In Vitro Production of Fumonisins by Fusarium verticillioides under Oxidative Stress Induced by H2O2

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 19, 2015, Pages 4879-4885

  Ferrigo, Davide ^a   Raiola, Alessandro ^a   Bogialli, Sara ^a   Bortolini, Claudio ^a   Tapparo, Andrea ^a   Causin, Roberto ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

fum genes; fumonisins; Fusarium verticillioides; H2O2; LC high resolution MS analysis; oxidative stress

Indexed keywords

BIOSYNTHESIS; FUNGI; GENES; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; OXIDATIVE STRESS; POPULATION STATISTICS; STRAIN;

DIVERGENT BEHAVIORS; F. VERTICILLIOIDES; FUMONISINS; FUSARIUM VERTICILLIOIDES; H2O2; HIGH RESOLUTION; HIGH RESOLUTION MASS SPECTROMETRY; NATURAL CONDITIONS;

TOXIC MATERIALS;

FUNGI; GIBBERELLA MONILIFORMIS;

FUMONISIN; FUNGAL PROTEIN; HYDROGEN PEROXIDE;

DRUG EFFECTS; FUSARIUM; GENETICS; METABOLISM; OXIDATIVE STRESS;

FUMONISINS; FUNGAL PROTEINS; FUSARIUM; HYDROGEN PEROXIDE; OXIDATIVE STRESS;

EID: 84930225548     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b00113     Document Type: Article

References (48)

