Plant-derived oxylipins modulate fumonisin production through transcriptional and lipid metabolic changes in Fusarium verticillioides

Plant-derived oxylipins play pivotal roles in plant immunity and have emerged as important mediators of cross-kingdom communication with fungal pathogens. Although several oxylipins exhibit antifungal activity, their impact on mycotoxin biosynthesis and the underlying molecular mechanisms remain poorly understood. Here, we investigated the effects of three maize-associated oxylipins, jasmonic acid (JA), trans-2-hexenal (T2H), and traumatic acid (TA), on mycotoxin production by Fusarium verticillioides , Aspergillus flavus and F. graminearum . Among the compounds tested, T2H and JA significantly reduced fumonisin (FB) accumulation in F. verticillioides , whereas aflatoxin and deoxynivalenol production remained unaffected in A. flavus and F. graminearum , respectively, highlighting species-specific responses to host-derived oxylipins. To elucidate the mechanisms underlying FB inhibition, transcriptomic and lipidomic analyses were performed on F. verticillioides following JA and T2H treatments. Both oxylipins induced extensive transcriptional reprogramming affecting genes involved in signal transduction, nutrient transport, chromatin remodeling, autophagy, fungal development, and endogenous oxylipin metabolism. Surprisingly, despite the marked reduction in FB accumulation, genes of the fumonisin ( FUM ) biosynthetic cluster were transcriptionally induced, suggesting that oxylipin-mediated inhibition occurs through regulatory networks acting upstream or independently of FUM gene expression. Lipidomic profiling further revealed substantial remodeling of fungal oxylipin metabolism, with pronounced accumulation of lipoxygenase- and linoleate diol synthase-derived metabolites, including hydroxyoctadecadienoic, dihydroxyoctadecadienoic and dihydroxyoctadecenoic acids, particularly following T2H treatment. Collectively, these findings demonstrate that host-derived oxylipins modulate FB production by reshaping fungal regulatory and metabolic networks rather than by directly repressing toxin biosynthetic genes. This work provides new insights into oxylipin-mediated cross-kingdom communication and identifies T2H as a promising candidate for sustainable strategies to mitigate FB contamination in maize.