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[Display omitted] • The critical mechanisms underlying the microbiome assembly in the tea plants are revealed. • There is a trade-off between stochastic and deterministic processes in microbiome assembly in the tea plants. • Assembly processes were dominated by deterministic processes in bulk and rhizosphere soils. • The stochastic processes in roots and leaves was critically driven by amino acids for environmental selection. • The core taxa assembled in phyllosphere could attenuate the virulence of a prevalent foliar pathogen. Assembly and co-occurrence of the host co-evolved microbiota are essential ecological and evolutionary processes, which is not only crucial for managing individual plant fitness but also ecological function. However, understanding of the microbiome assembly and co-occurrence in higher plants is not well understood. The tea plant was shown to contribute the forest fitness due to the microbiome assembled in the phyllosphere; the landscape of microbiome assembly in the tea plants and its potential implication on phyllosphere homestasis still remains untangled. This study aimed to deciphering of the microbiome networks of the tea plants at a continental scale. It would provide fundamental insights into the factors driving the microbiome assembly, with an extended focus on the resilience towards the potential pathogen in the phyllosphere. We collected 225 samples from 45 locations spanning approximately 2000-km tea growing regions across China. By integration of high-throughput sequencing data, physicochemical properties profiling and bioinformatics analyses, we investigated continental scale microbiome assembly and co-occurrence in the tea plants. Synthetic assemblages, interaction assay and RT-qPCR were further implemented to analyze the microbial interaction indexed in phyllosphere. A trade-off between stochastic and deterministic processes in microbiomes community assembly was highlighted. Assembly processes were dominated by deterministic processes in bulk and rhizosphere soils, and followed by stochastic processes in roots and leaves with amino acids as critical drivers for environmental selection. Sphingobacteria and Proteobacteria ascended from soils to leaves to sustain a core leaf taxa. The core taxa formed a close association with a prevalent foliar pathogen in the co-occurrence network and significantly attenuated the expression of a set of essential virulence genes in pathogen. Our study unveils the mechanism underpinning microbiome assembly in the tea plants, and a potential implication of the microbiome-mediated resilience framework on the phyllosphere homeostasis. [ABSTRACT FROM AUTHOR]

The increasing input of fungicides has emerged as a global concern for agroecosystem stability and sustainability. Agroecosystem resilience has been linked to microbiome response, however, is not well understood. Focusing on a widespread triazole-class fungicide triadimefon in the paddy ecosystem, we characterized that the soils and sediments were dominant triadimefon reservoirs with the peak level at 195 μg kg−1 and 31.3 μg kg−1, respectively, but essential for the resilience of paddy ecosystem to triadimefon. In paddy simulation models, the half-life of triadimefon in soil-sediment was 8.4–28.9 days, while it was prolonged to 86.6–115.5 days after elimination of resident microbial community. Phospholipid fatty acid profiling and high-throughput sequencing showed that the distinctive bacterial community responses contributed to variable degradation of triadimefon in paddy soils and sediments. Sphingomonas and Xanthomonas were identified as positive responders of the keystone taxa in the responsive bacteriome, whereas Enterobacter were negative responders that declined over time. Synthetic assemblages combined with quantitative polymerase chain reaction further validated that Sphingomonas and Xanthomonas were involved in sustaining soil-sediment resilience to triadimefon contamination. Collectively, our results revealed that the shaping of soil and sediment bacteriomes was responsible for the resilience of the paddy agroecosystem to fungicide contamination. [Display omitted] • The resilience of the paddy ecosystem to triadimefon was dominantly conferred by the soils and sediments. • The resilience in paddy soils and sediments was associated with bacterial community. • Distinctive bacteriome responses to triadimefon were observed between paddy soils and sediments. • The keystone taxa of triadimefon-responsive bacteriome were characterized in paddy soils and sediments. [ABSTRACT FROM AUTHOR]