Roles of the glyoxylate and methylcitrate cycles in sexual development and virulence in the cereal pathogen Gibberella zeae

Eukaryotic Cell

Volumn 8, Issue 8, 2009, Pages 1155-1164

  Lee, Seung Ho ^a   Han, You Kyoung ^b   Yun, Sung Hwan ^c   Lee, Yin Won ^a  

^a Seoul National University   (South Korea)

^b Rural Development Administration   (South Korea)

^c Soonchunhyang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYLCITRIC ACID; 2-METHYLCITRIC ACID; CITRIC ACID; FUNGAL PROTEIN; GLYOXYLIC ACID DERIVATIVE; ISOCITRATE LYASE; LYASE; METHYLISOCITRATE LYASE;

ARTICLE; CEREAL; ENZYMOLOGY; GENETICS; GIBBERELLA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; VIRULENCE;

CARBON-CARBON LYASES; CEREALS; CITRATES; FUNGAL PROTEINS; GIBBERELLA; GLYOXYLATES; ISOCITRATE LYASE; PLANT DISEASES; VIRULENCE;

FUNGI; GIBBERELLA; GIBBERELLA ZEAE; HORDEUM; TRITICUM AESTIVUM;

EID: 68549090821     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00335-08     Document Type: Article

References (50)

1. Amor, C., A. I. Domínguez, J. R. De Lucas, and F. Laborda. 2000. The catabolite inactivation of Aspergillus nidulans isocitrate lyase occurs by spe-cific autophagy of peroxisomes. Arch. Microbiol. 174:59-66.
2. Asakura, M., T. Okuno, and T. Takano. 2006. Multiple contributions of peroxisomal metabolic function to fungal pathogenicity in Colletotrichum lagenarium. Appl. Environ. Microbiol. 72:6345-6354.
3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. J. Biol. Chem. 72:248-254.
4. Brock, M. 2005. Generation and phenotypic characterization of Aspergillus nidulans methylisocitrate lyase deletion mutants: methylisocitrate inhibits growth and conidiation. Appl. Environ. Microbiol. 71:5465-5475.
5. Brock, M., D. Darley, S. Textor, and W. Buckel. 2001. 2-Methylisocitrate lyases from the bacterium Escherichia coli and the filamentous fungus Aspergillus nidulans: characterization and comparison of both enzymes. Eur. J. Biochem. 268:3577-3586.
6. Brock, M., R. Fischer, D. Linder, and W. Buckel. 2000. Methylcitrate synthase from Aspergillus nidulans: implications for propionate as an antifungal agent. Mol. Microbiol. 35:961-973.
7. Cánovas, D., and A. Andrianopoulos. 2006. Developmental regulation of the glyoxylate cycle in the human pathogen Penicillium marneffei. Mol. Microbiol. 62:1725-1738.
8. Capellini, R. A., and J. L. Peterson. 1965. Macroconidium formation in submerged cultures by a nonsprorulating strain of Gibberella zeae. Mycologia 57:962-966.
9. De Lucas, J. R., S. Valenciano, G. Turner, and F. Laborda. 1994. Glucoseinduced inactivation of isocitrate lyase in Aspergillus nidulans. Arch. Microbiol. 162:409-413.
10. Dixon, G. H., and H. J. Kornberg. 1959. Assay methods for key enzymes of the glyoxylate cycle. Biochem. J. 72:3.
11. Dyer, P. S., D. S. Ingram, and K. Johnstone. 1993. Evidence for the involvement of linoleic acid and other endogenous lipid factors in perithecial development of Nectria haematococca mating population VI. Mycol. Res. 97: 485-496.
12. Ebel, F., M. Schwienbacher, J. Beyer, J. Heesemann, A. A. Brakhage, and M. Brock. 2006. Analysis of the regulation, expression, and localisation of the isocitrate lyase from Aspergillus fumigatus, a potential target for antifungal drug development. Fungal Genet. Biol. 43:476-489.
