EFR

UniProt ID: C0LGT6
Organism: Arabidopsis thaliana
Review Status: INITIALIZED
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Gene Description

EFR (EF-TU RECEPTOR; At5g20480) is a plasma membrane-localized leucine-rich repeat receptor-like serine/threonine protein kinase (LRR-RLK) that serves as the pattern-recognition receptor (PRR) for the bacterial pathogen-associated molecular pattern (PAMP) elongation factor Tu (EF-Tu), specifically perceiving its conserved N-terminal epitope elf18. The protein is a single-pass type I membrane protein with an extracellular leucine-rich repeat ectodomain (the last two LRRs are required for elf18 binding), a single transmembrane helix, and an intracellular serine/threonine kinase domain. Upon binding elf18, EFR forms a ligand-induced complex with the co-receptor BAK1/SERK3 (and related SERK family kinases SERK4/BKK1, SERK1, SERK2), autophosphorylates, and is activated by tyrosine phosphorylation (notably Tyr-836). Activated EFR directly phosphorylates the receptor-like cytoplasmic kinase BIK1 and triggers PAMP-triggered immunity (PTI), including a calcium-associated plasma membrane anion channel/depolarization response, a reactive oxygen species burst, MAPK activation, defense gene induction, callose deposition, and modulation of defense hormones (jasmonic acid and salicylic acid) via a PRR-BIK1-WRKY axis. Proper biogenesis and folding of EFR require endoplasmic reticulum quality-control machinery, including the STT3a-containing oligosaccharyltransferase complex, calreticulin-3 (CRT3), UDP-glucose:glycoprotein glycosyltransferase (UGGT), and ER-resident chaperones. EFR-mediated immunity restricts bacterial pathogens and reduces Agrobacterium-mediated transformation, and it is a frequent target of bacterial effectors (e.g. AvrPto, AvrPtoB, HopAO1).

