Keystone taxa of phyllosphere microbiome confer resistance to citrus bacterial canker in pomelo via multiple mechanisms

doi:10.1111/jipb.70273

• Research Article • Next Articles

Keystone taxa of phyllosphere microbiome confer resistance to citrus bacterial canker in pomelo via multiple mechanisms

Weina Yuan^1,2†, Zengwei Feng^3†, Wei Zhang¹, Yang Liu³, Yang Zhou³, Yongqiang Qin³, Yang Bai⁴, Honghui Zhu^3* and Qing Yao^1*

1. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (South China), Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Guangdong Engineering Research Center for Litchi, College of Horticulture, South China Agricultural University, Ministry of Agriculture and Rural Affairs, Guangzhou 510642, China
2. School of Horticulture, Xinyang Agriculture and Forestry University, Xinyang 464100, China
3. Key Laboratory of Agricultural Microbiomics and Precision Application (MARA), Key Laboratory of Agricultural Microbiome (MARA), State Key Laboratory of Applied Microbiology Southern China, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, China
4. Peking-Tsinghua Center for Life Sciences, College of Life Sciences, Peking University, Beijing 100871, China
^†These authors contributed equally to this work.
^*Correspondences: Qing Yao (yaoqscau@scau.edu.cn, Dr. Yao is fully responsible for distributions of all materials associated with this article); Honghui Zhu (zhuhh@gdim.cn)

Received:2025-07-11 Accepted:2026-04-03 Online:2026-04-28
Supported by:
This study was supported by the National Key Research and Development Program of China (2022YFF1001800), the open competition program of top ten critical priorities of Agricultural Science and Technology Innovation for the 14th Five-Year Plan of Guangdong Province (2022SDZG09, 2023SDZG09, and 2024KJ19), the Guangdong Strategic Special Fund for Rural Revitalization (2022-440000-43010104-9463), and the Guangdong Special Support Program (2021JC06N628).

Abstract

Abstract: Citrus bacterial canker (CBC) is a globally important citrus disease caused by Xanthomonas citri subsp. citri (Xcc). Increasing evidence shows that the plant microbiome is crucial for host growth performance and health maintenance, among which the keystone taxa stand out due to their indispensable roles in microbiome homeostasis. However, how keystone taxa in the phyllosphere microbiome contribute to disease resistance remains unclear. In this study, we characterized the phyllosphere bacterial community of pomelo across an annual cycle and found that amino acids in leaves were the main drivers of the bacterial community structure. Meanwhile, five OTUs were identified as keystone taxa. A total of 587 phyllosphere bacterial strains were isolated, among which six strains belonging to Methylobacterium, Sphingomonas, Massilia, and Paenibacillus were identified as the corresponding keystone strains. We further constructed a consortium with these six strains to test its role in controlling CBC in planta. Network analysis reveals that consortium inoculation increased the phyllosphere bacterial community stability, whereas Xcc inoculation decreased it. However, dual inoculation of the consortium and Xcc restored community stability compared to the control. Interestingly, the inoculated keystone strains, if not all, still appeared as keystone taxa in the microbiomes of the control, consortium inoculation, and dual inoculation treatments, but not in the Xcc-inoculated treatment. Moreover, the consortium inoculation significantly increased the defense-related enzyme activities such as PPO, POD, and PAL in leaves, suggesting a triggered plant immune response. In vitro assays indicated that these keystone strains showed either antagonistic activity against Xcc or siderophore-producing activity. Finally, the consortium inoculation significantly reduced the disease index by 78% in planta. Taken together, these results suggest that the keystone taxa of the phyllosphere microbiome can confer disease resistance to the host via multiple mechanisms, especially by maintaining phyllosphere microbiome homeostasis.

Key words: citrus bacterial canker, disease resistance, keystone strains, microbiome homeostasis, phyllosphere microbiome, Xanthomonas citri subsp. Citri

Weina Yuan, Zengwei Feng, Wei Zhang, Yang Liu, Yang Zhou, Yongqiang Qin, Yang Bai, Honghui Zhu, Qing Yao. Keystone taxa of phyllosphere microbiome confer resistance to citrus bacterial canker in pomelo via multiple mechanisms[J]. J Integr Plant Biol., DOI: 10.1111/jipb.70273.

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Keystone taxa of phyllosphere microbiome confer resistance to citrus bacterial canker in pomelo via multiple mechanisms

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