Metabolomic insights on the response of winter wheat cultivars to Fusarium head blight infection and inoculation with a biocontrol strain in open field

• Trichoderma gamsii T6085 reduces Fusarium head blight (FHB) under field conditions • T6085 is less effective than conventional agrochemical (tetraconazole/prochloraz) • UHPLC/QTOF-HRMS metabolomics reveals cultivar-specific responses to FHB and T6085 • T6085 enhances resistance by modifying metabolic pathways in wheat under FHB • Metabolomics aids in decipher tri-trophic biological interaction in agriculture Fusarium head blight (FHB) poses a significant threat to wheat cultivation worldwide, leading to substantial yield and economic losses mainly due to mycotoxins contamination of grains. Developing new sustainable approaches to cope with FHB, such as using biocontrol agents (BCAs), is necessary to guarantee food safety and security worldwide. In this work, an untargeted metabolomics approach (UHPLC/QTOF-MS) was used to unveil the metabolic shifts in leaves and spikes of two cultivars of winter wheat, treated either with systemic agrochemicals (Syst; i.e., prochloraz and tetraconazole) or a BCA ( Trichoderma gamsii T6085), and subsequently inoculated with a spore suspension of Fusarium graminearum and F. langsethiae . To this aim, Bingo and Rebelde winter wheat cultivars (more and less susceptible to FHB, respectively), were used under field conditions. The treatments with Syst and T6085 reduced FHB index by 55 and 64%, on average, in Bingo and Rebelde, respectively. The multivariate analysis of metabolomic signatures revealed a dominant influence of the ‘cultivar’ factor, followed by ‘FHB’ and ‘treatment’. Supervised modeling (OPLS-DA) highlighted distinct metabolic differences between the cultivars, FHB infection, and treatment conditions. Pathway analysis indicated that nitrogen-containing compounds and terpenes played crucial roles in the response of the Bingo to the FHB-T6085 treatment, with different responses between leaves and spikes. Conversely, Rebelde spikes showed a significant up-modulation of the whole secondary metabolism following FHB-infection, especially in those previously inoculated with T6085. Our findings highlighted a complex response to FHB and BCA and unraveled the metabolic responses underlying the reduced susceptibility to FHB in Rebelde.