Ma SM, Li JW, Choi JW, Zhou H, Lee KK, Moorthie VA, Xie X, Kealey JT, Da Silva NA, Vederas JC, Tang Y. 2009. Complete reconstitution of a highly reducing iterative polyketide synthase. Science 326:589-592. http://dx.doi.org/10.1126/science.1175602.
26. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. http://dx.doi.org/10.1093/bioinformatics/bts199.
27. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
28. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
29. Chooi YH, Tang Y. 2012. Navigating the fungal polyketide chemical space: from genes to molecules. J Org Chem 77:9933-9953. http://dx.doi.org/10.1021/jo301592k.
30. Cox RJ. 2007. Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org Biomol Chem 5:2010-2026. http://dx.doi.org/10.1039/b704420h.
31. Schuemann J, Hertweck C. 2009. Biosynthesis of fungal polyketides, p 331-351. In Anke T, Weber D (ed), The Mycota: physiology and genetics, vol XV. Springer-Verlag, Berlin, Germany.
32. Fujii I, Ono Y, Tada H, Gomi K, Ebizuka Y, Sankawa U. 1996. Cloning of the polyketide synthase gene atX from Aspergillus terreus and its identification as the 6-methylsalicylic acid synthase gene by heterologous expression. Mol Gen Genet 253:1-10. http://dx.doi.org/10.1007/s004380050289.
33. 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. http://dx.doi.org/10.1021/ja304905e.
34. Glauser G, Gindro K, Fringeli J, De Joffrey JP, Rudaz S, Wolfender JL. 2009. Differential analysis of mycoalexins in confrontation zones of grapevine fungal pathogens by ultrahigh pressure liquid chromatography/timeof-flight mass spectrometry and capillary nuclear magnetic resonance. J Agric Food Chem 57:1127-1134. http://dx.doi.org/10.1021/jf8033539.
35. Beck J, Ripka S, Siegner A, Schiltz E, Schweizer E. 1990. The multifunctional 6-methylsalicylic acid synthase gene of Penicillium patulum. Its gene structure relative to that of other polyketide synthases. Eur J Biochem 192:487-498.
36. Lu P, Zhang A, Dennis LM, Dahl-Roshak AM, Xia YQ, Arison B, An Z, Tkacz JS. 2005. A gene (pks2) encoding a putative 6-methylsalicylic acid synthase from Glarea lozoyensis. Mol Genet Genomics 273:207-216. http://dx.doi.org/10.1007/s00438-005-1132-y.
37. Holm DK, Petersen LM, Klitgaard A, Knudsen PB, Jarczynska ZD, Nielsen KF, Gotfredsen CH, Larsen TO, Mortensen UH. 2014. Molecular and chemical characterization of the biosynthesis of the 6-MSAderived meroterpenoid yanuthone D in Aspergillus niger. Chem Biol 21: 519-529. http://dx.doi.org/10.1016/j.chembiol.2014.01.013.
38. Schmitt I, Lumbsch HT. 2009. Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 4:e4437. http://dx.doi.org/10.1371/journal.pone.0004437.
39. Evidente A, Punzo B, Andolfi A, Cimmino A, Melck D, Luque J. 2010. Lipophilic phytotoxins produced by Neofusicoccum parvum, a grapevine canker agent. Phytopathol Mediterr 49:74-79.
40. Moriguchi T, Kezuka Y, Nonaka T, Ebizuka Y, Fujii I. 2010. Hidden function of catalytic domain in 6-methylsalicylic acid synthase for product release. J Biol Chem 285:15637-15643. http://dx.doi.org/10.1074/jbc.M110.107391.
41. Ishiuchi K, Nakazawa T, Ookuma T, Sugimoto S, Sato M, Tsunematsu Y, Ishikawa N, Noguchi H, Hotta K, Moriya H, Watanabe K. 2012. Establishing a new methodology for genome mining and biosynthesis of polyketides and peptides through yeast molecular genetics. Chembiochem 13:846-854. http://dx.doi.org/10.1002/cbic.201100798.
