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Ligand-induced monoubiquitination of BIK1 regulates plant immunity

Author

Listed:
  • Xiyu Ma

    (Texas A&M University
    Texas A&M University)

  • Lucas A. N. Claus

    (Ghent University
    Center for Plant Systems Biology, VIB)

  • Michelle E. Leslie

    (University of Missouri-Columbia
    Elemental Enzymes)

  • Kai Tao

    (Oregon State University)

  • Zhiping Wu

    (St Jude Children’s Research Hospital
    St Jude Children’s Research Hospital)

  • Jun Liu

    (Texas A&M University
    Texas A&M University)

  • Xiao Yu

    (Texas A&M University
    Texas A&M University)

  • Bo Li

    (Texas A&M University
    Texas A&M University)

  • Jinggeng Zhou

    (Texas A&M University
    Texas A&M University)

  • Daniel V. Savatin

    (Ghent University
    Center for Plant Systems Biology, VIB)

  • Junmin Peng

    (St Jude Children’s Research Hospital
    St Jude Children’s Research Hospital)

  • Brett M. Tyler

    (Oregon State University)

  • Antje Heese

    (University of Missouri-Columbia)

  • Eugenia Russinova

    (Ghent University
    Center for Plant Systems Biology, VIB)

  • Ping He

    (Texas A&M University
    Texas A&M University)

  • Libo Shan

    (Texas A&M University
    Texas A&M University)

Abstract

Recognition of microbe-associated molecular patterns (MAMPs) by pattern recognition receptors (PRRs) triggers the first line of inducible defence against invading pathogens1–3. Receptor-like cytoplasmic kinases (RLCKs) are convergent regulators that associate with multiple PRRs in plants4. The mechanisms that underlie the activation of RLCKs are unclear. Here we show that when MAMPs are detected, the RLCK BOTRYTIS-INDUCED KINASE 1 (BIK1) is monoubiquitinated following phosphorylation, then released from the flagellin receptor FLAGELLIN SENSING 2 (FLS2)–BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) complex, and internalized dynamically into endocytic compartments. The Arabidopsis E3 ubiquitin ligases RING-H2 FINGER A3A (RHA3A) and RHA3B mediate the monoubiquitination of BIK1, which is essential for the subsequent release of BIK1 from the FLS2–BAK1 complex and activation of immune signalling. Ligand-induced monoubiquitination and endosomal puncta of BIK1 exhibit spatial and temporal dynamics that are distinct from those of the PRR FLS2. Our study reveals the intertwined regulation of PRR–RLCK complex activation by protein phosphorylation and ubiquitination, and shows that ligand-induced monoubiquitination contributes to the release of BIK1 family RLCKs from the PRR complex and activation of PRR signalling.

Suggested Citation

  • Xiyu Ma & Lucas A. N. Claus & Michelle E. Leslie & Kai Tao & Zhiping Wu & Jun Liu & Xiao Yu & Bo Li & Jinggeng Zhou & Daniel V. Savatin & Junmin Peng & Brett M. Tyler & Antje Heese & Eugenia Russinova, 2020. "Ligand-induced monoubiquitination of BIK1 regulates plant immunity," Nature, Nature, vol. 581(7807), pages 199-203, May.
  • Handle: RePEc:nat:nature:v:581:y:2020:i:7807:d:10.1038_s41586-020-2210-3
    DOI: 10.1038/s41586-020-2210-3
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    Citations

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    Cited by:

    1. Sha Tang & Zhiying Zhao & Xiaotong Liu & Yi Sui & Dandan Zhang & Hui Zhi & Yuanzhu Gao & Hui Zhang & Linlin Zhang & Yannan Wang & Meicheng Zhao & Dongdong Li & Ke Wang & Qiang He & Renliang Zhang & We, 2023. "An E2-E3 pair contributes to seed size control in grain crops," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Jiaojiao Bai & Yuanyuan Zhou & Jianhang Sun & Kexin Chen & Yufang Han & Ranran Wang & Yanmin Zou & Mingshuo Du & Dongping Lu, 2023. "BIK1 protein homeostasis is maintained by the interplay of different ubiquitin ligases in immune signaling," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Chen Bai & Gao-Jie Wang & Xiao-Hui Feng & Qiong Gao & Wei-Qing Wang & Ran Xu & Su-Jie Guo & Shao-Yan Shen & Ming Ma & Wen-Hui Lin & Chun-Ming Liu & Yunhai Li & Xian-Jun Song, 2024. "OsMAPK6 phosphorylation and CLG1 ubiquitylation of GW6a non-additively enhance rice grain size through stabilization of the substrate," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Hui Shi & Junjie Yin & Zhangjie Zhao & Hong Yu & Hong Yi & Li Xu & Huimin Tong & Min He & Xiaobo Zhu & Xiang Lu & Qing Xiong & Weitao Li & Yongyan Tang & Qingqing Hou & Li Song & Long Wang & Xiaoqiong, 2024. "Fine-tuning of IPA1 transactivation activity by E3 ligase IPI7-mediated non-proteolytic K29-ubiquitination during Magnaporthe oryzae infection," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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