Divergent Aspergillus flavus corn population is composed of prolific conidium producers: implications for saprophytic disease cycle

Authors: Sweany, Rebecca; Mack, Brian; GEBRU, SOLOMON - Food And Drug Administration(FDA); MAMMEL, MARK - Food And Drug Administration(FDA); Cary, Jeffrey; Moore, Geromy; Lebar, Matthew; Carter-Wientjes, Carol; Gilbert, Matthew

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/12/2024
Publication Date: 5/10/2024
Citation: Sweany, R.R., Mack, B.M., Gebru, S.T., Mammel, M.K., Cary, J.W., Moore, G.G., Lebar, M.D., Carter Wientjes, C.H., Gilbert, M.K. 2024. Divergent Aspergillus flavus corn population is composed of prolific conidium producers: implications for saprophytic disease cycle. Mycologia. https://doi.org/10.1080/00275514.2024.2343645.
DOI: https://doi.org/10.1080/00275514.2024.2343645

Interpretive Summary: Contamination of corn with acutely toxic and carcinogenic aflatoxins can result in poisonings and death in humans, livestock, pets and wildlife. Understanding the biology and genetics of the causal fungal agent Aspergillus flavus is crucial to devising better strategies to manage and minimize aflatoxin contamination of corn. We characterized the corn and soil population's phenotypes and discovered that those strains that infected corn the most also produced the most asexual spores (conidia), which serve as the infectious agents. We also sequenced the genomes and found that the highly infectious corn isolates were closely related and distantly related to isolates that produce sexual fruiting bodies sclerotia. This study support efforts to maximize conidial production of non-aflatoxigenic biocontrol strains for maximal efficacy in corn. This research suggests that monitoring of the spore population of A. flavus will allow for better prediction of infection and will help to fine-tune integrated pest management techniques including irrigation and biocontrol deployment.

Technical Abstract: The ascomycete fungus Aspergillus flavus infects and contaminates corn, peanuts, cottonseed and tree nuts with acutely toxic and carcinogenic aflatoxins. Subdivision between soil and host plant populations suggest certain A. flavus strains are specialized to infect peanut, cotton and corn crops despite having a broad host-range. In this study, the ability of strains isolated from corn and/or soil in 11 Louisiana fields to produce conidia (natural field inocula and male gamete source) and sclerotia (resting bodies and female gamete source) was assessed and compared to their abilities to move into corn, impact on effective breeding sizes and genotypic differences between whole genomes. Corn strains produced upwards of 47x more conidia than strains restricted to soil. Conversely, corn strains produced as much as 3000x fewer sclerotia than soil strains. A. flavus strains, typified by sclerotium diameter (small Sstrains < 400 µm, large L-strains > 400 µm), belonged to separate clades. Several strains produced a mixture (M) of S and L sclerotia, as well as an intermediate number of conidia and sclerotia, compared to typical S-strains (minimal conidia, copious sclerotia) and L-strains (copious conidia, minimal sclerotia). They also belonged to a unique phylogenetic mixed (M) clade. Migration from soil to corn positively correlated with conidium production and negatively correlated with sclerotium production. Additionally, genetic differences correlated with differences in conidium and sclerotium production. Due to opposite skews to female or male gametic production by soil and corn strains, effective breeding population sizes decreased when comparing relative male:female gamete ratio to mating type distribution. Combining both soil and corn populations increased the effective breeding population, presumably due to the contribution of male gametes from corn, which can fertilize sclerotia on the soil surface. Incongruencies between aflatoxin clusters, strain morphotype designation and whole genome phylogenies suggest a history of sexual reproduction within this Louisiana population, demonstrating the importance of conidium production, not only as infectious propagules, but also as fertilizers of the A. flavus soil population.