Insights into the Aggressiveness of the Emerging North American Population 3 (NA3) of Fusarium graminearum

Authors: LARABA, IMANE - Orise Fellow; Ward, Todd; CUPERLOVIC-CULF, MIROSLAVA - National Research Council - Canada; AZIMI, HILDA - National Research Council - Canada; XI, PENGCHENG - National Research Council - Canada; McCormick, Susan; Hay, William; Hao, Guixia; Vaughan, Martha

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/1/2023
Publication Date: 9/19/2023
Citation: Laraba, I., Ward, T.J., Cuperlovic-Culf, M., Azimi, H., Xi, P., McCormick, S.P., Hay, W.T., Hao, G., Vaughan, M.M. 2023. Insights into the Aggressiveness of the Emerging North American Population 3 (NA3) of Fusarium graminearum. PLoS Pathogens. https://doi.org/10.1094/PDIS-11-22-2698-RE.
DOI: https://doi.org/10.1094/PDIS-11-22-2698-RE

Interpretive Summary: Fusarium graminearum is among the most destructive fungal pathogens because it reduces cereal crop yield and poisons grain with harmful toxins. ARS researchers showed that the major Fusarium populations infecting wheat and barley in North America differ in aggressiveness. This work has helped understand how pathogen diversity influences disease. This knowledge is important to develop methods to reduce the negative impacts of fungal pathogens on agricultural production and on human and animal health

Technical Abstract: In the U.S. and Canada, Fusarium graminearum (Fg) is the predominant etiological agent of Fusarium head blight (FHB), an economically devastating fungal disease of wheat and other small grains. Besides yield losses, FHB leads to grain contamination with mycotoxins, particularly trichothecenes that are harmful to plant, human, and livestock health. Three genetically distinct North American populations of Fg, differing in their predominant trichothecene chemotype (i.e., NA1/15ADON, NA2/3ADON, and NA3/NX-2), have been identified. To improve our understanding of the newly discovered population NA3 and how Fg population-level diversity influences FHB outcomes, we inoculated heads of the moderately resistant wheat cultivar Alsen with 15 representative strains from each North American population and evaluated disease progression, mycotoxin accumulation, and mycotoxin production per unit Fg biomass. Additionally, we evaluated Fg population-specific differences in induced host defense responses. The NA3 population was significantly less aggressive than the NA1 and NA2 populations but posed a similar mycotoxigenic potential. Moreover, while differences between NA1 and NA2 were inconsistent across the experimental replicates, in one of the assays, NA2 caused significantly more FHB and toxin accumulation than NA1. Fg and host multi-omics analyses revealed patterns in mycotoxin production per unit Fg biomass as well as expression of select genes associated with Fg aggressiveness and host defense responses that did not always correlate with the observed NA3-specific FHB severity differences. Our comparative disease assay of NA3/NX-2 and admixed NA1/NX-2 strains indicated that the reduced NA3 aggressiveness is not due solely to their NX-2 chemotype. The NA3-specific disease difference was also noted on the susceptible cultivar Norm but not Apogee. Notably, the NA1 and NA2 populations did not show a significant advantage over the less aggressive NA3 population in perithecia production, a fitness-related trait. Together, our data highlight that the disease outcomes noted herein were not due to mycotoxin production or host defense responses alone, indicating that other virulence factors and/or host defense mechanisms are likely involved. The current study provides insights into the virulence of the NA3 population and the impact of Fg population-level diversity on FHB development.