Existing Annotations Review

GO Term Evidence Action Reason
GO:0004672 protein kinase activity
IEA
GO_REF:0000120
KEEP AS NON CORE
Summary: EFR is a protein kinase, so this term is correct, but it is a generic parent of the more specific (and experimentally supported) serine/threonine and serine kinase terms.
Reason: Correct but uninformative parent; the specific Ser/Thr kinase activity (GO:0106310/GO:0004674) is the core molecular function.
Supporting Evidence:
file:ARATH/EFR/EFR-notes.md
EC 2.7.11.1; serine/threonine protein kinase.
GO:0004674 protein serine/threonine kinase activity
IEA
GO_REF:0000003
ACCEPT
Summary: EFR is a serine/threonine protein kinase (EC 2.7.11.1) that autophosphorylates and phosphorylates BIK1. This EC-based mapping is correct and consistent with experimental kinase activity.
Reason: Accurate description of EFR catalytic activity, supported by experimental autophosphorylation and BIK1 phosphorylation.
Supporting Evidence:
PMID:29649442
EFR regulates the phytohormone jasmonic acid (JA) through direct phosphorylation of a receptor-like cytoplasmic kinase, BIK1
GO:0005524 ATP binding
IEA
GO_REF:0000002
ACCEPT
Summary: As a protein kinase EFR binds ATP; the cytoplasmic kinase domain has a defined ATP-binding region. Supportive molecular function consistent with its catalytic activity.
Reason: ATP binding is required for the kinase activity; consistent with the protein kinase ATP-binding site annotated in UniProt.
Supporting Evidence:
file:ARATH/EFR/EFR-notes.md
kinase requires ATP (BINDING 718-726, 741)
GO:0005886 plasma membrane
IEA
GO_REF:0000044
ACCEPT
Summary: EFR is a single-pass type I plasma membrane protein and acts as a cell-surface PRR at the plasma membrane. This is a core localization.
Reason: Well-established plasma membrane localization of this cell-surface pattern-recognition receptor.
Supporting Evidence:
PMID:27317676
Plasma membrane-localized pattern recognition receptors (PRRs) such as FLAGELLIN SENSING2 (FLS2), EF-TU RECEPTOR (EFR)
file:ARATH/EFR/EFR-deep-research-falcon.md
EFR is a surface-exposed transmembrane LRR-RK and the active signaling receptor functions at the plasma membrane.
GO:0009617 response to bacterium
IEA
GO_REF:0000117
KEEP AS NON CORE
Summary: EFR participates in the response to bacteria by perceiving bacterial EF-Tu, but this is a broad parent of the more specific experimentally supported terms (detection of bacterium, response to molecule of bacterial origin).
Reason: Correct but generic; more specific terms better capture EFR function.
Supporting Evidence:
PMID:16713565
Arabidopsis plants detect a variety of PAMPs including conserved domains of bacterial flagellin and of bacterial EF-Tu
GO:0012505 endomembrane system
IEA
GO_REF:0000044
KEEP AS NON CORE
Summary: EFR transits the secretory/endomembrane system during biogenesis (it is also annotated as single-pass type I endomembrane protein), but plasma membrane is the functionally relevant and more informative location.
Reason: True but broad; reflects ER transit/biogenesis rather than the site of receptor action.
Supporting Evidence:
PMID:19763087
act in concert with STT3A-containing oligosaccharyltransferase complex in an N-glycosylation pathway in the endoplasmic reticulum
GO:0031349 positive regulation of defense response
IEA
GO_REF:0000117
ACCEPT
Summary: EFR positively regulates plant defense; perception of EF-Tu/elf18 activates PTI defense responses and increases resistance, and loss of EFR enhances pathogen susceptibility.
Reason: EFR is a positive regulator of defense responses; consistent with experimental loss- and gain-of-function evidence.
Supporting Evidence:
PMID:16713565
plant defense responses induced by PAMPs such as EF-Tu reduce transformation by Agrobacterium
file:ARATH/EFR/EFR-deep-research-falcon.md
EFR contributes to antibacterial immunity and induced resistance, including restriction of Pseudomonas syringae pv. tomato DC3000 growth after elf18 pretreatment.
GO:0106310 protein serine kinase activity
IEA
GO_REF:0000116
ACCEPT
Summary: EFR is a protein serine kinase (Rhea/EC mapping). Same activity is also experimentally supported (EXP annotations below). Core molecular function.
Reason: Accurate; the same activity is corroborated by experimental EXP annotations.
Supporting Evidence:
PMID:18158241
AvrPto binds receptor kinases, including Arabidopsis FLS2 and EFR
GO:0005515 protein binding
IPI
PMID:23395902
Pseudomonas HopU1 modulates plant immune receptor levels by ...
MARK AS OVER ANNOTATED
Summary: GRP7/RBG7 associates with EFR at the plasma membrane and binds EFR mRNA; this is a real interaction but the bare protein binding term is uninformative about EFR's function. The biologically meaningful relationship is regulatory (RNA-binding-protein co-association).
Reason: Bare protein binding is not informative as a core molecular function; per curation guidance more specific terms should capture the relationship.
Supporting Evidence:
PMID:23395902
GRP7 directly interacts in vivo with the PRRs FLS2 and EFR in a specific manner
GO:0005515 protein binding
IPI
PMID:24625928
A bacterial tyrosine phosphatase inhibits plant pattern reco...
MARK AS OVER ANNOTATED
Summary: This IPI captures EFR interactions with BAK1 and with the bacterial effector HopAO1/hopD2 (effector that dephosphorylates EFR). Real interactions but the bare protein binding term is uninformative.
Reason: Generic protein binding; the meaningful co-receptor and effector-targeting relationships are better captured by specific terms.
Supporting Evidence:
PMID:24625928
A tyrosine phosphatase, HopAO1, secreted by P. syringae, reduces EFR phosphorylation
GO:0005515 protein binding
IPI
PMID:29320478
An extracellular network of Arabidopsis leucine-rich repeat ...
MARK AS OVER ANNOTATED
Summary: From a large-scale extracellular LRR-RK binary interaction network; multiple EFR ectodomain interactions (SERK5, BAK1, NIK1, etc.). Real high-throughput interactions but the bare protein binding term is uninformative.
Reason: Generic protein binding from a high-throughput screen; uninformative as a core function.
Supporting Evidence:
PMID:29320478
An extracellular network of Arabidopsis leucine-rich repeat receptor kinases
GO:0106310 protein serine kinase activity
EXP
PMID:18158241
Pseudomonas syringae effector AvrPto blocks innate immunity ...
ACCEPT
Summary: Experimental evidence for EFR protein serine kinase activity (autophosphorylation and catalytic activity; UniProt cites this PMID for EC 2.7.11.1). Core molecular function.
Reason: Experimentally supported core kinase activity of EFR.
Supporting Evidence:
file:ARATH/EFR/EFR-notes.md
EC 2.7.11.1; serine/threonine protein kinase. CATALYTIC ACTIVITY records cite PubMed:18158241 and PubMed:29649442.
GO:0106310 protein serine kinase activity
EXP
PMID:29649442
The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the N...
ACCEPT
Summary: Experimental evidence that EFR directly phosphorylates BIK1, demonstrating its protein serine kinase activity. Core molecular function.
Reason: Experimentally supported; EFR directly phosphorylates the substrate BIK1. Note from the Falcon deep-research synthesis - a more recent allosteric-activation model (Muhlenbeck/Bender/Zipfel 2024) proposes that EFR catalytic activity can be partly dispensable in vivo and that BIK1 trans-phosphorylation is driven largely by EFR-activated BAK1; the direct EFR->BIK1 kinase-substrate annotation is retained but this mechanistic nuance should be considered when interpreting EFR's catalytic role.
Supporting Evidence:
PMID:29649442
EFR regulates the phytohormone jasmonic acid (JA) through direct phosphorylation of a receptor-like cytoplasmic kinase, BIK1
GO:0140426 pathogen-associated molecular pattern receptor signaling pathway
IMP
PMID:20113440
Early signaling through the Arabidopsis pattern recognition ...
ACCEPT
Summary: EFR initiates PAMP-triggered immune signaling upon elf18 perception, including BAK1-dependent calcium-associated early signaling. This is the defining biological process for EFR.
Reason: Core biological process; EFR is the PRR that initiates the PAMP receptor signaling pathway.
Supporting Evidence:
PMID:20113440
activation of FLS2 and EFR lead to BAK1-dependent, calcium-associated plasma membrane anion channel opening as an initial step in the pathogen defense pathway
file:ARATH/EFR/EFR-deep-research-falcon.md
elf18 perception by EFR triggers canonical PTI outputs including ROS burst, MAPK activation, Ca2+-linked signaling, defense gene induction, callose deposition, and seedling growth inhibition.
GO:0002237 response to molecule of bacterial origin
IMP
PMID:29649442
The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the N...
ACCEPT
Summary: EFR responds to the bacterial molecule EF-Tu (elf18) to activate immune signaling. Core function consistent with its identity as the EF-Tu receptor.
Reason: EFR perceives bacterial EF-Tu/elf18; well-supported core process.
Supporting Evidence:
PMID:29649442
EFR is a PRR that recognizes bacterial EF-Tu and activates immune signaling
GO:0005515 protein binding
IPI
PMID:29649442
The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the N...
MARK AS OVER ANNOTATED
Summary: EFR binds the cytoplasmic kinase BIK1 (associates in absence of ligand, dissociates upon PAMP perception, and phosphorylates it). A real and functionally important interaction, but the bare protein binding term is uninformative; the kinase-substrate relationship is captured by the Ser/Thr kinase activity terms.
Reason: Bare protein binding; the meaningful EFR-BIK1 kinase-substrate relationship is better represented by the kinase activity annotations.
Supporting Evidence:
PMID:29649442
direct phosphorylation of a receptor-like cytoplasmic kinase, BIK1
GO:0005886 plasma membrane
ISM
GO_REF:0000122
ACCEPT
Summary: Predicted (AtSubP) plasma membrane localization, consistent with the experimentally and structurally supported plasma membrane location of this cell-surface PRR. Core localization.
Reason: Consistent with established plasma membrane localization of EFR.
Supporting Evidence:
PMID:27317676
Plasma membrane-localized pattern recognition receptors (PRRs) such as FLAGELLIN SENSING2 (FLS2), EF-TU RECEPTOR (EFR)
GO:0005515 protein binding
IPI
PMID:27317676
The Arabidopsis Malectin-Like/LRR-RLK IOS1 Is Critical for B...
MARK AS OVER ANNOTATED
Summary: EFR forms a complex with the malectin-like LRR-RLK IOS1, which primes PTI. Real interaction, but the bare protein binding term is uninformative about EFR function.
Reason: Generic protein binding with a regulatory partner; uninformative as a core molecular function.
Supporting Evidence:
PMID:27317676
complexes between the membrane-localized IOS1 and BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1)-dependent PRRs FLS2 and EFR
GO:0005515 protein binding
IPI
PMID:18158241
Pseudomonas syringae effector AvrPto blocks innate immunity ...
MARK AS OVER ANNOTATED
Summary: EFR binds the Pseudomonas effector AvrPto, which inhibits receptor kinase activity. Real interaction, but the bare protein binding term is uninformative; the relevant biology (effector targeting) is not captured by this generic term.
Reason: Generic protein binding (effector interaction); uninformative as core function.
Supporting Evidence:
PMID:18158241
AvrPto binds receptor kinases, including Arabidopsis FLS2 and EFR
GO:0002764 immune response-regulating signaling pathway
IMP
PMID:19763087
Receptor quality control in the endoplasmic reticulum for pl...
ACCEPT
Summary: EFR signaling regulates plant immune responses; this paper studies EFR function and its ER quality-control dependence (EFR accumulation and signalling impaired in psl/stt3a mutants). Consistent with EFR's role in immune signaling.
Reason: EFR initiates and regulates immune response signaling; supported by EFR functional/quality-control studies.
Supporting Evidence:
PMID:19763087
EFR accumulation and signalling, but not of FLS2, are impaired in psl1, psl2, and stt3a plants
GO:0009626 plant-type hypersensitive response
IMP
PMID:19763087
Receptor quality control in the endoplasmic reticulum for pl...
MARK AS OVER ANNOTATED
Summary: This paper concerns ER quality control of EFR and elf18-triggered (PTI) responses (anthocyanin de-repression, SA-dependent defense), not a classical EFR-dependent hypersensitive response (programmed cell death). Surface PRRs like EFR drive PTI and generally do not by themselves trigger HR, which is the hallmark of NLR-mediated effector-triggered immunity. The abstract does not mention hypersensitive response.
Reason: HR/programmed cell death is not a core EFR (surface PRR) output; this IMP annotation likely over-propagates a general defense role to the specific HR term. Retained (not removed) as an experimental TAIR annotation whose full reasoning cannot be fully verified from the cached text.
Supporting Evidence:
file:ARATH/EFR/EFR-notes.md
PTI by surface PRRs like EFR generally does NOT trigger HR/cell death (that is the hallmark of ETI/intracellular NLRs)
GO:0019199 transmembrane receptor protein kinase activity
TAS
PMID:19763087
Receptor quality control in the endoplasmic reticulum for pl...
ACCEPT
Summary: EFR is a single-pass transmembrane receptor that combines elf18 ligand perception (ectodomain) with intracellular serine/threonine kinase signaling. This is the most informative molecular function term for EFR, capturing both the receptor and catalytic activities.
Reason: Most informative MF term; matches the GO definition (combining with a signal and transmitting it across the membrane to initiate change via protein phosphorylation). Core function.
Supporting Evidence:
PMID:16713565
a receptor kinase essential for EF-Tu perception, which we called EFR
GO:0016045 detection of bacterium
IDA
PMID:16713565
Perception of the bacterial PAMP EF-Tu by the receptor EFR r...
ACCEPT
Summary: EFR detects the bacterial PAMP EF-Tu; transient expression in N. benthamiana confers EF-Tu binding and responsiveness, and efr mutants are altered in bacterial interaction. Core biological process.
Reason: Direct experimental evidence that EFR detects bacterial EF-Tu; core to its function as the EF-Tu receptor.
Supporting Evidence:
PMID:16713565
Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires EF-Tu binding sites and responsiveness upon transient expression of EFR

Core Functions

Pattern-recognition receptor that perceives the bacterial PAMP elongation factor Tu (epitope elf18) as a transmembrane receptor serine/threonine protein kinase at the plasma membrane

Supporting Evidence:
  • PMID:16713565
    we used this finding in a targeted reverse-genetic approach to identify a receptor kinase essential for EF-Tu perception, which we called EFR
  • PMID:16713565
    Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires EF-Tu binding sites and responsiveness upon transient expression of EFR
  • file:ARATH/EFR/EFR-deep-research-falcon.md
    EFR is a prototypical Arabidopsis PRR for proteinaceous bacterial EF‑Tu epitopes (elf18/elf26).

