Factors of the Fusarium verticillioides-maize environment modulating fumonisin production

Critical Reviews in Microbiology

Volumn 36, Issue 3, 2010, Pages 221-231

  Picot, Adeline ^a,b,c   Barreau, Christian ^b   Pinson Gadais, Laëtitia ^b   Caron, Daniel ^a   Lannou, Christian ^c   Richard Forget, Florence ^b  

^a ARVALIS   (France)

^b CEMAGREF   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Ecophysiological factors; Maize pathogen interaction; Nutrient sources; pH; Toxin regulation

Indexed keywords

AFLATOXIN; ANTIFUNGAL AGENT; CAFFEIC ACID; CHLOROPHORIN; FERULIC ACID; FUMONISIN; IROKO; LIMONENE; MAAKIANIN; PHENOL DERIVATIVE; THYMOL; TRICHOTHECENE; TRICHOTHECENE B; UNCLASSIFIED DRUG; VANILLIC ACID; MYCOTOXIN;

ANTIOXIDANT ACTIVITY; BIOSYNTHESIS; CONTAMINATION; DRUG ACTIVATION; ENVIRONMENTAL STRESS; ENVIRONMENTAL TEMPERATURE; FUNGAL COLONIZATION; FUSARIUM; FUSARIUM PROLIFERATUM; FUSARIUM VERTICILLIOIDES; GENE CLUSTER; GENETIC ASSOCIATION; HUMAN; MAIZE; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PH; PLANT DEFENSE; PRIORITY JOURNAL; REVIEW; WATER AVAILABILITY; ECOSYSTEM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY;

ANIMALIA; FUSARIUM; FUSARIUM PROLIFERATUM; GIBBERELLA MONILIFORMIS; ZEA MAYS;

ECOSYSTEM; FUMONISINS; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; MYCOTOXINS; SOIL MICROBIOLOGY; ZEA MAYS;

EID: 77954734909     PISSN: 1040841X     EISSN: 15497828     Source Type: Journal    
DOI: 10.3109/10408411003720209     Document Type: Review

References (80)

