Nitrogen fertilizer-regulated plant-fungi interaction is related to root invertase-induced hexose generation

The mechanisms underlying nitrogen (N)-regulated plant-fungi interactions are not well understood. N application modulates plant carbohydrate (C) sinks and is involved in the overall plant-fungal association. We hypothesized that N regulates plant-fungi interactions by influencing the carbohydrate metabolism. The mutualistic fungus Phomopsis liquidambaris was found to prioritize host hexose resources through in vitro culture assays and in planta inoculation. Rice-Ph. liquidambaris systems were exposed to N gradients ranging from N-deficient to N-abundant conditions to study whether and how the sugar composition was involved in the dynamics of N-mediated fungal colonization. We found that root soluble acid invertases were activated, resulting in increased hexose fluxes in inoculated roots. These fluxes positively influenced fungal colonization, especially under N-deficient conditions. Further experiments manipulating the carbohydrate composition and root invertase activity through sugar feeding, chemical treatments and the use of different soil types revealed that the external disturbance of root invertase could reduce endophytic colonization and eliminate endophyte-induced host benefits under N-deficient conditions. Collectively, these results suggest that the activation of root invertase is related to N deficiency-enhanced endophytic colonization via increased hexose generation. Certain combinations of farmland ecosystems with suitable N inputs could be implemented to maximize the benefits of plant-fungi associations.