B-series fumonisins (FBs) are a family of carcinogenic mycotoxins that commonly occur in maize. These mycotoxins cause multiple diseases in animals and are epidemiologically associated with several human diseases in populations for which maize is a dietary staple. FBs are produced by multiple genera of the fungiAspergillus,Fusarium andTolypocladium, but the plant pathogenFusarium verticillioides is considered the primary cause of FB contamination in maize. OneF. verticillioides strain, MRC 826, is reported to produce high levels of FBs. However, in the current study, 18 isolates derived from strain MRC 826 exhibited highly variable levels of FB, which negatively correlated (r=-0.333;P<0.008) with fungal growth. Microsatellite analysis confirmed that all MRC 826 derived isolates examined were clonal, and 100% DNA sequence identity was observed across theFUM gene clusters of two high FB producing and two low FB producing isolates. At the gene expression level, qRT-PCR at each time point (7, 14, 21 and 28 days of incubation) showed differential upregulation of selectedFUM genes in the high compared to the low FB isolates. Variation in FB production appears due to differences inFUM gene expression, most likely caused by sequence differences at unexamined loci not part of theFUM cluster or from epigenetic influences. Clarification of the genetic/epigenetic basis for quantitative differences in fumonisin production among strains and isolates ofF. verticillioides has potential to reveal targets for reducing FB contamination in maize.
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Abd-Elsalam, K.A., Yassin, M.A., Moslem, M.A., Bahkali, A.H., De Wit, P.J.G.M., McKenzie, E.H.C., Stephenson, S.L., Cai, L. and Hyde, K.D., 2010. Culture collections, the new herbaria for fungal pathogens. Fungal Diversity 45: 21-32.https://doi.org/10.1007/s13225-010-0063-z
Aerts, D., Hauer, E.E., Ohm, R.A., Arentshorst, M., Teertstra, W.R., Phippen, C., Ram, A.F., Frisvad, J.C. and Wösten, H.A., 2018. The FlbA-regulated predicted transcription factor Fum21 ofAspergillus niger is involved in fumonisin production. Antonie Van Leeuwenhoek 111: 311-22.https://doi.org/10.1007/s10482-017-0952-1
Alberts, J.F., Gelderblom, W.C., Thiel, P.G., Marasas, W.F., Van Schalkwyk, D.J. and Behrend, Y., 1990. Effects of temperature and incubation period on production of fumonisin B1 byFusarium moniliforme. Applied and Environmental Microbiology 56: 1729-1733.https://doi.org/0099-2240/90/061729-05$02.00/0
Alberts, J.F., Lilly, M., Rheeder, J.P., Burger, H.M., Shephard, G.S. and Gelderblom, W.C., 2017. Technological and community-based methods to reduce mycotoxin exposure. Food Control 73: 101-109.https://doi.org/10.1016/j.foodcont.2016.05.029
Alberts, J., Schatzmayr, G., Mol, W-D., Davids, I., Rheeder, J., Burger, H-M., Shephard, G. and Gelderblom, W., 2019. Detoxification of the fumonisin mycotoxins in maize: An enzymatic approach. Toxins 11: 523.https://doi.org/10.3390/toxins11090523
Alexander, N.J., Proctor, R.H. and McCormick, S.P., 2009. Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins inFusarium. Toxin Reviews 28: 198-215.https://doi.org/10.1080/15569540903092142
Bhattacharya, A., Kourmpetli, S., War, D.A., Thomas, S.G., Gong, F., Powers, S.J., Carrera, E., Taylor, B., Gonzalez, F.N., Tudzynski, B., Phillips, A.L., Davey, M.R. and Hedden, P., 2012. Characterization of the fungal gibberellin desaturase as a 2-oxoglutarate-dependent dioxygenase and its utilization for enhancing plant growth. Plant Physiology 160: 837-884.https://doi.org/10.1104/pp.112.201756
Bluhm, B.H. and Woloshuk, C.P., 2006. Fck1, a C-type cyclin-dependent kinase, interacts with Fcc1 to regulate development and secondary metabolism inFusarium verticillioides. Fungal Genetics and Biology 43: 146-54.https://doi.org/10.1016/j.fgb.2005.09.006
Booth, C., 1971. The genusFusarium. Commonwealth Mycological Institute, Kew, Surrey, England.
