DOI QR코드

DOI QR Code

Regulation of Fumonisin Biosynthesis in Fusarium verticillioides-Maize System

  • Sagaram Uma Shankar (Department of Plant Pathology and Microbiology, Program for the Biology of Filamentous Fungi, Texas A&M University, College Station) ;
  • Kolomiets Mike (Department of Plant Pathology and Microbiology, Program for the Biology of Filamentous Fungi, Texas A&M University, College Station) ;
  • Shim Won-Bo (Department of Plant Pathology and Microbiology, Program for the Biology of Filamentous Fungi, Texas A&M University, College Station)
  • Published : 2006.09.01

Abstract

Fumonisins are a group of mycotoxins produced by a pathogen Fusarium verticillioides in infected maize kernels. Consumption of fumonisin-contaminated maize has been implicated in a number of animal and human illnesses, including esophageal cancer and neural tube defects. Since the initial discovery, chemistry, toxicology, and biology of fumonisins as well as the maize-Fusarium pathosystem have been extensively studied. Furthermore, in the past decade, significant progress has been made in terms of understanding the molecular biology of toxin biosynthetic genes. However, there is a critical gap in our understanding of the regulatory mechanisms involved in fumonisin biosynthesis. Here, we review and discuss our current knowledge about the molecular mechanisms by which fumonisin biosynthesis is regulated in F. verticillioides. In addition, we discuss the impact of maize kernel environment, particularly sugar and lipid molecules, on fumonisin biosynthesis.

