Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Differential regulation of G protein signaling in Arabidopsis through two distinct pathways that internalize AtRGS1

Journal Article · · Science Signaling
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [3];  [4];  [5];  [6]
  1. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
  2. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA., Department of Biochemistry and Molecular Biology/Bioagro, Universidade Federal de Viçosa, Viçosa, MG, Brazil.
  3. School of Agriculture and Food Science, University of Queensland, St. Lucia, Queensland Q4072, Australia.
  4. Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
  5. Department of Horticulture, University of Wisconsin Madison, Madison, WI 53706, USA.
  6. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA., Department of Pharmacology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.

In animals, endocytosis of a seven-transmembrane GPCR is mediated by arrestins to propagate or arrest cytoplasmic G protein–mediated signaling, depending on the bias of the receptor or ligand, which determines how much one transduction pathway is used compared to another. In Arabidopsis thaliana , GPCRs are not required for G protein–coupled signaling because the heterotrimeric G protein complex spontaneously exchanges nucleotide. Instead, the seven-transmembrane protein AtRGS1 modulates G protein signaling through ligand-dependent endocytosis, which initiates derepression of signaling without the involvement of canonical arrestins. Here, we found that endocytosis of AtRGS1 initiated from two separate pools of plasma membrane: sterol-dependent domains and a clathrin-accessible neighborhood, each with a select set of discriminators, activators, and candidate arrestin-like adaptors. Ligand identity (either the pathogen-associated molecular pattern flg22 or the sugar glucose) determined the origin of AtRGS1 endocytosis. Different trafficking origins and trajectories led to different cellular outcomes. Thus, in this system, compartmentation with its associated signalosome architecture drives biased signaling.

Sponsoring Organization:
USDOE
Grant/Contract Number:
FG02-05ER15671
OSTI ID:
1812769
Alternate ID(s):
OSTI ID: 1849582
Journal Information:
Science Signaling, Journal Name: Science Signaling Journal Issue: 695 Vol. 14; ISSN 1945-0877
Publisher:
American Association for the Advancement of Science (AAAS)Copyright Statement
Country of Publication:
United States
Language:
English

References (107)