Ligand-activated protein serine/threonine kinase that autophosphorylates upon elf18 perception and directly phosphorylates the cytoplasmic kinase BIK1 to propagate immune signaling

Supporting Evidence:
  • PMID:29649442
    EFR regulates the phytohormone jasmonic acid (JA) through direct phosphorylation of a receptor-like cytoplasmic kinase, BIK1
  • PMID:24625928
    is activated upon ligand binding by phosphorylation on its tyrosine residues. Phosphorylation of a single tyrosine residue, Y836, is required for activation of EFR and downstream immunity

Initiates PAMP-triggered immunity downstream of elf18 perception, including BAK1-dependent calcium-associated early signaling and activation of defense responses

Supporting Evidence:
  • PMID:20113440
    activation of FLS2 and EFR lead to BAK1-dependent, calcium-associated plasma membrane anion channel opening as an initial step in the pathogen defense pathway
  • PMID:16713565
    flagellin and EF-Tu activate a common set of signaling events and defense responses
  • file:ARATH/EFR/EFR-deep-research-falcon.md
    elf18 perception by EFR triggers canonical PTI outputs including ROS burst, MAPK activation, Ca2+-linked signaling, defense gene induction, callose deposition, and seedling growth inhibition.

References

Gene Ontology annotation through association of InterPro records with GO terms
Gene Ontology annotation based on Enzyme Commission mapping
Gene Ontology annotation based on UniProtKB/Swiss-Prot Subcellular Location vocabulary mapping, accompanied by conservative changes to GO terms applied by UniProt
Automatic Gene Ontology annotation based on Rhea mapping
Electronic Gene Ontology annotations created by ARBA machine learning models
Combined Automated Annotation using Multiple IEA Methods
AtSubP analysis
Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.
Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases.
Receptor quality control in the endoplasmic reticulum for plant innate immunity.
Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca-associated opening of plasma membrane anion channels.
Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7.
A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation.
The Arabidopsis Malectin-Like/LRR-RLK IOS1 Is Critical for BAK1-Dependent and BAK1-Independent Pattern-Triggered Immunity.
An extracellular network of Arabidopsis leucine-rich repeat receptor kinases.
The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the Nucleus and Regulates Defense Hormone Expression during Plant Innate Immunity.
file:ARATH/EFR/EFR-deep-research-falcon.md
Falcon/Edison deep research report: EFR

Suggested Questions for Experts

Q: Does EFR-mediated PTI ever contribute to localized cell death/hypersensitive-response-like outputs, or is the GO:0009626 annotation an over-extension of a general defense role?

Suggested experts: Plant immunity researchers

Q: What is the complete set of direct EFR kinase substrates beyond BIK1, and how does tyrosine phosphorylation (e.g. Y836) shape substrate selection?

Suggested experts: Plant receptor kinase signaling researchers

Suggested Experiments

Experiment: Compare elf18-triggered responses (ROS, MAPK, callose, defense gene induction) versus cell-death markers in wild-type and efr mutants, and test whether HR-associated readouts are EFR-independent.

Hypothesis: EFR-dependent PTI does not require a hypersensitive-response/programmed cell death module

Experiment: Use EFR Y836F and kinase-dead (D849N) variants to measure BIK1 phosphorylation, JA/SA accumulation, and resistance to P. syringae, dissecting the contribution of tyrosine versus serine/threonine phosphorylation.

Hypothesis: Tyrosine phosphorylation of EFR (Y836) gates substrate phosphorylation of BIK1 and downstream hormone outputs

Deep Research

Falcon

(EFR-deep-research-falcon.md)
Gene Research for GO Annotation Review Falcon citations file

Gene Research for GO Annotation Review

Target

  • Gene symbol: EFR
  • Organism: Arabidopsis thaliana

UniProt Context

=== UNIPROT METADATA ===
UniProt ID: C0LGT6
Entry Name: EFR_ARATH
Gene Name: EFR
Locus Tag: At5g20480 {ECO:0000312|Araport:AT5G20480}
Protein Name: LRR receptor-like serine/threonine-protein kinase EFR
EC Number: 2.7.11.1
Organism: Arabidopsis thaliana (Mouse-ear cress)
NCBI Taxonomy ID: 3702
Function: Constitutes the pattern-recognition receptor (PPR) that determines the specific perception of elongation factor Tu (EF-Tu), a potent elicitor of the defense response to pathogen-associated molecular patterns (PAMPs); phosphorylates BIK1 upon elicitation to regulate immune responses such as defense hormone expression (e.g. jasmonic acid (JA) and salicylic acid (SA)) (PubMed:29649442). Reduces transformation by Rhizobium radiobacter probably by inducing plant defense during the interaction. Binding to the effector AvrPto1 from P.syringae blocks the downstream plant immune response while interaction with hopD2 decreases the phosphorylation level of EFR upon elf18 treatment. Specific endoplasmic reticulum quality control components (ERD2B, CRT3, UGGT and STT3A) are required for the biogenesis of EFR.
Subcellular Location: Cell membrane; Single-pass type I membrane protein. Endomembrane system; Single-pass type I membrane protein.
Subunit: Binds to Pseudomonas syringae AvrPto1 and (via the kinase and cytoplasmic domains) to hopD2. Interacts with SERK3/BAK1, SERK4/BKK1, SERK1 and SERK2 in a specific ligand-induced manner. Binds to IOS1 (PubMed:27317676). Binds to BIK1 in the absence of pathogen elicitor; dissociates upon pathogen-associated molecular pattern (PAMP)-triggered activation (PubMed:29649442).
======================

Research Objective

Prepare a comprehensive literature-backed research report for GO annotation review of the target gene.

Focus on:

  1. The core biochemical activity of the gene product and any substrate specificity.
  2. The activation or maturation mechanism of the protein, including proteolytic processing if relevant.
  3. The best-supported subcellular localization and complexes where the active protein functions.
  4. The strongest experimentally supported biological processes in the target organism, or in very close orthologs when transfer is justified.
  5. Which annotations appear to reflect core function versus context-specific, pleiotropic, or over-extended roles.
  6. Any evidence bearing on apoptosis, developmental cell death, neuronal roles, inflammatory signaling, pyroptosis, synaptic remodeling, protein processing, and localization to cytoplasm, cytosol, nucleus, or signaling complexes.

Output Requirements

Structure the report as:

  1. Executive summary
  2. Molecular function
  3. Biological process roles
  4. Cellular localization and complexes
  5. Annotation-risk assessment
  6. Key literature

Use citations for all substantive claims.

Gene Research Report for GO Annotation Review: EFR (At5g20480), Arabidopsis thaliana

1. Executive summary

EF-TU RECEPTOR (EFR; At5g20480) encodes a plasma-membrane, single-pass leucine-rich repeat receptor-like kinase (LRR-RK) that functions as a pattern-recognition receptor (PRR) for the bacterial elongation factor Tu (EF‑Tu)–derived N-terminal peptides elf18/elf26, thereby initiating pattern-triggered immunity (PTI). EFR activation involves rapid ligand-induced recruitment of SERK-family co-receptors (especially BAK1/SERK3, also BKK1/SERK4 and others) and extensive phosphorylation dynamics in the receptor complex. Recent work (2024) shows that EFR signaling is not explained solely by “EFR kinase phosphorylates downstream substrates”; rather, EFR can act non-catalytically to allosterically activate the co-receptor kinase BAK1, enabling BAK1 to phosphorylate downstream cytosolic kinases such as BIK1. Key EFR phosphosites (Y836 and activation-loop S887/S888) are required for productive receptor-complex activation, while EFR’s own catalytic activity can be dispensable for antibacterial immunity in vivo. (muhlenbeck2024allostericactivationof pages 3-5, henning2024allostericactivationof pages 3-5, bender2021activationloopphosphorylation pages 1-2, bender2021activationloopphosphorylation pages 5-6)

EFR biogenesis is unusually dependent on endoplasmic reticulum (ER) quality control (ER-QC) and N-glycosylation factors (e.g., CRT3, UGGT, STT3A; and a separate SDF2–ERdj3B–BiP complex). Disruption of these ER-QC components reduces stable accumulation of functional EFR and impairs elf18/elf26 binding and signaling, highlighting an annotation-relevant distinction between where the mature active receptor signals (plasma membrane) and where it is matured/inspected (ER). (nekrasov2009controlofthe pages 1-1, saijo2009receptorqualitycontrol pages 3-4)

Across the EFR-focused literature retrieved here, there is no direct experimental support for annotating EFR to apoptosis/animal-style inflammatory signaling, pyroptosis, neuronal functions, or stable nuclear localization; “cell death” appears mainly as a generic immune-context concept or linked to other signaling hubs (e.g., BAK1/BKK1), not as a demonstrated core EFR function. (roux2011thearabidopsisleucinerich pages 1-2, saijo2009receptorqualitycontrol pages 1-2)

