The role of flowering in root-fungal symbiosis is not well understood. Because flowering and fungal symbionts are supported by carbohydrates, we hypothesized that flowering modulates root-beneficial fungal associations through alterations in carbohydrate metabolism and transport. We monitored fungal colonization and soluble sugars in the roots of Arabidopsis thaliana following inoculation with a mutualistic fungus Phomopsis liquidambari across different plant developmental stages. Jasmonate signalling of wild-type plants, sugar transport, and root invertase of wild-type and jasmonate-insensitive plants were exploited to assess whether and how jasmonate-dependent sugar dynamics are involved in flowering-mediated fungal colonization alterations. We found that flowering restricts root-fungal colonization and activates root jasmonate signalling upon fungal inoculation. Jasmonates reduce the constitutive and fungus-induced accumulation of root glucose and fructose at the flowering stage. Further experiments with sugar transport and metabolism mutant lines revealed that root glucose and fructose positively influence fungal colonization. Diurnal, jasmonate-dependent inhibitions of sugar transport and soluble invertase activity were identified as likely mechanisms for flowering-mediated root sugar depletion upon fungal inoculation. Collectively, our results reveal that flowering drives root-fungus cooperation loss, which is related to jasmonate-dependent root soluble sugar depletion. Limiting the spread of root-fungal colonization may direct more resources to flower development.

Abstract 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.

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