1. Bartók T, Szecsi A, Szekeres A, Mesteráhzy A, Bartók M. (2006). Detection of new fumonisin mycotoxins and fumonisin-like compounds by reversed-phase high-performance liquid chro-matography/electrospray ionization ion trap mass spectrometry. Rapid Commun Mass Spectrom, 20, 2447-62.
2. Beekrum S, Govinden R, Padayachee T, Odhav B. (2003). Naturally occurring phenols: a detoxifcation strategy for fumonisin B1. Food Addit Contam, 20, 490-3.
3. Bell AA. (1981). Biochemical mechanisms of disease resistance. Ann Rev Plant Physio, 32, 21-81.
4. Bezuidenhout SC, Gelderblom WC, Gorst-Allman CP, Horak RM, Marasas W F, Spiteller G, Vleggaar R. (1988). Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme. J Chem Soc Chem Commun, 743-45.
5. Blandino M, Reyneri A. (2007). Comparison between normal and waxy maize hybrids for Fusarium-toxin contamination in NW Italy. Maydica, 52, 127-34.
6. Bluhm BH, Woloshuk CP. (2005). Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels. Mol Plant Microbe Interact, 18, 1333-39.
7. Bluhm BH, Woloshuk CP. (2006). Fck1, a C-type cyclin-dependent kinase, interacts with Fcc1 to regulate development and secondary metabolism in Fusarium verticillioides. Fungal Genet Biol, 43, 146-54.
8. Bluhm BH, Kim H, Butchko RA, Woloshuk CP. (2008). Involvement of ZFR1 of Fusarium verticillioides in kernel colonization and the regulation of FST1, a putative sugar transporter gene required for fumonisin biosynthesis on maize kernels. Mol Plant Pathol, 9, 203-11.
9. Boutigny AL, Richard-Forget F, Barreau C. (2008). Natural mechanisms for cereal resistance to the accumulation of Fusarium tri-chothecenes. Eur J Plant Pathol, 121, 411-23.
10. Brodhagen M, Keller NP. (2006). Signalling pathways connecting myco-toxin production and sporulation. Mol Plant Pathol, 7, 285-301.
11. Brodhagen M, Tsitsigiannis DI, Hornung E, Göebel C, Feussner I, Keller NP. (2008). Reciprocal oxylipin-mediated cross-talk in the Aspergillus-seed pathosystem. Mol Microbiol, 67, 378-91.
12. Brown DW, Butchko RAE, Busman M, Proctor RH. (2007). Te Fusarium verticillioides FUM gene cluster encodes a Zn(II)2Cys6 protein that afects FUM gene expression and fumonisin production. Eukaryot Cell, 6, 1210-18.
13. Bush BJ, Carson ML, Cubeta MA, Hagler WM, Payne GA. (2004). Infection and fumonisin production by Fusarium verticillioides in developing maize kernels. Phytopathology, 94, 88-93.
14. Choi YE, Shim WB. (2008). Functional characterization of Fusarium verticillioides CPP1, a gene encoding a putative protein phos-phatase 2A catalytic subunit. Microbiology, 154, 326-36.
15. Desjardins A, Plattner RD. (1998). Distribution of fumonisins in maize ears infected with strains of Fusarium moniliforme that difer in fumonisin production. Plant Dis, 82, 953-58.
16. Desjardins AE, Munkvold GP, Plattner RD, Proctor RH. (2002). FUM1-a gene required for fumonisin biosynthesis but not for maize ear rot and ear infection by Gibberella moniliformis in feld tests. Mol Plant Microbe Interact, 15, 1157-64.
17. Desjardins AE, Proctor RH. (2007). Molecular biology of Fusarium mycotoxins. Int J Food Microbiol, 119, 47-50.
18. Duvick J. (2001). Prospects for reducing fumonisin contamination of maize through genetic modifcation. Environ Health Perspect, 109 Suppl 2, 337-42.
19. Flaherty JE, Pirttilä AM, Bluhm BH, Woloshuk CP. (2003). PAC1, a pH-regulatory gene from Fusarium verticillioides. Appl Environ Microbiol, 69, 5222-27.
20. Flaherty JE, Woloshuk CP. (2004). Regulation of fumonisin biosynthesis in Fusarium verticillioides by a zinc binuclear cluster-type gene, ZFR1. Appl Environ Microbiol, 70, 2653-59.
21. Gao X, Shim WB, Göbel C, Kunze S, Feussner I, Meeley R, Balint-Kurti P, Kolomiets M. (2007). Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin. Mol Plant Microbe Interact, 20, 922-33.