2. Molecular function

2.1 Key concepts and definitions (current understanding)

Pattern-recognition receptor (PRR): a host cell-surface receptor that recognizes conserved microbial molecules (MAMPs/PAMPs) and triggers innate immune responses. EFR is a prototypical Arabidopsis PRR for proteinaceous bacterial EF‑Tu epitopes (elf18/elf26). (roux2011thearabidopsisleucinerich pages 1-2, nekrasov2009controlofthe pages 1-1)

Non-RD receptor kinase: protein kinases lacking the canonical Arg in the HRD catalytic motif, frequently associated with innate immune signaling across kingdoms. EFR is a non-RD LRR-RK; its complex activation can rely on phosphorylation-driven conformational changes and co-receptor kinase activity, not necessarily EFR’s own catalysis. (bender2021activationloopphosphorylation pages 1-2, muhlenbeck2024allostericactivationof pages 1-2)

2.2 Core biochemical activity and substrate specificity

EFR is biochemically a receptor-like Ser/Thr protein kinase (EC 2.7.11.1) with an active kinase domain in vitro and ligand-induced phosphorylation in vivo, which supports GO molecular function annotation to protein kinase activity. (bender2021activationloopphosphorylation pages 1-2)

However, in planta genetics/functional complementation demonstrate that EFR catalytic activity can be dispensable for elf18-triggered immune outputs and antibacterial immunity: catalytically impaired mutants (e.g., D849N, K851E) can still support elf18-triggered ROS, MAPK activation, seedling growth inhibition and pathogen restriction, implying EFR has a non-catalytic signaling role within the receptor complex. (bender2021activationloopphosphorylation pages 2-3, bender2021activationloopphosphorylation pages 1-2, bender2021activationloopphosphorylation pages 5-6)

Downstream phosphorylation and the BIK1 question (direct vs indirect): the best-supported current model (2024) is that EFR (once appropriately phosphorylated at Y836 and S887/S888) promotes BAK1 catalytic activation allosterically, and BAK1 then performs key phosphorylations including BIK1 trans-phosphorylation; kinase-dead EFR still retains some capacity to enhance BAK1→BIK1 phosphorylation, supporting the “non-catalytic EFR” model. (henning2024allostericactivationof pages 3-5, henning2024allostericactivationof pages 2-3)

This is important for GO: the strongest evidence supports EFR as a PRR and complex activator, but not as the sole/primary kinase directly phosphorylating BIK1 under physiological conditions. (bender2021activationloopphosphorylation pages 2-3, henning2024allostericactivationof pages 3-5)

2.3 Activation/maturation mechanisms

Ligand perception and co-receptor recruitment

Elf18 perception triggers rapid receptor complex formation: EFR heteromerizes with BAK1 within ~5 minutes of elf18 treatment, and MS of EFR immunoprecipitates identifies multiple SERK-family peptides detected only after elf18 elicitation. (roux2011thearabidopsisleucinerich pages 2-3)

Proteomic immunoprecipitation shows ligand-enhanced co-purification consistent with stimulus-dependent recruitment, with marked spectral count increases for BAK1 and SERK4 after elf18 treatment (e.g., BAK1 0/0/2 → 9/2/7; SERK4 0/0/0 → 12/4/6 across replicates). (roux2011identificationandcharacterization pages 172-176)

Phosphorylation logic, phosphosites, and “non-catalytic” activation

Recent mechanistic work identifies specific required EFR phosphosites for receptor-complex activation: EFR Y836 and activation-loop S887/S888 are required for in vivo signaling; phospho-ablative mutants block ligand-induced BAK1 S612 phosphorylation (an active-complex marker). (henning2024allostericactivationof pages 3-5, henning2024allostericactivationof pages 2-3)

In a complementary study, phosphoproteomics identified 12 high-confidence Ser/Thr phosphorylation sites on EFR, some detected only after elf18 stimulation, supporting ligand-triggered phosphoregulation. (bender2021activationloopphosphorylation pages 5-6)

2.4 Recent developments and expert analysis (2023–2024 priority)

A central 2024 advance is the proposed conformational toggle/allosteric activation model: BAK1 phosphorylates EFR in the activation loop to stabilize an active-like EFR conformation; EFR then allosterically enhances BAK1 activity (likely affecting BAK1 αC-helix positioning), enabling BAK1-driven phosphorylation of downstream targets such as BIK1. (muhlenbeck2024allostericactivationof pages 1-2)

This shifts interpretation of EFR from a purely catalytic kinase to a receptor whose structural state and phosphorylation determine its ability to activate co-receptors and transmit immune signals. (henning2024allostericactivationof pages 3-5)

3. Biological process roles

3.1 Best-supported processes in Arabidopsis

EFR-mediated recognition of elf18/elf26 triggers canonical PTI outputs: Ca2+ influx/ion fluxes, ROS burst, MAPK and CDPK activation, defense gene induction, callose deposition, seedling growth inhibition, and enhanced resistance to bacterial infection. (roux2011thearabidopsisleucinerich pages 1-2, bender2021activationloopphosphorylation pages 2-3, nekrasov2009controlofthe pages 1-1)

EFR is experimentally linked to antibacterial immunity, including induced resistance restricting Pseudomonas syringae pv. tomato DC3000 after elf18 pretreatment; this induced resistance is lost in efr mutants but retained in lines expressing catalytically impaired EFR variants. (bender2021activationloopphosphorylation pages 5-6)

EFR also contributes to reduced susceptibility to Agrobacterium transformation/interaction, consistent with PTI restricting transformation efficiency; in one assay, WT and catalytic-site complementation lines show ~100-fold lower GUS readout than the efr-1 knockout after Agrobacterium-mediated transient transformation. (bender2021activationloopphosphorylation pages 5-6)

3.2 Context-specific and “non-core” process claims

An OMV (outer membrane vesicle) priming study (2023) reports that mutations in EFR (as well as FLS2 and BAK1) did not significantly affect OMV-mediated priming, indicating that not all immune priming phenomena are EFR-dependent and cautioning against over-general “immune priming” annotations for EFR. (chalupowicz2023bacterialoutermembrane pages 1-2)

4. Cellular localization and complexes

4.1 Subcellular localization

EFR is a cell-surface transmembrane receptor whose mature signaling-competent pool functions at the plasma membrane. Defects in ER quality control cause ER retention and degradation rather than plasma-membrane accumulation. (nekrasov2009controlofthe pages 1-1)

Biochemical fractionation in an ER-QC study detected endogenous EFR in both PM-enriched and ER/microsomal fractions (EFR co-fractionated with PM and ER markers), consistent with transit through the secretory system and a biogenesis pool in ER/microsomes. (saijo2009receptorqualitycontrol pages 3-4)

4.2 Receptor complexes

Ligand-induced SERK co-receptor complex

EFR forms ligand-induced complexes with BAK1 and other SERK family members after elf18 elicitation, supporting a “receptor/co-receptor complex” cellular component concept. (roux2011thearabidopsisleucinerich pages 2-3, roux2011identificationandcharacterization pages 198-201)

ER quality-control and biogenesis dependencies

EFR is an ER-QC client:
* CRT3 and UGGT are required for stable accumulation of functional EFR and for elf26 binding, with strong alleles causing reduced steady-state EFR protein without corresponding transcript decrease. (saijo2009receptorqualitycontrol pages 3-4)
* A distinct ER luminal complex SDF2–ERdj3B–BiP is required for plasma-membrane EFR accumulation; sdf2 mutants show ER retention and degradation of EFR. (nekrasov2009controlofthe pages 1-1)

These findings support separating CC annotations (PM for function; ER for maturation/quality control) and avoiding overstatement that EFR “localizes to ER” as its functional signaling site. (nekrasov2009controlofthe pages 1-1, saijo2009receptorqualitycontrol pages 3-4)

5. Annotation-risk assessment (GO curation guidance)

5.1 Core vs context-specific annotations

Core function (high confidence): PRR activity for EF‑Tu-derived elf peptides; PTI signaling at the plasma membrane; stimulus-dependent receptor complex formation with SERKs/BAK1. (roux2011thearabidopsisleucinerich pages 1-2, roux2011thearabidopsisleucinerich pages 2-3)

Core mechanistic nuance (important for MF interpretation): EFR has kinase activity in vitro, but EFR catalytic activity is not strictly required for antibacterial immunity; EFR’s key role may be structural/allosteric activation of BAK1 and organization of a productive signaling complex. (bender2021activationloopphosphorylation pages 2-3, henning2024allostericactivationof pages 3-5)

Context-specific/downstream consequences (moderate confidence, annotate carefully): reduction of Agrobacterium-mediated transformation (likely a PTI consequence), and additional phenotypes that are indirect outcomes of broad immune activation. (bender2021activationloopphosphorylation pages 5-6)

