Large-scale multi-omics unveils host-microbiome interactions driving root development and nitrogen acquisition

The microbiome influences the performance and fitness of the host plant. Nevertheless, the biotic interaction between host genetic variation, gene regulation and the impact of the microbiome on the host phenotype remain unknown. Here, we generated 1,341 paired datasets, including root transcriptomes, rhizosphere prokaryotic taxa, and root ionomes, to conduct multi-omics analyses of the host-microbe associations at the root-soil interface using 175 rapeseed ( Brassica napus L.) ecotypes that were resequenced and evaluated at two field environments. We observed the high prediction ability of nitrogen uptake, with a prediction accuracy of 0.67, accounting for about 45% of the variance in nitrogen levels among natural ionomic variations. This significant proportion of explained variance was driven by the overall transcriptome-wide gene expression and 203 highly heritable microbial amplicon sequence variants (ASVs). These microbial variations were strongly associated with root nitrogen uptake, underscoring the role of the microbiome in plant nutrition. We also identified significant genome-wide associations for the 203 heritable ASVs at multiple genetic loci, regulated by eQTL hotspots, particularly those involved in carbon and nitrogen metabolism. These associations involved a dominant bacterial genus, Sphingopyxis , which exhibited a strong gene regulatory effect on its variation, regulated by the eQTL hotspots. In addition, we performed high-throughput bacterial cultivation from rapeseed roots and subjected the isolated bacterial isolate to whole-genome sequencing. Finally, targeted plant metabolite profiling of auxin biosynthesis and root confocal imaging assays demonstrated that Sphingopyxis regulates lateral root development and impacts plant nitrogen nutrition. These results suggest a host-microbiome regulatory effect that connects bacterial abundance with plant root architecture and nutrient acquisition. In summary, this study reveals the genetic basis of host-microbiome trait associations across transcriptional, nutritional and environmental domains and suggests that the potential of bacterial microbiome might have consistent effects on root development with implications towards the breeding of nutrient-efficient crops.