42. Lackner G, Bohnert M, Wick J, Hoffmeister D. 2013. Assembly of melleolide antibiotics involves a polyketide synthase with cross-coupling activity. Chem Biol 20:1101-1106. http://dx.doi.org/10.1016/j.chembiol.2013.07.009.
43. Schroeckh V, Scherlach K, Nutzmann HW, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA. 2009. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106:14558-14563. http://dx.doi.org/10.1073/pnas.0901870106.
44. Gaisser S, Trefzer A, Stockert S, Kirschning A, Bechthold A. 1997. Cloning of an avilamycin biosynthetic gene cluster from Streptomyces viridochromogenes Tu57. J Bacteriol 179:6271-6278.
45. Ahlert J, Shepard E, Lomovskaya N, Zazopoulos E, Staffa A, Bachmann BO, Huang K, Fonstein L, Czisny A, Whitwam RE, Farnet CM, Thorson JS. 2002. The calicheamicin gene cluster and its iterative type I enediyne PKS. Science 297:1173-1176. http://dx.doi.org/10.1126/science.1072105.
46. Ding W, Lei C, He Q, Zhang Q, Bi Y, Liu W. 2010. Insights into bacterial 6-methylsalicylic acid synthase and its engineering to orsellinic acid synthase for spirotetronate generation. Chem Biol 17:495-503. http://dx.doi.org/10.1016/j.chembiol.2010.04.009.
47. Nishikawa H. 1933. Biochemistry of filamentous fungi. II. A metabolic product of Aspergillus melleus Yukawa. Part I. J Agric Chem Soc Jpn 9:107-109.
48. Blair J, Newbold G. 1955. Lactones. Part II. The structure of mellein. J Chem Soc. 2871-2875.
49. Arakawa H. 1968. Absolute configuration of mellein. Bull Chem Soc Jpn 41:2541. http://dx.doi.org/10.1246/bcsj.41.2541.
50. Camarda L, Merlini L, Nasini G. 1976. Metabolites of Cercospora. Taiwapyrone, an alpha-pyrone of unusual structure from Cercospora taiwanensis Phytochemistry 15:537-539.
51. Pongcharoen W, Rukachaisirikul V, Phongpaichit S, Sakayaroj J. 2007. A new dihydrobenzofuran derivative from the endophytic fungus Botryosphaeria mamane PSU-M76. Chem Pharm Bull (Tokyo) 55:1404-1405. http://dx.doi.org/10.1248/cpb.55.1404.
52. Rukachaisirikul V, Arunpanichlert J, Sukpondma Y, Phongpaichit S, Sakayaroj J. 2009. Metabolites from the endophytic fungi Botryosphaeria rhodina PSU-M35 and PSU-M114. Tetrahedron 65:10590-10595. http://dx.doi.org/10.1016/j.tet.2009.10.084.
53. Venkatasubbaiah P, Sutton TB, Chilton WS. 1991. Effect of phytotoxins produced by Botryosphaeria obtusa, the cause of black rot of apple fruit and frogeye leaf-spot. Phytopathology 81:243-247. http://dx.doi.org/10.1094/Phyto-81-243.
54. 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. http://dx.doi.org/10.1016/0031-9422(93)85221-C.
55. Edwards RL, Maitland DJ, Oliver CL, Pacey MS, Shields L, Whalley AJS. 1999. Metabolites of the higher fungi. Part 31. Longianone, a C7H6O4 spiro bicyclic lactone from the fungus Xylaria longiana (Rehm). J Chem Soc Perkin Trans 1:715-719.
56. Holler U, Konig GM, Wright AD. 1999. Three new metabolites from marine-derived fungi of the genera Coniothyrium and Microsphaeropsis. J Nat Prod 62:114-118. http://dx.doi.org/10.1021/np980341e.
