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

The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections 1 – 3 . Plant immune receptors include cell surface-resident pattern recognition receptors (PRRs, including receptor-like kinases (RLKs)), and intracellular nucleotide-binding domain le...

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Published inNature plants Vol. 6; no. 9; pp. 1106 - 1115
Main Authors Liu, Jun, Huang, Yanyan, Kong, Liang, Yu, Xiao, Feng, Baomin, Liu, Derui, Zhao, Baoyu, Mendes, Giselle C., Yuan, Peiguo, Ge, Dongdong, Wang, Wen-Ming, Fontes, Elizabeth P. B., Li, Pingwei, Shan, Libo, He, Ping
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.09.2020
Nature Publishing Group
Subjects
13
13/44
14/19
14/35
38/22
38/90
631/449/1659
631/449/1736
631/449/2169
631/449/448
82
82/1
82/29
82/80
82/83
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Autoimmunity
Biomedical and Life Sciences
Cell surface
Dwarfism
F-box protein
Gene Expression Regulation, Plant
Genes, Plant
Genetic screening
Immune system
Innate immunity
Kinases
Letter
Leucine
Life Sciences
MAP kinase
MAP Kinase Signaling System - genetics
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mutation
Nlr protein
Nucleotides
Pattern recognition
Pattern recognition receptors
Phenotypes
Plant Immunity - genetics
Plant Sciences
Proteins
Receptors
RNA-mediated interference
Scaffolding
Signal transduction
Signaling
Suppressors
Ubiquitination
United States > US
Texas
China
Online AccessGet full text

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Abstract The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections 1 – 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 autoimmunity 4 – 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. Plants with loss of function mutations in the MEKK1–MKK1/2–MPK4 MAP kinase pathway show strong autoimmunity phenotypes and dwarfism. Through a suppressor genetic screen, the malectin-like receptor kinase LET1 is identified as a new regulator of immune signalling.
AbstractList The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections . 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 autoimmunity . 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.
The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections1-3. 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 autoimmunity4-9. 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.The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections1-3. 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 autoimmunity4-9. 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.
The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections 1 – 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 autoimmunity 4 – 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. Plants with loss of function mutations in the MEKK1–MKK1/2–MPK4 MAP kinase pathway show strong autoimmunity phenotypes and dwarfism. Through a suppressor genetic screen, the malectin-like receptor kinase LET1 is identified as a new regulator of immune signalling.
Plants have evolved both cell surface-resident receptor-like kinases (RLKs) and intracellular nucleotide-binding leucine-rich repeat (NLR) proteins as immune receptors to detect infections. It remains enigmatic how RLK- and NLR-mediated signaling is connected. Disruption of an immune-activated MEKK1-MKK1/2-MPK4 MAPK cascade activates the NLR SUMM2 via the MAPK kinase kinase MEKK2, leading to autoimmunity. To gain insights into the mechanisms underlying SUMM2 activation, we deployed an RNAi-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 homeostasis caused by the deficiency in immune-activated signaling, and activates the NLR SUMM2-mediated autoimmunity via MEKK2 scaffolding.
The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections1–3. 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 autoimmunity4–9. 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.Plants with loss of function mutations in the MEKK1–MKK1/2–MPK4 MAP kinase pathway show strong autoimmunity phenotypes and dwarfism. Through a suppressor genetic screen, the malectin-like receptor kinase LET1 is identified as a new regulator of immune signalling.
Author Wang, Wen-Ming
Feng, Baomin
Ge, Dongdong
Yuan, Peiguo
Kong, Liang
He, Ping
Yu, Xiao
Fontes, Elizabeth P. B.
Huang, Yanyan
Mendes, Giselle C.
Li, Pingwei
Zhao, Baoyu
Shan, Libo
Liu, Derui
Liu, Jun
AuthorAffiliation 1 Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA
2 Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA
6 These authors contributed equally
4 Department of Plant Pathology & Microbiology, Texas A&M University, College Station, TX 77843, USA
5 National Institute of Science and Technology in Plant-Pest Interactions, and Department of Biochemistry and Molecular Biology, Universidade Federal de Viçosa, Minas Gerais, 36570.000, Brazil
3 State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu 611130, P. R. China
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  organization: Institute for Plant Genomics & Biotechnology, Texas A&M University, Department of Plant Pathology & Microbiology, Texas A&M University
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  surname: Zhao
  fullname: Zhao, Baoyu
  organization: Department of Biochemistry & Biophysics, Texas A&M University
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  surname: Mendes
  fullname: Mendes, Giselle C.
  organization: Institute for Plant Genomics & Biotechnology, Texas A&M University, Department of Biochemistry & Biophysics, Texas A&M University, National Institute of Science and Technology in Plant–Pest Interactions and Department of Biochemistry and Molecular Biology, Universidade Federal de Viçosa
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  organization: Institute for Plant Genomics & Biotechnology, Texas A&M University, Department of Plant Pathology & Microbiology, Texas A&M University
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  surname: Shan
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  orcidid: 0000-0002-5926-8349
  surname: He
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  email: pinghe@tamu.edu
  organization: Institute for Plant Genomics & Biotechnology, Texas A&M University, Department of Biochemistry & Biophysics, Texas A&M University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32839517$$D View this record in MEDLINE/PubMed
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Y.H., J.L., L.S., and P.H. conceived the project, designed experiments and analyzed 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 analyzed data. W.M.W, E.P.B.F., and P.L. analyzed data and provided critical feedback. L.S., and P.H. wrote the manuscript with inputs from all co-authors.
Author Contributions
ORCID 0000-0001-7688-0997
0000-0002-7986-1369
0000-0002-1815-3107
0000-0002-5926-8349
0000-0002-9272-9602
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Snippet The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections 1 – 3 . Plant immune receptors include cell...
The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections . Plant immune receptors include cell...
The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections1–3. Plant immune receptors include cell...
The innate immune system detects pathogen-derived molecules via specialized immune receptors to prevent infections1-3. Plant immune receptors include cell...
Plants have evolved both cell surface-resident receptor-like kinases (RLKs) and intracellular nucleotide-binding leucine-rich repeat (NLR) proteins as immune...
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springer
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SubjectTerms 13
13/44
14/19
14/35
38/22
38/90
631/449/1659
631/449/1736
631/449/2169
631/449/448
82
82/1
82/29
82/80
82/83
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Autoimmunity
Biomedical and Life Sciences
Cell surface
Dwarfism
F-box protein
Gene Expression Regulation, Plant
Genes, Plant
Genetic screening
Immune system
Innate immunity
Kinases
Letter
Leucine
Life Sciences
MAP kinase
MAP Kinase Signaling System - genetics
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mutation
Nlr protein
Nucleotides
Pattern recognition
Pattern recognition receptors
Phenotypes
Plant Immunity - genetics
Plant Sciences
Proteins
Receptors
RNA-mediated interference
Scaffolding
Signal transduction
Signaling
Suppressors
Ubiquitination
Title The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding
URI https://link.springer.com/article/10.1038/s41477-020-0748-6
https://www.ncbi.nlm.nih.gov/pubmed/32839517
https://www.proquest.com/docview/2441669205
https://www.proquest.com/docview/2437121218
https://pubmed.ncbi.nlm.nih.gov/PMC7492416
Volume 6
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