2014, Number 1
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TIP Rev Esp Cienc Quim Biol 2014; 17 (1)
Fumonisinas –síntesis y Función en la interacción Fusarium verticillioides-maíz
de la Torre-Hernández ME, Sánchez-Rangel D, Galeana-Sánchez E, Plasencia-de la Parra J
Language: Spanish
References: 105
Page: 77-91
PDF size: 420.73 Kb.
ABSTRACT
Fusarium verticillioides is the main fungal pathogen that affects the productivity of maize worldwide. The
fungus penetrates the plant by different routes and infects roots, stem and cob. The pathogen produces
several toxins in tissue and corn kernels, which affect their quality. Fumonisins are the major toxins produced
by this fungus. The ability to produce them depends on the presence of several genes encoding the
enzymes responsible for biosynthesis. The regulation of the synthesis is very complex and depends on
environmental and nutritional factors, as well as multiple signaling pathways. This is reflected by the high
variability in fumonisin production among
F. verticillioides strains. Fumonisins are virulence factors because
their production is associated with a greater capacity to infect maize seedlings. However, this role is not
clear for ear infection and rotting. In maize, fumonisins have three molecular targets: sphinganine
N-acyltransferase,
plasma membrane proton ATPase and the basic β-1,3-glucanases. These three enzymes
have important physiological functions and also participate in the plant defense response against fungal
pathogens.
REFERENCES
Deacon, J.W. Modern Mycology (Blackwell, Boston, 1997).
Leslie, J.F & Summerell, B.A. The Fusarium Laboratory Manual (Blackwell Publishing, Ames, 2006). 1st Edition.
Wollenweber, H. & Reinking, O.A. Die Fusarien, ihre Beschreibung, Schadwirkung und Bekampfung (Paul Parey, Berlin, 1935).
Nelson, P.E., Toussoun, T.A. & Marasas, W.F.O. Fusarium species: An illustrated manual for identification (The Pennsylvania State University Press, Pennsylvania, 1983).
Kedera, C.J., Leslie, J.F. & Claflin, L.E. Genetic diversity of Fusarium Section Liseola (Gibberella fujikuroi) in individual maize stalks. Phytophatology 84, 603-607 (1994).
Desjardins, A.E., Plattner, R.D., Nelson, T.C. & Leslie, J.F. Genetic analysis of fumonisin production and virulence of Gibberella fujikuroi mating population A (Fusarium moniliforme) on maize (Zea mays) seedlings. Appl. Environ. Microbiol. 61, 79-86 (1995).
Duncan, K.E. & Howard, R.J. Biology of maize kernel infection by Fusarium verticillioides. Mol. Plant-Microbe Interact. 23, 6-16 (2010).
Bacon, C.W., Yates, I.E., Hinton, D.M. & Meredith, F. Biological control of Fusarium moniliforme in maize. Environ. Health Persp. 109, 325-332 (2001).
Torres, M.R., Ramos, A.J., Soler, J., Sanchis, V. & Marín, S. SEM study of water activity and temperature effects on the initial growth of Aspergillus ochraceus, Alternaria alternata and Fusarium verticillioides on maize grain. Int. J. Food Microbiol. 81, 185-193 (2003).
Samapundo, S., De Meulenaer, B., Atukwase, A., Debevere, J. & Devlieghere, F. The influence of modified atmospheres and their interaction with water activity on the radial growth and fumonisin B1 production of Fusarium verticillioides and F. proliferatum on corn. Part I: The effect of initial headspace oxygen concentration. Int. J. Food Microbiol. 114, 160–167 (2007).
Murillo, I., Cavallarin, L. & San Segundo, B. Citology of infection of maize seedlings by Fusarium verticillioides and immunolocalization of the pathogenesis-related PRms protein. Phytopathology. 89, 737-747 (1999).
Oren, L., Ezrati, S., Cohen, D. & Sharon, A. Early events in the Fusarium verticilliodes maize interaction characterized by using green fluorescent protein-expressing transgenic isolate. Appl. Environ. Microbiol. 69, 1695-1701 (2003).
Munkvold, G.P., McGee, D.C. & Cariton, W.M. Importance of different pathways for maize kernel infection by Fusarium moniliforme. Phytopathology. 87, 209-217 (1997).
Gilbertson, R.L., Brown, M. Jr., Ruppel, E.G. & Capinera, J.L. Association of corn stalk rot Fusarium spp. and western corn rootworm beetles in Colorado. Phytopathology. 76, 1309-1314 (1986).
