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Drought is a major threat to crop productivity and causes decreased plant growth, poor yields, and crop failure. Nevertheless, the frequency of droughts is expected to increase in the coming decades. The microbial communities associated with crop plants can influence how plants respond to various stresses; hence, microbiome manipulation is fast becoming an effective strategy for improving the stress tolerance of plants. The effect of drought stress on the root microbiome of perennial woody plants is currently poorly understood. Using Populus trees as a model ecosystem, we found that the diversity of the root microbial community decreased during drought treatment and that compositional shifts in microbes during drought stress were driven by the relative abundances of a large number of dominant phyla, including Actinobacteria, Firmicutes, and Proteobacteria. A subset of microbes, including Streptomyces rochei, Bacillus arbutinivorans, B. endophyticus, B. megaterium, Aspergillus terreus, Penicillium raperi, Trichoderma ghanense, Gongronella butleri, and Rhizopus stolonifer, was isolated from the drought-treated poplar rhizosphere soils, which have potentially beneficial to plant fitness. Further controlled inoculation experiments showed that the isolated bacterial and fungal isolates positively impacted plant growth and drought tolerance. Collectively, our results demonstrate the impact of drought on root microbiome structure and provide a novel example of manipulating root microbiomes to improve plant tolerance.

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Root microbiota composition shifts during the development of most annual plants. Although some perennial plants can live for centuries, the host-microbiome partnerships and interaction mechanisms underlying their longevity remain unclear.To address this gap, we investigated age-related changes in the root metabolites, transcriptomes, and microbiome compositions of 1-to 35-yr-old Populus tomentosa trees.Ten co-response clusters were obtained according to their accumulation patterns, and members of each cluster displayed a uniform and clear pattern of abundance. Multi-omics network analysis demonstrated that the increased abundance of Actinobacteria with tree age was strongly associated with the flavonoid biosynthesis. Using genetic approaches, we demonstrate that the flavonoid biosynthesis regulator gene Transparent Testa 8 is associated with the recruitment of flavonoid-associated Actinobacteria. Further inoculation experiments of Actinobacteria isolates indicated that their colonization could significantly improve the host's phenotype. Site-directed mutagenesis revealed that the hyBl gene cluster, involved in biosynthesis of an aminocyclitol hygromycin B analog in Streptomyces isolate bj1, is associated with disease suppression.We hypothesize that interactions between perennial plants and soil microorganisms lead to gradual enrichment of a subset of microorganisms that may harbor a wealth of currently unknown functional traits.