DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Flg22‐induced Ca2+ increases undergo desensitization and resensitization

Journal Article · · Plant, Cell and Environment
DOI: https://doi.org/10.1111/pce.14186 · OSTI ID:1980641
ORCiD logo [1];  [2];  [3];  [2];  [4];  [4];  [5];  [5];  [6];  [7]; ORCiD logo [5]
  1. Zhejiang University, Hangzhou (China); Duke University, Durham, NC (United States); Hangzhou Normal University Hangzhou (China); Shenzhen University, Shenzhen (China); OSTI
  2. Hangzhou Normal University Hangzhou (China)
  3. Zhejiang University, Hangzhou (China); Hangzhou Normal University Hangzhou (China)
  4. Duke University, Durham, NC (United States); Shenzhen University, Shenzhen (China)
  5. Duke University, Durham, NC (United States)
  6. Duke University, Durham, NC (United States); Hangzhou Normal University Hangzhou (China)
  7. Duke University, Durham, NC (United States); Hangzhou Normal University Hangzhou (China); Shenzhen University, Shenzhen (China)

The flagellin epitope flg22, a pathogen-associated molecular pattern (PAMP), binds to the receptor-like kinase FLAGELLIN SENSING2 (FLS2), and triggers Ca2+ influx across the plasma membrane (PM). The flg22-induced increases in cytosolic Ca2+ concentration ([Ca2+]i) (FICA) play a crucial role in plant innate immunity. It's well established that the receptor FLS2 and reactive oxygen species (ROS) burst undergo sensitivity adaptation after flg22 stimulation, referred to as desensitization and resensitization, to prevent over responses to pathogens. However, whether FICA also mount adaptation mechanisms to ensure appropriate and efficient responses against pathogens remains poorly understood. Here, we analysed systematically [Ca2+]i increases upon two successive flg22 treatments, recorded and characterized rapid desensitization but slow resensitization of FICA in Arabidopsis thaliana. Pharmacological analyses showed that the rapid desensitization might be synergistically regulated by ligand-induced FLS2 endocytosis as well as the PM depolarization. The resensitization of FICA might require de novo FLS2 protein synthesis. FICA resensitization appeared significantly slower than FLS2 protein recovery, suggesting additional regulatory mechanisms of other components, such as flg22-related Ca2+ permeable channels. Taken together, we have carefully defined the FICA sensitivity adaptation, which will facilitate further molecular and genetic dissection of the Ca2+-mediated adaptive mechanisms in PAMP-triggered immunity.

Research Organization:
Duke University, Durham, NC (United States)
Sponsoring Organization:
USDOE Office of Science (SC); China Scholarship Council; National Science Foundation (NSF); Chinese National Science Foundation
Grant/Contract Number:
SC0014077
OSTI ID:
1980641
Journal Information:
Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Journal Issue: 12 Vol. 44; ISSN 0140-7791
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (76)

Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation journal May 2006
The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling journal June 2021
Channeling plant immunity journal June 2021
The FLS2-Associated Kinase BIK1 Directly Phosphorylates the NADPH Oxidase RbohD to Control Plant Immunity journal March 2014
The Calcium-Dependent Protein Kinase CPK28 Buffers Plant Immunity and Regulates BIK1 Turnover journal November 2014
The MAP4 Kinase SIK1 Ensures Robust Extracellular ROS Burst and Antibacterial Immunity in Plants journal September 2018
Pattern-recognition receptors in plant innate immunity journal February 2008
Plant–Pathogen Warfare under Changing Climate Conditions journal May 2018
The Receptor Kinases BAK1/SERK4 Regulate Ca2+ Channel-Mediated Cellular Homeostasis for Cell Death Containment journal November 2019
Sensing of molecular patterns through cell surface immune receptors journal August 2017
Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium journal August 1991
MAP kinase signalling cascade in Arabidopsis innate immunity journal February 2002
Adaptation by target remodelling journal April 2012
The plant immune system journal November 2006
OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis journal August 2014
Endocytosis-dependent desensitization and protein synthesis–dependent resensitization in retinal growth cone adaptation journal January 2005
How do plants achieve immunity? Defence without specialized immune cells journal January 2012
Calcium signalling: dynamics, homeostasis and remodelling journal July 2003
Endocytosis and signalling: intertwining molecular networks journal September 2009
Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants journal March 2013
Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx journal July 2019
Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis journal February 2020
Ligand-induced monoubiquitination of BIK1 regulates plant immunity journal April 2020
The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity journal August 2020
Mutual potentiation of plant immunity by cell-surface and intracellular receptors journal March 2021
Pattern-recognition receptors are required for NLR-mediated plant immunity journal March 2021
Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis journal May 2001
Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases journal September 2016
Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination journal February 2018
Phosphorylation-dependent subfunctionalization of the calcium-dependent protein kinase CPK28 journal May 2021
Wind-induced plant motion immediately increases cytosolic calcium. journal June 1992
Agonist- and Ca2+-dependent Desensitization of TRPV1 Channel Targets the Receptor to Lysosomes for Degradation journal June 2012
The calcium-dependent protein kinase CPK28 negatively regulates the BIK1-mediated PAMP-induced calcium burst journal May 2015
Plant organellar calcium signalling: an emerging field journal December 2011
Flagellin Perception Varies Quantitatively in Arabidopsis thaliana and Its Relatives journal January 2012
Defense-Related Calcium Signaling Mutants Uncovered via a Quantitative High-Throughput Screen in Arabidopsis thaliana journal January 2012
Differential regulation of the calcium-dependent protein kinase CPK28 by site-specific modification journal May 2021
Widely Conserved Attenuation of Plant MAMP-Induced Calcium Influx by Bacteria Depends on Multiple Virulence Factors and May Involve Desensitization of Host Pattern Recognition Receptors journal May 2019
Cation Fluxes Cause Plasma Membrane Depolarization Involved in β-Glucan Elicitor-Signaling in Soybean Roots journal September 2005
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis journal March 2006
Plant Receptors Go Endosomal: A Moving View on Signal Transduction journal August 2008
Molecular Steps in the Immune Signaling Pathway Evoked by Plant Elicitor Peptides: Ca2+-Dependent Protein Kinases, Nitric Oxide, and Reactive Oxygen Species Are Downstream from the Early Ca2+ Signal   journal September 2013
Sensitivity to Flg22 Is Modulated by Ligand-Induced Degradation and de Novo Synthesis of the Endogenous Flagellin-Receptor FLAGELLIN-SENSING2 journal November 2013
BRASSINOSTEROID-SIGNALING KINASE1 Phosphorylates MAPKKK5 to Regulate Immunity in Arabidopsis journal February 2018
How Plants Sense and Respond to Stressful Environments journal March 2020
Plant Cyclic Nucleotide-Gated Channels: New Insights on Their Functions and Regulation journal June 2020
The Chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 Activates Multiple Pathogen Resistance Responses journal February 2006
Spatio-Temporal Cellular Dynamics of the Arabidopsis Flagellin Receptor Reveal Activation Status-Dependent Endosomal Sorting journal October 2012
Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition journal March 2017
Cellular Ca 2+ Signals Generate Defined pH Signatures in Plants journal October 2018
Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels: Flagellin-activated ion channels journal January 2010
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
Ca2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades: Minireview journal December 2010
The crossroads of receptor-mediated signaling and endocytosis in plants: Endocytosis and signaling in plants journal August 2018
Advances and current challenges in calcium signaling journal January 2018
Calcium transport across plant membranes: mechanisms and functions journal June 2018
Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex journal October 2013
Alteration of Stimulus-Specific Guard Cell Calcium Oscillations and Stomatal Closing in Arabidopsis det3 Mutant journal September 2000
Identification of a Plant Receptor for Extracellular ATP journal January 2014
Plant “helper” immune receptors are Ca 2+ -permeable nonselective cation channels journal June 2021
Mitogen-Activated Protein Kinase Signaling in Plants journal June 2010
Plant Innate Immunity: Perception of Conserved Microbial Signatures journal June 2012
Reactive Oxygen Species in Plant Signaling journal April 2018
Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling journal April 2018
Defense Priming: An Adaptive Part of Induced Resistance journal April 2017
From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition journal August 2017
A Moving View: Subcellular Trafficking Processes in Pattern Recognition Receptor–Triggered Plant Immunity journal August 2015
MAPK Cascades in Plant Disease Resistance Signaling journal August 2013
THE GENERATION OF Ca 2+ SIGNALS IN PLANTS journal June 2004
A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors journal June 2009
Desensitization of g Protein–Coupled Receptors and Neuronal Functions journal July 2004
Ion Channels in Plants journal October 2012
Microbe-associated molecular pattern-induced calcium signaling requires the receptor-like cytoplasmic kinases, PBL1 and BIK1 journal December 2014
Cell Surface Receptors for Signal Transduction and Ligand Transport: A Design Principles Study journal June 2007
To respond or not to respond, the recurring question in plant mechanosensitivity journal August 2014
Biotic and Abiotic Stresses Activate Different Ca2+ Permeable Channels in Arabidopsis journal January 2017