Munkvold, G.P. & Desjardins, A.E. Fumonisins in Maize. Can we reduce their occurence? Plant Dis. 81, 556-565 (1997).
Farrar, J.J. & Davis, R.M. Relationships among ear morphology, western flower thrips and Fusarium ear rot of corn. Phytopathology. 81, 661-666 (1991).
Rabie, C.J., Marasas, W.F.O., Thiel, P.G., Lübben, A. & Vleggaar, R. Moniliformin production and toxicity of different Fusarium species from Southern Africa. Appl. Environ. Microbiol. 43, 517-521 (1982).
Bacon, C.W., Marijanovic, D.R., Norred, W.P. & Hinton, D.M. Production of fusarin C on cereal and soybean by Fusarium moniliforme. Appl. Environ. Microbiol. 55, 2745-2748 (1989).
Bacon, C.W., Porter, J.K., Norred, W.P. & Leslie, J.F Production of fusaric acid by Fusarium species. Appl. Environ. Microbiol. 62, 4039-4043 (1996).
Desjardins, A.E. Fusarium mycotoxins: chemistry, genetics and biology (American Phytophatological Society, St. Paul, MN, 2006).
Reddy, K.R.N. et al. Mycotoxin contamination of commercially important agricultural commodities. Toxin Rev. 28, 154-168 (2009).
Reddy, K.R.N. et al. An overview of mycotoxin contamination in foods and its implications for human health. Toxin Rev. 29, 23-26 (2010).
Gelderblom, W.C. et al. Fumonisins--novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl. Environ. Microbiol. 54, 1806-1811 (1988).
Bezuidenhout, S. C. et al. Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme. J. Chem. Soc. Chem. Commun. 11, 743-745 (1988).
Bartók, T., Szécsi, A., Szekeres, A., Mesterházy, A. & Bartók, M. Detection of new fumonisin mycotoxins and fumonisin- like compounds by reversed-phase high-performance liquid chromatography/electrospray ionization ion trap mass spectrometry. Rapid Commun Mass Spectrom. 20, 2447-2462 (2006).
Rheeder, J.P., Marasas, W.F.O. & Vismer, H.F. Production of fumonisin analogs by Fusarium species. Appl. Environ. Microbiol. 68, 2101-2105 (2002).
Marín, S.V., Sanchis-Vinas, I., Canela, R. & Magan, N. Effect on water activity and temperature on growth and fumonisin B1 and B2 production by Fusarium proliferatum and F. moniliforme in grain. Lett. Appl. Microbiol. 21, 298-301 (1995).
Proctor, R.H., Plattner, R.D., Desjardins, A.E., Busaman, M. & Butchko, R. Fumonisin production in the maize pathogen Fusarium verticillioides: genetic basis of naturally occurring chemical variation. J. Agric. Food Chem. 54, 2424-2430 (2006).
Proctor, R.H., Desjardins, A.E., Plattner, R.D. & Hohn, T.M. A poliketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet. Biol. 27, 100-112 (1999).
Proctor, R.H., Brown, D.W., Plattner, R.D. & Desjardins, A.E. Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet. Biol. 38, 237-249 (2003).
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. 34, 155-165 (2001).
Du, L. et al. Biosynthesis of sphinganine-analog mycotoxins. J. Ind. Microbiol. Biotechnol. 35, 455–464 (2008).
Huffman, J., Gerber, R. & Du, L. Recent advancements in the biosynthetic mechanisms for polyketide-derived mycotoxins. Biopolymers 93, 764-776 (2010).
Thiel, P.G. et al. Survey of fumonisin production by Fusarium species. Appl. Environ. Microbiol. 57, 1089-1093 (1991).
Desjardins, A.E., Plattner, R.D. & Nelson, P.E. Fumonisin production and other traits of Fusarium moniliforme strains from maize in northeast Mexico. Appl. Environ. Microbiol. 60, 1695-1697 (1994).
Ghiasian, S.A. et al. Fumonisin production by Fusarium species isolated from freshly harvested corn in Iran. Mycopathologia 159, 31–40 (2005).
Sánchez-Rangel, D., SanJuan-Badillo, A. & Plasencia, J. Fumonisin production by Fusarium verticillioides strains isolated from maize in México and development of a polymerase chain reaction to detect potential toxigenic strains in grains. J. Agric. Food Chem. 53, 8565-8571 (2005).
van der Walt, A.M. et al. Fumonisin-producing Fusarium strains and fumonisins in traditional African vegetables (morogo). South African J. Sci. 102, 151-155 (2006).
