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

Ping Xu; Erinne Stirling; Hengtong Xie; Wenbing Li; Xiaofei Lv; Haruna Matsumoto; Haiyan Cheng; Anan Xu; Wanyi Lai; Yuefei Wang; Zuntao Zheng; Mengcen Wang; Xingmei Liu; Bin Ma; Jianming Xu

doi:10.1016/j.jare.2022.04.002

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

J Adv Res. 2023 Feb:44:13-22. doi: 10.1016/j.jare.2022.04.002. Epub 2022 Apr 16.

Authors

Ping Xu¹, Erinne Stirling², Hengtong Xie¹, Wenbing Li³, Xiaofei Lv⁴, Haruna Matsumoto⁵, Haiyan Cheng¹, Anan Xu¹, Wanyi Lai¹, Yuefei Wang¹, Zuntao Zheng⁶, Mengcen Wang⁷, Xingmei Liu⁸, Bin Ma⁹, Jianming Xu⁸

Affiliations

¹ Department of Tea Science, Zhejiang University, Hangzhou 310058, China.
² College of Environmental and Natural Resource Sciences, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou 310058, China; Acid Sulfate Soils Centre, School of Biological Sciences, The University of Adelaide, Adelaide 5005, Australia.
³ Key Laboratory of Hangzhou City for Ecosystem Protection and Restoration, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, PR China.
⁴ Department of Environmental Engineering, China Jiliang University, Hangzhou 310018, China.
⁵ Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Zhejiang University, Hangzhou 310058, China.
⁶ Institute for the Control of Agrochemicals, Ministry of Agriculture and Rural Affairs, Beijing 100125, China.
⁷ Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Zhejiang University, Hangzhou 310058, China. Electronic address: wmctz@zju.edu.cn.
⁸ College of Environmental and Natural Resource Sciences, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou 310058, China.
⁹ College of Environmental and Natural Resource Sciences, Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Zhejiang University, Hangzhou 310058, China; Hangzhou Innovation Center, Zhejiang University, Hangzhou 311200, China. Electronic address: bma@zju.edu.cn.

Abstract

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.

Keywords: Co-occurrence; Homeostasis; Microbiome assembly; Phyllosphere; Tea plant; Trade-off.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Microbiota*
Plants
Rhizosphere
Soil
Tea

Substances

Soil
Tea