Luciferase Complementation Assay for Protein-Protein Interactions in Plants: Luciferase Complementation Assay for Protein-Protein Interactions journal March 2018
Long-distance communication in Arabidopsis involving a self-activating G protein journal February 2018
High-level production of the non-cariogenic sucrose isomer palatinose in transgenic tobacco plants strongly impairs development journal August 2001
A short amino acid sequence able to specify nuclear location journal December 1984
Identification of a signal for rapid export of proteins from the nucleus journal August 1995
The influence of bound GDP on the kinetics of guanine nucleotide binding to G proteins. journal June 1986
Molecular Architecture and Functional Model of the Endocytic AP2 Complex journal May 2002
Structural basis for engineering of retinoic acid receptor isotype-selective agonists and antagonists journal August 1999
Fls2 journal June 2000
Sugar transporters in higher plants – a diversity of roles and complex regulation journal July 2000
Decoy receptor 3: A pleiotropic immunomodulator and biomarker for inflammatory diseases, autoimmune diseases and cancer journal April 2011
A Large-Scale Conformational Change Couples Membrane Recruitment to Cargo Binding in the AP2 Clathrin Adaptor Complex journal June 2010
Reciprocal Encoding of Signal Intensity and Duration in a Glucose-Sensing Circuit journal February 2014
Structural Mechanism for Cargo Recognition by the Retromer Complex journal December 2016
Clathrin-Mediated Constitutive Endocytosis of PIN Auxin Efflux Carriers in Arabidopsis journal March 2007
d -Glucose sensing by a plasma membrane regulator of G signaling protein, At RGS1 journal September 2008
Constitutive expression of clathrin hub hinders elicitor-induced clathrin-mediated endocytosis and defense gene expression in plant cells journal July 2012
Live Cell Imaging with R-GECO1 Sheds Light on flg22- and Chitin-Induced Transient [Ca 2+ ] cyt Patterns in Arabidopsis journal August 2015
Dynamic and diverse sugar signaling journal October 2016
Subcellular Organization of GPCR Signaling journal February 2018
Endocytosis and its regulation in plants journal June 2015
μ-Opioid receptor desensitization by β-arrestin-2 determines morphine tolerance but not dependence journal December 2000
MAP kinase signalling cascade in Arabidopsis innate immunity journal February 2002
Arabidopsis G‐protein interactome reveals connections to cell wall carbohydrates and morphogenesis journal January 2011
A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex journal December 2008
Sugar transporters for intercellular exchange and nutrition of pathogens journal November 2010
Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis journal September 2012
Fluorescent castasterone reveals BRI1 signaling from the plasma membrane journal May 2012
Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification journal June 2016
Phospho-selective mechanisms of arrestin conformations and functions revealed by unnatural amino acid incorporation and 19F-NMR journal September 2015
Fiji: an open-source platform for biological-image analysis journal June 2012
Biased signalling: from simple switches to allosteric microprocessors journal January 2018
Teaching old receptors new tricks: biasing seven-transmembrane receptors journal May 2010
The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain journal May 2006
Ligand-triggered de-repression of Arabidopsis heterotrimeric G proteins coupled to immune receptor kinases journal March 2018
Phosphorylation-induced conformation of β2-adrenoceptor related to arrestin recruitment revealed by NMR journal January 2018
Disruption of endocytosis through chemical inhibition of clathrin heavy chain function journal April 2019
Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane journal October 1998
Plants have a sensitive perception system for the most conserved domain of bacterial flagellin: Plants perceive a conserved domain of bacterial flagellin journal May 1999
Activation and targeting of extracellular signal-regulated kinases by  -arrestin scaffolds journal February 2001
Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2 -cargo complexes journal July 2006
GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling journal October 2007
 -arrestin- but not G protein-mediated signaling by the "decoy" receptor CXCR7 journal December 2009
Distinct cortical and striatal actions of a β-arrestin–biased dopamine D2 receptor ligand reveal unique antipsychotic-like properties journal December 2016
Functional desensitization of the isolated beta-adrenergic receptor by the beta-adrenergic receptor kinase: potential role of an analog of the retinal protein arrestin (48-kDa protein). journal December 1987
Direct Modulation of Heterotrimeric G Protein-coupled Signaling by a Receptor Kinase Complex journal May 2016
β-Arrestins Regulate Protease-activated Receptor-1 Desensitization but Not Internalization or Down-regulation journal January 2002
Differential G-protein-coupled Receptor Phosphorylation Provides Evidence for a Signaling Bar Code journal April 2011
Functional Reconstitution of an Atypical G Protein Heterotrimer and Regulator of G Protein Signaling Protein (RGS1) from Arabidopsis thaliana journal February 2011
Mechanisms Governing the Endosomal Membrane Recruitment of the Core Retromer in Arabidopsis journal January 2013
Protease-activated Receptor-4 Signaling and Trafficking Is Regulated by the Clathrin Adaptor Protein Complex-2 Independent of β-Arrestins journal August 2016
Tyrphostin A23 Inhibits Internalization of the Transferrin Receptor by Perturbing the Interaction between Tyrosine Motifs and the Medium Chain Subunit of the AP-2 Adaptor Complex journal April 2003
β-Arrestin–Dependent Endocytosis of Proteinase-Activated Receptor 2 Is Required for Intracellular Targeting of Activated Erk1/2 journal March 2000
Flagellin peptide flg22 gains access to long-distance trafficking in Arabidopsis via its receptor, FLS2 journal March 2017
Heterotrimeric G protein signaling in plant immunity journal November 2018
Arabidopsis Heterotrimeric G-protein Regulates Cell Wall Defense and Resistance to Necrotrophic Fungi journal January 2012
Growth–Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness journal August 2014
