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Small world but large differences: cultivar-specific secondary metabolite-mediated phyllosphere fungal homeostasis in tea plant (Camellia sinensis)

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Abstract

Aims

Phyllosphere microbes are closely linked to plant health and are important for the maintenance of host community stability. Tea plants (Camellia sinensis) can synthesize abundant secondary metabolites (SMs), however, it is unclear how they affect tea plant phyllosphere homeostasis.

Methods

We investigated the effects of secondary metabolites of two tea plant cultivars (Longjing43 and Zhongcha108) that have different levels of resistance to anthracnose on the composition, function, assembly and network of phyllosphere fungi.

Results

We found that the phyllosphere fungal compositions of Longjing43 and Zhongcha108 were distinct, with certain fungal pathogens significantly enriched in the susceptible cultivar Longjing43 (e.g., Fusarium), which had a higher relative abundance of phytopathogenic functional groups. In addition, the phyllosphere fungal community assembly of the resistant cultivar Zhongcha108 with a higher habitat niche breadth was more influenced by stochastic processes. More importantly, the fungal network of Zhongcha108 exhibited higher complexity and stability, indicating a more resilient network structure. Random forest and partial least squares path models revealed that secondary metabolites, fungal community diversity, composition and function essentially determined network stability. (−)-Epigallocatechin-3-gallate (EGCG) and caffeine (CAF) were the most important predictors of phyllosphere fungal network stability in 2018 and 2019, respectively. Rare fungal taxa were particularly important in maintaining phyllosphere homeostasis.

Conclusions

Our study suggests that secondary metabolites may mediate phyllosphere fungal homeostasis in tea plants. These findings highlight the importance of secondary metabolites in shaping the phyllosphere fungal community and provide ideas for regulating plant resistance to pathogenic fungi.

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Data availability

The raw data of ITS amplicon sequencing has been uploaded to NCBI BioProject database under accession number: PRJNA942060. The other data of this study are available from the FigShare: https://doi.org/10.6084/m9.figshare.22770863.

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Acknowledgements

We sincerely thank Xiaoshan Xu and Huimin Zhang for their help with the manuscript figure.

Funding

This study was financially supported by the Zhejiang Provincial Natural Science Foundation (LY22C160001), the Fundamental Research Funds for the Provincial Universities of Zhejiang (2020YQ001), Zhejiang Science and Technology Major Program on Agricultural New Variety Breeding-Tea Plant (2021C02067-7), the Scientific Research and Development Foundation of Zhejiang A & F University (2020FR016; 2021LFR046) and the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2021-TRICAAS).

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  1. Kai Ding and Wuyun Lv contributed equally to this work.

Authors and Affiliations

  1. College of Tea Science and Tea Culture, State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, 311300, Zhejiang, China

    Kai Ding, Wuyun Lv, Hengze Ren, Yuting Zhang, Junhong Zhang, Zaikang Tong & Yuchun Wang

  2. Tea Research Institute, Chinese Academy of Agricultural Sciences/National Center for Tea Improvement/Key Laboratory of Biology, Genetics and breeding of Special Economic Animals and Plants, Ministry of Agriculture and Rural Affairs, Hangzhou, 310008, Zhejiang, China

    Fei Xiong, Xinchao Wang & Yuchun Wang

  3. Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, 50829, Cologne, Germany

    Fei Xiong

  4. Hangzhou, China

    Zaikang Tong, Xinchao Wang & Yuchun Wang

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Contributions

ZKT, XCW, and YCW proposed ideas, designed experiments and supervised the study. KD and WYL performed experiments, analyzed data, and wrote the manuscript. HZR and FX conducted field experiments, collected the data, and performed laboratory analyses. YTZ and JHZ provided critical comments on the study and revised the manuscript. The authors contributed to and approved the final manuscript.

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Correspondence to Zaikang Tong, Xinchao Wang or Yuchun Wang.

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Ding, K., Lv, W., Ren, H. et al. Small world but large differences: cultivar-specific secondary metabolite-mediated phyllosphere fungal homeostasis in tea plant (Camellia sinensis). Plant Soil (2024). https://doi.org/10.1007/s11104-024-06579-w

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