Temporal Wheat Proteome Remodeling by Deoxynivalenol Reveals Novel Detoxification Signatures and Strategies Across Cultivars

Fusarium head blight (FHB) is a globally devastating fungal disease resulting in reduced grain yield and quality, along with contamination of grains with dangerous mycotoxins. Consumption of such mycotoxins through processed food or livestock feed has downstream implications for human and animal health. This interconnectivity across the environment, animal, and human health defines the One Health problem of threatened food safety and security. In this study, we explore remodeling of the wheat proteome upon exposure to a common mycotoxin, deoxynivalenol (DON). We investigate cultivar-specific responses to DON exposure in FHB-susceptible (Norwell) and -resistant (Sumai#3) cultivars across a continuum of exposure (i.e., 24 and 120 h post inoculation) and upon low (i.e., 0.1 mg/ml) and high (1.0 mg/ml) levels of the mycotoxin. This complex experimental design enables us to tease apart the dynamic relationship between each cultivar and DON tolerance. Specifically, we define precise proteins and broad categories of remodeling that are common (i.e., reduction in photosynthesis) and exclusive (i.e., glycosyltransferase) to the cultivars and align with anticipated protective mechanisms. Moreover, we adapted an in vitro DON tolerance expression system and determined that induction of an ubiquinol oxidase (UniProt ID: A0A3B6B5K8) provides heightened protection for yeast growth relative to the negative control as well as increased protection compared to a well-defined DON detoxifying protein. Our study suggests a new avenue for the identification and characterization of novel DON detoxifying proteins as putative biomarkers for selected breeding strategies. Such strategies support the production of wheat varieties with increased tolerance to DON for improved global food safety and security.