Heterotrimeric G protein signalling in the plant kingdom journal March 2013
Metabolizable and Non-Metabolizable Sugars Activate Different Signal Transduction Pathways in Tomato journal April 2002
Isomaltulose Is Actively Metabolized in Plant Cells journal October 2011
The Endocytosis of Cellulose Synthase in Arabidopsis Is Dependent on μ2, a Clathrin-Mediated Endocytosis Adaptin journal July 2013
Sensitivity to Flg22 Is Modulated by Ligand-Induced Degradation and de Novo Synthesis of the Endogenous Flagellin-Receptor FLAGELLIN-SENSING2 journal November 2013
Glucose and Disaccharide-Sensing Mechanisms Modulate the Expression of α-amylase in Barley Embryos journal July 2000
The Sucrose Analog Palatinose Leads to a Stimulation of Sucrose Degradation and Starch Synthesis When Supplied to Discs of Growing Potato Tubers journal April 2001
PBL13 is a serine/threonine protein kinase that negatively regulates Arabidopsis immune responses. journal October 2015
Differential Regulation of Clathrin and Its Adaptor Proteins during Membrane Recruitment for Endocytosis journal March 2016
The β-Subunit of the Arabidopsis G Protein Negatively Regulates Auxin-Induced Cell Division and Affects Multiple Developmental Processes journal January 2003
Sugar Sensing and Signaling in Plants journal May 2002
Plant Retromer, Localized to the Prevacuolar Compartment and Microvesicles in Arabidopsis , May Interact with Vacuolar Sorting Receptors journal March 2006
The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception journal December 2005
Heterotrimeric G Protein γ Subunits Provide Functional Selectivity in Gβγ Dimer Signaling in Arabidopsis journal April 2007
Remorin, a Solanaceae Protein Resident in Membrane Rafts and Plasmodesmata, Impairs Potato virus X Movement journal May 2009
Single-Molecule Analysis of PIP2;1 Dynamics and Partitioning Reveals Multiple Modes of Arabidopsis Plasma Membrane Aquaporin Regulation   journal October 2011
A Membrane Microdomain-Associated Protein, Arabidopsis Flot1, Is Involved in a Clathrin-Independent Endocytic Pathway and Is Required for Seedling Development journal May 2012
Adaptor Protein Complex 2–Mediated Endocytosis Is Crucial for Male Reproductive Organ Development in Arabidopsis journal August 2013
Clathrin and Membrane Microdomains Cooperatively Regulate RbohD Dynamics and Activity in Arabidopsis journal April 2014
Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns: Calcium signalling in Arabidopsis innate immunity journal July 2011
Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes journal December 1989
The Heterotrimeric G-protein Complex Modulates Light Sensitivity in Arabidopsis thaliana Seed Germination journal July 2009
BAK1‐mediated phosphorylation of canonical G protein alpha during flagellin signaling in Arabidopsis journal October 2019
Alteration of cell wall xylan acetylation triggers defense responses that counterbalance the immune deficiencies of plants impaired in the β‐subunit of the heterotrimeric G‐protein journal September 2017
Vacuolar Protein Sorting 26C encodes an evolutionarily conserved large retromer subunit in eukaryotes that is important for root hair growth in Arabidopsis thaliana journal April 2018
A Förster resonance energy transfer sensor for live‐cell imaging of mitogen‐activated protein kinase activity in A rabidopsis journal January 2019
A G Protein-Biased Ligand at the μ -Opioid Receptor Is Potently Analgesic with Reduced Gastrointestinal and Respiratory Dysfunction Compared with Morphine journal January 2013
Phosphorylation of G Protein-Coupled Receptors: From the Barcode Hypothesis to the Flute Model journal February 2017
A Seven-Transmembrane RGS Protein That Modulates Plant Cell Proliferation journal September 2003
Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex journal October 2013
beta-Arrestin: a protein that regulates beta-adrenergic receptor function journal June 1990
An Antagonist Decoy Receptor and a Death Domain-Containing Receptor for TRAIL journal August 1997
Interaction of tyrosine-based sorting signals with clathrin-associated proteins journal September 1995
The Crystal Structure of a Self-Activating G Protein   Subunit Reveals Its Distinct Mechanism of Signal Initiation journal February 2011
Distinct Phosphorylation Sites on the  2-Adrenergic Receptor Establish a Barcode That Encodes Differential Functions of  -Arrestin journal August 2011
Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom journal September 2016
Genetic evidence that β-arrestins are dispensable for the initiation of β 2 -adrenergic receptor signaling to ERK journal June 2017
G protein–coupled receptor kinases (GRKs) orchestrate biased agonism at the β 2 -adrenergic receptor journal August 2018
Plant Receptor-Like Kinase Gene Family: Diversity, Function, and Signaling journal December 2001
Comparative Protein Structure Modeling of Genes and Genomes journal June 2000
On the origins of arrestin and rhodopsin journal January 2008
Roles of AP-2 in Clathrin-Mediated Endocytosis journal May 2010
Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes journal February 2017
Dose-Duration Reciprocity for G protein activation: Modulation of kinase to substrate ratio alters cell signaling journal December 2017
A simple microfluidic device for live cell imaging of Arabidopsis cotyledons, leaves, and seedlings journal June 2018
Cellular reprogramming through mitogen-activated protein kinases journal October 2015
Photosynthate Regulation of the Root System Architecture Mediated by the Heterotrimeric G Protein Complex in Arabidopsis journal August 2016
Predicted Functional Implications of Phosphorylation of Regulator of G Protein Signaling Protein in Plants journal August 2017
Optimization and Utilization of Agrobacterium-mediated Transient Protein Production in Nicotiana journal January 2014
Biased signalling: from simple switches to allosteric microprocessors journal January 2018

Similar Records

VPS26 Moonlights as an Arrestin-like Adapter for a 7-transmembrane RGS 2 protein in Arabidopsis thaliana
Technical Report · Mon Mar 06 23:00:00 EST 2023 · OSTI ID:1959926

VPS26 Moonlights as a β-Arrestin-like Adapter for a 7-Transmembrane RGS Protein in Arabidopsis thaliana
Journal Article · Sun Oct 27 20:00:00 EDT 2024 · Biochemistry · OSTI ID:2475196

Related Subjects