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.

Temporal metabolite responsiveness of microbiota in the tea plant phyllosphere promotes continuous suppression of fungal pathogens.

INTRODUCTION: A broad spectrum of rhizosphere bacteria and fungi were shown to play a central role for health, fitness and productivity of their host plants. However, implications of host metabolism on microbiota assembly in the phyllosphere and potential consequences for holobiont functioning were sparsely addressed. Previous observations indicated that tea plants might reduce disease occurrence in various forests located in their proximity; the underlying mechanisms and potential implications of the phyllosphere microbiota remained elusive. OBJECTIVES: This study aimed atdeciphering microbiome assembly in the tea plant phyllosphere throughout shoot development as well as elucidating potential implications of host metabolites in this process. The main focus was to explore hidden interconnections between the homeostasis of the phyllosphere microbiome and resistance to fungal pathogens. METHODS: Profiling of host metabolites and microbiome analyses based on high-throughput sequencing were integrated to identify drivers of microbiome assembly throughout shoot development in the phyllosphere of tea plants. This was complemented by tracking of beneficial microorganisms in all compartments of the plant. Synthetic assemblages (SynAss), bioassays and field surveys were implemented to verify functioning of the phyllosphere microbiota. RESULTS: Theophylline and epigallocatechin gallate, two prevalent metabolites at the early and late shoot development stage respectively, were identified as the main drivers of microbial community assembly. Flavobacterium and Myriangium were distinct microbial responders at the early stage, while Parabacteroides and Mortierella were more enriched at the late stage. Reconstructed, stage-specific SynAss suppressed various tree phytopathogens by 13.0%-69.3% in vitro and reduced disease incidence by 8.24%-41.3% in vivo. CONCLUSION: The findings indicate that a functional phyllosphere microbiota was assembled along with development-specific metabolites in tea plants, which continuously suppressed prevalent fungal pathogens. The insights gained into the temporally resolved metabolite response of the tea plant microbiota could provide novel solutions for disease management.

Nonvolatile metabolite alterations during Zijuan black tea processing affect the protective potential on HOECs exposed to nicotine.

Understanding nonvolatile metabolite alterations during processing and their impacts on potential function is crucial for technological innovations in tea manufacturing. In the present work, specific metabolite alterations during Zijuan black tea processing and their potential effects on nicotine-induced human oral epithelial cell (HOEC) injury were investigated. The results showed that leucine, isoleucine, and tyrosine were the main hydrolysis products during withering, and theaflavin-3-gallate (TF-3-G), theaflavin-3'-gallate (TF-3'-G) and theaflavin-3,3'-gallate (TFDG) were mainly formed during rolling. Moreover, oxidation of flavonoid glycosides, catechins and dimeric catechins took place during fermentation. During drying, amino acid conversion became dominant. Meanwhile, processing samples effectively attenuated nicotine-induced oxidative stress and inflammation in HOECs. TF-3'-G, TF-3-G, phenylalanine, and kaempferol-3-coumaroylglucoside exhibited strong associations with protective action, which indicates that modifying the processes in which black tea are produced to be rich in those specific components could be beneficial for the oral health of people who smoke.

Transcriptome and Phytochemical Analysis Reveals the Alteration of Plant Hormones, Characteristic Metabolites, and Related Gene Expression in Tea (Camellia sinensis L.) Leaves During Withering.

Plant hormones play an important role in the chemical metabolism of postharvest plants. However, alterations in plant hormones of postharvest tea and their potential modulation of quality-related metabolites are unknown. In this study, the dynamic alterations of abscisic acid (ABA), salicylic acid (SA), jasmonic acid (JA), and critical metabolites, such as catechins, theanine, and caffeine, in tea leaves were analyzed during withering from 0 to 24 h. It was found that the ABA content increased from 0 to 9 h but decreased thereafter, JA continuously increased, and the SA content showed no significant change. With the exception of gallocatechin (GC) and epicatechin (EC), the amounts of other critical components were significantly reduced at 24 h. Transcriptome analysis showed that compared with 0 h, 2256, 3654, and 1275 differentially expressed genes (DEGs) were identified at 9, 15, and 24 h, respectively. For all comparisons, DEGs corresponding to the pathways of "phenylalanine, tyrosine, and tryptophan biosynthesis" and "phenylalanine metabolism", involved in the biosynthesis of catechins, were significantly enriched. Weighted correlation network analysis (WGCNA) of co-expression genes indicated that many of the modules were only correlated with a specific trait during the withering process; the dark olive-green module, however, was correlated with two traits, ABA and theanine. Our study indicates that withering induced dramatic alterations in gene transcription as well as levels of hormones (ABA, JA, and SA) and important components, and that ABA regulated theanine metabolism during this process.