Flavones enrich rhizosphere <i>Pseudomonas</i> to enhance nitrogen utilization and secondary root growth in Populus

Plant growth behavior is a function of genetic network architecture. The importance of root microbiome variation driving plant functional traits is increasingly recognized, but the genetic mechanisms governing this variation are less studied. Here, we collected roots and rhizosphere soils from nine Populus species belonging to four sections (Leuce, Aigeiros, Tacamahaca, and Turanga), generated metabolite and transcription data for roots and microbiota data for rhizospheres, and conducted comprehensive multi-omics analyses. We demonstrated that the roots of vigorous Leuce poplar enriched more Pseudomonas, compared with the poorly performing poplar. Moreover, we confirmed that Pseudomonas was strongly associated with tricin and apigenin biosynthesisand identified that gene GLABRA3 (GL3) was critical for tricin secretion. The elevated tricin secretion via constitutive transcription of PopGL3 and Chalcone synthase (PopCHS4) could drive Pseudomonas colonization in the rhizosphere and further enhance poplar growth, nitrogen acquisition, and secondary root development in nitrogen-poor soil. This study revealed plant-metabolite-microbe regulation patterns contribute to the poplar fitness and thoroughly decoded the key regulatory mechanisms of tricin, and provided new insights into the interactions of the plant’s key metabolites with its transcriptome, rhizosphere microbes.