22. Gao X, Brodhagen M, Isakeit T, Horowitz Brown S, Göbel C, Betran J, Feussner I, Keller N, Kolomiets MV. (2009). Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Mol Plant Microbe Interact, 22, 222-31.
23. Glenn AE, Zitomer NC, Zimeri AM, Williams LD, Riley RT, Proctor RH. (2008). Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonsin production and pathogenicity on maize seedlings. Mol Plant Microbe Interact, 21, 87-97.
24. Harris LJ, Desjardins AE, Plattner RD, Nicholson P, Butler G, Young JC, Weston G, Proctor RH, Hohn TM. (1999). Possible role of tri-chothecene mycotoxins in virulence of Fusarium graminearum on maize. Plant Dis, 83, 954-60.
25. Harrison LR, Colvin BM, Green JT, Newman LE, Cole JR. (1990). Pulmonary edema and hydrothorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. J Vet Diagn Invest, 2, 217-21.
26. Holmes RA, Boston RS, Payne GA. (2008). Diverse inhibitors of afa-toxin biosynthesis. Appl Microbiol Biotechnol, 78, 559-72.
27. Howe GA, Schilmiller AL. (2002). Oxylipin metabolism in response to stress. Curr Opin Plant Biol, 5, 230-36.
28. Jaskiewicz K, Marasas WFO, Van Der Walt FE. (1987). Oesophageal and other main cancer patterns in four districts of Transkei, 1981-1984. S Afr Med J, 72, 27-30.
29. Jayashree T, Subramanyam C. (2000). Oxidative stress as a prerequisite for afatoxin production by Aspergillus parasiticus. Free Radic Biol Med, 29, 981-85.
30. Jiménez M, Mateo JJ, Hinojo MJ, Mateo R. (2003). Sugars and amino acids as factors afecting the synthesis of fumonisins in liquid cultures by isolates of the Gibberella fujikuroi complex. Int J Food Microbiol, 89, 185-93.
31. Jurado M, Marín P, Magan N, González-Jaén MT. (2008). Relationship between solute, matric potential stress, temperature, growth, and FUM1 gene expression in two Fusarium verticillioides strains from Spain. Appl Environ Microbiol, 74, 2032-36.
32. Keller SE, Sullivan TM, Chirtel S. (1997). Factors afecting the growth of Fusarium proliferatum and the production of fumonisin B1: oxygen and pH. J Ind Microbiol Biotechnol, 19, 305-09.
33. Kellerman TS, Marasas WFO, Tiel PG, Gelderblom WCA, Cawood M, Coetzer JAW. (1990). Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1. Onderstepoort J Vet Res, 57, 269-75.
34. Kim H, Woloshuk CP. (2008). Role of AREA, a regulator of nitrogen metabolism, during colonization of maize kernels and fumoni-sin biosynthesis in Fusarium verticillioides. Fungal Genet Biol, 45, 947-53.
35. Kim JH, Campbell BC, Mahoney NE, Chan KL, Molyneux RJ. (2004). Identifcation of phenolics for control of Aspergillus favus using Saccharomyces cerevisiae in a model target-gene bioassay. J Agric Food Chem, 52, 7814-21.
36. Kim JH, Mahoney N, Chan KL, Molyneux RJ, Campbell BC. (2006). Controlling food-contaminating fungi by targeting their antioxi-dative stress-response system with natural phenolic compounds. Appl Microbiol Biotechnol, 70, 735-39.
37. Kim JH, Yu J, Mahoney N, Chan KL, Molyneux RJ, Varga J, Bhatnagar D, Cleveland TE, Nierman WC, Campbell BC. (2007). Elucidation of the functional genomics of antioxidant-based inhibition of afa-toxin biosynthesis. Int J Food Microbiol, 122, 49-60.
38. Kohut G, Ádám AL, Fazekas B, Hornok L. (2009). N-starvation stress induced FUM gene expression and fumonisin production is mediated via the HOG-type MAPK pathway in Fusarium proli-feratum. Int J Food Microbiol, 130, 65-69.
39. Li M, Lu S, Ji C, Wang Y, Wang M, Cheng S, Tian G. (1980). Experimental studies on the carcinogenicity of fungus-contaminated food from Linxian county. Tokyo, Japan: Japan Science Society Press.