1. Leslie, J. F. Mating population in Gibberella fujikuroi (Fusarium section Liseola) Phytopathology. 1991, 81, 1058 - 1060
2. Bacon, C. W.; Hinton, D. M. Symptomless endophytic colonization of maize by Fusarium moniliforme Can. J. Bot. 1996, 74, 1195 - 1202 10.1139/b96-144
3. White, D. G. Compendium of Corn Diseases, 3rd ed.; American Phytopathological Society Press: Saint Paul, MN, 1999; p 128.
4. Placinta, C.; D'Mello, J. P.; Macdonald, A. M. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins Anim. Feed Sci. Technol. 1999, 78, 21 - 37 10.1016/S0377-8401(98)00278-8
5. Marasas, W. F. O. Fumonisins: Their implications for human and animal health Nat. Toxins 1995, 3, 193 - 198 10.1002/nt.2620030405
6. Logrieco, A.; Mulè, G.; Moretti, A.; Bottalico, A. Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe Eur. J. Plant Pathol. 2002, 108, 597 - 609 10.1023/A:1020679029993
7. Schmidt-Heydt, M.; Magan, N.; Geisen, R. Stress induction of mycotoxin biosynthesis genes by abiotic factors FEMS Microbiol. Lett. 2008, 284, 142 - 149 10.1111/j.1574-6968.2008.01182.x
8. Jayashree, T.; Subramanyam, C. Oxidative stress as a prerequisite for aflatoxin production by Aspergillus parasiticus Free Radical Biol. Med. 2000, 29, 981 - 985 10.1016/S0891-5849(00)00398-1
9. Boutigny, A. L.; Richard-Forget, F.; Barreau, C. Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes Eur. J. Plant Pathol. 2008, 121, 411 - 423 10.1007/s10658-007-9266-x
10. Ponts, N.; Pinson-Gadais, L.; Verdal-Bonnin, M. N.; Barreau, C.; Richard-Forget, F. Accumulation of deoxynivalenol and its 15-acetylated form is significantly modulated by oxidative stress in liquid cultures of Fusarium graminearum FEMS Microbiol. Lett. 2006, 258, 102 - 107 10.1111/j.1574-6968.2006.00200.x
11. Reverberi, M.; Punelli, M.; Smith, C. A.; Zjalic, S.; Scarpari, M.; Scala, V.; Cardinali, G.; Aspite, N.; Pinzari, F.; Payne, G. A.; Fabbri, A. A.; Fanelli, A. How peroxisomes affect aflatoxin biosynthesis in Aspergillus flavus PLoS One 2012, 7, e48097 10.1371/journal.pone.0048097
12. 2 and catalase treatments interfere with Tri genes expression in liquid cultures of Fusarium graminearum FEBS Lett. 2007, 581, 443 - 447 10.1016/j.febslet.2007.01.003
13. Apel, K.; Hirt, H. Reactive oxygen species, metabolism, oxidative stress, and signal transduction Annu. Rev. Plant Biol. 2004, 55, 373 - 399 10.1146/annurev.arplant.55.031903.141701
14. Zhao, Z.; Chen, G.; Zhang, C. Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings Funct. Plant Biol. 2001, 28, 1055 - 1061 10.1071/PP00143
15. Torres, M. A.; Jones, J. D. G.; Dangl, J. L. Reactive oxygen species signaling in response to pathogens Plant Physiol. 2006, 141, 373 - 378 10.1104/pp.106.079467
16. Dat, J.; Vandenabeele, S.; Vranová, E.; Montagu, M. V.; Inzé, D.; Breusegem, F. V. Dual action of the active oxygen species during plant stress responses Cell. Mol. Life Sci. 2000, 57, 779 - 795 10.1007/s000180050041
17. 2 production by a strain of Fusarium verticillioides under different environmental factors J. R. Soc., Interface 2013, 10, 20130320 10.1098/rsif.2013.0320
18. 1 biosynthesis Food Addit. Contam., Part A 2011, 28, 218 - 225 10.1080/19440049.2010.540721
19. Pani, G.; Scherm, B.; Azara, E.; Balmas, V.; Jahanshiri, Z.; Carta, P.; Fabbri, D.; Dettori, M. A.; Fadda, A.; Dessì, A.; Dallocchio, R.; Migheli, Q.; Delogu, G. Natural and natural-like phenolic inhibitors of type B trichothecene in vitro production by the wheat (Triticum sp.) pathogen Fusarium culmorum J. Agric. Food Chem. 2014, 62, 4969 - 4978 10.1021/jf500647h
20. Tuite, J. In Plant Pathological Methods: Fungi and Bacteria; Tuite, J., Ed., Burgess: Minneapolis, MN, 1969; p 239.
21. Mulè, G.; Susca, A.; Stea, G.; Moretti, A. A species-specific PCR assay based on the calmodulin partial gene for identification of Fusarium verticillioides, F. proliferatum and F. subglutinans. In Molecular Diversity and PCR-detection of Toxigenic Fusarium Species and Ochratoxigenic Fungi; Mulè, G.; Bailey, J. A.; Cooke, B. M.; Logrieco, A., Eds.; Springer: Dordrecht, The Netherlands, 2004; pp 495 - 502.
22. Brown, D. W.; Butchko, R. A. E.; Busman, M.; Proctor, R. H. The Fusarium verticillioides FUM gene cluster encodes a Zn(II)2Cys6 protein that affects FUM gene expression and fumonisin production Eukaryotic Cell 2007, 6, 1210 - 1218 10.1128/EC.00400-06
23. Rozen, S.; Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols; Misener, S.; Krawetz, S. A., Eds.; Humana Press: New York, 1999; Vol. 132, pp 365 - 386.
24. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 2001, 29, e45 10.1093/nar/29.9.e45
25. Muller, P. Y.; Janovjak, H.; Miserez, A.; Dobbie, Z. Processing of gene expression data generated by quantitative real-time RT-PCR BioTechniques. 2002, 32, 1372 - 1379
26. Jurado, M.; Marín, P.; Magan, N.; González-Jaén, M. T. Relationship between solute and matric potential stress, temperature, growth, and FUM1 gene expression in two Fusarium verticillioides strains from Spain Appl. Environ. Microbiol. 2008, 74, 2032 - 2036 10.1128/AEM.02337-07
27. 1-4-producing capacity of Hungarian Fusarium verticillioides isolates World Mycotoxin J. 2010, 3, 67 - 76 10.3920/WMJ2009.1152
