Browse > Article
http://dx.doi.org/10.5423/PPJ.2008.24.1.008

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)
Publication Information
The Plant Pathology Journal / v.24, no.1, 2008 , pp. 8-16 More about this Journal
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
a gene cluster; aurofusarin biosynthesis; Gibberella zeae; polyketide;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
Times Cited By Web Of Science : 7  (Related Records In Web of Science)
연도 인용수 순위
1 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.   DOI   ScienceOn
2 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.   DOI
3 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.   DOI   ScienceOn
4 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.
5 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.   DOI   ScienceOn
6 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.   과학기술학회마을   DOI   ScienceOn
7 Leslie, J. F. and Summerell, B. A. 2006. The Fusarium Lab Manual. Blackwell, Ames.
8 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.   DOI   ScienceOn
9 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.   DOI   ScienceOn
10 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.
11 Sambrook, J. and Russell, D. W. 2001. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
12 Tudzynski, B. and Holter, K. 1998. Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet. Biol. 25:157-170.   DOI   ScienceOn
13 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.   DOI   ScienceOn
14 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.   DOI
15 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.   DOI   ScienceOn
16 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.   DOI   ScienceOn
17 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.
18 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.   DOI   ScienceOn
19 Marshall, M. R., Kim, J. and Wei, C.-I. 2000. Enzymatic browning in fruits, vegetables and seafoods. FAO rapport.
20 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.   DOI   ScienceOn
21 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.   DOI
22 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.   DOI   ScienceOn
23 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.   DOI   ScienceOn
24 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.   DOI   ScienceOn
25 Keller, N. P. and Hohn, T. M. 1997. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol. 21:17-29.   DOI   ScienceOn
26 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.   DOI   ScienceOn
27 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.   DOI   ScienceOn
28 Gray, J. S., Martin, G. C. J. and Rigby, W. 1967. Aurofusarin. J. Chem. Soc. (C) 2580-2587.
29 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.
30 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.   DOI   ScienceOn
31 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.   DOI   ScienceOn
32 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.   DOI
33 Chang, P.-K. 2003. The Aspergillus parasiticus protein AFLJ interacts with the aflatoxin pathway-specific regulator AFLR. Mol. Gen. Genomics 268:711-719.
34 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.   DOI   ScienceOn
35 Claus, H. 2004. Laccase: structure, reactions, distribution. Micron 35:93-96.   DOI   ScienceOn
36 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.   DOI   ScienceOn
37 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.   DOI   ScienceOn
38 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.   과학기술학회마을