13. Fernando, W. G. D., J. D. Miller, W. L. Seaman, K. Seifert, and T. C. Paulitz. 2000. Daily and seasonal dynamics of airborne spores of Fusarium graminearum and other Fusarium species samples over wheat pots. Can. J. Bot. 78:497-505.
14. Fleck, C. B., and M. Brock. 2008. Characterization of an acyl-CoA: carbox-ylate-CoA transferase from Aspergillus nidulans involved in propionyl-CoA detoxification. Mol. Microbiol. 68:642-656.
15. Gainey, L. D., I. F. Connerton, E. H. Lewis, G. Turner, and D. J. Balance. 1992. Characterization of the glyoxysomal isocitrate lyase genes of Aspergillus nidulans (acuD) and Neurospora crassa (acu-3). Curr. Genet. 21:43-47.
16. Goldman, G. H., E. dos Reis Marques, D. C. D Ribeiro, L. A. de Souza Bernardes, A. C. Quiapin, P. M. Vitorelli, M. Savoldi, C. P. Semighini, R. C. de Oliveira, et al. 2003. Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes. Eukaryot. Cell 2:34-48.
17. Gould, T. A., H. van de Langemheen, E. J. Muñoz-Elías, J. D. McKinney, and J. C. Sacchettini. 2006. Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol. Microbiol. 61: 940-947.
18. Han, Y.-K., T. Lee, K.-H. Han, S.-H. Yun, and Y.-W. Lee. 2004. Functional analysis of the homoserine O-acetyltransferase gene and its identification as a selectable marker in Gibberella zeae. Curr. Genet. 46:205-212.
19. Ibrahim-Granet, O., M. Dubourdeau, J.-P. Latge, P. Ave, M. Huerre, A. A. Brakhage, and M. Brock. 2008. Methylcitrate synthase from Aspergillus fumigatus is essential for manifestation of invasive aspergillosis. Cell. Microbiol. 10:134-148.
20. Idnurm, A., and B. J. Howlett. 2002. Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassia napus). Eukaryot. Cell 1:719-724.
21. Jansen, C., D. von Werrstein, W. Schäfer, K. H. Kogel, A. Felk, and F. J. Maier. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichothecene synthase gene disrupted Fusarium graminearum. Proc. Natl. Acad. Sci. USA 102:16892-16897.
22. Jung, S., J.-E. Kim, S.-H. Yun, and Y.-W. Lee. 2006. Possible negative effect of pigmentation on biosynthesis of polyketide mycotoxin zearalenone in Gibberella zeae. J. Microbiol. Biotechnol. 16:1392-1398.
23. Kim, J.-E., K.-H. Han, J. Jin, H. Kim, J.-C. Kim, S.-H. Yun, and Y.-W. Lee. 2005. Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl. Environ. Microbiol. 71:1701-1708.
24. Lacourt, I., S. Duplessis, S. Abbà, P. Bonfante, and F. Martin. 2002. Isolation and characterization of differentially expressed genes in the mycelium and fruit body of Tuber borchii. Appl. Environ. Microbiol. 68:4574-4582.
25. Lee, J., T. Lee, Y.-W. Lee, S.-H. Yun, and B. G. Turgeon. 2003. Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol. Microbiol. 50:145-152.
26. Leslie, J. F., and B. A. Summerell. 2006. The Fusarium laboratory manual. Blackwell Professional, Ames, IA.
27. Lorenz, M. C., and G. R. Fink. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412:83-86.
28. Lorenz, M. C., and G. R. Fink. 2002. Life and death in a macrophage: role of the glyoxylate cycle in virulence. Eukaryot. Cell 1:657-662.
29. Lorenz, M. C., J. A. Bender, and G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3:1076-1087.
30. Luttik, M. A., P. Kotter, F. A. Salomons, I. J. van Der Klei, J. P. Dijken, and J. T. Pronk. 2000. The Saccharomyces cerevisiae ICL2 gene encodes a mitochondrial 2-methylisocitrate lyase involved in propionyl-coenzyme A metabolism. J. Bacteriol. 182:7007-7013.
