Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions

Background Arbuscular mycorrhizal (AM) fungi contribute to plant nutrient uptake in systems managed with reduced fertilizer and pesticide inputs such as organic agriculture by extending the effective size of the rhizosphere and delivering minerals to the root. Connecting the molecular study of the AM symbiosis with agriculturally- and ecologically-relevant field environments remains a challenge and is a largely unexplored research topic. Methods This study utilized a cross-disciplinary approach to examine the transcriptional, metabolic, and physiological responses of tomato (Solanum lycopersicum) AM roots to a localized patch of nitrogen (N). A wild-type mycorrhizal tomato and a closely-related non-mycorrhizal mutant were grown at an organic farm in soil that contained an active AM extraradical hyphal network and soil microbe community. Results The majority of genes regulated by upon enrichment of nitrogen were similarly expressed in mycorrhizal and non-mycorrhizal roots, suggesting that the primary response to an enriched N patch is mediated by mycorrhiza-independent root processes. However where inorganic N concentrations in the soil were low, differential regulation of key tomato N transport and assimilation genes indicate a transcriptome shift towards mycorrhiza-mediated N uptake over direct root supplied N. Furthermore, two novel mycorrhizal-specific tomato ammonium transporters were also found to be regulated under low N conditions. A conceptual model is presented integrating the transcriptome response to low N and highlighting the mycorrhizal-specific ammonium transporters. Conclusions These results enhance our understanding of the role of the AM symbiosis in sensing and response to an enriched N patch, and demonstrate that transcriptome analyses of complex plant-microbe-soil interactions provide a global snapshot of biological processes relevant to soil processes in organic agriculture.