Rhizosphere Functional Plasticity and the Keystone Taxon Sphingomonas Facilitate Sweet Cherry Adaptation to Semi-Arid Stress

Translocation of elite cultivars across distinct climatic regions often induces transplantation shock. Although the rhizosphere microbiome can facilitate host acclimation, the underlying functional mechanisms remain unclear. Here, we investigated microbiome-mediated adaptation in “Hongdeng” sweet cherry (Prunus avium L.) moved from a humid coastal region (Dalian, DL) to a semi-arid inland habitat (Hohhot, HS). We integrated plant physiological assays, metagenomic sequencing, and structural equation modeling (SEM) to compare the source population (DL), the introduced population (HS), and a locally acclimated reference cultivar (“Summit”, HSY). The introduced trees adjusted physiologically to the semi-arid environment by elevating proline levels and antioxidant enzyme activities. Although environmental stress reduced microbial alpha diversity, the core taxonomic framework persisted. Community assembly analysis indicated that the semi-arid climate intensified environmental filtering. Network analysis identified Sphingomonas as a keystone taxon; notably, it maintained a highly connected topological role despite a stable relative abundance. Furthermore, structural equation modeling showed that the environmental stress index positively correlated with the upregulation of microbial DNA repair pathways (R = 0.81, p < 0.001). Ultimately, the SEM demonstrated that environmental stress primarily shapes microbial functional profiles rather than driving species turnover, thereby contributing to host adaptation. The successful establishment of introduced sweet cherry in semi-arid regions is tied more closely to rhizosphere functional plasticity than to taxonomic restructuring. These findings highlight the role of the keystone taxon Sphingomonas in maintaining rhizosphere homeostasis, offering a theoretical framework for targeted microbiome engineering to mitigate transplant shock and enhance crop resilience.