31. Maerker, C., M. Rohde, A. A. Brakhage, and M. Brock. 2005. Methylcitrate synthase from Aspergillus fumigatus propionyl-CoA affects polyketide synthesis, growth, and morphology of conidia. FEBS J. 272:3615-3630.
32. Marasas, W. F. O., P. E. Nelson, and T. A. Toussoun. 1984. Toxigenic Fusarium species; identity and mycotoxicology. The Pennsylvania State University Press, University Park.
33. McMullen, M., R. Jones, and D. Gallenberg. 1997. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis. 81:1340-1348.
34. Muñoz-Elías, E. J., and J. D. McKinney. 2005. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11:638-644.
35. Muñoz-Elías, E. J., A. M. Upton, J. Cherian, and J. D. McKinney. 2006. Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol. Microbiol. 60:109-1122.
36. Namiki, F., M. Matsunaga, M. Okuda, I. Inoue, K. Nishi, Y. Fujita, and T. Tsuge. 2001. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol. Plant-Microbe Interact. 14:580-584.
37. O'Donnell, K., H. C. Kistler, B. K. Tacke, and H. H. Casper. 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.
38. Olivas, I., M. Royuela, B. Romero, M. C. Monteiro, J. M Mínguez, F. Laborda, and R. De Lucas. 2008. Ability to grown on lipids accounts for the fully virulent phenotype in neutopenic mice of Aspergillus fumigatus null mutants in the key glyoxylate cycle enzymes. Fungal Genet. Biol. 45:45-60.
39. Parry, D. W., P. Jenkinson, and L. McLeod. 1995. Fusarium ear blight (scab) in small grain cereals: a review. Plant Pathol. 44:207-238.
40. Pronk, J. T., A. van der Linden-Beuman, C. Verduyn, W. A. Scheffers, and J. P. van Dijken. 1994. Propionate metabolism in Saccharomyces cerevisae: implications for the metabolon hypothesis. Microbiology 140:717-722.
41. Rude, T. H., D. L. Toffaletti, G. M. Cox, and J. R. Perfect. 2002. Relationship of the glyoxylate pathway to the pathogenesis of Cryptococcus neoformans. Infect. Immun. 70:5684-5694.
42. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Schöbel, F., O. Ibrahim-Granet, P. Aveá, J.-P. Latgeá, A. A. Brakhage, and M. Brock. 2007. Aspergillus fumigatus does not require fatty acid metabolism via isocitrate lyase for development of invasive aspergillosis. Infect. Immun. 75:1237-1244.
44. Solomon, P. S., R. C. Lee, T. J. Wilson, and R. P. Oliver. 2004. Pathogenicity of Stagonospora nodorum requires malate synthase. Mol. Microbiol. 53:1065-1073.
45. Trail, F., H. Xu, R. Loranger, and D. Gadoury. 2002. Physiological and environmental aspects of ascospore discharge in Gibberella zeae. Mycologia 92:130-138.
46. Wang, Z. Y., C. R. Thornton, M.-J. Kershaw, L. Debao, and N. J. Talbot. 2003. The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenicic fungus Magnaporthe grisea. Mol. Microbiol. 47:1601-1612.
47. Yoon, J. J., T. Hattori, and M. Shimada. 2002. A metabolic role of the glyoxylate and tricarboxylic acid cycles for development of the copper-tolerant brown-rot fungus Fomitopsis palustris. FEMS Microbiol. Lett. 217:9-14.
48. Yu, J.-H., Z. Hamari, K.-H. Han, J.-A. Seo, Y. Reyes-Dominguez, and C. Scazzocchio. 2004. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41:973-981.
49. Zhang, Y.-Q., M. Brock, and N. P. Keller. 2004. Connection of propionyl-CoA metabolism to polyketide biosynthesis in Aspergillus nidulans. Genetics 168:785-794.
50. Zhang, Y.-Q., and N. P. Keller. 2004. Blockage of methylcitrate cycle inhibits polyketide production in Aspergillus nidulans. Mol. Microbiol. 52:541-550.