Crop host influences on outcomes of competition between Aspergillus section Flavi species co-infecting maize and groundnuts

Authors: CHING'ANDA, CONNEL - University Of Arizona; BANDYOPADHYAY, RANAJIT - International Institute Of Tropical Agriculture (IITA); Callicott, Kenneth; ORBACH, MARC - University Of Arizona; COTTY, PETER - Ocean University Of China; Mehl, Hillary

Submitted to: PhytoFrontiers
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/4/2022
Publication Date: 8/9/2023
Citation: Ching'anda, C., Bandyopadhyay, R., Callicott, K.A., Orbach, M.J., Cotty, P.J., Mehl, H.L. 2023. Crop host influences on outcomes of competition between Aspergillus section Flavi species co-infecting maize and groundnuts. PhytoFrontiers. 3(2):369-381. https://doi.org/10.1094/PHYTOFR-07-22-0076-R.
DOI: https://doi.org/10.1094/PHYTOFR-07-22-0076-R

Interpretive Summary: Several species of Aspergillus are known for producing aflatoxins, toxic fungal metabolites that contaminate food and feed. Aflatoxin contamination of crops affects human health and impedes trade. Aflatoxin contamination is caused by several species that co-occur and compete on crops, and the extent to which crops are contaminated with aflatoxins is likely influenced by the interaction between the competing fungi and the host. Maize and groundnuts, two crop hosts that differ in nutrient composition and physiology, are staple crops that are highly susceptible to aflatoxin contamination. Maize is high in carbohydrate content and low in oil and protein content, whereas groundnuts are relatively low in carbohydrates but high in oil and protein content. Since there are distinct differences between maize and groundnuts, the current study aimed to characterize crop host influences on aflatoxin production, sporulation, and competition between four aflatoxin-producing Aspergillus species. The ability of one Aspergillus species to outcompete another species was host-dependent with some species more competitive on maize and others more competitive on groundnuts. However, isolates within a species varied in the extent to which they were able to outcompete other species on the two hosts. Results indicate that complex interactions between crop hosts and different Aspergillus species modulate Aspergillus community structure and subsequent aflatoxin contamination. Understanding factors that impact sporulation, dispersal, crop infection, and aflatoxin production by different Aspergillus species is critical for developing crop management practices that will minimize aflatoxin contamination.

Technical Abstract: Aspergillus section Flavi species co-occur and contaminate crops, including maize and groundnuts, with aflatoxins. Competition among A. flavus genotypes is influenced by crop host, but competition between Aspergillus species has not been examined. The objectives of the current study were to (i) assess competition among four aflatoxin-producing species on maize and groundnuts and (ii) evaluate within-species variation in competitive ability during coinfection with another species on the two crops. For the first objective, maize and groundnut kernels were coinoculated with all possible pairs of A. flavus, A. parasiticus, A. aflatoxiformans, and an unnamed taxon known as the Lethal Aflatoxicosis Fungus (LAF). For the second objective, three isolates from each of the four species were coinoculated with a representative isolate of a competing species on the two hosts. In all experiments, isolates were cocultured for 7 days at 30°C, and then aflatoxins and total conidia were measured, and the percentages of each species within a treatment were assessed with quantitative pyrosequencing. Maize kernels supported greater aflatoxin production than groundnuts, whereas groundnuts supported greater sporulation than maize. Hosts differentially influenced competition between species, with A. flavus generally more competitive on maize and LAF more competitive on groundnuts. Overall, A. flavus and LAF were the most competitive species, whereas A. parasiticus was the least competitive. However, isolates within a species varied in competitive ability and in their response to host and competing species. Results suggest that although crop hosts influence Aspergillus community composition, within-species variability makes it difficult to predict outcomes of competition on a particular crop.