Flavones enrich rhizosphere Pseudomonas to enhance nitrogen utilization and lateral 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, generated metabolite and transcription data for roots and microbiota data for rhizospheres, and conducted comprehensive multi-omics analyses. We demonstrated that the roots of robust Leuce poplar enriched more plant growth-promoting rhizobacteria, which compared with the poorly performing poplar, agreeing with the ‘Matthew effect’ on poplar-microbe interaction. Moreover, we confirmed that Pseudomonas was strongly associated with tricin and apigenin biosynthesis and identified that gene GL3 was critical for tricin secretion. The elevated tricin secretion via constitutive transcription of PopGL3 and PopCHS4 could drive Pseudomonas colonization in the rhizosphere and further enhance poplar growth, nitrogen acquisition, and lateral root development in nitrogen-poor soil. This study reveals 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.