Sensitivity to Flg22 Is Modulated by Ligand-Induced Degradation and de Novo Synthesis of the Endogenous Flagellin-Receptor FLAGELLIN-SENSING2

Smith, John L.; Salamango, Daniel J.; Leslie, Michelle E.; Collins, Carina A.; Heese, Antje

doi:10.1104/pp.113.229179

Cited by 131 publications

(161 citation statements)

References 74 publications

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“…S7F). These results suggest that clathrin is not required for the transient activation of MAPKs, and are consistent with previous results obtained from chemical interference and drp2b mutants (11,28). Although it is possible that both clathrin depletion in N. benthamiana leaves and chc2 knockout in Arabidopsis do not fully inhibit endocytosis, our data suggest that plasma membrane-resident FLS2 is sufficient to induce transient MAPK activation.…”

Section: Resultssupporting

confidence: 82%

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Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases

Mbengue

Bourdais

Gervasi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

175

213

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Sensing of potential pathogenic bacteria is of critical importance for immunity. In plants, this involves plasma membrane-resident pattern recognition receptors, one of which is the FLAGELLIN SENSING 2 (FLS2) receptor kinase. Ligand-activated FLS2 receptors are internalized into endosomes. However, the extent to which these spatiotemporal dynamics are generally present among pattern recognition receptors (PRRs) and their regulation remain elusive. Using live-cell imaging, we show that at least three other receptor kinases associated with plant immunity, PEP RECEPTOR 1/2 (PEPR1/2) and EF-TU RECEPTOR (EFR), internalize in a ligand-specific manner. In all cases, endocytosis requires the coreceptor BRI1-ASSOCIATED KINASE 1 (BAK1), and thus depends on receptor activation status. We also show the internalization of liganded FLS2, suggesting the transport of signaling competent receptors. Trafficking of activated PRRs requires clathrin and converges onto the same endosomal vesicles that are also shared with the hormone receptor BRASSINOSTERIOD INSENSITIVE 1 (BRI1). Importantly, clathrin-dependent endocytosis participates in plant defense against bacterial infection involving FLS2-mediated stomatal closure and callose deposition, but is uncoupled from activation of the flagellin-induced oxidative burst and MAP kinase signaling. In conclusion, immunity mediated by pattern recognition receptors depends on clathrin, a critical component for the endocytosis of signaling competent receptors into a common endosomal pathway.pattern-triggered immunity | clathrin | FLS2 | PEPR1 | EFR

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Section: Resultssupporting

confidence: 82%

“…This induces trafficking of FLS2 into the late endosomal pathway and is associated with receptor degradation (10,11). Induced trafficking into late endosomes was also observed for the receptor-like proteins Cf-4 and LeEix2, which recognize fungal Avr4 and xylanase, respectively (12,13).…”

mentioning

confidence: 92%

Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases

Mbengue

Bourdais

Gervasi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

175

213

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“…The TAMRA-pep1 localization correlated with the expression pattern of the PEPR1-GFP protein. TAMRA-pep1 and PEPR-GFP were simultaneously internalized and transported to the vacuole, most probably as a mechanism to desensitize cells after the AtPep1 stimulation, as reported for other ligands (8,25). Interestingly, the temporal dynamics of the AtPep1-PEPR complexes differed from those of BR-BRI1, which internalize very rapidly (8), but were similar to those of the FLS2 receptor (7).…”