28. Etcheverry, M.; Torres, A.; Ramirez, M. L.; Chulze, S.; Magan, N. In vitro control of growth and fumonisin production by Fusarium verticillioides and F. proliferatum using antioxidants under different water availability and temperature regimes J. Appl. Microbiol. 2002, 92, 624 - 632 10.1046/j.1365-2672.2002.01566.x
29. Picot, A.; Barreau, C.; Pinson-Gadais, L.; Caron, D.; Lannou, C.; Richard-Forget, F. Factors of the Fusarium verticillioides-maize environment modulating fumonisin production Crit. Rev. Microbiol. 2010, 36, 221 - 231 10.3109/10408411003720209
30. 2 is trichothecene chemotype-dependent FEMS Microbiol. Lett. 2009, 293, 255 - 262 10.1111/j.1574-6968.2009.01521.x
31. Carter, J. P.; Rezanoor, H. N.; Holden, D.; Desjardins, A. E.; Plattner, R. D.; Nicholson, P. Variation in pathogenicity associated with the genetic diversity of Fusarium graminearum Eur. J. Plant Pathol. 2002, 108, 573 - 583 10.1023/A:1019921203161
32. Glenn, A. E.; Zitomer, N. C.; Zimeri, A. M.; Williams, L. D.; Riley, R. T.; Proctor, R. H. Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings Mol. Plant-Microbe Interact. 2007, 21, 87 - 97 10.1094/MPMI-21-1-0087
33. Overmyer, K.; Brosché, M.; Kangasjärvi, J. Reactive oxygen species and hormonal control of cell death Trends Plant Sci. 2003, 8, 335 - 342 10.1016/S1360-1385(03)00135-3
34. Eaton, C. J.; Cox, M. P.; Scott, B. What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci. 2011, 180, 190 - 195 10.1016/j.plantsci.2010.10.002
35. Visentin, I.; Montis, V.; Döll, K.; Alabouvette, C.; Tamietti, G.; Karlovsky, P.; Cardinale, F. Transcription of genes in the biosynthetic pathway for fumonisin mycotoxins is epigenetically and differentially regulated in the fungal maize pathogen Fusarium verticillioides Eukaryotic Cell 2012, 11, 252 - 259 10.1128/EC.05159-11
36. Montis, V.; Pasquali, M.; Visentin, I.; Karlovsky, P.; Cardinale, F. Identification of a cis-acting factor modulating the transcription of FUM1, a key fumonisin-biosynthetic gene in the fungal maize pathogen Fusarium verticillioides Fungal Genet. Biol. 2013, 51, 42 - 49 10.1016/j.fgb.2012.11.009
37. Marín, P.; de Ory, A.; Cruz, A.; Magan, N.; González-Jaén, M. T. Potential effects of environmental conditions on the efficiency of the antifungal tebuconazole controlling Fusarium verticillioides and Fusarium proliferatum growth rate and fumonisin biosynthesis Int. J. Food Microbiol. 2013, 165, 251 - 258 10.1016/j.ijfoodmicro.2013.05.022
38. Ochiai, N.; Tokai, T.; Nishiuchi, T.; Takahashi-Ando, N.; Fujimura, M.; Kimura, M. Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum Biochem. Biophys. Res. Commun. 2007, 363, 639 - 644 10.1016/j.bbrc.2007.09.027
39. 1 biosynthesis and conidiation in Fusarium verticillioides by a cyclin-like (C-Type) gene, FCC1 Appl. Environ. Microbiol. 2001, 67, 1607 - 1612 10.1128/AEM.67.4.1607-1612.2001
40. Bluhm, B. H.; Woloshuk, C. P. Fck1, a C-type cyclin-dependent kinase, interacts with Fcc1 to regulate development and secondary metabolism in Fusarium verticillioides Fungal Genet. Biol. 2006, 43, 146 - 154 10.1016/j.fgb.2005.09.006
41. Kohut, G.; Ádám, A. L.; Fazekas, B.; Hornok, L. N-starvation stress induced FUM gene expression and fumonisin production is mediated via the HOG-type MAPK pathway in Fusarium proliferatum Int. J. Food Microbiol. 2009, 130, 65 - 69 10.1016/j.ijfoodmicro.2009.01.002
42. Langfelder, K.; Jahn, B.; Gehringer, H.; Schmidt, A.; Wanner, G.; Brakhage, A. A. Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence Med. Microbiol. Immunol. 1998, 187, 79 - 89 10.1007/s004300050077
43. Brakhage, A. A.; Liebmann, B. Aspergillus fumigatus conidial pigment and cAMP signal transduction, significance for virulence Med. Mycol. 2005, 43, 75 - 82 10.1080/13693780400028967
44. López-Errasquín, E.; Vázquez, C.; Jiménez, M.; González-Jaén, M. T. Real-Time RT-PCR assay to quantify the expression of fum1 and fum19 genes from the fumonisin-producing Fusarium verticillioides J. Microbiol. Methods 2007, 68, 312 - 317 10.1016/j.mimet.2006.09.007
45. Cruz, A.; Marín, P.; Magan, N.; González-Jaén, M. T. Combined effects of benomyl and environmental factors on growth and expression of the fumonisin biosynthetic genes FUM1 and FUM19 by Fusarium verticillioides Int. J. Food Microbiol. 2014, 191, 17 - 23 10.1016/j.ijfoodmicro.2014.08.026
46. Zaleta-Rivera, K.; Xu, C.; Yu, F.; Butchko, R. A. E.; Proctor, R. H.; Hidalgo-Lara, M. E.; Raza, A.; Dussault, P. H.; Du, L. A bidomain nonribosomal peptide synthetase encoded by FUM14 catalyzes the formation of tricarballylic esters in the biosynthesis of fumonisins Biochemistry 2006, 45, 2561 - 2569 10.1021/bi052085s
47. Seo, J. A.; Proctor, R. H.; Plattner, R. D. Characterization of four clustered and coregulated genes associated with fumonisin biosynthesis in Fusarium verticillioides Fungal Genet. Biol. 2001, 34, 155 - 165 10.1006/fgbi.2001.1299
48. Butchko, R. A. E.; Plattner, R. D.; Proctor, R. H. Deletion analysis of FUM genes involved in tricarballylic ester formation during fumonisin biosynthesis J. Agric. Food Chem. 2006, 54, 9398 - 9404 10.1021/jf0617869