PagMYB74 orchestrates flavonoid-mediated plant-microbe feedback for drought resilience in poplar

The interactions between plants and the soil microbiome play critical roles in regulating plant resistance to stresses. However, the process partly results from the complex interaction between root exudates and microbes, a relationship that remains poorly understood. Here, we investigated the interconnected responses of the root microbiome associated with the perennial tree Populus under drought stress. This was achieved via molecular genetics approaches and multi-omics analyses, combined with integrative comparisons of microbiome structure against both the host plant's metabolomic profiles and transcriptomic data, using samples collected over a 13-wk period of progressive drought treatment. We demonstrate that progressive drought triggers a phased transcriptional cascade in roots, culminating in the activation of a flavonoid biosynthesis program. Moreover, we confirm that Pseudomonas is strongly associated with flavonoid biosynthesis and identify that gene PagMYB74 is critical for quercetin and kaempferol secretion. We further found that Pseudomonas putida S110 colonization establishes positive feedback through enhanced phenylpropanoid metabolism and activation of nutrient transport pathways in PagMYB74-overexpressing plants, reinforcing the symbiotic interaction. Our findings establish a complete mechanistic continuum from a single host gene to metabolite-driven recruitment and symbiotic reprogramming, facilitating the improvement of environmental adaptation by regulating their interaction with beneficial soil microorganisms.