5.2 Avoiding over-extended or incorrect annotations

Apoptosis / programmed cell death / pyroptosis / neuronal / inflammatory signaling: No direct evidence in the retrieved EFR-centered studies supports these as EFR biological processes or molecular functions; “cell death” appears mainly as a general immune-system context or linked to other hubs, not EFR execution. (roux2011thearabidopsisleucinerich pages 1-2, saijo2009receptorqualitycontrol pages 1-2)

Nucleus/cytosol localization: No evidence here supports stable EFR localization to nucleus or cytosol. ER-associated degradation may involve cytosolic steps for misfolded proteins, but that does not justify cytosolic/nuclear CC annotations for functional EFR. (nekrasov2009controlofthe pages 1-1)

6. Key literature (URLs and publication dates)

High-priority mechanistic and EFR-specific primary studies

  1. Mühlenbeck H. et al. “Allosteric activation of the co-receptor BAK1 by the EFR receptor kinase initiates immune signaling.” eLife (Jul 2024). https://doi.org/10.7554/elife.92110 (henning2024allostericactivationof pages 3-5)
  2. Bender K.W. et al. “Activation loop phosphorylation of a non-RD receptor kinase initiates plant innate immune signaling.” PNAS (Sep 2021). https://doi.org/10.1073/pnas.2108242118 (bender2021activationloopphosphorylation pages 1-2)
  3. Roux M. et al. “The Arabidopsis LRR-RLKs BAK1/SERK3 and BKK1/SERK4 are required for innate immunity…” The Plant Cell (Jun 2011). https://doi.org/10.1105/tpc.111.084301 (roux2011thearabidopsisleucinerich pages 2-3)
  4. Saijo Y. et al. “Receptor quality control in the endoplasmic reticulum for plant innate immunity.” The EMBO Journal (Nov 2009). https://doi.org/10.1038/emboj.2009.263 (saijo2009receptorqualitycontrol pages 3-4)
  5. Nekrasov V. et al. “Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity.” The EMBO Journal (Nov 2009). https://doi.org/10.1038/emboj.2009.262 (nekrasov2009controlofthe pages 1-1)

Recent contextual studies and reviews (authoritative expert synthesis)

  1. Bender K.W., Zipfel C. “Paradigms of receptor kinase signaling in plants.” Biochemical Journal (Jun 2023). https://doi.org/10.1042/bcj20220372 (retrieved but not evidence-extracted here; see paper_search output)
  2. Chalupowicz L. et al. “Bacterial outer membrane vesicles induce a transcriptional shift…” Journal of Extracellular Vesicles (Jan 2023). https://doi.org/10.1002/jev2.12285 (chalupowicz2023bacterialoutermembrane pages 1-2)

GO-focused synthesis table

GO aspect (MF/BP/CC) Proposed term Evidence summary (1-2 clauses) Key citations Annotation risk notes
MF pattern recognition receptor activity EFR specifically perceives the bacterial EF-Tu epitope elf18/elf26 and initiates immune signaling; loss of EFR abolishes elf-ligand responsiveness. (bender2021activationloopphosphorylation pages 2-3, roux2011thearabidopsisleucinerich pages 1-2, nekrasov2009controlofthe pages 1-1) Core function; strongest MF annotation. Keep ligand specificity centered on EF-Tu-derived peptides, not broad all-bacteria recognition.
MF protein serine/threonine kinase activity EFR has an active cytoplasmic kinase domain in vitro and is phosphorylated in vivo, consistent with receptor kinase biochemistry. (bender2021activationloopphosphorylation pages 1-2) Support exists, but signaling output does not strictly require EFR catalytic activity in vivo; annotate cautiously as biochemical capability rather than sole signaling mechanism.
MF non-RD receptor kinase signaling activity EFR is a non-RD LRR-RK whose activation depends on phosphorylation-dependent conformational change rather than simple reciprocal catalysis. (muhlenbeck2024allostericactivationof pages 1-2, henning2024allostericactivationof pages 1-2) Useful mechanistic note for review, but may not map cleanly to a standard GO MF term; avoid inventing overly specific GO-like labels if unsupported in ontology.
BP pattern-triggered immunity elf18 perception by EFR triggers canonical PTI outputs including ROS burst, MAPK activation, Ca2+-linked signaling, defense gene induction, callose deposition, and seedling growth inhibition. (roux2011thearabidopsisleucinerich pages 1-2, bender2021activationloopphosphorylation pages 5-6, bender2021activationloopphosphorylation pages 2-3, nekrasov2009controlofthe pages 1-1) Core biological process; strongest BP annotation.
BP defense response to bacterium EFR contributes to antibacterial immunity and induced resistance, including restriction of Pseudomonas syringae pv. tomato DC3000 growth after elf18 pretreatment. (bender2021activationloopphosphorylation pages 5-6, saijo2009receptorqualitycontrol pages 3-4) Well supported; keep framed as bacterial defense, not generalized resistance to all pathogens.
BP regulation of immune receptor signaling by receptor complex activation Ligand perception drives rapid EFR association with BAK1/SERKs and activation-loop-dependent signaling, with BAK1 S612 phosphorylation marking active complexes. (muhlenbeck2024allostericactivationof pages 3-5, henning2024allostericactivationof pages 3-5, roux2011thearabidopsisleucinerich pages 2-3) Strong mechanistic process support; avoid overextending to direct phosphorylation of all downstream substrates by EFR.
BP positive regulation of BAK1-mediated phosphorylation events Recent work supports an allosteric model in which phosphorylated EFR promotes BAK1 activity and thereby BAK1-mediated BIK1 phosphorylation. (muhlenbeck2024allostericactivationof pages 3-5, henning2024allostericactivationof pages 3-5, henning2024allostericactivationof pages 2-3) Supported mechanistically, but context-specific and relatively specialized; not equivalent to direct EFR→BIK1 kinase-substrate annotation.
BP protein maturation involved in receptor biogenesis Functional EFR accumulation requires ER quality-control and N-glycosylation factors including CRT3, UGGT, STT3A, and SDF2-ERdj3B-BiP. (nekrasov2009controlofthe pages 1-1, saijo2009receptorqualitycontrol pages 3-4, saijo2009receptorqualitycontrol pages 1-2) Best treated as maturation/biogenesis dependency rather than EFR “performing” ERQC; avoid annotating EFR as an ERQC factor itself.
BP negative regulation of Agrobacterium-mediated transformation EFR-dependent immune activation reduces Agrobacterium transformation/transient transformation efficiency. (bender2021activationloopphosphorylation pages 5-6) Supported but context-specific; likely downstream consequence of immune activation rather than core dedicated function.
CC plasma membrane EFR is a surface-exposed transmembrane LRR-RK and the active signaling receptor functions at the plasma membrane. (nekrasov2009controlofthe pages 1-1, saijo2009receptorqualitycontrol pages 3-4, roux2011thearabidopsisleucinerich pages 2-3) Core CC annotation; strongest localization term.
CC receptor complex Upon elf18 treatment, EFR forms ligand-induced complexes with BAK1 and additional SERK family co-receptors. (roux2011thearabidopsisleucinerich pages 2-3, roux2011identificationandcharacterization pages 172-176, roux2011identificationandcharacterization pages 198-201) Strong support for signaling-complex membership; complex is stimulus-dependent.
CC endoplasmic reticulum / endomembrane system EFR is detected in ER/microsomal fractions during biogenesis and interacts with ER-QC machinery before plasma membrane accumulation. (saijo2009receptorqualitycontrol pages 3-4, nekrasov2009controlofthe pages 1-1) Appropriate as biogenesis/localization context; avoid implying the mature active receptor primarily signals from ER.
CC cytosol / nucleus No direct evidence in the retrieved EFR literature supports stable cytosolic or nuclear localization of EFR itself. (nekrasov2009controlofthe pages 1-1, saijo2009receptorqualitycontrol pages 1-2, roux2011identificationandcharacterization pages 130-134) Do not annotate EFR to cytosol or nucleus based on downstream partners such as BIK1.
BP apoptosis / programmed cell death / hypersensitive response Retrieved EFR-focused studies do not directly support EFR as an executor of apoptosis, PCD, HR, pyroptosis, or animal-style inflammatory pathways. (nekrasov2009controlofthe pages 1-1, roux2011thearabidopsisleucinerich pages 1-2, saijo2009receptorqualitycontrol pages 1-2, chalupowicz2023bacterialoutermembrane pages 1-2) Avoid overextension; cell-death mentions are generic immune-context statements or relate to BAK1/BKK1, not direct EFR function.

Table: This table summarizes conservative, evidence-based GO annotation proposals for Arabidopsis EFR (At5g20480). It highlights core functions and locations while flagging context-specific or unsupported annotations that should be avoided during review.

