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

ABSTRACT: Arbuscular mycorrhizal (AM) fungi contribute to plant nutrient uptake in systems managed with reduced fertilizer inputs such as organic agriculture and natural ecosystems by extending the effective size of the rhizosphere and delivering mineral. 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. 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 nonmycorrhizal mutant were grown at an organic farm in soil that contained an active AM extraradical hyphal network and soil microbe community. The majority of genes regulated by upon enrichment of nitrogen were similarly expressed in mycorrhizal and nonmycorrhizal 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. 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.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE30270 | GEO | 2011/06/29

SECONDARY ACCESSION(S): PRJNA143733

REPOSITORIES: GEO

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Project description:Arbuscular mycorrhizal (AM) fungi contribute to plant nutrient uptake in systems managed with reduced fertilizer inputs such as organic agriculture and natural ecosystems by extending the effective size of the rhizosphere and delivering mineral. 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. 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 nonmycorrhizal mutant were grown at an organic farm in soil that contained an active AM extraradical hyphal network and soil microbe community. The majority of genes regulated by upon enrichment of nitrogen were similarly expressed in mycorrhizal and nonmycorrhizal 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. 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. 30 samples were analyzed. There were 2 genotypes (wildtype and mutant) and 3 treatments (two N treatments and a water control) for a total of 6 groups. Each group had 5 biological replicates.

Project description:Nitrogen (N), the primary limiting factor for plant growth and yield in agriculture, has a patchy distribution in soils due to fertilizer application or decomposing organic matter. Studies in solution culture over-simplify the complex soil environment where microbial competition and spatial and temporal heterogeneity challenge rootsâ ability to acquire adequate amounts of nutrients required for plant growth. In this study, various ammonium treatments (as 15N) were applied to a discrete volume of soil containing tomato (Solanum lycopersicum) roots to simulate encounters with a localized enriched patch of soil. Transcriptome analysis was used to identify genes differentially expressed in roots 53 hrs after treatment. Results: The ammonium treatments resulted in significantly higher concentrations of both ammonium and nitrate in the patch soil. The plant roots and shoots exhibited increased levels of 15N over time, indicating a sustained response to the enriched environment. Root transcriptome analysis identified 585 genes differentially regulated 53 hrs after the treatments. Nitrogen metabolism and cell growth genes were induced by the high ammonium (65 ug NH4+-N g-1 soil), while stress response genes were repressed. The complex regulation of specific transporters following the ammonium pulse reflects a simultaneous and synergistic response to rapidly changing concentrations of both forms of inorganic N in the soil patch. Transcriptional analysis of the phosphate transporters demonstrates cross-talk between N and phosphate uptake pathways and suggests that roots increase phosphate uptake via the arbuscular mycorrhizal symbiosis in response to N. Conclusion: This work enhances our understanding of root function by providing a snapshot of the response of the tomato root transcriptome to a pulse of ammonium in a complex soil environment. This response includes an important role for the mycorrhizal symbiosis in the utilization of an N patch. 9 Total samples were analyzed across 3 treatment groups (3 biological replicates per group). We generated the following pairwise comparisons using JMP Genomics software: Control vs. Low N, Control vs. high N, and low N vs. high N. One way ANOVA was used to determine significantly different expression. Genes with an FDRâ¤10% were presented.

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

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