'The genusFusarium', ().
Boutigny, A-L., Beukes, I., Small, I., Zühlke, S., Spiteller, M., Van Rensburg, B.J., Flett, B. and Viljoen, A., 2012. Quantitative detection ofFusarium pathogens and their mycotoxins in South African maize. Plant Pathology 61: 522-531.https://doi.org/10.1111/j.1365-3059.2011.02544
Brown, D.W., Cheung, F., Proctor, R.H., Butchko, R.A., Zheng, L., Lee, Y., Utterback, T., Smith, S., Feldblyum, T., Glenn, A.E. and Plattner, R.D., 2005. Comparative analysis of 87,000 expressed sequence tags from the fumonisin-producing fungusFusarium verticillioides. Fungal Genetics and Biololgy 42: 848-861.https://doi.org/10.1016/j.fgb.2005.06.001
Brown, D.W., Butchko, R.A.E., Busman, M. and Proctor, R.H., 2007. TheFusarium verticillioides FUM gene cluster encodes a Zn(II)2Cys6 protein that affectsFUM gene expression and fumonisin production. Eucaryotic Cell 6: 1210-1218.https://doi.org/10.1128/EC.00400-06
Brown, D.W., Villani, A., Susca, A., Moretti, A., Hao, G., Kim, H.S., Proctor, R.H. and McCormick, S.P., 2020. Gain and loss of a transcription factor that regulates late trichothecene biosynthetic pathway genes inFusarium. Fungal Genetics and Biology 136: 103317.https://doi.org/10.1016/j.fgb.2019.103317
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L. and Vandesompele, J., 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611-622.https://doi.org/10.1373/clinchem.2008.112797
Butchko, R.A.E., Plattner, R.D. and Proctor, R.H., 2003a.FUM9 is required for C-5 hydroxylation of fumonisins and complements the meiotically definedFum3 locus inGibberella moniliformis. Applied and Environmental Microbiology 69: 6935-6937.https://doi.org/10.1128/AEM.69.11.6935-6937.2003
Butchko, R.A.E., Plattner, R.D. and Proctor, R.H., 2003b.FUM13 encodes a short chain dehydrogenase/reductase required for C-3 carbonyl reduction during fumonisin biosynthesis inGibberella moniliformis. Journal of Agricultural and Food Chemistry 51: 3000-3006.https://doi.org/10.1021/jf0262007
Butchko, R.A., Plattner, R.D. and Proctor, R.H., 2006. Deletion analysis ofFUM genes involved in tricarballylic ester formation during fumonisin biosynthesis. Journal of Agricultural and Food Chemistry 54: 9398-9404.https://doi.org/10.1021/jf0617869
Chang, P-K. and Ehrlich, K.C., 2013. Genome-wide analysis of the Zn(II)2Cys6 zinc cluster-encoding gene family inAspergillus flavus. Applied Microbiology and Biotechnology 97: 4289-4300.https://doi.org/10.1007/s00253-013-4865-2
Divakara. S.T., Santosh, P., Aiyaz, M., Ramana, M.V., Hariprasad, P., Nayaka, S.C. and Niranjana, S.R., 2014. Molecular identification and characterization ofFusarium spp. associated with sorghum seeds. Journal of the Science of Food and Agriculture 94: 1132-1139.https://doi.org/10.1002/jsfa.6380
Durairaj, P., Hur, J-S. and Yun, H., 2016. Versatile biocatalysis of fungal cytochrome P450 monooxygenases. Microbial Cell Factories 15: 125.https://doi.org/10.1186/s12934-016-0523-6
Fisher, N.L., Burgess, L.W., Toussoun, T.A. and Nelson, P.E., 1982. Carnation leaves as a substrate and for preserving cultures ofFusarium species. Phytopathology 72: 151-153.https://doi.org/10.1094/Phyto-72-151
