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  3. The antagonistic role of an E3 ligase pair in regulating plant NLR-mediated autoimmunity and fungal pathogen resistance

The antagonistic role of an E3 ligase pair in regulating plant NLR-mediated autoimmunity and fungal pathogen resistance

  • Cell Host Microbe. 2024 Jul 10;32(7):1114-1128.e10. doi: 10.1016/j.chom.2024.06.004.
Jun Liu 1,  Yong Yang 2,  Fausto Andres Ortiz-Morea 3,  Yulu Zhou 4,  Derui Liu 5,  Yanyan Huang 2,  Jiarui Zheng 6,  Yan Chen 6,  Liang Kong 7,  Zunyong Liu 7,  Dongdong Ge 2,  Mingli Yong 2,  Wenwei Lin 2,  Eugenia Russinova 8,  Libo Shan 7,  Ping He 9
Affiliations

Affiliations

  • 1 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, China.
  • 2 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA.
  • 3 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; Department of Molecular, Cellular, & Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA; Amazonian Research Center Cimaz-Macagual, University of the Amazon, Florencia 180002622, Colombia.
  • 4 Department of Molecular, Cellular, & Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA.
  • 5 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; Department of Plant Biotechnology & Bioinformatics, Ghent University, and Center for Plant Systems Biology, VIB, Ghent 9052, Belgium.
  • 6 State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, China.
  • 7 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; Department of Molecular, Cellular, & Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA.
  • 8 Department of Plant Biotechnology & Bioinformatics, Ghent University, and Center for Plant Systems Biology, VIB, Ghent 9052, Belgium.
  • 9 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; Department of Molecular, Cellular, & Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: pinghemi@umich.edu.
PMID: 38955187 DOI: 10.1016/j.chom.2024.06.004
Abstract

Plant immune homeostasis is achieved through a balanced immune activation and suppression, enabling effective defense while averting autoimmunity. In Arabidopsis, disrupting a mitogen-activated protein (MAP) kinase cascade triggers nucleotide-binding leucine-rich-repeat (NLR) SUPPRESSOR OF mkk1/2 2 (SUMM2)-mediated autoimmunity. Through an RNAi screen, we identify PUB5, a putative plant U-box E3 Ligase, as a critical regulator of SUMM2-mediated autoimmunity. In contrast to typical E3 Ligases, PUB5 stabilizes CRCK3, a calmodulin-binding receptor-like cytoplasmic kinase involved in SUMM2 activation. A closely related E3 Ligase, PUB44, functions oppositely with PUB5 to degrade CRCK3 through monoubiquitylation and internalization. Furthermore, CRCK3, highly expressed in roots and conserved across plant species, confers resistance to Fusarium oxysporum, a devastating soil-borne Fungal pathogen, in both Arabidopsis and cotton. These findings demonstrate the antagonistic role of an E3 Ligase pair in fine-tuning kinase proteostasis for the regulation of NLR-mediated autoimmunity and highlight the function of autoimmune activators in governing plant root immunity against Fungal pathogens.

Keywords

E3 ligase; autoimmunity; fungal pathogen; protein kinase; proteostasis; ubiquitylation.

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