The effect of Fusarium verticillioides fumonisins on fatty acids, sphingolipids, and oxylipins in maize germlings

Authors: BECCACCIOLI, MARZIA - University Of Rome Sapienza; SALUSTRI, MANUEL - University Of Rome Sapienza; SCALA, VALERIA - Crea; LUDOVICI, MATTEO - University Of Rome Sapienza; CACCIOTTI, ANDREA - University Of Rome Sapienza; D'ANGELI, S - University Of Rome Sapienza; Brown, Daren; REVERBERI, MASSIMO - University Of Rome Sapienza

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/23/2021
Publication Date: 2/28/2021
Citation: Beccaccioli, M., Salustri, M., Scala, V., Ludovici, M., Cacciotti, A., D'Angeli, S., Brown, D.W., Reverberi, M. 2021. The effect of Fusarium verticillioides fumonisins on fatty acids, sphingolipids, and oxylipins in maize germlings. International Journal of Molecular Sciences. 22(5). Article 2435. https://doi.org/10.3390/ijms22052435.
DOI: https://doi.org/10.3390/ijms22052435

Interpretive Summary: Although usually harmless to corn, the fungus Fusarium verticillioides can cause disease at any stage of corn growth and can contaminate corn kernels with a toxic chemical called fumonisins. Ingestion of this toxin poses a threat to humans and animals by disrupting the synthesis of sphingolipids involved in critical cell processes. In plants, changes in sphingolipid levels can cause cell death and disease or increase the synthesis of salicylic acid, a plant hormone involved in defense. To understand how fungal infection and fumonisin exposure affect sphingolipid metabolism, we determined the amounts of 50 sphingolipids in corn kernels infected with a fumonisin producing strain of F. verticillioides and a fumonisin non-producing strain. Because sphingolipids profoundly affect corn, we also evaluated the expression of corn genes associated with programed cell death, as well as an antifungal protein, and determined salicylic acid content in infected corn kernels. We identified a set of sphingolipids that responded to fumonisins and another set that responded to the fungal infection itself. We also verified that the altered sphingolipid profiles turns on programed cell death genes and increases salicylic acid production. Understanding which sphingolipids change in fungal infected corn and how this effects plant growth and health is important for resistance breeding efforts aimed at limiting crop losses and reducing fumonisin contamination of corn.

Technical Abstract: Fusarium verticillioides causes worldwide ear rot of Zea mays spoiling its quality and safety by producing the neurotoxin fumonisins. Fumonisins are not virulence factors but do inhibit the activity of ceramide synthases in plant host cell: leading to accumulation of specific sphingolipids such as sphingoid bases and phytoceramides. It seems possible that these changing sphingolipid profiles play a significant role in transitioning the fungus from a benign biotroph or endophyte to a destructive necrotroph. In this study, we explored the complex relation among sphingolipids, fumonisins and necrotrophic growth of F. verticillioides in maize kernels. Levels of over 50 sphingolipids and salicylic acid was evaluated by LC-MS/MS, in maize kernels artificially infected with F. verticillioides WT and a mutant unable to synthesise fumonisins, at different times post inoculation. We found a specific response of sphingolipids containing certain very long chain fatty acids to fumonisins that correlated with the expression of plant factors related to PCD onset and execution. We suggest that fumonisins produced by F. verticillioides, alter maize sphingolipid metabolism that then switches the fungus from endophytic to necrotrophic growth