Nanoscale-specific bioassimilation of sulfur: Time and coating specific modulation of transcriptomic and metabolomic pathways in diseased tomato

<title>Abstract</title> Nanoscale sulfur was investigated as a multi-functional agricultural amendment to simultaneously enhance crop nutrition and suppress disease damage. Pristine (nS) and stearic acid coated (cS) sulfur nanoparticles were added to soil (0, 100, or 200 mg/L) that was planted with tomato (<italic>Solanum lycopersicum</italic>) and infested with the <italic>Fusarium</italic> wilt pathogen. Bulk sulfur (bS), ionic sulfate (iS), and healthy controls were included. In two greenhouse experiments, measured endpoints included time-dependent agronomic and photosynthetic parameters, disease severity/suppression, and a range of mechanistic biochemical and molecular endpoints, including the expression of 13 genes related to two S bioassimilation pathways and pathogenesis-response, and tissue-specific metabolomic profiles. The impact of treatment on the rhizosphere bacterial microbiome was also evaluated. Disease reduced tomato biomass by up to 87%, but amendment with nS and cS significantly reduced disease progress by 54 and 56%, respectively, compared to the infested controls. Increased S accumulation was evident in plant roots and leaves, independent of S type. Molecular analysis revealed particle size and coating-specific impacts on the plants. For nS and cS, two-photon microscopy and time-dependent gene expression data revealed a nanoscale specific elemental S bioassimilation pathway within the plant tissues. These findings correlated well with detailed metabolomic profiling of plant tissues at 4, 8, and 16 d, which exhibited increased disease resistance and plant immunity related metabolites with nanoscale treatment. The data also demonstrate a time-sensitive physiological window whereby nanoscale stimulation of plant immunity will be effective. An analysis of the rhizosphere soil bacterial community revealed minimal impacts from S soil treatments. These findings provide significant mechanistic insight into non-metal nanomaterial-based suppression of plant disease, and significantly advance efforts to develop sustainable nano-enabled agricultural strategies to increase food production.