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

ABSTRACT

The ascomycete fungus Aspergillus flavus infects and contaminates corn, peanuts, cottonseed, and tree nuts with toxic and carcinogenic aflatoxins. Subdivision between soil and host plant populations suggests that certain A. flavus strains are specialized to infect peanut, cotton, and corn 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 (field inoculum and male gamete) and sclerotia (resting bodies and female gamete) was assessed and compared with genotypic single-nucleotide polymorphism (SNP) differences between whole genomes. Corn strains produced upward of 47× more conidia than strains restricted to soil. Conversely, corn strains produced as much as 3000× fewer sclerotia than soil strains. Aspergillus flavus strains, typified by sclerotium diameter (small S-strains, <400 μm; large L-strains, >400 μm), belonged to separate clades. Several strains produced a mixture (M) of S and L sclerotia, and an intermediate number of conidia and sclerotia, compared with 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. Genetic differences correlated with differences in conidium and sclerotium production. Opposite skews in female (sclerotia) or male (conidia) gametic production by soil or corn strains, respectively, resulted in reduced effective breeding population sizes when comparing male:female gamete ratio with mating type distribution. Combining both soil and corn populations increased the effective breeding population, presumably due to contribution of male gametes from corn, which 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, as infectious propagules and as fertilizers of the A. flavus soil population.

KEYWORDS:

• Aflatoxin conidia
• female sterility
• fungal ecology
• fungal life cycle
• fungal sexual cycle
• niche specialization

ACKNOWLEDGMENTS

This work was initiated under the supervision of Kenneth E. Damann Jr. in the Department of Plant Pathology and Crop Physiology at Louisiana State University. We thank Ken for his mentorship and contributions to our understanding of the A. flavus–corn interaction. We thank Joshua Martin for his technical assistance at the U.S. Department of Agriculture (USDA). We thank Dr. John Leslie at Kansas State University for his advice on consequences of female and male sterility on host-pathogen interactions.

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the author(s).

SUPPLEMENTARY MATERIAL

Supplemental data for this article can be accessed online at https://doi.org/10.1080/00275514.2024.2343645.

Additional information

Funding

This research was supported by the U.S. Food and Drug Administration (FDA), Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA) and U.S. Department of Agriculture (USDA), Agricultural Research Service (ARS), Food and Feed Safety Research Unit [project number 6054-41420-009-000-D].