Flaherty, J.E., Pirttilä, A.M., Bluhm, B.H. and Woloshuk, C.P., 2003.PAC1, a pH-regulatory gene fromFusarium verticillioides. Applied and Environmental Microbiology 69: 5222-5227.https://doi.org/10.1128/AEM.69.9.5222-5227.2003
Frisvad, J.C., Smedsgaard, J., Samson, R.A., Larsen, T.O. and Thrane, U., 2007. Fumonisin B2 production byAspergillus niger. Journal of Agriculture and Food Chemistry 55: 9727-9732.https://doi.org/10.1021/jf0718906
Gelderblom, W.C., Seier, J.V., Snijman, P.W., Van Schalkwyk, D.J., Shephard, G.S. and Marasas, W.F., 2001. Toxicity of culture material ofFusarium verticillioides strain MRC 826 to nonhuman primates. Environmental Health Perspectives 109: 267-276.https://doi.org/10.2307/3435018
He, C., Zhang, Z., Li, B. and Tian, S., 2020. The pattern and function of DNA methylation in fungal plant pathogens. Microorganism 8: 227.https://doi.org/10.3390/microorganisms8020227
Huffman, J., Gerber, R. and Du, L., 2010. Recent advancements in the biosynthetic mechanisms for polyketide-derived mycotoxins. Biopolymers 93: 764-776.https://doi.org/10.1002/bip.21483
International Agency for Research on Cancer (IARC), 2002. Fumonisin B1. In: Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. WHO IARC monographs on the evaluation of carcinogenic risks to humans, Volume 82. IARC, Lyon, France, pp. 301-366.
Jeschke, N., Nelson, P.E. and Marasas, W.F., 1987. Toxicity to ducklings ofFusarium moniliforme isolated from corn intended for use in poultry feed. Poultry Science Journal 66: 1619-1623.https://doi.org/10.3382/ps.0661619
Kimura, M., Tokai, T., Takahashi-Ando, N., Ohsato, S. and Fujimura, M., 2007. Molecular and genetic studies ofFusarium trichothecene biosynthesis: pathways, genes, and evolution. Bioscience, Biotechnology and Biochemistry 71: 2105-2123.https://doi.org/10.1271/bbb.70183
Kohli, G.S., John, U., Van Dolah, F.M. and Murray, S.A., 2016. Evolutionary distinctiveness of fatty acid and polyketide synthesis in eukaryotes. Journal of the International Society for Microbial Ecology 10: 1877.https://doi.org/10.1038/ismej.2015.263
Leslie, J.F. and Summerell, B.A., 2008. TheFusarium laboratory manual. John Wiley & Sons, Hoboken, NJ, USA.
'TheFusarium laboratory manual', ().
Lindo, L., McCormick, S.P., Cardoza, R.E., Kim, H.S., Brown, D.W., Alexander, N.J., Proctor, R.H. and Gutiérrez, S., 2019. Role ofTrichoderma arundinaceum tri10 in regulation of terpene biosynthetic genes and in control of metabolic flux. Fungal Genetics and Biology 122: 31-46.https://doi.org/10.1016/j.fgb.2018.11.001
Livak, K.J. and Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408.https://doi.org/10.1006/meth.2001.1262
Magan, N. and Medina, A., 2016. Integrating gene expression, ecology and mycotoxin production byFusarium andAspergillus species in relation to interacting environmental factors. World Mycotoxin Journal 9: 673-684.https://doi.org/10.3920/WMJ2016.2076.
Marasas, W.F.O., Gelderblom, W.C.A., Shephard, G.S. and Vismer, H.F., 2012. Mycotoxicological research in South Africa 1910-2011. World Mycotoxin Journal 5: 89-102.https://doi.org/10.3920/WMJ2011.1322
Marasas, W.F.O., Nelson Paul, E. and Toussoun, T.A., 1984. ToxigenicFusarium species: identity and mycotoxicology. Pennsylvania State University Press, London, PA, USA.
'ToxigenicFusarium species: identity and mycotoxicology', ().