Prom, L.K., Isakeit, T., Wheeler, M., Puckhaber, L.S. & Liu, J. Mycotoxigenic potential of ten Fusarium species grown on sorghum and in vitro. Plant Pathol. J. 7, 183-186 (2008).
Wang, J., Wang, X., Zhou, Y., Du, L. & Wang, Q. Fumonisin detection and analysis of potential fumonisin-producing Fusarium spp. in asparagus (Asparagus officinalis L.) in Zhejiang Province of China. J. Sci. Food Agric. 90, 836–842 (2010).
Goertz, A. et al. Fusarium species and mycotoxin profiles on comercial maize hybrids in Germany. Eur. J. Plant Pathol. 128, 101–111 (2010).
Nayaka, S.C. et al. Detection and quantification of fumonisins from Fusarium verticillioides in maize grown in southern India. World J. Microbiol. Biotechnol. 26, 71–78 (2010).
Ono, E.Y.S. et al. Fusarium verticillioides strains isolated from corn feed: characterization by fumonisin production and RAPD Fingerprinting. Braz. Arch. Biol. Technol. 53, 953-960 (2010).
Jurado, M. et al. Genetic variability and fumonisin production by Fusarium proliferatum. Food Microbiol. 27, 50–57 (2010).
de Oliveira Rocha, L. et al. Molecular characterization and fumonisin production by Fusarium verticillioides isolated from corn grains of different geographic origins in Brazil. Int. J. Food Microbiol. 145, 9–21 (2011).
Covarelli, L. et al. Characterization of Fusarium verticillioides strains isolated from maize in Italy: fumonisin production, pathogenicity and genetic variability. Food Microbiol. 31, 17-24 (2012).
Atukwase, A., Muy, C. & Kaaya, A.N. Potential for fumonisin production by strains of Gibberella fujikuroi species complex isolated from maize produced in Uganda. J. Biol. Sci. 12, 225- 231 (2012).
Uhlig, S. et al. Identification of early fumonisin biosynthetic intermediates by inactivation of the FUM6 gene in Fusarium verticillioides. J. Agric. Food Chem. 60, 10293-10301 (2012).
Butchko, R.A., Plattner, R.D. & Proctor, R.H. FUM13 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 (2003).
Blackwell, B.A., Edwards, O.E., Fruchier, A., ApSimon, J.W. & Miller, J.D. NMR structural studies of fumonisin B1 and related compounds from Fusarium moniliforme. Adv. Exp. Med. Biol. 392, 75-91 (1996).
Bojja, R.S., Cerny, R.L., Proctor, R.H. & Du, L. Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J. Agric. Food Chem. 19, 2855-2860 (2004).
Stergiopoulos, I., Zwiers, L.H. & De Waard, M.A. Secretion of natural and synthetic toxic compounds from filamentous fungi by membrane transporters of the ATP-binding cassette and major facilitator superfamily. Europ. J. Plant Pathol. 108, 719–734 (2002).
Brown, D.W., Butchko, R.A., 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. Eukaryot. Cell 6, 1210-1218 (2007).
Glenn, A.E., et al. 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. 21, 87–97 (2008).
Sagaram, U.S., Butchko, R.A.E. & Shim, W.B. The putative monomeric G-protein GBP1 is negatively associated with fumonisin B1 production in Fusarium verticillioides. Mol. Plant Pathol. 7, 381–389 (2006).
Picot, A., et al. Factors of the Fusarium verticillioides-maize environment modulating fumonisin production. Crit. Rev. Microbiol. 36, 221-231 (2010).
Flaherty, J.E., Pirttil, A.M., Bluhm, B.H. & Woloshuk, C.P. PAC1, a pH regulatory gene from Fusarium verticillioides. Appl. Environ. Microbiol. 69, 5222–5227 (2003).
Bluhm, B.H. & Woloshuk, C.P. Amylopectin induces fumonisin B1 production by Fusarium verticillioides during colonization of maize kernels. Mol. Plant-Microbe Interact. 18, 1333-1339 (2005).
Kim, H. & Woloshuk, C.P. Role of AREA, a regulator of nitrogen metabolism, during colonization of maize and fumonisin biosynthesis in Fusarium verticillioides. Fungal Genet. Biol. 45, 947-953 (2008).
Kim, H. Smith, J.E., Ridenour, J.B., Woloshuk, C.P. & Bluhm, B.H. HXK1 regulates carbon catabolism, sporulation, fumonisin B1production and pathogenesis in Fusarium verticillioides. Microbiology 157, 2658–2669 (2011).
