Cai, Jinxiu , Liu, Ying , Yang, Shuwen , Guo, Yong , Zhu, Ziyang
2026-03-01 RHIZOSPHERE 2026 37(卷), null(期), (null页)
Mechanical injury is a widespread and ecologically relevant stress experienced by woody plants, yet the capacity of the root-microbiome interface to buffer such disturbance through metabolic regulation remains poorly quantified. Here, we conducted an in situ manipulative experiment with a root-severance gradient (0, 25%, 50%, 75%, and 100%; n = 3 biological replicates per level) on Populus trees in a semi-arid field environment to investigate the coupled responses of rhizosphere chemistry (rhizosphere soil metabolome) and the rhizosphere microbiome. After a 20-day post-severance equilibration period, we characterized rhizosphere metabolite profiles (untargeted LC-MS) and bacterial communities (16S rRNA sequencing) concurrently. Multiomics integration revealed a non-linear trajectory in rhizosphere reorganization: metabolite composition exhibited a distinct threshold-like transition at approximately 75% root severance, shifting from growth-oriented metabolism to a defense-dominant state (e.g., accumulation of phenolics and isoflavonoids), thereby reshaping rhizosphere chemical niches. This metabolic reprogramming coincided with a synchronous reassembly of the bacterial community (Procrustes m2 = 0.63, P = 0.006), characterized by a stepwise turnover from copiotrophs to stress-tolerant taxa, with a concomitant shift in dominant phyla (e.g., Acidobacteriota). Correlation network analysis further supported a "defense-recruitment" pattern, in which defense-associated specialized metabolites (e.g., terpenoid lactones and phenolics) emerged as topological hubs in co-occurrence networks, coinciding with selective enrichment of stress-tolerant bacterial taxa. Collectively, these findings uncover a threshold-controlled regulatory mode by which woody plant roots coordinate rhizosphere metabolic reprogramming and microbiome assembly in response to mechanical injury, highlighting a critical boundary at which rhizosphere chemical niches and microbial assembly shift states. These insights advance mechanistic understanding of root injury responses and provide a physiological basis for hypothesis-driven manipulation of rhizosphere processes in physically disturbed habitats.