Low molecular weight acids differentially impact Fusarium verticillioides transcription

Authors: Brown, Daren; Kim, Hye-Seon; Proctor, Robert; WICKLOW, DONALD - Retired ARS Employee

Submitted to: Fungal Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/14/2024
Publication Date: 8/15/2024
Citation: Brown, D.W., Kim, H.-S., Proctor, R.H., Wicklow, D.T. 2024. Low molecular weight acids differentially impact Fusarium verticillioides transcription. Fungal Biology. https://doi.org/10.1016/j.funbio.2024.08.007.
DOI: https://doi.org/10.1016/j.funbio.2024.08.007

Interpretive Summary: Species of the fungi Aspergillus, Fusarium and Penicillium can infect corn, cause kernel rot, and produce multiple metabolites, including toxins that pose threats to food and feed safety. Together, the rots and toxins can cause hundreds of millions of dollars in annual losses to the U.S. agricultural economy. The fungi can also occur in the same corn plant, but it is not clear how metabolites produced by one fungus affect the other fungi. Therefore, we determined how four metabolites produced by species of Fusarium, Aspergillus and/or Penicillium impact expression of genes in Fusarium verticillioides, which causes corn kernel rot and produces one of the groups of toxins (fumonisins) that are of most concern to food and feed safety. We found that each metabolite markedly increased or decreased expression of different sets of genes in F. verticillioides. However, two of the metabolites (citric acid and oxalic acid), which are produced by a wide range of fungi, caused increased expression of some of the same genes. The observed changes in gene expression indicate that the metabolites are part of the mechanism that F. verticillioides uses to detect the presence of and compete with other fungi in corn. These results are an important first step in understanding how the presence of multiple fungi in corn impact one another and the agricultural problems each fungus causes. Such information will inform efforts to improve agriculture.

Technical Abstract: Fusarium verticillioides is both an endophyte and a pathogen of maize. During growth on maize, the fungus often synthesize the mycotoxins fumonisins, which have been linked to a variety of diseases, including cancer in some animals. How F. verticillioides responds to fungi, such as Fusarium proliferatum, Aspergillus flavus, Aspergillus niger, and Penicillium oxalicum, that coinfect maize, have potential to impact mycotoxin synthesis and disease. We hypothesize that low molecular weight acids produced by these fungi play a role in communication between microbes in planta/nature. To address this hypothesis, we exposed a 48-hour maize culture of F. verticillioides to oxalic acid, citric acid, fusaric acid, or kojic acid and then compared transcriptomes after 30 minutes and six hours. Transcription of some genes were affected by multiple acids and others were affected by only one of the acids. The most significant positive response was observed after exposure to fusaric acid with 225 genes upregulated > 2-fold, including genes involved in fusaric acid synthesis. Exposure to the other three acids increased expression of between 3 - 15 genes, which with their predicted function and frequent co-localization, support specific roles for some and general roles for others. This tailored response supports our hypothesis that these acids can be signaling molecules (infochemicals) that diffuse in advance of infecting hyphae informing F. verticillioides of its neighbors and helping it respond accordingly.