Bluhm, B.H., Kim, H., Butchko, R.A. & Woloshuk, C.P. 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, 203–211 (2008).
Flaherty, J.E. & Woloshuk, C.P. Regulation of fumonisin biosynthesis in Fusarium verticillioides by a zinc binuclear cluster-type gene, ZFR1. Appl. Environ. Microbiol. 70, 2653–2659 (2004).
Malapi-Wight, M., Smith, J., Campbell, J., Bluhm, B.H. & Shim, W.B. Sda1, a Cys2-His2 Zinc finger transcription factor, is involved in polyol metabolism and fumonisin B1 production in Fusarium verticillioides. PLoS ONE 8, e67656 (2013).
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. 51, 42–49 (2013).
Shim, W.B. & Woloshuk, C.P. Regulation of fumonisin B1 biosynthesis and conidiation in Fusarium verticillioides by a cyclin–like (C–type) gene, FCC1. Appl. Environ. Microbiol. 67, 1607–1612 (2001).
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. 43, 146–154 (2006).
Sagaram, U.S. & Shim, W.B. Fusarium verticillioides GBB1, a gene encoding heterotrimeric G protein B subunit, is associated with fumonisin B1 biosynthesis and hyphal development but not with fungal virulence. Mol. Plant Pathol. 8, 375-384 (2007).
Choi, Y.E. & Shim, W.B. Functional characterization of Fusarium verticillioides CPP1, a gene encoding a putative protein phosphatase 2A catalytic subunit. Microbiology 154, 326–336 (2008).
Shin, J.H. et al. Protein phosphatase 2A regulatory subunits perform distinct functional roles in the maize pathogen Fusarium verticillioides. Mol. Plant Pathol. 14, 518–529 (2013).
Visentin, I. et al. Transcription of genes in the biosynthetic pathway for fumonisin mycotoxins is epigenetically and differentially regulated in the fungal maize pathogen Fusarium verticillioides. Euk. Cell 11, 252-259 (2012).
Bayram, O. & Braus, G.H. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol. Rev. 36, 1–24 (2012).
Myung, K., et al. FvVE1 regulates biosynthesis of the mycotoxins fumonisins and fusarins in Fusarium verticillioides. J. Agric. Food Chem. 57, 5087–5094 (2009).
Williams, L.D., Glenn, A.E., Bacon, C.W., Smith, M.A. & Riley, R.T. Fumonisin production and bioavailability to maize seedlings grown from seeds inoculated with Fusarium verticillioides and grown in natural soils. J. Agric. Food Chem. 54, 5694-5700 (2006).
Williams, L.D., et al. Fumonisin disruption of ceramide biosynthesis in maize roots and the effects on plant development and Fusarium. J. Agric. Food Chem. 55, 2937-2946 (2007).
Sánchez-Rangel, D., Sánchez-Nieto, S. & Plasencia, J. Fumonisin B1, a toxin produced by Fusarium verticillioides, modulates maize β-1,3glucanase activities involved in defense response. Planta 235, 965-978. (2012).
van Asch, M.A.J., Rijkenberg, F.H.J. & Coutinho, T.A. Phytotoxicity of fumonisin B1, moniliformin, and T-2 toxin to corn callus cultures. Phytopathology 82, 1330-1332 (1992).
Doehlert, D.C., Knutson, C.C. & Vesonder, R.F. Phytotoxic effects of fumonisin B1 on maize seedling growth. Mycopathologia 127, 117-121 (1994).
Lamprecht, S.C., et al. Phytotoxicity of fumonisins and TA-toxin to corn and tomato. Phytopathology 84, 383-391(1994).
Abbas, H.K. & Boyette, C.D. Phytotoxicity of fumonisin B1 on weed and crop species. Weed Technol. 6, 548-552 (1992).
Jardine, D.J. & Leslie, J.F. Aggressiveness to mature maize plants of Fusarium strains differing in ability to produce fumonisin. Plant Dis. 83, 690-693 (1999).
Desjardins, A.E. & Plattner, R.D. Fumonisin B1-nonproducing strains of Fusarium verticillioides cause maize (Zea mays) ear infection and ear rot. J. Agric. Food Chem. 48, 5773-5780 (2000).
Desjardins, A.E., Munkvold, G.P., Plattner, R.D. & Proctor, R.H. FUM1—a gene required for fumonisin biosynthesis but not for maize ear rot and ear infection by Gibberella moniliformis in field tests. Mol. Plant-Microbe Int. 15, 1157–1164 (2002).
