Direct Modulation of Heterotrimeric G Protein-coupled Signaling by a Receptor Kinase Complex*

Plants and some protists have heterotrimeric G protein complexes that activate spontaneously without canonical G protein-coupled receptors (GPCRs). In Arabidopsis, the sole 7-transmembrane regulator of G protein signaling 1 (AtRGS1) modulates the G protein complex by keeping it in the resting state (GDP-bound). However, it remains unknown how a myriad of biological responses is achieved with a single G protein modulator. We propose that in complete contrast to G protein activation in animals, plant leucine-rich repeat receptor-like kinases (LRR RLKs), not GPCRs, provide this discrimination through phosphorylation of AtRGS1 in a ligand-dependent manner. G protein signaling is directly activated by the pathogen-associated molecular pattern flagellin peptide 22 through its LRR RLK, FLS2, and co-receptor BAK1.

[1]  Alan M. Jones,et al.  Cell-free translation and purification of Arabidopsis thaliana regulator of G signaling 1 protein. , 2016, Protein expression and purification.

[2]  K. Shimamoto,et al.  Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis , 2016, EMBO Reports.

[3]  She Chen,et al.  Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor , 2016, eLife.

[4]  Jia Li,et al.  Nucleocytoplasmic trafficking is essential for BAK1- and BKK1-mediated cell-death control. , 2016, The Plant journal : for cell and molecular biology.

[5]  K. Chung,et al.  Structural mechanism of G protein activation by G protein-coupled receptor. , 2015, European journal of pharmacology.

[6]  A. Pioszak,et al.  Structural insights into ligand recognition and selectivity for classes A, B, and C GPCRs. , 2015, European journal of pharmacology.

[7]  C. Zipfel,et al.  Regulation of the NADPH Oxidase RBOHD During Plant Immunity. , 2015, Plant & cell physiology.

[8]  Xiaofeng Wang,et al.  An autophosphorylation site database for leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. , 2015, The Plant journal : for cell and molecular biology.

[9]  C. Zipfel,et al.  Importance of tyrosine phosphorylation in receptor kinase complexes. , 2015, Trends in plant science.

[10]  K. Shimamoto,et al.  Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis , 2014, EMBO reports.

[11]  Z. Lou,et al.  Assessment of BAK1 activity in different plant receptor-like kinase complexes by quantitative profiling of phosphorylation patterns. , 2014, Journal of proteomics.

[12]  T. Stehle,et al.  BIR2 affects complex formation of BAK1 with ligand binding receptors in plant defense , 2014, Plant signaling & behavior.

[13]  Alan M. Jones,et al.  Heterotrimeric G protein-coupled signaling in plants. , 2014, Annual review of plant biology.

[14]  C. Zipfel,et al.  Plant PRRs and the activation of innate immune signaling. , 2014, Molecular cell.

[15]  Timothy C. Elston,et al.  Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit , 2014, Cell.

[16]  Y. Saijo,et al.  The Arabidopsis PEPR pathway couples local and systemic plant immunity , 2014, EMBO Journal.

[17]  B. Je,et al.  The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size , 2013, Nature.

[18]  H. Dohlman,et al.  Regulation of Yeast G Protein Signaling by the Kinases That Activate the AMPK Homolog Snf1 , 2013, Science Signaling.

[19]  Xiangzong Meng,et al.  MAPK cascades in plant disease resistance signaling. , 2013, Annual review of phytopathology.

[20]  Alan M. Jones,et al.  Heterotrimeric G protein signalling in the plant kingdom , 2013, Open Biology.

[21]  O. Dong,et al.  Heterotrimeric G Proteins Serve as a Converging Point in Plant Defense Signaling Activated by Multiple Receptor-Like Kinases1[C][W][OA] , 2013, Plant Physiology.

[22]  Alan M. Jones,et al.  “Round Up the Usual Suspects”: A Comment on Nonexistent Plant G Protein-Coupled Receptors1[C][W] , 2013, Plant Physiology.

[23]  Alan M. Jones,et al.  Endocytosis of Seven-Transmembrane RGS Protein Activates G- protein Coupled Signaling in Arabidopsis , 2012, Nature Cell Biology.

[24]  Alan M. Jones,et al.  G Protein Activation without a GEF in the Plant Kingdom , 2012, PLoS genetics.

[25]  J. Botella,et al.  Gγ1+Gγ2+Gγ3=Gβ: the search for heterotrimeric G-protein γ subunits in Arabidopsis is over. , 2012, Journal of plant physiology.

[26]  E. Danchin,et al.  An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease. , 2011, Plant, cell & environment.

