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The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding

Nature Plants volume 6, pages 1106–1115 (2020)Cite this article

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Abstract

The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections1,2,3. Plant immune receptors include cell surface-resident pattern recognition receptors (PRRs, including receptor-like kinases (RLKs)), and intracellular nucleotide-binding domain leucine-rich repeat proteins (NLRs). It remains enigmatic how RLK- and NLR-mediated signalling are connected. Disruption of an immune-activated MEKK1–MKK1/2–MPK4 MAPK cascade activates the NLR SUMM2 via the MAPK kinase kinase MEKK2, leading to autoimmunity4,5,6,7,8,9. To gain insights into the mechanisms underlying SUMM2 activation, we used an RNA interference-based genetic screen for mekk1 autoimmune suppressors and identified an uncharacterized malectin-like RLK, named LETUM1 (LET1), as a specific regulator of mekk1–mkk1/2–mpk4 autoimmunity via complexing with both SUMM2 and MEKK2. MEKK2 scaffolds LET1 and SUMM2 for protein stability and association, and counter-regulates the F-box protein CPR1-mediated SUMM2 ubiquitination and degradation, thereby regulating SUMM2 accumulation and activation. Our study indicates that malectin-like RLK LET1 senses the perturbance of cellular homoeostasis caused by the deficiency in immune-activated signalling and activates the NLR SUMM2-mediated autoimmunity via MEKK2 scaffolding.

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Fig. 1: The let1 mutants suppress autoimmunity triggered by silencing MEKK1.
Fig. 2: LET1 functions genetically downstream of MEKK2 and upstream of SUMM2 in cell death control.
Fig. 3: MEKK2 stabilizes LET1 and SUMM2 and promotes cell death.
Fig. 4: MEKK2 counter-regulates CPR1-mediated SUMM2 ubiquitination and degradation.

Data availability

Original data that support the findings of this study are available from the corresponding author upon request. Source data are provided with this paper.

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Acknowledgements

We thank the ABRC for Arabidopsis T-DNA insertion library and various mutant seeds. We thank P. Krysan (University of Wisconsin, United States), Y. Zhang (University of British Columbia, Canada) and J. Hua (Cornell University, United States) for Arabidopsis seeds. We thank C. Franck and C. Zipfel for the critical reading of the manuscript and members of the laboratories of L.S. and P.H. for discussions and comments on the experiments. The work was supported by National Institutes of Health (NIH) grant no. R01GM092893 and National Science Foundation (NSF) grant no. MCB-1906060 to P.H. and NIH grant no. R01GM097247 and the Robert A. Welch Foundation grant no. A-1795 to L.S. Y.H. and D.G. were partially supported by China Scholarship Council (CSC) and G.C.M was partially supported by INCT/CNPq Fellowship, Brazil.

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  1. These authors contributed equally: Jun Liu, Yanyan Huang.

Authors and Affiliations

  1. Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX, USA

    Jun Liu, Yanyan Huang, Liang Kong, Xiao Yu, Baomin Feng, Derui Liu, Giselle C. Mendes, Peiguo Yuan, Dongdong Ge, Libo Shan & Ping He

  2. Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX, USA

    Jun Liu, Yanyan Huang, Liang Kong, Baomin Feng, Baoyu Zhao, Giselle C. Mendes, Pingwei Li & Ping He

  3. State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, P. R. China

    Yanyan Huang & Wen-Ming Wang

  4. Department of Plant Pathology & Microbiology, Texas A&M University, College Station, TX, USA

    Xiao Yu, Derui Liu, Peiguo Yuan, Dongdong Ge & Libo Shan

  5. National Institute of Science and Technology in Plant–Pest Interactions and Department of Biochemistry and Molecular Biology, Universidade Federal de Viçosa, Viçosa, Brazil

    Giselle C. Mendes & Elizabeth P. B. Fontes

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Contributions

Y.H., J.L., L.S. and P.H. conceived the project, designed experiments and analysed data. J.L., Y.H., L.K., X.Y., B.F., D.L., B.Z., G.C.M., P.Y. and D.G. performed experiments and analysed data. W.M.W, E.P.B.F. and P.L. analysed data and provided critical feedback. L.S. and P.H. wrote the manuscript with inputs from all authors.

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Correspondence to Ping He.

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Liu, J., Huang, Y., Kong, L. et al. The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding. Nat. Plants 6, 1106–1115 (2020). https://doi.org/10.1038/s41477-020-0748-6

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