Desjardins, A.E. & Plattner, R.D. Distribution of fumonisins in maize ears infected with strains of Fusarium moniliforme that differ in fumonisin production. Plant Dis. 82, 953-958 (1998).
Nascimento, V., et al. Characterization and genetic variability of Fusarium verticillioides strains isolated from corn and sorghum in Brazil based on fumonisins production, microsatellites, mating type locus, and mating crosses. Can. J. Microbiol. 52, 798-804 (2006).
Wang, E., Norred, W. P., Bacon, C.W., Riley, R.T. & Merrill, A.H. Jr. Inhibition of sphingolipid biosynthesis by fumonisins. J.Biol. Chem. 266, 14486-14490 (1991).
Ryland, L.K., Fox, T.E., Liu, X., Loughran, T.P. & Kester, M. Dysregulation of sphingolipid metabolism in cancer. Canc. Biol. Ther. 11, 138-149 (2011).
Hla, T. & Dannenberg, A.J. Sphingolipid signaling in metabolic disorders. Cell Metabol. 16, 420-434 (2012).
Abbas, H.K., et al. Fumonisin- and AAL-toxin-induced disruption of sphingolipid metabolism with accumulation of free sphingoid bases. Plant Physiol. 106, 1085–1093 (1994).
de la Torre-Hernández, M.E., Rivas-San Vicente, M., Greaves- Fernández, N., Cruz-Ortega, R. & Plasencia, J. Fumonisin B1 induces nuclease activation and salicylic acid accumulation through long-chain sphingoid base build-up in germinating maize. Physiol. Mol. Plant Pathol. 74, 337–345 (2010).
Zitomer, N.C., et al. Translocation of sphingoid bases and their 1-phosphates, but not fumonisins, from roots to aerial tissues of maize seedlings watered with fumonisins. J. Agric. Food Chem. 58, 7446-7481 (2010).
Gutiérrez-Nájera N, et al. Fumonisin B1, a sphingoid toxin, is a potent inhibitor of the plasma membrane H+-ATPase. Planta 221, 589–596 (2005).
Sperling, P., Franke, S., Luthje, S. & Heinz, E. Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? Plant Physiol. Biochem. 43, 1031-1038 (2005).
Chen, M., Cahoon, E.B., Saucedo-García, M., Plasencia, J. & Gavilanes-Ruiz, M. Plant sphingolipids: structure, synthesis and function. In: Wada, H., Murata, N., eds. Lipids in photosynthesis: essential and regulatory functions. (2009). Dordrecht, the Neatherlands Springer; 77-115.
Mongrand, S., et al. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J. Biol. Chem. 279, 36277–36286 (2004).
Borner, G.H., et al. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104–116 (2005).
Ng, C.K. & Hetherington, A.M. Sphingolipid-mediated signalling in plants. Ann. Bot. 88, 57–65 (2001).
Coursol, S., Fan, L.M., LeStunff, H., Spiegel, S., Gilroy, S., Assman, S.M. Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature423, 651–654 (2003).
Townley, H.E., McDonald, K., Jenkins, G.I., Knight, M.R. & Leaver, C.J. Ceramides induce programmed cell death in Arabidopsis cells in a calcium-dependent manner. Biol. Chem. 386, 161-166 (2005).
Pata, M.O., Hannun, Y.A. & Ng, C.K.Y. Plant sphingolipids: decoding the enigma of the Sphinx. New Phytol. 185, 611–630 (2010).
Saucedo-García, M., et al. MPK6, sphinganine and LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis. New Phytol. 191, 943-957 (2011).
Elmore, J.M. & Coaker, G. The role of plasma membrane H+- ATPase in plant-microbe interactions. Mol. Plant. 4, 416-427 (2011).
Vera-Estrella, R., Barkla, B.J. Higgins, V.J. & Blumwald, E. Plant defense response to fungal pathogens (activation of host-plasma membrane H+-ATPase by elicitor-induced enzyme dephosphorylation). Plant Physiol. 104, 209-215 (1994).
Liu, J. et al. RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol. 7, e1000139 (2009).
Ferreira, R. et al. The role of plant defence proteins in fungal pathogenesis. Mol. Plant Pathol. 8, 677-700 (2007).
Leubner-Metzger, G. & Meins, F. Functions and regulation of plant β -1,3-glucanases (PR-2) in Pathogenesis-related proteins in plants (eds. in Datta, S.K. & Muthukrishnan, S.) 49–76 (CRC Press, Boca Raton, 1999).