Keywords

References

  1. ApSimon, J. W. 2001.Structure, synthesis, and biosynthesis of fumonisin B1 and related compounds. Environ. Health Perspect. 109 (Suppl. 2):245-249
  2. Bluhm, B. H. and Woloshuk, C. P. 2005. Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels. Mol. Plant-Microbe. Interact. 18:1333-1339 https://doi.org/10.1094/MPMI-18-1333
  3. Bluhm, B. H. and Woloshuk, C. P. 2006. Fck1, a C-type cyclin-dependent kinase, interacts with Fcc1 to regulate development and secondary metabolism in Fusarium verticillioides. Fungal Genet. Biol. 43:146-154 https://doi.org/10.1016/j.fgb.2005.09.006
  4. Bojja, R. S., Cerny, R. L., Proctor, R. H. and Du, L. C. 2004. Determining the biosynthetic sequence in the early steps the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J. Agric. Food Chem. 52:2855-2860 https://doi.org/10.1021/jf035429z
  5. Brown, D. W., Yu, J. H., Kelkar, H. S., Fernandes, M., Nesbitt, T. C., Keller, N. P., Adams, T. H. and Leonard, T. J. 1996. Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 93:1418-1422
  6. Brown, D. W., Cheung, F., Proctor, R. H., Butchko, R. A., Zheng, L., Lee, Y., Utterback, T., Smith, S., Feldblyum, T., Glenn, A. E., Plattner, R. D., Kendra, D. F., Town, C. D. and Whitelaw, C. A. 2005. Comparative analysis of 87,000 expressed sequence tags from the fumonisin-producing fungus Fusarium verticillioides. Fungal Genet BioI. 42:848-61 https://doi.org/10.1016/j.fgb.2005.06.001
  7. Burow, G B., Gardner, H. W. and Keller, N. P. 2000. Characterization of an Aspergillus responsive peanut seed lipoxygenase. Plant Mol. BioI. 42:689-701 https://doi.org/10.1023/A:1006361305703
  8. Burow, G. B., Nesbitt, T. C., Dunlap, J. and Keller, N. P. 1997. Seed lipoxygenase products modulate Aspergillus mycotoxins biosynthesis. Mol. Plant-Microbe Interact. 10:689-701
  9. Butchko, R. A. E., Plattner, R. D. and Proctor, R. H. 2003. FUMl3 encodes a short chain dehydrogenase/reductase required for C-3 carbonyl reduction during fumonisin biosynthesis in Gibberella moniliformis. J. Agric. Food Chem. 51:3000-3006 https://doi.org/10.1021/jf0262007
  10. Calvo, A., Hinze, L., Gardner, H. W. and Keller, N. P. 1999. Sporogenic effect of polyunsaturated fatty acids on Aspergillus spp. development. Appl. Environ. Microbiol. 65:3668-3673
  11. Champe, S. P. and El-Zayat, A. A. E. 1987. Isolation of a sexual sporulation hormone from Aspergillus nidulans. J. Bacteriol. 171:3982-3988
  12. Ding, Y, Bojja, R. S. and Du, L. C.2004. Fum3p, a 2-ketoglutarate-dependent dioxygenase required for C-5 hydroxylation of fumonisins in Fusarium verticillioides. Appl. Envir. Microbiol. 70:1931-1934 https://doi.org/10.1128/AEM.70.4.1931-1934.2004
  13. Eddine A. N., Hannemann, F. and Schafer, W. 2001. Cloning and expression analysis of NhL1, a gene encoding an extracellular lipase from the fungal pea pathogen Nectria haematococca MP VI (Fusarium solani f. sp. pisi) that is expressed in planta. Mol. Genet. Genomics 265(2):215-24 https://doi.org/10.1007/s004380000410
  14. Feng, J., Liu, G., Selvaraj, G., Hughes, G. R. and Wei, Y. 2005. A secreted lipase encoded by LIP1 is necessary for efficient use of saturated triglyceride lipids in Fusarium graminearum. Microbiology 151:3911-3921 https://doi.org/10.1099/mic.0.28261-0
  15. Feussner, I. and Wastemack, C. 2002. The lipoxygenase pathway. Annu. Rev. PIant BioI. 53:275-97 https://doi.org/10.1146/annurev.arplant.53.100301.135248
  16. Flaherty, J. E. and Woloshuk, C. P. 2004. Regulation of fumonisin biosynthesis in Fusarium verticillioides by a zinc binuclear cluster-type gene, ZFRl. Appl. Environ. Microbiol. 70:2653-2659 https://doi.org/10.1128/AEM.70.5.2653-2659.2004
  17. Flaherty, J. E., Pirttila, A. M., Bluhm, B. H. and Woloshuk, C. P. 2003. PACl, a pH-regulatory gene from Fusarium verticillioides. Appl. Environ. Microbiol. 69:5222-5227 https://doi.org/10.1128/AEM.69.9.5222-5227.2003
  18. Kennedy, J., Auclair, K., Kendrew, S. G., Park, C., Vederas, J. C. and Hutchinson, C. R.1999. Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis. Science 284:1368-1372 https://doi.org/10.1126/science.284.5418.1368
  19. Gelderblom, W. C. A, Jaskiewick, K., Marasas, W. F. O., Thiel, P. G., Horak, M. J., Vleggaar, R. and Kreik, N. P. J. 1988. Fumonisins-novel mycotoxins with cancer promoting activity produced by Fusarium moniliforme. Appl. Environ. Microbial. 54:1806-1811
  20. Goodrich-Tanrikulu, M., Mahoney, N. and Rodriguez, S. B. 1995. The plant growth regulator methy1 jasmonate inhibits aflatoxin production by Aspergillus flavus. Microbiolgy 141:2831-2837
  21. Keller, S. E., Sullivan, T. M. and Chirtel, S. 1997. Factors affecting the growth of Fusarium proliferatum and the production of fumonisin B1: oxygen and PH. J. Indust. Microbiol. Biotechnol. 19:305-309 https://doi.org/10.1038/sj.jim.2900466
  22. Kock, J. L., Strauss, T., Pohl, C. H., Smith, D. P., Botes, P. J., Pretorius, E. E., Tepeny, T., Sebolai, Botha, A. and Nigam, S. 2001. Bioprospecting for novel oxylipins in fungi: the presence of 3-hydroxy oxylipins in Pilobolus. Antonie van Leeuwenhoek 80:93-99 https://doi.org/10.1023/A:1012200119681
  23. Kommedahl, T. and Windels, C. E. 1981.Root-, stalk-, and earinfecting Fusarium species on com in the USA. In: Fusarium: Disease, biology, and taxonomy, ed. by P. E. Nelson, T. A. Toussoun and R. J. Cook. pp. 94-103. The Pennsylvania State University Press, University Park
  24. Marasas, W. F. O. 2001. Discovery and occurrence of the fumonisins: A historical perspective. Environ. Health Perspect. 109:239-243 https://doi.org/10.1289/ehp.01109s2239