References

  1. (muhlenbeck2024allostericactivationof pages 3-5): Henning Mühlenbeck, Yuko Tsutsui, Mark A. Lemmon, Kyle W. Bender, and Cyril Zipfel. Allosteric activation of the co-receptor bak1 by the efr receptor kinase initiates immune signaling. Unknown journal, Nov 2024. URL: https://doi.org/10.7554/elife.92110.1, doi:10.7554/elife.92110.1.

  2. (henning2024allostericactivationof pages 3-5): Henning Mühlenbeck, Yuko Tsutsui, Mark A Lemmon, Kyle W Bender, and Cyril Zipfel. Allosteric activation of the co-receptor bak1 by the efr receptor kinase initiates immune signaling. eLife, Jul 2024. URL: https://doi.org/10.7554/elife.92110, doi:10.7554/elife.92110. This article has 32 citations and is from a domain leading peer-reviewed journal.

  3. (bender2021activationloopphosphorylation pages 1-2): Kyle W. Bender, Daniel Couto, Yasuhiro Kadota, Alberto P. Macho, Jan Sklenar, Paul Derbyshire, Marta Bjornson, Thomas A. DeFalco, Annalise Petriello, Maria Font Farre, Benjamin Schwessinger, Vardis Ntoukakis, Lena Stransfeld, Alexandra M. E. Jones, Frank L. H. Menke, and Cyril Zipfel. Activation loop phosphorylation of a non-rd receptor kinase initiates plant innate immune signaling. Proceedings of the National Academy of Sciences, Sep 2021. URL: https://doi.org/10.1073/pnas.2108242118, doi:10.1073/pnas.2108242118. This article has 30 citations and is from a highest quality peer-reviewed journal.

  4. (bender2021activationloopphosphorylation pages 5-6): Kyle W. Bender, Daniel Couto, Yasuhiro Kadota, Alberto P. Macho, Jan Sklenar, Paul Derbyshire, Marta Bjornson, Thomas A. DeFalco, Annalise Petriello, Maria Font Farre, Benjamin Schwessinger, Vardis Ntoukakis, Lena Stransfeld, Alexandra M. E. Jones, Frank L. H. Menke, and Cyril Zipfel. Activation loop phosphorylation of a non-rd receptor kinase initiates plant innate immune signaling. Proceedings of the National Academy of Sciences, Sep 2021. URL: https://doi.org/10.1073/pnas.2108242118, doi:10.1073/pnas.2108242118. This article has 30 citations and is from a highest quality peer-reviewed journal.

  5. (nekrasov2009controlofthe pages 1-1): Vladimir Nekrasov, Jing Li, Martine Batoux, Milena Roux, Zhao-Hui Chu, Severine Lacombe, Alejandra Rougon, Pascal Bittel, Marta Kiss-Papp, Delphine Chinchilla, H Peter van Esse, Lucia Jorda, Benjamin Schwessinger, Valerie Nicaise, Bart P H J Thomma, Antonio Molina, Jonathan D G Jones, and Cyril Zipfel. Control of the pattern‐recognition receptor efr by an er protein complex in plant immunity. The EMBO Journal, 28:3428-3438, Nov 2009. URL: https://doi.org/10.1038/emboj.2009.262, doi:10.1038/emboj.2009.262. This article has 362 citations.

  6. (saijo2009receptorqualitycontrol pages 3-4): Yusuke Saijo, Nico Tintor, Xunli Lu, Philipp Rauf, Karolina Pajerowska-Mukhtar, Heidrun Häweker, Xinnian Dong, Silke Robatzek, and Paul Schulze-Lefert. Receptor quality control in the endoplasmic reticulum for plant innate immunity. The EMBO Journal, 28:3439-3449, Nov 2009. URL: https://doi.org/10.1038/emboj.2009.263, doi:10.1038/emboj.2009.263. This article has 310 citations.

  7. (roux2011thearabidopsisleucinerich pages 1-2): Milena Roux, Benjamin Schwessinger, Catherine Albrecht, Delphine Chinchilla, Alexandra Jones, Nick Holton, Frederikke Gro Malinovsky, Mahmut Tör, Sacco de Vries, and Cyril Zipfel. The arabidopsis leucine-rich repeat receptor–like kinases bak1/serk3 and bkk1/serk4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Jun 2011. URL: https://doi.org/10.1105/tpc.111.084301, doi:10.1105/tpc.111.084301. This article has 851 citations.

  8. (saijo2009receptorqualitycontrol pages 1-2): Yusuke Saijo, Nico Tintor, Xunli Lu, Philipp Rauf, Karolina Pajerowska-Mukhtar, Heidrun Häweker, Xinnian Dong, Silke Robatzek, and Paul Schulze-Lefert. Receptor quality control in the endoplasmic reticulum for plant innate immunity. The EMBO Journal, 28:3439-3449, Nov 2009. URL: https://doi.org/10.1038/emboj.2009.263, doi:10.1038/emboj.2009.263. This article has 310 citations.

  9. (muhlenbeck2024allostericactivationof pages 1-2): Henning Mühlenbeck, Yuko Tsutsui, Mark A. Lemmon, Kyle W. Bender, and Cyril Zipfel. Allosteric activation of the co-receptor bak1 by the efr receptor kinase initiates immune signaling. Unknown journal, Nov 2024. URL: https://doi.org/10.7554/elife.92110.1, doi:10.7554/elife.92110.1.

  10. (bender2021activationloopphosphorylation pages 2-3): Kyle W. Bender, Daniel Couto, Yasuhiro Kadota, Alberto P. Macho, Jan Sklenar, Paul Derbyshire, Marta Bjornson, Thomas A. DeFalco, Annalise Petriello, Maria Font Farre, Benjamin Schwessinger, Vardis Ntoukakis, Lena Stransfeld, Alexandra M. E. Jones, Frank L. H. Menke, and Cyril Zipfel. Activation loop phosphorylation of a non-rd receptor kinase initiates plant innate immune signaling. Proceedings of the National Academy of Sciences, Sep 2021. URL: https://doi.org/10.1073/pnas.2108242118, doi:10.1073/pnas.2108242118. This article has 30 citations and is from a highest quality peer-reviewed journal.

  11. (henning2024allostericactivationof pages 2-3): Henning Mühlenbeck, Yuko Tsutsui, Mark A Lemmon, Kyle W Bender, and Cyril Zipfel. Allosteric activation of the co-receptor bak1 by the efr receptor kinase initiates immune signaling. eLife, Jul 2024. URL: https://doi.org/10.7554/elife.92110, doi:10.7554/elife.92110. This article has 32 citations and is from a domain leading peer-reviewed journal.

  12. (roux2011thearabidopsisleucinerich pages 2-3): Milena Roux, Benjamin Schwessinger, Catherine Albrecht, Delphine Chinchilla, Alexandra Jones, Nick Holton, Frederikke Gro Malinovsky, Mahmut Tör, Sacco de Vries, and Cyril Zipfel. The arabidopsis leucine-rich repeat receptor–like kinases bak1/serk3 and bkk1/serk4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Jun 2011. URL: https://doi.org/10.1105/tpc.111.084301, doi:10.1105/tpc.111.084301. This article has 851 citations.

  13. (roux2011identificationandcharacterization pages 172-176): M Roux. Identification and characterization of efr-interacting proteins. Unknown journal, 2011.

  14. (chalupowicz2023bacterialoutermembrane pages 1-2): Laura Chalupowicz, Gideon Mordukhovich, Nofar Assoline, Leron Katsir, Noa Sela, and Ofir Bahar. Bacterial outer membrane vesicles induce a transcriptional shift in arabidopsis towards immune system activation leading to suppression of pathogen growth in planta. Journal of Extracellular Vesicles, Jan 2023. URL: https://doi.org/10.1002/jev2.12285, doi:10.1002/jev2.12285. This article has 39 citations and is from a domain leading peer-reviewed journal.

  15. (roux2011identificationandcharacterization pages 198-201): M Roux. Identification and characterization of efr-interacting proteins. Unknown journal, 2011.

  16. (henning2024allostericactivationof pages 1-2): Henning Mühlenbeck, Yuko Tsutsui, Mark A Lemmon, Kyle W Bender, and Cyril Zipfel. Allosteric activation of the co-receptor bak1 by the efr receptor kinase initiates immune signaling. eLife, Jul 2024. URL: https://doi.org/10.7554/elife.92110, doi:10.7554/elife.92110. This article has 32 citations and is from a domain leading peer-reviewed journal.

  17. (roux2011identificationandcharacterization pages 130-134): M Roux. Identification and characterization of efr-interacting proteins. Unknown journal, 2011.