40. Magbanua Z V, De Moraes CM, Brooks TD, Paul Williams W, Luthe DS. (2007). Is catalase activity one of the factors associated with maize resistance to Aspergillus favus. Mol Plant Microbe Interact, 20, 697-706.
41. Makaula NA, Marasas WFO, Venter FS, Badenhorst CJ, Bradshaw D, Swanevelder S. (1996). Oesophageal and other cancer patterns in four selected districts of Transkei, southern Africa: 1985-1990. Afr J Health Sci, 3, 11-15.
42. Marasas WF, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WC, Allegood J, Martinez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman AV, Voss KA, Wang E, Merrill AH, Jr. (2004). Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr, 134, 711-16.
43. Marín S, Sanchis V, Ramos A. (1998a). Environmental factors, in vitro interactions, and niche overlap between Fusarium moniliforme, F. proliferatum, and F. graminearum, Aspergillus and Penicillium species from maize. Mycol Res, 102, 831-37.
44. Marín S, Sanchis V, Ramos AJ, Magan N. (1998b). Efect of water activity on hydrolytic enzyme production by Fusarium moniliforme and Fusarium proliferatum during colonisation of maize. Int J Food Microbiol, 42, 185-94.
45. Marín S, Homedesa V, Sanchis AJ, Ramosa N, Magan N. (1999a). Impact of Fusarium moniliforme and F. proliferatum colonisation of maize on calorifc losses and fumonisin production under diferent environmental conditions. J Stored Prod Res, 35, 15-26.
46. Marín S, Magan N, Bellí N, Ramos AJ, Canela R, Sanchis V. (1999b). Two-dimensional profles of fumonisin B1 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, 159-67.
47. Merrill AH, Sullards MC, Wang E, Voss KA, Riley RT. (2001). Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ Health Perspect, 109, 283-89.
48. Miller JD, Savard ME, Schaafsma AW, Seifert KA, Reid LM. (1995). Mycotoxin production by Fusarium moniliforme and Fusarium proliferatum from Ontario and occurrence of fumonisin in the 1993 corn crop. Can J Plant Pathol, 17, 233-39.
49. Munkvold GP, Desjardins AE. (1997). Fumonisin: can we reduce their occurrence? Plant Dis, 81, 556-65.
50. Myung K, Li S, Butchko RAE, Busman M, Proctor RH, Abbas HK, Calvo AM. (2009). FvVE1 regulates biosynthesis of the mycoto-xins fumonisins and fusarins in Fusarium verticillioides. J Agric Food Chem, 57, 5087-94.
51. Narasaiah KV, Sashidhar RB, Subramanyam C. (2006). Biochemical analysis of oxidative stress in the production of afatoxin and its precursor intermediates. Mycopathologia, 162, 179-89.
52. Nesci A, Gsponer N, Etcheverry M. (2007). Natural maize phenolic acids for control of afatoxigenic fungi on maize. J Food Sci, 72, 180-85.
53. Nicholson RL, Hammerschidt R. (1992). Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol, 30, 369-89.
54. Pascale M, Visconti A, Chelkowski J. (2002). Ear rot susceptibility and mycotoxin contamination of maize hybrids inoculated with Fusarium species under feld conditions. Eur J Plant Pathol, 108, 645-51.
55. Ponts N, Pinson-Gadais L, Verdal-Bonnin MN, Barreau C, Richard-Forget F. (2006). Accumulation of deoxynivalenol and its 15-acetylated form is signifcantly modulated by oxidative stress in liquid cultures of Fusarium graminearum. FEMS Microbiol Lett, 258, 102-07.
56. Ponts N, Pinson-Gadais L, Barreau C, Richard-Forget F, Ouellet T. (2007). Exogenous H2O2, catalase treatments interfere with Tri genes expression in liquid cultures of Fusarium graminearum. FEBS Lett, 581, 443-47.
57. Proctor RH, Desjardins AE, Plattner RD, Hohn TM. (1999). A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet Biol, 27, 100-12.
58. Proctor RH, Brown DW, Plattner RD, Desjardins AE. (2003). Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet Biol, 38, 237-49.
59. Reid LM, Nicol RW, Ouellet T, Savard M, Miller JD, Young JC, Stewart DW, Schaafsma AW. (1999). Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology, 89, 1028-37.
