CsPRMT5-mediated histone H4R3 dimethylation negatively regulates resistance to gray blight in tea plants (Camellia sinensis L.)

Abstract

Gray blight is a serious foliar disease that significantly threatens tea plant cultivation. Although dynamic histone methylation was reported in regulating plant immunity, the specific roles of this epigenetic modification in tea plant disease resistance have yet to be fully elucidated. This study demonstrates that the protein arginine methyltransferase CsPRMT5, which catalyzes the symmetric dimethylation of histone H4R3 (H4R3sme2), is involved in the tea plant response to gray blight. Transcription of CsPRMT5 and the level of histone H4R3 methylation in tea were downregulated following infection by the fungal pathogen Pseudopestalotiopsis (Ps). A negative correlation was observed between the resistance of tea plants to Ps and the expression level of CsPRMT5 across various cultivars. Downregulation of CsPRMT5 expression led to reduced H4R3sme2 levels, elevated expression of defense-related genes, and lower reactive oxygen species (ROS) production after Ps infection, thus enhancing pathogen resistance of tea. Furthermore, complementation of Atprmt5 mutant with CsPRMT5 restored the susceptibility to Ps infection in Arabidopsis. Chromatin Immunoprecipitation Sequencing (ChIP-seq)and Chromatin Immunoprecipitation quantitative PCR (ChIP-qPCR) analyses revealed that CsPRMT5 binds to defense-related genes, including CsMAPK3, and regulates their expression through H4R3sme2 modification. Collectively, the results indicate that CsPRMT5 negatively regulates the immune response to pathogens through repressing CsMAPK3 expression in tea plants.

Acknowledgements

We thank Chaoling Wei (State Key Laboratory of Tea Plant Biology and Utilization) for kindly providing Ps strain. This research was supported by the National Natural Science Foundation of China (32072624, 32402622, 32402623), the National Key R&D Program of China (2021YFD1601101), the Postdoctoral Fellowship Program of CPSF under Grant Number GZC20240006 and China Postdoctoral Science Foundation (2024 M750020), the Open Fund of State Key Laboratory of Tea Plant Biology and Utilization, SKLTOF20220115.

Author contributions

H.P. and Y.W. made equal contributions to this work. Z.Z. and F.W. formulated the study and devised the experiments. The experiments were conducted by H.P., Y.W., B.Z., and M.H. H.P. and Z.Z. authored the manuscript. All writers evaluated and sanctioned the final manuscript.

Data availability

The data presented in this study are available on request from the corresponding author. The raw transcriptome data have been deposited in the National Center for Biotechnology Information bioproject database under the accession number PRJNA1223124 for the RNA-seq (CsPRMT5 suppression in tea plants) and PRJNA1223117 for the ChIP-seq data, respectively.

Conflict of interest statement

None declared.

Supplementary data

Supplementary data is available at Horticulture Research online.

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