Volatilized Metabolites Produced by Soilborne Aspergillus flavus Regulate Fungal Conidiation, and Production of Secondary Metabolites

Abstract Corn plants are susceptible to infection by fungi such as Aspergillus flavus that have the potential to produce several types of mycotoxins, one of the most potent ones known to exist is aflatoxin. Since aflatoxin contaminated corn must be destroyed, causing annual monetary losses in billions of dollars, it would be helpful to detect the presence of aflatoxin producing fungi at pre-harvest and pre-planting stages. To this end, it may be possible to capture volatile organic compounds these fungi produce while overwintering in the soil or while infecting corn plants. In this study, we acquired A. flavus VOCs from conidia and sclerotia, while residing in the soil environment. We concluded that soilborne conidia and sclerotia have specific VOC signatures, and sclerotia tend to emit specific VOCs at greater abundance compared to soilborne conidia or fungus-free soil. These sclerotium-specific VOCs include geranyl acetone, caryophyllene compounds, and methanone. Bioassays using toxin producing and non-producing fungi showed that β-caryophyllene increased spore concentration, and both β-caryophyllene and caryophyllene oxide were able to modulate aerial hyphae, sclerotia production and decrease aflatoxin, cyclopiazonic acid and ditryptophenaline production in A. flavus strains. Our results show insights into the ecological roles that β-caryophyllene and caryophyllene oxide have over A. flavus’ development and metabolism, although their effect on multitrophic interactions among corn, fungi and other potential organisms are still not fully understood. These VOCs could serve as an agricultural surveillance management system that enables early mitigation of aflatoxin producing fungi outbreaks in the field.