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Functional Characterization of Genes Located at the Aurofusarin Biosynthesis Gene Cluster in Gibberella zeae

  • Kim, Jung-Eun (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University) ;
  • Kim, Jin-Cheol (Sustainable Chemical Technologies Division, Korea Research Institute of Chemical Technology) ;
  • Jin, Jian-Ming (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University) ;
  • Yun, Sung-Hwan (Department of Medical Biotechnology, Soonchunhyang University) ;
  • Lee, Yin-Won (Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University)
  • Published : 2008.03.31

Abstract

Aurofusarin is a polyketide pigment produced by some Fusarium species. The PKS12 and GIP1 genes, which encode a putative type I polyketide synthase (PKS) and a fungal laccase, respectively, are known to be required for aurofusarin biosynthesis in Gibberella zeae (anamorph: Fusarium graminearum). The ten additional genes, which are located within a 30 kb region of PKS12 and GIP1 and regulated by a putative transcription factor (GIP2), organize the aurofusarin biosynthetic cluster. To determine if they are essential for aurofusarin production in G. zeae, we have employed targeted gene deletion, complementation, and chemical analyses. GIP7, which encodes O-methyltransferase, is confirmed to be required for the conversion of norrubrofusarin to rubrofusarin, an intermediate of aurofusarin. GIP1-, GIP3-, and GIP8-deleted strains accumulated rubrofusarin, indicating those gene products are essential enzymes for the conversion of rubrofusarin to aurofusarin. Based on the phenotypic changes in the gene deletion strains examined, we propose a possible pathway for aurofusarin biosynthesis in G. zeae. Our results would provide important information for better understanding of naphthoquinone biosynthesis in other fdarnentous fungi as well as the aurofusarin biosynthesis in G. zeae.

