Continental scale deciphering of microbiome networks untangles the phyllosphere homeostasis in tea plant.

INTRODUCTION: 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. OBJECTIVES: 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. METHODS: 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. RESULTS: 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. CONCLUSION: 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.

Host genetic determinants drive compartment-specific assembly of tea plant microbiomes.

Diverse host factors drive microbial variation in plant-associated environments, whereas their genetic mechanisms remain largely unexplored. To address this, we coupled the analyses of plant genetics and microbiomes in this study. Using 100 tea plant (Camellia sinensis) cultivars, the microbiomes of rhizosphere, root endosphere and phyllosphere showed clear compartment-specific assembly, whereas the subpopulation differentiation of tea cultivars exhibited small effects on microbial variation in each compartment. Through microbiome genome-wide association studies, we examined the interactions between tea genetic loci and microbial variation. Notably, genes related to the cell wall and carbon catabolism were heavily linked to root endosphere microbial composition, whereas genes related to the metabolism of metal ions and small organic molecules were overrepresented in association with rhizosphere microbial composition. Moreover, a set of tea genetic variants, including the cytoskeleton-related formin homology interacting protein 1 gene, were strongly associated with the ß-diversity of phyllosphere microbiomes, implying their interactions with the overall structure of microbial communities. Our results create a catalogue of tea genetic determinants interacting with microbiomes and reveal the compartment-specific microbiome assembly driven by host genetics.

L-theanine exuded from Camellia sinensis roots regulates element cycling in soil by shaping the rhizosphere microbiome assembly.

Root exudate metabolites are a key medium for the interaction between plants and soil microbiota. L-theanine is a unique non-protein amino acid critical for the flavor and potential health benefits of tea products; however, its biological function in tea plants is not well understood. As L-theanine is mainly synthesized in the roots of tea plants, we hypothesized that L-theanine could affect the function of the rhizosphere microbiota by modulating microbial assembly. In the present study, L-theanine was detected in the exudates of tea plant roots using liquid chromatography-mass spectrometry. Additionally, 16S rRNA gene sequencing revealed that L-theanine significantly altered the structure of the rhizosphere microbiota and selectively shaped rhizosphere microbial assembly. Moreover, metagenomic data showed that L-theanine affected the abundance of genes encoding element cycling in soil. Interestingly, the denitrification and complete nitrification pathways were significantly inhibited by L-theanine by decreasing the narH, napA, and napB genes abundance. These findings provide new insights into the biological function of L-theanine, as well as the implications of interactions between tea plant root exudates and the rhizosphere microbiome.

Implications of endophytic microbiota in Camellia sinensis: a review on current understanding and future insights.

Endophytic fungi and bacteria are the most ubiquitous and representative commensal members that have been studied so far in various higher plants. Within colonization and interaction with their host plants, endophytic microbiota are reportedly to modulate not only the host's growth but also holobiont resilience to abiotic and biotic stresses, providing a natural reservoir and a promising solution for sustainable agricultural development challenged by global climate change. Moreover, possessing the talent to produce a wide array of high-value natural products, plant endophytic microbiota also serve as an alternative way for novel drug discovery. In this review, tea, one of the world's three largest nonalcoholic beverages and a worldwide economic woody crop, was highlighted in the context of endophytic microbiota. We explore the recent studies regarding isolation approaches, distribution characteristics and diversity, and also biological functions of endophytic microbiota in Camellia sinensis (L.) O. Kuntze. Profoundly, the future insight into interaction mechanism between endophytic microbiota and tea plants will shed light on in-depth exploration of tea microbial resources.