Flavonoids modulate the accumulation of toxins from Aspergillus flavus in maize kernels

Authors: Castano-Duque, Lina; Gilbert, Matthew; Mack, Brian; Lebar, Matthew; Carter-Wientjes, Carol; Sickler, Christine; Cary, Jeffrey; Rajasekaran, Kanniah - Rajah

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2021
Publication Date: 11/26/2021
Citation: Castano-Duque, L.M., Gilbert, M.K., Mack, B.M., Lebar, M.D., Carter-Wientjes, C.H., Sickler, C.M., Cary, J.W., Rajasekaran, K. 2021. Flavonoids modulate the accumulation of toxins from Aspergillus flavus in maize kernels. Frontiers in Plant Science. 12:761446. https://doi.org/10.3389/fpls.2021.761446.
DOI: https://doi.org/10.3389/fpls.2021.761446

Interpretive Summary: Aspergillus flavus (A. flavus) is a fungus that infects crops such as corn and peanuts. This fungus is capable of then producing aflatoxins which are potent cancer-causing toxins that accumulate in corn kernels after infection. To better understand how the corn naturally resists A. flavus growth and aflatoxin accumulation, we examined which genes are activated in corn kernels that are infected with A. flavus. We looked at three different corn lines: 2 lines that are known to resist growth of the fungus, and one corn line that is more susceptible to infection. The results indicated that several genes were highly expressed (turned on) in the infected corn kernels, and many of these genes were identified as contributing to the defense responses of the corn plant against harmful fungi and other microbes. In this study we also incorporated the results of experiments that examined resistance in other A. flavus-resistant corn lines, which allowed us to identify new areas of the plant's genome that also contribute to fungal resistance. In addition to identifying genes and specific regions of the plant genome, these experiments showed that one of our resistant lines has a higher fold-increase of certain chemical metabolites, also contributing to plant resistance. Chemical messengers such as naringenin and luteolin were higher in the resistant plants than in the susceptible plants. These results suggest that certain genes and specific chemical messengers contribute to plant resistance, and will allow us to further explore scientific methods to reduce the harmful impacts of A. flavus contamination in food crops.

Technical Abstract: Aspergillus flavus is an opportunistic fungal pathogen capable of producing aflatoxins, potent carcinogenic toxins that accumulate in maize kernels after infection. To better understand the molecular mechanisms of maize resistance to A. flavus growth and aflatoxin accumulation we performed a high-throughput transcriptomic study in situ using maize kernels infected with A. flavus strain 3357. Three maize lines were evaluated: aflatoxin-contamination resistant line TZAR102, semi resistant MI82, and susceptible line Va35. Redundancy analysis (RDA) of the transcriptomic data indicated that maize line, fungal treatment, and duration of infection significantly co-vary to influence the overall maize gene expression patterns. Gene ontology enrichment analysis of genes highly expressed in infected kernels identified molecular pathways associated with defense responses to fungi and other microbes such as production of Pathogenesis-related (PR) proteins and lipid bilayer formation. To further identify novel genes of interest, we incorporated genomic and phenotypic field data from a genome wide association analysis with gene expression data, allowing us to detect significantly expressed quantitative trait loci (eQTL). These results identified significant association between flavonoid biosynthetic pathway genes and infection by A. flavus. In planta fungal infections showed that resistant line, TZAR102, has a higher fold-increase of the metabolites naringenin and luteolin than susceptible line, Va35, when comparing untreated and fungal infected plants. These results suggest flavones contribute to plant resistance mechanisms against aflatoxin contamination through modulation of toxin accumulation in maize kernels.