57. 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. http://dx.doi.org/10.1007/s10658-006-9006-7.
58. Zhao JH, Zhang YL, Wang LW, Wang JY, Zhang CL. 2012. Bioactive secondary metabolites from Nigrospora sp. LLGLM003, an endophytic fungus of the medicinal plant Moringa oleifera Lam. World J Microbiol Biotechnol 28:2107-2112. http://dx.doi.org/10.1007/s11274-012-1015-4.
59. Ramos HP, Simao MR, de Souza JM, Magalhaes LG, Rodrigues V, Ambrosio SR, Said S. 2013. Evaluation of dihydroisocoumarins produced by the endophytic fungus Arthrinium state of Apiospora montagnei against Schistosoma mansoni. Nat Prod Res 27:2240-2243. http://dx.doi.org/10.1080/14786419.2013.811659.
60. Krohn K, Bahramsari R, Florke U, Ludewig K, Kliche-Spory C, Michel A, Aust HJ, Draeger S, Schulz B, Antus S. 1997. Dihydroisocoumarins from fungi: isolation, structure elucidation, circular dichroism and biological activity. Phytochemistry 45:313-320. http://dx.doi.org/10.1016/S0031-9422(96)00854-0.
61. Bestmann HJ, Kern F, Schafer D, Witschel MC. 1992. Pheromones. 86. 3,4-Dihydroisocoumarins, a new class of ant trail pheromones. Angew Chem Int Ed Engl 31:795-796. http://dx.doi.org/10.1002/anie.199207951.
62. Herzner G, Schlecht A, Dollhofer V, Parzefall C, Harrar K, Kreuzer A, Pilsl L, Ruther J. 2013. Larvae of the parasitoid wasp Ampulex compressa sanitize their host, the American cockroach, with a blend of antimicrobials. Proc Natl Acad Sci U S A 110:1369-1374. http://dx.doi.org/10.1073/pnas.1213384110.
63. Kern F, Klein RW, Janssen E, Bestmann HJ, Attygalle AB, Schafer D, Maschwitz U. 1997. Mellein, a trail pheromone component of the ant Lasius fuliginosus. J Chem Ecol 23:779-792. http://dx.doi.org/10.1023/B:JOEC.0000006410.35938.49.
64. Dai J, Carte BK, Sidebottom PJ, Sek Yew AL, Ng S, Huang Y, Butler MS. 2001. Circumdatin G, a new alkaloid from the fungus Aspergillus ochraceus. J Nat Prod 64:125-126. http://dx.doi.org/10.1021/np000381u.
65. Djoukeng JD, Polli S, Larignon P, Abou-Mansour E. 2009. Identification of phytotoxins from Botryosphaeria obtusa, a pathogen of black dead arm disease of grapevine. Eur J Plant Pathol 124:303-308. http://dx.doi.org/10.1007/s10658-008-9419-6.
66. Ramirez-Suero M, Benard-Gellon M, Chong J, Laloue H, Stempien E, Abou-Mansour E, Fontaine F, Larignon P, Mazet-Kieffer F, Farine S, Bertsch C. 2014. Extracellular compounds produced by fungi associated with Botryosphaeria dieback induce differential defence gene expression patterns and necrosis in Vitis vinifera cv. Chardonnay cells. Protoplasma 251:1417-1426. http://dx.doi.org/10.1007/s00709-014-0643-y.
67. Keller B, Winzeler H, Winzeler M, Fried PM. 1994. Differential sensitivity of wheat embryos against extracts containing toxins of Septoria nodorum-first steps towards in-vitro selection. J Phytopathol 141:233-240. http://dx.doi.org/10.1111/j.1439-0434.1994.tb01466.x.
68. Essad S, Bousquet JF. 1981. Action de l'ochracine, phytotoxine de Septoria nodorum Berk., sur le cycle mitotique de Triticum aestivum L. Agronomie 1:684-694.