Root endophyte differentially regulates plant response to NO3- and NH4+ nutrition by modulating N fluxes at the plant-fungal interface.

Abstract

In the soil, plant roots associated with fungi often encounter uneven distribution of nitrate (NO3- )/ammonium (NH4+ ) patches, but the mechanism underlying N form-influenced plant-fungal interactions remains limited. We inoculated Arabidopsis with a root endophyte Phomopsis liquidambaris, and evaluated the effects of P. liquidambaris on plant performance under NO3- or NH4+ nutrition. Under NO3- nutrition, P. liquidambaris inoculation promoted seedling growth, whereas under NH4+ nutrition, P. liquidambaris suppressed seedling growth. Under high NH4+ conditions, fungus-colonized roots displayed increased NH4+ accumulation and NH4+ efflux, similar to the effect of ammonium stress caused by elevated NH4+ levels. Notably, this fungus excluded NH4+ during interactions with host roots, thereby leading to increased NH4+ levels at the plant-fungal interface under high NH4+ conditions. A nitrite reductase-deficient strain that excludes NO3- but absorbs NH4+ , decreased NH4+ levels in Arabidopsis shoots and rescued plant growth and nitrogen metabolism under high NH4+ levels. Transcriptomic analysis highlighted that P. liquidambaris had altered transcriptional responses associated with plant response to inorganic N forms. Our results demonstrate that fungus-regulated NO3- /NH4+ dynamics at the plant-fungal interface alters plant response to NO3- /NH4+ nutrition. This study highlights the essential functions of root endophytes in plant adaptation to soil nitrogen nutrients.