Keywords

References

  1. Ashley, J. N., Hobbs, B. C. and Raistrick, H. 1937. LV. Studies in the biochemistry of micro-organisms. LIII. The crystalline coloring matters of Fusarium culmorum (W. G. Smith) Sacc. and related forms. Biochemical J. 31:385-397. https://doi.org/10.1042/bj0310385
  2. Chang, P.-K. 2003. The Aspergillus parasiticus protein AFLJ interacts with the aflatoxin pathway-specific regulator AFLR. Mol. Gen. Genomics 268:711-719.
  3. Chang, P.-K., Yu, J. and Yu, J.-H. 2004. aflT, a MFS transporterencoding gene located in the aflatoxin gene cluster, does not have a significant role in aflatoxin secretion. Fungal Genet. Biol. 41:911-920. https://doi.org/10.1016/j.fgb.2004.06.007
  4. Claus, H. 2004. Laccase: structure, reactions, distribution. Micron 35:93-96. https://doi.org/10.1016/j.micron.2003.10.029
  5. Dvorska, J. E. and Surai, P. F. 2004. Protective effect of modified glucomannans against changes in antioxidant systems of quail egg and embryo due to aurofusarin consumption. Asian Austral.J. Anim. 17:434-440. https://doi.org/10.5713/ajas.2004.434
  6. Dvorska, J. E., Surai, P. F., Speake, B. K. and Sparks, N. H. C. 2001. Effect of the mycotoxin aurofusarin on the antioxidant composition and fatty acid profile of quail eggs. Brit. Poultry Sci. 42:643-649. https://doi.org/10.1080/00071660120088470
  7. Frandsen, R. J. N., Nielsen, N. J., Maolanon, N., Sorensen, J. C., Olsson, S., Nielsen, J. and Giese, H. 2006. The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol. Microbiol. 61:1069-1080. https://doi.org/10.1111/j.1365-2958.2006.05295.x
  8. Graham, J. G., Zhang, H. J., Pendland, S. L., Santarsiero, B. D., Mesecar, A. D., Cabieses, F. and Farnsworth, N. R. 2004. Antimycobacterial naphthopyrones from Senna obliqua. J.Nat. Prod. 67:225-227. https://doi.org/10.1021/np030348i
  9. Gray, J. S., Martin, G. C. J. and Rigby, W. 1967. Aurofusarin. J. Chem. Soc. (C) 2580-2587.
  10. Han, Y.-K., Lee, T., Han, K.-H., Yun, S.-H. and Lee, Y.-W. 2004. Functional analysis of the homoserine O-acetyltransferase gene and its identification as a selectable marker in Gibberella zeae. Curr. Genet. 46:205-212. https://doi.org/10.1007/s00294-004-0528-2
  11. Hohn, T. M., Krishna, R. and Proctor, R. H. 1995. Characterization of a transcription activator controlling trichothecene toxin biosynthesis. Fungal Genet. Biol. 26:224-235. https://doi.org/10.1006/fgbi.1999.1122
  12. Jahn, B., Boukhallouk, F., Lotz, J., Langfelder, K., Wanner, G. and Brakhage, A. A. 2000. Interaction of human phagocytes with pigmentless Aspergillus conidia. Infect. Immun. 68:3736- 3739. https://doi.org/10.1128/IAI.68.6.3736-3739.2000
  13. Jung, S., Kim, J.-E., Yun, S.-H. and Lee, Y.-W. 2006. Possible negative effect of pigmentation on biosynthesis of polyketide mycotoxin zearalenone in Gibberella zeae. J. Microbiol. Biotechnol. 16:1392-1398.
  14. Keller, N. P. and Hohn, T. M. 1997. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol. 21:17-29. https://doi.org/10.1006/fgbi.1997.0970
  15. Kim, J.-E., Han, K.-H., Jin, J., Kim, H., Kim, J.-C., Yun, S.-H. and Lee, Y.-W. 2005a. Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl. Environ. Microbiol. 71:1701-1708. https://doi.org/10.1128/AEM.71.4.1701-1708.2005
  16. Kim, J.-E., Jin, J., Kim, H., Kim, J.-C., Yun, S.-H. and Lee, Y.-W. 2006. GIP2, a putative transcription factor that regulates the aurofusarin biosynthetic gene cluster in Gibberella zeae. Appl. Environ. Microbiol. 72:1645-1652. https://doi.org/10.1128/AEM.72.2.1645-1652.2006
  17. Kim, Y.-T., Lee, Y.-R., Jin, J., Han, K.-H., Kim, H., Kim, J.-C., Lee, T., Yun, S.-H. and Lee, Y.-W. 2005b. Two different polyketide synthase genes are required for synthesis of zearalenone in Gibberella zeae. Mol. Microbiol. 58:1102- 1113. https://doi.org/10.1111/j.1365-2958.2005.04884.x
  18. Kimura, Y., Shimada, A., Nakajima, H. and Hamasaki, T. 1988. Structures of naphthoquinones produced by the fungus, Fusarium sp., and their biological activity toward pollen germination. Agric. Biol. Chem. 52:1253-1259. https://doi.org/10.1271/bbb1961.52.1253