60. Reverberi M, Zjalic S, Ricelli A, Punelli F, Camera E, Fabbri C, Picardo M, Fanelli C, Fabbri AA. (2008). Modulation of anti-oxidant defense in Aspergillus parasiticus is involved in afa-toxin biosynthesis: a role for the ApyapA gene. Eukaryot Cell, 7, 988-1000.
61. Reynoso MM, Torres AM, Ramirez ML. (2002). Efcacy of antioxi-dant mixtures on growth, fumonisin production and hydrolytic enzyme production by Fusarium verticillioides and F. proliferatum in vitro on maize-based media. Mycol Res, 106, 1093-99.
62. Riley RT, Hinton DM, Chamberlain WJ, Bacon CW, Wang EM, Merrill AHJ, Voss KA. (1994). Dietary fumonisin B1 induces disruption of sphingolipid metabolism in Sprague-Dawley rats: a new mechanism of nephrotoxicity. J Nutr, 124, 594-603.
63. Sagaram US, Butchko RAE, Shim WB. (2006a). Te putative mono-meric G-protein GBP1 is negatively associated with fumonisin B1 production in Fusarium verticillioides. Mol Plant Pathol, 7, 381-89.
64. Sagaram US, Kolomiets M, Shim WB. (2006b). Regulation of Fumonisin Biosynthesis in Fusarium verticillioides-Maize System. Plant Pathol J, 22, 203-10.
65. 1 biosynthesis and hyphal development but not with fungal virulence. Mol Plant Pathol, 8, 375-84.
66. Samapundo S, Devliehgere F, De Meulenaer B, Debevere J. (2005). Efect 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, 1054-9.
67. Sanchis V, Marín S, Magan N, Ramos AJ. (2006). Ecophysiology of fumonisin producers in Fusarium Section Liseola. Adv Exp Med Biol, 571, 115-22.
68. Schmidt-Heydt M, Magan N, Geisen R. (2008). Stress induction of mycotoxin biosynthesis genes by abiotic factors. FEMS Microbiol Lett, 284, 142-49.
69. Shelby R, White DG, Burke EM. (1994). Diferential fumonisin production in maize hybrids. Plant Dis, 78, 582-84.
70. Shim WB, Woloshuk CP. (1999). Nitrogen repression of fumonisin B1 biosynthesis in Gibberella fujikuroi. FEMS Microbiol Lett, 177, 109-16.
71. Shim WB, Woloshuk CP. (2001). Regulation of fumonisin B1 biosynthesis and conidiation in Fusarium verticillioides by a cyclin-like (C-type) gene, FCC1. Appl Environ Microbiol, 67, 1607-12.
72. Tilburn J, Sarkar S, Widdick DA, Espeso EA, Orejas M, Mungroo J, Peñalva MA, Arst HN, Jr. (1995). Te Aspergillus PacC zinc fn-ger transcription factor mediates regulation of both acidic-and alkaline-expressed genes by ambient pH. Eur Mol Biol Organ, 14, 779-90.
73. Turner JG, Ellis C, Devoto A. (2002). Te jasmonate signal pathway. Plant Cell, 14, 153-54.
74. Wallace G, Fry SC. (1994). Phenolic components of the plant cell wall. Int Rev Cytol, 151, 229-67.
75. Wang E, Norred WP, Bacon CW, Riley RT, Merrill AH. (1991). Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. J Biol Chem, 266, 14486-90.
76. Wicklow DT, Horn BW, Shotwell OL, Hesseltine CW, Caldwell RW. (1988). Fungal interference with Aspergillus favus infection and afatoxin contamination of maize grown in a controlled environment. Phytopathology, 78, 68-74.
77. Yang CS. (1980). Research on esophageal cancer in China: a review. Cancer Res, 40, 2633-44.
78. Yu JH, Keller N. (2005). Regulation of secondary metabolism in fla-mentous fungi. Annu Rev Phytopathol, 43, 437-58.
79. Zhang JJ, Hu YF, Huang YB. (2008). Relationship between activities of key enzymes involved in starch synthesis and accumulation in maize inbred lines during grain flling. Russ J Plant Physiol, 55, 249-55.
80. Zorzete P, Castro RS, Pozzi CR, Israel ALM, Fonseca H, Yanaguibashi G, Corrêa B. (2008). Relative populations and toxin production by Aspergillus favus and Fusarium verticillioides in artifcially inoculated corn at various stages of development under feld conditions. J Sci Food Agric, 88, 48-55.