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BIK1 protein homeostasis is maintained by the interplay of different ubiquitin ligases in immune signaling

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  • Jiaojiao Bai

    (Chinese Academy of Sciences
    Shanghai Jiao Tong University
    Jiujiang University
    University of Chinese Academy of Sciences)

  • Yuanyuan Zhou

    (Chinese Academy of Sciences
    Shanghai Jiao Tong University
    University of Chinese Academy of Sciences)

  • Jianhang Sun

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Kexin Chen

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yufang Han

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Ranran Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yanmin Zou

    (Chinese Academy of Sciences)

  • Mingshuo Du

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Dongping Lu

    (Shanghai Jiao Tong University)

Abstract

Pathogen-associated molecular patterns (PAMPs) trigger plant innate immunity that acts as the first line of inducible defense against pathogen infection. A receptor-like cytoplasmic kinase BOTRYTIS-INDUCED KINASE 1 (BIK1) functions as a signaling hub immediately downstream of multiple pattern recognition receptors (PRRs). It is known that PLANT U-BOX PROTEIN 25 (PUB25) and PUB26 ubiquitinate BIK1 and mediate BIK1 degradation. However, how BIK1 homeostasis is maintained is not fully understood. Here, we show that two closely related ubiquitin ligases, RING DOMAIN LIGASE 1 (RGLG1) and RGLG2, preferentially associate with the hypo-phosphorylated BIK1 and promote the association of BIK1 with the co-receptor for several PRRs, BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1). PUB25 interacts with RGLG2 and mediates its degradation. In turn, RGLG2 represses the ubiquitin ligase activity of PUB25. RGLG1/2 suppress PUB25-mediated BIK1 degradation, promote BIK1 protein accumulation, and positively regulate immune signaling in a ubiquitin ligase activity-dependent manner. Our work reveals how BIK1 homeostasis is maintained by the interplay of different ubiquitin ligases.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40364-0
    DOI: 10.1038/s41467-023-40364-0
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    1. Wang Tian & Congcong Hou & Zhijie Ren & Chao Wang & Fugeng Zhao & Douglas Dahlbeck & Songping Hu & Liying Zhang & Qi Niu & Legong Li & Brian J. Staskawicz & Sheng Luan, 2019. "A calmodulin-gated calcium channel links pathogen patterns to plant immunity," Nature, Nature, vol. 572(7767), pages 131-135, August.
    2. Delphine Chinchilla & Cyril Zipfel & Silke Robatzek & Birgit Kemmerling & Thorsten Nürnberger & Jonathan D. G. Jones & Georg Felix & Thomas Boller, 2007. "A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence," Nature, Nature, vol. 448(7152), pages 497-500, July.
    3. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    4. Kathrin Thor & Shushu Jiang & Erwan Michard & Jeoffrey George & Sönke Scherzer & Shouguang Huang & Julian Dindas & Paul Derbyshire & Nuno Leitão & Thomas A. DeFalco & Philipp Köster & Kerri Hunter & S, 2020. "The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity," Nature, Nature, vol. 585(7826), pages 569-573, September.
    5. 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.
    6. Tsuneaki Asai & Guillaume Tena & Joulia Plotnikova & Matthew R. Willmann & Wan-Ling Chiu & Lourdes Gomez-Gomez & Thomas Boller & Frederick M. Ausubel & Jen Sheen, 2002. "MAP kinase signalling cascade in Arabidopsis innate immunity," Nature, Nature, vol. 415(6875), pages 977-983, February.
    7. DongHyuk Lee & Neeraj K. Lal & Zuh-Jyh Daniel Lin & Shisong Ma & Jun Liu & Bardo Castro & Tania Toruño & Savithramma P. Dinesh-Kumar & Gitta Coaker, 2020. "Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    8. Lingyao Kong & Jinkui Cheng & Yujuan Zhu & Yanglin Ding & Jingjing Meng & Zhizhong Chen & Qi Xie & Yan Guo & Jigang Li & Shuhua Yang & Zhizhong Gong, 2015. "Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases," Nature Communications, Nature, vol. 6(1), pages 1-13, December.
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