  25. Marin, S., Magan, N., Belli, A., Ramos, A. J., Canela, R. and Sanchis, V.1999. Two-dimensional profiles of fumonisin B-1 production by Fusarium moniliforme and Fusarium proliferatum in relation to environmental factors and potential for modelling toxin formation in maize grain. Int. J. Food Microbiol. 51:519-167
  26. Merrill, A. H., Sullards, M. C., Wang, E., Voss, K. A. and Riley, R. T. 2001. Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ. Health Perspect. 109(SuppI 2):283-289 https://doi.org/10.1289/ehp.01109s2283
  27. Missmer, S. A., Suarez, L., Felkner, M., Wang, E., Merrill, A. H., Rothman, K. J. and Hendricks, K. A. 2006. Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border. Environ. Health Perspect. 114:237-241 https://doi.org/10.1289/ehp.8221
  28. Munkvold, G. P. and Desjardins, A. E. 1997. Fumonisins in maize - Can we reduce their occurrence? Plant Disease 81:556-565 https://doi.org/10.1094/PDIS.1997.81.6.556
  29. Nelson, P. E., Desjardins, A. E. and Plattner, R. D. 1993. Fumonisins, Mycotoxins Produced by Fusarium Species: Biology, Chemistry, and Significance. Ann. Rev. Phytopathol. 31:233-252 https://doi.org/10.1146/annurev.py.31.090193.001313
  30. Noverr, M. C., Erb-Downward, J. R. and Huffnagle, G. B. 2003. Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin. Microbiol. Rev. 16:517-33 https://doi.org/10.1128/CMR.16.3.517-533.2003
  31. Noverr, M. C. and Huffnagle, G. B. 2004. Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect. Immun. 72:6206-6210 https://doi.org/10.1128/IAI.72.11.6206-6210.2004
  32. PirttiHi, A. M., McIntyre, L. M., Payne, G. A. and Woloshuk, C. P. 2004. Expression profile analysis of wild-type and fcc1 mutant strains of Fusarium verticillioides during fumonisin biosynthesis. Fungal Genet. Biol. 41:647-56 https://doi.org/10.1016/j.fgb.2004.02.001
  33. Proctor, R. H., Desjardins, A. E., Plattner, R. D. and Hohn, T. M. 1999. A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet. Biol. 27:100-112 https://doi.org/10.1006/fgbi.1999.1141
  34. Proctor, R. H., Brown, D. W., Plattner, R. D. and Desjardins, A. E. 2003. Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet. Biol. 38:237-249 https://doi.org/10.1016/S1087-1845(02)00525-X
  35. Sagaram, U. S., Butchko, R. A. E. and Shim, W. B. 2006. The putative monomeric G-protein GBP1 is negatively associated with fumonisin $B_1$ production in Fusarium verticillioides. Mol. Plant Pathol. in press
  36. Samapundo, S., Devliehgere, E, De Meulenaer, B. and Debevere, J. 2005. Effect of water activity and temperature on growth and the relationship between fumonisin production and the radial growth of Fusarium verticillioides and Fusarium proliferatum on corn. J. Food Prot. 68:1054-1059 https://doi.org/10.4315/0362-028X-68.5.1054
  37. 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. BioI. 34:155-165 https://doi.org/10.1006/fgbi.2001.1299
  38. Shim, W. B.and Woloshuk, C. P. 1999. Nitrogen repression of fumonisin B1 biosynthesis in Gibberella fujikuroi. FEMS Microbiol. Lett. 177:109-116 https://doi.org/10.1111/j.1574-6968.1999.tb13720.x
  39. Shim, W. B. and Woloshuk, C. P 2001. Regulation of fumonisin B-1 biosynthesis and conidiation in Fusarium verticillioides by a cyclin-like (C-type) gene, FCC1. Appl. Environ. MicrobioI. 67:1607-1612 https://doi.org/10.1128/AEM.67.4.1607-1612.2001
  40. Shim, W. B., Flaherty, J. E. and Woloshuk, C. P. 2003. Comparison of fumonisin B-1 biosynthesis in maize germ and degermed kernels by Fusarium verticillioides. J. Food Prot. 66:2116-2122 https://doi.org/10.4315/0362-028X-66.11.2116
  41. Tsitsigiannis, D. I., Koweiski, T., Zamowski, R. and Keller, N. P. 2005. Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiology 151:1809-21 https://doi.org/10.1099/mic.0.27880-0
  42. Tsitsigiannis, D. I. and Keller, N. P. 2006. Oxylipins act as determinants of natural product biosynthesis and seed colonization in Aspergillus nidulans. Mol. Microbiol. 59:882-892 https://doi.org/10.1111/j.1365-2958.2005.05000.x
  43. Voigt, C. A., Schafer, W. and Salomon, S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42:364-375 https://doi.org/10.1111/j.1365-313X.2005.02377.x
  44. Warfield, C. Y. and Gilchrist, D. G. 1999. Influence of kernel age on fumonisin B1 production in maize by Fusarium moniliforme. Appl. Envir. Microbiol. 65:2853-2856
  45. Wilson, R. A., Gardner, H. W. and Keller, N. P. 2001. Cultivardependent expression of a maize Ipioxygenase responsive to seed infesting fungi. Mol. Plant-Microbe Interact. 8:980-987
  46. Woloshuk, C. P., Foutz, K. R., Brewer, J. E., Bhatnagar, D., Cleveland, T. E. and Payne, G. A.1994. Molecular characterization of aflR, a regulatory locus for aflatoxin biosynthesis. Appl. Environ. Microbiol. 60:2408-2414
  47. Wright, M. S., Greene, D. M., Zeringue, H. J., Bhatnagar, D. and Cleveland, T. E. 2000. Effects of volatile aldehydes from Aspergillus-resistant varieties of com on Aspergillus parasiticus growth and aflatoxin accumulation. Toxicon. 38:1215-1223 https://doi.org/10.1016/S0041-0101(99)00221-4
  48. Yu, J. H. and Keller, N. P. 2005. Regulation of secondary metabolism in filamentous fungi. Annu. Rev. Phytopathol. 43:437-458 https://doi.org/10.1146/annurev.phyto.43.040204.140214
  49. Zeringue, Jr., H. J., Brown, R. L., Neucere, J. N. and Cleveland, T. E. 1996. Relationship between C6-C12 alkanal and alkenal volatile contens and resistance of maize genotypes to Aspergillus flavus and aflatoxin production. J. Agric, Food. Chem. 44:403-407 https://doi.org/10.1021/jf950313r

