Fumonisin Disruption of Ceramide Biosynthesis in Maize Roots and the Effects on Plant Development and Fusarium verticillioides-Induced Seedling Disease

Authors: Williams, Lonnie; Glenn, Anthony - Tony; Zimeri, Anne; Bacon, Charles; SMITH, MARY - ENV HEALTH SCI./U.GEORGIA; Riley, Ronald

Submitted to: Journal of Agricultural and Food Chemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/22/2007
Publication Date: 4/24/2007
Citation: Williams, L.D., Glenn, A.E., Zimeri, A.M., Bacon, C.W., Smith, M.A., Riley, R.T. 2007. Fumonisin Disruption of Ceramide Biosynthesis in Maize Roots and the Effects on Plant Development and Fusarium verticillioides-Induced Seedling Disease. Journal of Agricultural and Food Chemistry. 55:2937-2946.

Interpretive Summary: The fungus Fusarium verticillioides infects corn and produces a toxin called fumonisin. This toxin inhibits the synthesis of a group of unusual fats known as sphingolipids. This work was undertaken to better understand the role of fumonisin in diseases of corn that are caused by Fusarium verticillioides. We were particularly interested in the effects of the toxin on the development of the roots in corn seedling disease. We found that the toxin and the fungus can inhibit the synthesis of the unique fats (sphingolipids) in the roots and that the inhibition of the synthesis of these fats was very closely correlated with the effects on root development in corn seedlings. The correlation between fungal pathogenicity, fumonisin production, inhibition of sphingolipid synthesis, the production of qualitatively similar pathology by both pathogenic strains of F. verticillioides and direct exposure to fumonisin, and the known biological activity of sphingolipids as regulators of cell function in plants strongly support the hypothesis that fumonisin is necessary and sufficient to produce F. verticillioides corn seedling disease and that the proximate cause of effects on root development is inhibition of sphingolipid synthesis. The data offer additional evidence for the importance of sphingolipids in the physiological well being of plants and indicate the need for developing a better understanding of the role of sphingolipids in physiological and disease processes in plants.

Technical Abstract: The fungus Fusarium verticillioides infects maize (Zea mays) and produces fumonisins, inhibitors of acyl coenzyme A dependent ceramide synthase. To determine the role of fumonisins on maize root development, seeds were inoculated with pathogenic or non- pathogenic strains of F. verticillioides. Roots were analyzed for sphingoid bases, sphingoid base 1-phosphates, and fumonisins; potting soils were analyzed for fumonisins. Seedlings grown from seeds inoculated with the pathogenic strain had detectable fumonisins in roots and soils, and elevated levels of sphingoid bases and sphingoid base 1-phosphates in roots. In a subsequent study, un-inoculated seeds were grown in soil watered with fumonisin B1. In addition to aboveground symptoms indicative of F. verticillioides-induced seedling disease, there was a dose-dependent reduction in root mass that was inversely correlated with accumulated fumonisin B1, sphingoid bases and sphingoid base 1-phosphates in roots. The correlation between fungal pathogenicity, fumonisin production, ceramide synthase inhibition, the production of qualitatively similar pathology by both pathogenic strains of F. verticillioides and direct exposure to fumonisin B1, and the known biological activity of sphingolipids as regulators of cell function in plants strongly support the hypothesis that fumonisin is necessary and sufficient to produce F. verticillioides maize seedling disease and that the proximate cause of effects on root development is disruption of sphingolipid metabolism. The data offer additional evidence for the importance of sphingolipids in the physiological well being of plants and indicate the need for developing a better understanding of the role of sphingolipids in physiological and disease processes in plants.