Multi-omics integration uncovers terpenoid-centered plant-microbe interactions underpinning the adaptive resilience of Thuja sutchuenensis

Understanding the interaction among metabolites, microbes, and gene regulation is crucial for deciphering plant adaptation in extreme habitats . Here, we integrated metabolomic, metagenomic, and transcriptomic analyses to investigate the terpenoid-centered plant-microbe interactions of the endangered conifer Thuja sutchuenensis across natural, restored, and cultivated populations . LC-MS/MS profiling revealed that natural populations accumulate higher levels of terpenoids, flavonoids, and phenolic derivatives . Metagenomic analysis showed that Actinobacteria- and Bradyrhizobium-dominated microbial communities were functionally enriched in terpenoid-backbone, monoterpenoid, and xenobiotic-degradation pathways, indicating strong microbial specialization within the limestone rhizosphere . Transcriptomic profiling of roots showed coordinated alterations of key pathway genes ( HMGR , DXS , SQE1 , SS1 , and VTE4 ) . These transcriptional changes were accompanied by the expression of downstream oxidoreductases and cytochrome P450s, supporting terpenoid diversification and antioxidant capacity . Cross-omics correlation networks revealed strong associations among terpenoid-related genes, metabolites, and Actinobacteria taxa, highlighting a metabolic feedback loop that links microbial symbiosis with host secondary metabolism . Integrative analyses further suggested that wild populations maintain a more complex and functionally interconnected host-microbe system than cultivated ones . Collectively, these findings uncover a finely tuned plant-microbe-metabolite regulatory network that underpins the adaptive plasticity of T. sutchuenensis and provide a molecular framework for microbiome-assisted conservation, restoration, and sustainable management of this relict conifer species . • Integrated metabolomic, metagenomic, and transcriptomic analysis of T. sutchuenensis. • Natural roots showed enriched terpenoids and flavonoids under limestone stress. • Actinobacteria and Bradyrhizobium dominated terpenoid-related microbial networks. • Multi-omics correlations revealed plant–microbe–metabolite feedback adaptation.