Cited by

  1. Natural functions of mycotoxins and control of their biosynthesis in fungi vol.87, pp.3, 2010, https://doi.org/10.1007/s00253-010-2657-5
  2. GAC1, a gene encoding a putative GTPase-activating protein, regulates bikaverin biosynthesis in Fusarium verticillioides vol.100, pp.5, 2008, https://doi.org/10.3852/08-015
  3. Constitutive expression of pathogenesis-related proteins and antioxydant enzyme activities triggers maize resistance towards Fusarium verticillioides vol.200, 2016, https://doi.org/10.1016/j.jplph.2016.06.006
  4. Resistance to Fusarium verticillioides and fumonisin accumulation in maize inbred lines involves an earlier and enhanced expression of lipoxygenase (LOX) genes vol.188, 2015, https://doi.org/10.1016/j.jplph.2015.09.003
  5. Factors of theFusarium verticillioides-maize environment modulating fumonisin production vol.36, pp.3, 2010, https://doi.org/10.3109/10408411003720209
  6. Metabolomics ofAspergillus fumigatus vol.47, pp.s1, 2009, https://doi.org/10.1080/13693780802307720
  7. Fusarium species—a promising tool box for industrial biotechnology vol.101, pp.9, 2017, https://doi.org/10.1007/s00253-017-8255-z
  8. Exploration of industrially important pigments from soil fungi vol.100, pp.4, 2016, https://doi.org/10.1007/s00253-015-7231-8
  9. Disruption of a Maize 9-Lipoxygenase Results in Increased Resistance to Fungal Pathogens and Reduced Levels of Contamination with Mycotoxin Fumonisin vol.20, pp.8, 2007, https://doi.org/10.1094/MPMI-20-8-0922
  10. Sequencing, physical organization and kinetic expression of the patulin biosynthetic gene cluster from Penicillium expansum vol.189, 2014, https://doi.org/10.1016/j.ijfoodmicro.2014.07.028
  11. Host-derived lipids and oxylipins are crucial signals in modulating mycotoxin production by fungi vol.28, pp.2-3, 2009, https://doi.org/10.1080/15569540802420584
  12. dl-β-Aminobutyric Acid–Induced Resistance of Potato AgainstPhytophthora infestansRequires Salicylic Acid but Not Oxylipins vol.23, pp.5, 2010, https://doi.org/10.1094/MPMI-23-5-0585
  13. Enhanced Homologous Recombination in Fusarium verticillioides by Disruption of FvKU70, a Gene Required for a Non-homologous End Joining Mechanism vol.24, pp.1, 2008, https://doi.org/10.5423/PPJ.2008.24.1.001
  14. Protein phosphatase 2A regulatory subunits perform distinct functional roles in the maize pathogenFusarium verticillioides vol.14, pp.5, 2013, https://doi.org/10.1111/mpp.12023
  15. Transcriptional changes in developing maize kernels in response to fumonisin-producing and nonproducing strains of Fusarium verticillioides vol.210, 2013, https://doi.org/10.1016/j.plantsci.2013.05.020