📚 Additional Documentation

Notes

(EFR-notes.md)

EFR (EF-TU RECEPTOR) — Arabidopsis thaliana, UniProt C0LGT6, At5g20480

Research journal for the GO annotation review. Provenance is inline as
[PMID:xxxx "verbatim quote"] or from the UniProt record (C0LGT6).

Summary of biology

EFR is a plasma-membrane-localized leucine-rich repeat receptor-like
serine/threonine kinase (LRR-RLK) that is the pattern-recognition receptor (PRR)
for the bacterial pathogen-associated molecular pattern (PAMP) elongation factor
Tu (EF-Tu), specifically perceiving its N-terminal epitope elf18. Ligand
perception triggers PAMP-triggered immunity (PTI). EFR is a single-pass type I
membrane protein: extracellular LRR ectodomain (residues 25–653, 21 LRRs),
transmembrane helix (654–674), cytoplasmic kinase domain (712–1001)
(UniProt C0LGT6 FT lines).

Identity / discovery

Catalytic / kinase activity

  • UniProt: EC 2.7.11.1; serine/threonine protein kinase. CATALYTIC ACTIVITY records cite PubMed:18158241 and PubMed:29649442.
  • Autophosphorylation upon elicitation [UniProt PTM: "Autophosphorylated after elicitation with elfl18"].
  • EFR directly phosphorylates the RLCK BIK1 PMID:29649442.
  • Active-site/catalytic D849; D849N abolishes kinase activity [UniProt MUTAGEN 849 "D->N: Loss of kinase activity"].
  • Tyrosine phosphorylation: EFR is activated by phosphorylation on tyrosines; Y836 is required PMID:24625928. Y836F: "Loss of elf18-triggered immunity, but no effect on the kinase activity" [UniProt MUTAGEN 836].

Receptor / transmembrane signaling

  • Type I single-pass membrane protein; combines elf18 ligand binding (ectodomain) with intracellular kinase signaling — fits GO:0019199 transmembrane receptor protein kinase activity (def: "Combining with a signal and transmitting the signal from one side of the membrane to the other to initiate a change in cell activity by catalysis of the reaction: a protein + ATP = a phosphoprotein + ADP").
  • Last two LRRs (561–597) necessary for elf18 binding [UniProt DOMAIN "The last two LRR (561-597) are necessary for elf18 binding and functionality"].
  • Co-receptor: ligand-induced complex with SERK3/BAK1 (and SERK4/BKK1, SERK1, SERK2) [UniProt SUBUNIT "Interacts with SERK3/BAK1, SERK4/BKK1, SERK1 and SERK2 in a specific ligand-induced manner"]. BAK1 required for early elf18 signaling PMID:20113440.

Downstream signaling / PTI outputs

  • elf18 (via EFR) and flg22 (via FLS2) "activate a common set of signaling events and defense responses" PMID:16713565.
  • Early signaling: Ca2+-associated plasma-membrane anion channel opening / depolarization PMID:20113440. This is the IMP support for GO:0140426 (PAMP receptor signaling pathway).
  • ROS burst, phosphorylation, gene expression, callose PMID:23395902.
  • Hormone branch: EFR–BIK1 axis regulates JA/SA; PRR–BIK1–WRKY PMID:29649442.

Subcellular location & ER quality control

  • Cell membrane (plasma membrane); endomembrane system (single-pass type I) [UniProt SUBCELLULAR LOCATION]. ISM:TAIR plasma membrane (GO_REF:0000122 AtSubP), IEA UniProtKB-SubCell.
  • ER quality control needed for biogenesis/maturation: STT3a-OST, CRT3 (calreticulin-3), UGGT, ERdj3B/ERD2B; N-glycosylation PMID:19763087. UniProt: "Specific endoplasmic reticulum quality control components (ERD2B, CRT3, UGGT and STT3A) are required for the biogenesis of EFR."
  • PMID:19763087 also annotated by TAIR for immune response-regulating signaling pathway (IMP) and plant-type hypersensitive response (IMP); it is fundamentally an EFR-function + subcellular-location paper (UniProt FUNCTION, SUBCELLULAR LOCATION). It does NOT report an EFR-driven hypersensitive response per se — see below.

Protein interactions (GO:0005515 IPI entries)

  • PMID:18158241 → AvrPto1 (Q87Y16): bacterial effector that binds and inhibits EFR (and FLS2) kinase PMID:18158241. Also the source for catalytic activity (autophosphorylation).
  • PMID:24625928 → BAK1 (Q94F62) and HopAO1/hopD2 (Q79LY0): EFR–co-receptor and EFR–effector phosphatase interactions.
  • PMID:23395902 → GRP7/RBG7 (Q03250): GRP7 associates with EFR (and FLS2) at the PM and binds EFR mRNA; HopU1 blocks GRP7–mRNA interaction. PMID:23395902. This is a regulatory RNA-binding-protein co-association, not core receptor function.
  • PMID:27317676 → IOS1 (Q9C8I6): malectin-like LRR-RLK that complexes with EFR/FLS2/CERK1 and primes PTI PMID:27317676.
  • PMID:29320478 → high-throughput extracellular LRR-RK interaction network (Nature 2018); reports many ectodomain interactions (SERK5/Q8LPS5, At4g30520/Q8VYT3, BAK1/Q94F62, NIK1/Q9LFS4, LRR-RLK/Q9ZVD4). Large-scale binary IPI screen.
  • PMID:29649442 → BIK1 (O48814): EFR binds BIK1 in absence of ligand, dissociates upon PAMP, and phosphorylates it.

GO annotation review decisions (rationale)

Molecular function:
- GO:0019199 transmembrane receptor protein kinase activity (TAS, PMID:19763087): ACCEPT, CORE. Most informative MF term — captures both receptor (ligand→transmembrane signal) and Ser/Thr kinase nature. Definition matches EFR exactly.
- GO:0106310 protein serine kinase activity (EXP PMID:18158241, EXP PMID:29649442): ACCEPT, CORE. Backed by experimental autophosphorylation + BIK1 phosphorylation; EC 2.7.11.1.
- GO:0004674 protein serine/threonine kinase activity (IEA EC): ACCEPT (core kinase activity; consistent with EC mapping).
- GO:0004672 protein kinase activity (IEA): KEEP_AS_NON_CORE — correct but a generic parent of the more specific Ser/Thr term; redundant.
- GO:0005524 ATP binding (IEA InterPro): ACCEPT — kinase requires ATP (BINDING 718-726, 741); supportive MF.
- GO:0005515 protein binding (IPI, ×8 across 6 papers): all real interactions, but uninformative bare term. MARK_AS_OVER_ANNOTATED per curation guidance (avoid endorsing bare protein binding as core); the biologically meaningful relationship (co-receptor binding, substrate, effector targeting) belongs in more specific MF/process terms.

Cellular component:
- GO:0005886 plasma membrane (IEA UniProtKB-SubCell; and ISM:TAIR): ACCEPT, CORE — EFR is a PM PRR.
- GO:0012505 endomembrane system (IEA UniProtKB-SubCell): KEEP_AS_NON_CORE — reflects ER transit/biogenesis and broad CC; true but less informative than plasma membrane.

Biological process:
- GO:0140426 PAMP receptor signaling pathway (IMP PMID:20113440): ACCEPT, CORE — the defining process.
- GO:0002237 response to molecule of bacterial origin (IMP PMID:29649442): ACCEPT (core; elf18/EF-Tu response).
- GO:0016045 detection of bacterium (IDA PMID:16713565): ACCEPT, CORE — EFR detects bacterial EF-Tu; gain-of-function and loss-of-function support.
- GO:0009617 response to bacterium (IEA ARBA): KEEP_AS_NON_CORE — correct but a broad parent of the IMP/IDA terms.
- GO:0031349 positive regulation of defense response (IEA ARBA): ACCEPT — EFR positively regulates defense (PTI activation; positive regulator).
- GO:0002764 immune response-regulating signaling pathway (IMP PMID:19763087): ACCEPT — EFR signaling regulates immune responses; supported by EFR functional studies.
- GO:0009626 plant-type hypersensitive response (IMP PMID:19763087): UNDECIDED → leaning MARK_AS_OVER_ANNOTATED. PMID:19763087 is about ER quality control of EFR and elf18-triggered (PTI) responses/anthocyanin de-repression, not a classic EFR-dependent HR (programmed cell death). PTI by surface PRRs like EFR generally does NOT trigger HR/cell death (that is the hallmark of ETI/intracellular NLRs). The abstract does not mention hypersensitive response. Cached full text is available but the abstract foregrounds N-glycosylation QC, anthocyanin, and SA-dependent (EFR-independent) defense. Mark as over-annotated: HR is not a core EFR output; the IMP TAIR annotation likely over-propagates "defense" to HR. Not REMOVE because it is an experimental TAIR annotation whose full reasoning I cannot fully verify (use MARK_AS_OVER_ANNOTATED rather than REMOVE).

