The tRNA thiolation-mediated translational control is essential for plant immunity

  1. Xueao Zheng
  2. Hanchen Chen
  3. Zhiping Deng
  4. Yujing Wu
  5. Linlin Zhong
  6. Chong Wu
  7. Xiaodan Yu
  8. Qiansi Chen
  9. Shunping Yan  Is a corresponding author
  1. Huazhong Agricultural University, China
  2. ZheJiang Academy of Agricultural Sciences, China
  3. Zhengzhou Tobacco Research Institute of CNTC, China

Abstract

Plants have evolved sophisticated mechanisms to regulate gene expression to activate immune responses against pathogen infections. However, how the translation system contributes to plant immunity is largely unknown. The evolutionarily conserved thiolation modification of tRNA ensures efficient decoding during translation. Here we show that tRNA thiolation is required for plant immunity in Arabidopsis. We identify a cgb mutant that is hyper-susceptible to the pathogen Pseudomonas syringae. CGB encodes ROL5, a homolog of yeast NCS6 required for tRNA thiolation. ROL5 physically interacts with CTU2, a homolog of yeast NCS2. Mutations in either ROL5 or CTU2 result in loss of tRNA thiolation. Further analyses reveal that both transcriptome and proteome reprogramming during immune responses are compromised in cgb. Notably, the translation of salicylic acid receptor NPR1 is reduced in cgb, resulting in compromised salicylic acid signaling. Our study not only reveals a regulatory mechanism for plant immunity but also uncovers an additional biological function of tRNA thiolation.

Data availability

RNA sequencing datasets have been deposited to GSE database (https://www.ncbi.nlm.nih.gov/geo/) with an accession number GSE183087. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the iProX partner repository with the dataset identifier PXD028189. Data analysis scripts are available on GitHub: https://github.com/XueaoZHENG/cgb_project. Source data files has provided for Figure 1B, 1D, 1E, 2D, 2E, 3B, 3C, Figure 4, and Figure 5.

Article and author information

Author details

  1. Xueao Zheng

    College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Hanchen Chen

    College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zhiping Deng

    Institute of Virology and Biotechnology, ZheJiang Academy of Agricultural Sciences, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9663-3088
  4. Yujing Wu

    College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Linlin Zhong

    Key Laboratory of Horticultural Plant Biology, Huazhong Agricultural University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1908-1413
  6. Chong Wu

    College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Xiaodan Yu

    College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Qiansi Chen

    Zhengzhou Tobacco Research Institute of CNTC, Zhengzhou, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2800-5703
  9. Shunping Yan

    College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China
    For correspondence
    spyan@mail.hzau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3665-1310

Funding

National Natural Science Foundation of China (31970311 and 32270306)

  • Shunping Yan

HZAU-AGIS Cooperation Fund (SZYJY2022004)

  • Shunping Yan

National Natural Science Foundation of China (32000373)

  • Xiaodan Yu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2024, Zheng et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Xueao Zheng
  2. Hanchen Chen
  3. Zhiping Deng
  4. Yujing Wu
  5. Linlin Zhong
  6. Chong Wu
  7. Xiaodan Yu
  8. Qiansi Chen
  9. Shunping Yan
(2024)
The tRNA thiolation-mediated translational control is essential for plant immunity
eLife 13:e93517.
https://doi.org/10.7554/eLife.93517

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https://doi.org/10.7554/eLife.93517