McCormick, S.P., Alexander, N.J., Proctor, R.H., 2006.Fusarium Tri4 encodes a multifunctional oxygenase R required for trichothecene biosynthesis. Canadian Journal of Microbiology 52: 636-642.https://doi.org/10.1139/w06-011
Nelson, P.E., Dignani, M.C. and Anaissie, E.J., 1994. Taxonomy, biology, and clinical aspects ofFusarium species. Clinical Microbiology Reviews 7: 479-504.https://doi.org/10.1128/cmr.7.4.479
Pfannenstiel, B.T. and Keller, N.P., 2019. On top of biosynthetic gene clusters: How epigenetic machinery influences secondary metabolism in fungi. Biotechnology Advances 37: 107345.https://doi.org/10.1016/j.biotechadv.2019.02.001
Picot, A., Barreau, C., Pinson-Gadais, L., Caron, D., Lannou, C. and Richard-Forget, F., 2010. Factors of theFusarium verticillioides-maize environment modulating fumonisin production. Critical Reviews in Microbiology 36: 221-231.https://doi.org/10.3109/10408411003720209
Proctor, R.H., Desjardins, A.E., Plattner, R.D. and Hohn, T.M., 1999. A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins inGibberella fujikuroi mating population A. Fungal Genetics and Biology 27: 100-112.https://doi.org/10.1006/fgbi.1999.1141
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 inGibberella moniliformis. Fungal Genetics and Biology 38: 237-249.https://doi.org/10.1016/s1087-1845(02)00525-x
Proctor, R.H., Butchko, R.A.E., Plattner, R.D., Brown, D.W. and Desjardins, A.E., 2004. Functional analysis of the fumonisin biosynthetic gene cluster inFusarium verticillioides. Mycopathologia 157: 406.https://doi.org/10.1128/EC.00400-06
Proctor, R.H., Plattner, R.D., Desjardins, A.E., Busman, M. and Butchko, R.A.E., 2006. Fumonisin production in the maize pathogenFusarium Verticillioides: genetic basis of naturally occurring chemical variation. Journal of Agriculture and Food Chemistry 54: 2424-2430.https://doi.org/10.1021/jf0527706
Proctor, R.H., Busman, M., Seo, J-A., Lee, Y.W. and Ronald Plattner, D., 2008. A fumonisin biosynthetic gene cluster inFusarium oxysporum strain O-1890 and the genetic basis for B versus C fumonisin production. Fungal Genetics and Biology 45: 1016-1026.https://doi.org/10.1016/j.fgb.2008.02.004
Rheeder, J.P., Marasas, W.F.O. and Vismer, H.F., 2002. Production of fumonisin analogs byFusarium species. Applied and Environmental Microbiology 68: 2101-2105.https://doi.org/10.1128/AEM.68.5.2101-2105.2002
Sagaram, U.S. and Shim, W.B., 2007.Fusarium verticillioides GBB1, a gene encoding heterotrimeric G protein β subunit, is associated with fumonisin B1 biosynthesis and hyphal development but not with fungal virulence. Molecular Plant Pathology 8: 375-384.https://doi.org/10.1111/j.1364-3703.2007.00398.x
Seo, J.A., Proctor, R.H. and Plattner, R.D., 2001. Characterization of four clustered and coregulated genes associated with fumonisin biosynthesis inFusarium verticillioides. Fungal Genetics and Biology 34: 155-165.https://doi.org/10.1006/fgbi.2001.1299
Shephard, G.S., Kimanya, M.E., Kpodo, K.A., Gnonlonfin, G.J.B. and Gelderblom, W.C.A., 2013. The risk management dilemma for fumonisin mycotoxins. Food Control 34: 596-600.https://doi.org/10.1016/j.foodcont.2013.05.019
Shi, W., Tan, Y., Wang, S., Gardiner, D.M., De Saeger, S., Liao, Y., Wang, C., Fan, Y., Wang, Z. and Wu, A., 2017. Mycotoxigenic potentials ofFusarium species in various culture matrices revealed by mycotoxin profiling. Toxins 9: 6.https://doi.org/10.3390/toxins9010006
Shim, W.B. and Woloshuk, C.P., 2001. Regulation of fumonisin B1 biosynthesis and conidiation inFusarium verticillioides by a cyclin-like (C-type) gene,FCC1. Applied and Environmental Microbiology 67: 1607-1612.https://doi.org/10.1128/AEM.67.4.1607-1612.2001