  19. Kitanaka, S., Nakayama, T., Shibano, T., Ohkoshi, E. and Takido, M. 1998. Antiallergic agent from natural sources. Structures and inhibitory effect of histamine release of naphthoquinone glycosides from seeds of Cassia obtusifola L. Chem. Pharm. Bull. 46:1650-1652. https://doi.org/10.1248/cpb.46.1650
  20. Kommedahl, T. and Windels, C. E. 1981. Root-, stalk- and earinfecting Fusarium species on corn in the USA. In: Fusarium Diseases, Biology and Taxonomy, ed. by P.E. Nelson and T.A. Toussoun, pp. 94-103. The Pennsylvania State University Press, University Park, USA.
  21. Langfelder, K., Jahn, B., Gehringer, H., Schmidt, A., Wanner, G. and Brakhage, A. A. 1998. Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med. Microbial. Immunol. 187:79-89. https://doi.org/10.1007/s004300050077
  22. Langfelder, K., Streibel, M., Jahn, B., Hasse, G. and Brakhage, A. A. 2003. Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet. Biol. 38:143-158. https://doi.org/10.1016/S1087-1845(02)00526-1
  23. Lee, S.-H., Kim, H.-K., Hong, S.-Y., Lee, Y.-W. and Yun, S.-H. 2006. A large genomic deletion in Gibberella zeae causes a defect in the production of two polyketides but not in sexual development or virulence. Plant Pathol. J. 22:215-221. https://doi.org/10.5423/PPJ.2006.22.3.215
  24. Leslie, J. F. and Summerell, B. A. 2006. The Fusarium Lab Manual. Blackwell, Ames.
  25. Linnemannstons, P., Schulte, J., Prado, M. D., Proctor, R. H., Avalos, J. and Tudzynski, B. 2002. The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet. Biol. 37:134-148. https://doi.org/10.1016/S1087-1845(02)00501-7
  26. Malz, S., Grell, M. N., Thrane, C., Maier, F. J., Rosager, P., Felk, A., Albertsen, K. S., Salomon, S., Bohn, L., Schäfer, W. and Giese, H. 2005. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet. Biol. 42:420-433. https://doi.org/10.1016/j.fgb.2005.01.010
  27. Marasas, W. F. O., Nelson, P. E. and Toussoun, T. A. 1984. Toxigenic Fusarium Species; Identity and Mycotoxicology. The Pennsylvania State University Press, University Park.
  28. Marshall, M. R., Kim, J. and Wei, C.-I. 2000. Enzymatic browning in fruits, vegetables and seafoods. FAO rapport.
  29. McMullen, M., Jones, R. and Gallenberg, D. 1997. Scab of wheat and barley: A re-emerging disease of devastating impact. Plant Dis. 81:1340-1348. https://doi.org/10.1094/PDIS.1997.81.12.1340
  30. Medentsev, A. G., Kotyk, A. N., Trufanova, V. A. and Akimenko, V. K. 1993. Identification of aurofusarin in Fusarium graminearum isolates, causing a syndrome of worsening of egg quality in chickens. Prikl. Biokhim. Mikrobiol 29:542-546.
  31. Medentsev, A. G., Arinbasarova, A. Y. and Akimenko, A. K. 2005. Biosynthesis of naphthoquinone pigments by fungi of the genus Fusarium. Appl. Biochem. Microbiol. 41:503-507. https://doi.org/10.1007/s10438-005-0091-8
  32. O'Donnell, K., Kistler, H. C., Tacke, B. K. and Casper, H. H. 2000. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc. Natl. Acad. Sci. USA 97:7905-7910. https://doi.org/10.1073/pnas.130193297
  33. Sambrook, J. and Russell, D. W. 2001. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
  34. Seo, J.-A., Proctor, R. H. and Plattner, R. D. 2001. Characterization of four clustered and coregulated genes associated with fumonisin biosynthesis in Fusarium verticillioides. Fungal Genet. Biol. 34:155-165. https://doi.org/10.1006/fgbi.2001.1299
  35. Tanaka, H. and Tamura, T. 1962. The chemical constitution of rubrofusarin, a pigment from Fusarium graminearum. Part. I. The zinc dust distillation of rubrofusarin and methylxanthones. Agr. Biol. Chem. 26:767-770. https://doi.org/10.1271/bbb1961.26.767
  36. Tudzynski, B. and Holter, K. 1998. Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet. Biol. 25:157-170. https://doi.org/10.1006/fgbi.1998.1095
  37. Yu, J.-H., Hamari, Z., Han, K.-H., Seo, J.-A., Reyes-Dominguez, Y. and Scazzocchio, C. 2004. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41:973-981. https://doi.org/10.1016/j.fgb.2004.08.001
  38. Yun, S.-H. 1998. Molecular genetics and manipulation of pathogenicity and mating determinants in Mycosphaerella zeaemaydis and Cochliobolus heterostrophus. Ph.D. thesis. Cornell University, Ithaca, USA.

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