Section: Discussionmentioning

confidence: 72%

Danger-associated peptide signaling in Arabidopsis requires clathrin

Ortiz-Morea

Savatin

Dejonghe

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

108

107

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The Arabidopsis thaliana endogenous elicitor peptides (AtPeps) are released into the apoplast after cellular damage caused by pathogens or wounding to induce innate immunity by direct binding to the membrane-localized leucine-rich repeat receptor kinases, PEP RECEPTOR1 (PEPR1) and PEPR2. Although the PEPR-mediated signaling components and responses have been studied extensively, the contributions of the subcellular localization and dynamics of the active PEPRs remain largely unknown. We used live-cell imaging of the fluorescently labeled and bioactive pep1 to visualize the intracellular behavior of the PEPRs in the Arabidopsis root meristem. We found that AtPep1 decorated the plasma membrane (PM) in a receptor-dependent manner and cointernalized with PEPRs. Trafficking of the AtPep1-PEPR1 complexes to the vacuole required neither the trans-Golgi network/early endosome (TGN/EE)-localized vacuolar H + -ATPase activity nor the function of the brefeldin A-sensitive ADP-ribosylation factor-guanine exchange factors (ARF-GEFs). In addition, AtPep1 and different TGN/EE markers colocalized only rarely, implying that the intracellular route of this receptor-ligand pair is largely independent of the TGN/EE. Inducible overexpression of the Arabidopsis clathrin coat disassembly factor, Auxilin2, which inhibits clathrin-mediated endocytosis (CME), impaired the AtPep1-PEPR1 internalization and compromised AtPep1-mediated responses. Our results show that clathrin function at the PM is required to induce plant defense responses, likely through CME of cell surface-located signaling components.Arabidopsis | clathrin | endogenous peptides | PEPR | endocytosis

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“…One possible explanation is if the duration of MAPK activation may be more a function of the signal input from the receptors. It is known that FLS2, the receptor for flagellin, is removed via endocytosis between 30 and 60 min after PAMP treatment, which has been proposed as a mechanism for attenuating PAMP signaling (Smith et al, 2014). It is not clear how UV-B activates MAPKs, as the MKP1-dependent misregulation of the MAPKs is independent of the UVR8 photoreceptor , but is has been proposed that the activation results from cellular damage when UV-B protection is not sufficient.…”

Section: Mkp1 Stabilization Likely Confers a Negative Feedback Loop Umentioning

confidence: 90%

Phosphorylation of Arabidopsis MAP Kinase Phosphatase 1 (MKP1) Is Required for PAMP Responses and Resistance against Bacteria

et al. 2017

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Plants perceive potential pathogens via the recognition of pathogen-associated molecular patterns (PAMPs) by surface-localized pattern recognition receptors, which initiates a series of intracellular responses that ultimately limit bacterial growth. PAMP responses include changes in intracellular protein phosphorylation, including the activation of mitogen-activated protein kinase (MAPK) cascades. MAP kinase phosphatases (MKPs), such as Arabidopsis (Arabidopsis thaliana) MKP1, are important negative regulators of MAPKs and play a crucial role in controlling the intensity and duration of MAPK activation during innate immune signaling. As such, the mkp1 mutant lacking MKP1 displays enhanced PAMP responses and resistance against the virulent bacterium Pseudomonas syringae pv tomato DC3000. Previous in vitro studies showed that MKP1 can be phosphorylated and activated by MPK6, suggesting that phosphorylation may be an important mechanism for regulating MKP1. We found that MKP1 was phosphorylated during PAMP elicitation and that phosphorylation stabilized the protein, resulting in protein accumulation after elicitation. MKP1 also can be stabilized by the proteasome inhibitor MG132, suggesting that MKP1 is constitutively degraded through the proteasome in the resting state. In addition, we investigated the role of MKP1 posttranslational regulation in plant defense by testing whether phenotypes of the mkp1 Arabidopsis mutant could be complemented by expressing phosphorylation site mutations of MKP1. The phosphorylation of MKP1 was found to be required for some, but not all, of MKP1's functions in PAMP responses and defense against bacteria. Together, our results provide insight into the roles of phosphorylation in the regulation of MKP1 during PAMP signaling and resistance to bacteria.

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Sensitivity to Flg22 Is Modulated by Ligand-Induced Degradation and de Novo Synthesis of the Endogenous Flagellin-Receptor FLAGELLIN-SENSING2

Cited by 131 publications

References 74 publications

Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases

Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases

Danger-associated peptide signaling in Arabidopsis requires clathrin

Phosphorylation of Arabidopsis MAP Kinase Phosphatase 1 (MKP1) Is Required for PAMP Responses and Resistance against Bacteria

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