[27]  D. Ren,et al.  BON1 interacts with the protein kinases BIR1 and BAK1 in modulation of temperature-dependent plant growth and cell death in Arabidopsis. , 2011, The Plant journal : for cell and molecular biology.

[28]  Alexandra M. E. Jones,et al.  The Arabidopsis Leucine-Rich Repeat Receptor–Like Kinases BAK1/SERK3 and BKK1/SERK4 Are Required for Innate Immunity to Hemibiotrophic and Biotrophic Pathogens[W] , 2011, Plant Cell.

[29]  H. Dohlman,et al.  Cell Cycle-dependent Phosphorylation and Ubiquitination of a G Protein α Subunit* , 2011, The Journal of Biological Chemistry.

[30]  L. Graves,et al.  Regulation of Human Cytidine Triphosphate Synthetase 2 by Phosphorylation* , 2010, The Journal of Biological Chemistry.

[31]  S. Postel,et al.  The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. , 2010, European journal of cell biology.

[32]  T. Boller,et al.  Rapid Heteromerization and Phosphorylation of Ligand-activated Plant Transmembrane Receptors and Their Associated Kinase BAK1* , 2010, The Journal of Biological Chemistry.

[33]  She Chen,et al.  Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. , 2009, Cell host & microbe.

[34]  S. He,et al.  The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. , 2008, The Plant journal : for cell and molecular biology.

[35]  Xiaofeng Wang,et al.  Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. , 2008, Developmental cell.

[36]  Alan M. Jones,et al.  GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling , 2007, Proceedings of the National Academy of Sciences.

[37]  Jia Li,et al.  BAK1 and BKK1 Regulate Brassinosteroid-Dependent Growth and Brassinosteroid-Independent Cell-Death Pathways , 2007, Current Biology.

[38]  J. Goedhart,et al.  Plant G protein heterotrimers require dual lipidation motifs of Gα and Gγ and do not dissociate upon activation , 2006, Journal of Cell Science.

[39]  Eric Reiter,et al.  GRKs and β-arrestins: roles in receptor silencing, trafficking and signaling , 2006, Trends in Endocrinology & Metabolism.

[40]  D. Robinson,et al.  Plant Retromer, Localized to the Prevacuolar Compartment and Microvesicles in Arabidopsis, May Interact with Vacuolar Sorting Receptors[W] , 2006, The Plant Cell Online.

[41]  T. Boller,et al.  The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception[W] , 2005, The Plant Cell Online.

[42]  L. Jordá,et al.  ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. , 2005, The Plant journal : for cell and molecular biology.

[43]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

[44]  A. Diévart,et al.  LRR-containing receptors regulating plant development and defense , 2003, Development.

[45]  Alan M. Jones,et al.  A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation , 2003, Science.

[46]  S. Shiu,et al.  Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis1[w] , 2003, Plant Physiology.

[47]  Jianming Li,et al.  BRI1/BAK1, a Receptor Kinase Pair Mediating Brassinosteroid Signaling , 2002, Cell.

[48]  Jia Li,et al.  BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates Brassinosteroid Signaling , 2002, Cell.

[49]  E. Liscum,et al.  A mutant Arabidopsis heterotrimeric G-protein beta subunit affects leaf, flower, and fruit development. , 2001, The Plant cell.

[50]  E. Liscum,et al.  A Mutant Arabidopsis Heterotrimeric G-Protein β Subunit Affects Leaf, Flower, and Fruit Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010315. , 2001, The Plant Cell Online.

[51]  T. Boller,et al.  Both the Extracellular Leucine-Rich Repeat Domain and the Kinase Activity of FLS2 Are Required for Flagellin Binding and Signaling in Arabidopsis , 2001, Plant Cell.

[52]  T. Wieland,et al.  Species- and tissue-dependent diversity of G-protein beta subunit phosphorylation: evidence for a cofactor. , 1996, The Biochemical journal.

[53]  Alan M. Jones,et al.  Cautions in Measuring In Vivo Interactions Using FRET and BiFC in Nicotiana benthamiana. , 2016, Methods in molecular biology.

[54]  W. Schulze,et al.  The plant kinome. , 2015, Methods in molecular biology.

[55]  Alan M. Jones,et al.  “Round up the usual suspects” A Comment on Nonexistent Plant GPCRs , 2013 .

[56]  K. Torii.  Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. , 2004, International review of cytology.

[57]  S R Sprang,et al.  G protein mechanisms: insights from structural analysis. , 1997, Annual review of biochemistry.