Shin, J., Kim, J.E., Lee, Y.W. and Son, H., 2018. Fungal cytochrome P450s and the P450 complement (CYPome) ofFusarium graminearum. Toxins 10: 112.https://doi.org/10.3390/toxins10030112
Uhlig, S., Busman, M., Shane, D.S., Ronning, H., Rise, F. and Proctor, R., 2012. Identification of early fumonisin biosynthetic intermediates by inactivation of theFUM6 gene inFusarium verticillioides. Journal of Agriculture and Food Chemistry 60: 10293-10301.https://doi.org/10.1021/jf302967b
Visentin, I., Montis, V., Döll, K., Alabouvette, C., Tamietti, G., Karlovsky, P. and Cardinale, F., 2012. Transcription of genes in the biosynthetic pathway for fumonisin mycotoxins is epigenetically and differentially regulated in the fungal maize pathogenFusarium verticillioides. Eukaryotic Cell 11: 252-259.https://doi.org/10.1128/EC.05159-11
World Health Organization (WHO), 2017. Fumonisins. Evaluation of certain contaminants in food. WHO technical report series 1002, Prepared by the 83rd meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA). WHO, Geneva, Switzerland, pp. 55-73.
Xu, R., Zhen-dong, Z., Hong-jie, L., Can-xing, D. and Xiao-ming, D., 2012. SSR marker development and analysis of genetic diversity ofFusarium verticillioides isolated from maize in China. Scientia Agricultura Sinica 45: 52-66.https://doi.org/10.3864/j.issn.0578-1752.2012.01.007
Zafra, G., Absalón, A.E. and Cortés-Espinosa, D.V., 2015. Morphological changes and growth of filamentous fungi in the presence of high concentrations of PAHs. Brazilian Journal of Microbiology 46: 937-941.https://doi.org/10.1590/S1517-838246320140575
Zhang, C., Huang, H., Deng, W. and Li, T., 2019. Genome-wide analysis of the Zn(II)2Cys6 Zinc cluster-encoding gene family inTolypocladium guangdongense and its light-induced expression. Genes 10: 179.https://doi.org/10.3390/genes10030179
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
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B-series fumonisins (FBs) are a family of carcinogenic mycotoxins that commonly occur in maize. These mycotoxins cause multiple diseases in animals and are epidemiologically associated with several human diseases in populations for which maize is a dietary staple. FBs are produced by multiple genera of the fungiAspergillus,Fusarium andTolypocladium, but the plant pathogenFusarium verticillioides is considered the primary cause of FB contamination in maize. OneF. verticillioides strain, MRC 826, is reported to produce high levels of FBs. However, in the current study, 18 isolates derived from strain MRC 826 exhibited highly variable levels of FB, which negatively correlated (r=-0.333;P<0.008) with fungal growth. Microsatellite analysis confirmed that all MRC 826 derived isolates examined were clonal, and 100% DNA sequence identity was observed across theFUM gene clusters of two high FB producing and two low FB producing isolates. At the gene expression level, qRT-PCR at each time point (7, 14, 21 and 28 days of incubation) showed differential upregulation of selectedFUM genes in the high compared to the low FB isolates. Variation in FB production appears due to differences inFUM gene expression, most likely caused by sequence differences at unexamined loci not part of theFUM cluster or from epigenetic influences. Clarification of the genetic/epigenetic basis for quantitative differences in fumonisin production among strains and isolates ofF. verticillioides has potential to reveal targets for reducing FB contamination in maize.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 408 | 149 | 13 |
| Full Text Views | 24 | 2 | 0 |
| PDF Views & Downloads | 16 | 2 | 0 |