IBA terms present in UniProt DR block but NOT in GOA stub (not part of existing_annotations to review): GO:0038023 signaling receptor activity (IBA), GO:0009755 hormone-mediated signaling pathway (IBA). Noted for completeness; GO:0009755 (hormone-mediated signaling) is a questionable IBA propagation for a PRR — EFR regulates hormone levels downstream (via BIK1) but is not itself a hormone-signaling receptor.

Core functions (for synthesis)

  1. elf18/EF-Tu pattern recognition receptor — transmembrane receptor Ser/Thr kinase (GO:0019199) at the plasma membrane (GO:0005886) that detects bacterial EF-Tu (GO:0016045).
  2. Ligand-activated protein serine/threonine kinase (GO:0106310) that autophosphorylates and phosphorylates BIK1.
  3. Initiation of PAMP-triggered immune signaling (GO:0140426) leading to PTI defense outputs.

Augmentation note (Falcon/Edison deep-research, 2026-06-15)

Incorporated the Falcon/Edison deep-research report
(file:ARATH/EFR/EFR-deep-research-falcon.md) as supporting context. It corroborates
the core verdicts (PRR for EF-Tu elf18/elf26; plasma-membrane signaling; PTI outputs
ROS/MAPK/Ca2+/callose; antibacterial immunity restricting Pto DC3000), which were
added as supported_by entries on the PRR, PTI-signaling, plasma-membrane,
PAMP-receptor-signaling-pathway, and positive-regulation-of-defense annotations/core
functions.

Refinement (not a verdict flip): the report emphasizes a recent allosteric-activation
model (Muhlenbeck/Bender/Zipfel 2024, eLife; Bender et al. 2021 PNAS) in which EFR's
own catalytic activity can be partly dispensable in vivo for antibacterial immunity,
and BIK1 trans-phosphorylation is driven largely by EFR-activated BAK1 rather than by
EFR acting as the sole/primary BIK1 kinase [file:ARATH/EFR/EFR-deep-research-falcon.md
"kinase-dead EFR still retains some capacity to enhance BAK1->BIK1 phosphorylation,
supporting the non-catalytic EFR model"]. The direct EFR->BIK1 kinase-substrate
annotation (PMID:29649442, EXP) is retained but a mechanistic caveat was appended to
its reason field. This is conservative; the curator-asserted experimental annotation
is not overruled.

The report also reinforces the existing MARK_AS_OVER_ANNOTATED verdict on
GO:0009626 (plant-type hypersensitive response): "Retrieved EFR-focused studies do
not directly support EFR as an executor of apoptosis, PCD, HR, pyroptosis."

📄 View Raw YAML

id: C0LGT6
gene_symbol: EFR
product_type: PROTEIN
status: INITIALIZED
taxon:
  id: NCBITaxon:3702
  label: Arabidopsis thaliana
description: EFR (EF-TU RECEPTOR; At5g20480) is a plasma membrane-localized
  leucine-rich repeat receptor-like serine/threonine protein kinase (LRR-RLK) that
  serves as the pattern-recognition receptor (PRR) for the bacterial
  pathogen-associated molecular pattern (PAMP) elongation factor Tu (EF-Tu),
  specifically perceiving its conserved N-terminal epitope elf18. The protein is a
  single-pass type I membrane protein with an extracellular leucine-rich repeat
  ectodomain (the last two LRRs are required for elf18 binding), a single
  transmembrane helix, and an intracellular serine/threonine kinase domain. Upon
  binding elf18, EFR forms a ligand-induced complex with the co-receptor BAK1/SERK3
  (and related SERK family kinases SERK4/BKK1, SERK1, SERK2), autophosphorylates,
  and is activated by tyrosine phosphorylation (notably Tyr-836). Activated EFR
  directly phosphorylates the receptor-like cytoplasmic kinase BIK1 and triggers
  PAMP-triggered immunity (PTI), including a calcium-associated plasma membrane
  anion channel/depolarization response, a reactive oxygen species burst, MAPK
  activation, defense gene induction, callose deposition, and modulation of defense
  hormones (jasmonic acid and salicylic acid) via a PRR-BIK1-WRKY axis. Proper
  biogenesis and folding of EFR require endoplasmic reticulum quality-control
  machinery, including the STT3a-containing oligosaccharyltransferase complex,
  calreticulin-3 (CRT3), UDP-glucose:glycoprotein glycosyltransferase (UGGT), and
  ER-resident chaperones. EFR-mediated immunity restricts bacterial pathogens and
  reduces Agrobacterium-mediated transformation, and it is a frequent target of
  bacterial effectors (e.g. AvrPto, AvrPtoB, HopAO1).
references:
- id: GO_REF:0000002
  title: Gene Ontology annotation through association of InterPro records with GO
    terms
  findings: []
- id: GO_REF:0000003
  title: Gene Ontology annotation based on Enzyme Commission mapping
  findings: []
- id: GO_REF:0000044
  title: Gene Ontology annotation based on UniProtKB/Swiss-Prot Subcellular Location
    vocabulary mapping, accompanied by conservative changes to GO terms applied by
    UniProt
  findings: []
- id: GO_REF:0000116
  title: Automatic Gene Ontology annotation based on Rhea mapping
  findings: []
- id: GO_REF:0000117
  title: Electronic Gene Ontology annotations created by ARBA machine learning models
  findings: []
- id: GO_REF:0000120
  title: Combined Automated Annotation using Multiple IEA Methods
  findings: []
- id: GO_REF:0000122
  title: AtSubP analysis
  findings: []
- id: PMID:16713565
  title: Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated
    transformation.
  findings: []
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "Founding paper identifying EFR as the EF-Tu/elf18 receptor; gain-of-function
      in N. benthamiana and efr loss-of-function (enhanced Agrobacterium transformation).
      Abstract-only in cache but claims verified against UniProt FUNCTION/discovery
      annotations."
- id: PMID:18158241
  title: Pseudomonas syringae effector AvrPto blocks innate immunity by targeting
    receptor kinases.
  findings: []
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "AvrPto binds EFR (and FLS2); source of EFR autophosphorylation/catalytic
      activity (UniProt CATALYTIC ACTIVITY cites this PMID). Abstract-only in cache;
      EFR involvement confirmed by UniProt EC 2.7.11.1 evidence."
- id: PMID:19763087
  title: Receptor quality control in the endoplasmic reticulum for plant innate immunity.
  findings: []
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "Full text available. Establishes ER quality-control (CRT3, UGGT,
      STT3A, N-glycosylation) requirement for EFR accumulation and signalling, and
      EFR subcellular localization. Supports immune signaling annotation; does not
      report an EFR-dependent hypersensitive response."
- id: PMID:20113440
  title: Early signaling through the Arabidopsis pattern recognition receptors FLS2
    and EFR involves Ca-associated opening of plasma membrane anion channels.
  findings: []
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "Abstract-only in cache. Characterizes EFR/FLS2 early PTI signaling
      (elf18-triggered, BAK1-dependent Ca-associated anion channel/depolarization).
      Supports PAMP receptor signaling pathway annotation."
- id: PMID:23395902
  title: Pseudomonas HopU1 modulates plant immune receptor levels by blocking the
    interaction of their mRNAs with GRP7.
  findings: []
  reference_review:
    relevance: MEDIUM
    correctness: VERIFIED
    review_notes: "Full text available. GRP7/RBG7 associates with EFR (and FLS2) at
      the plasma membrane and binds EFR mRNA; HopU1 blocks GRP7-mRNA binding. Source
      of an EFR protein-binding (IPI) annotation; a regulatory RNA-binding-protein
      association rather than core receptor function."
- id: PMID:24625928
  title: A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor
    activation.
  findings: []
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "Abstract-only in cache, but UniProt cites this PMID for Tyr-836/Tyr-897
      phosphorylation and BAK1/hopD2 interaction. EFR is activated by tyrosine phosphorylation;
      Y836 required for elf18-triggered immunity."
- id: PMID:27317676
  title: The Arabidopsis Malectin-Like/LRR-RLK IOS1 Is Critical for BAK1-Dependent
    and BAK1-Independent Pattern-Triggered Immunity.
  findings: []
  reference_review:
    relevance: MEDIUM
    correctness: VERIFIED
    review_notes: "Full text available. IOS1 forms complexes with EFR/FLS2/CERK1 and
      primes PTI. Source of an EFR protein-binding (IPI) annotation; supporting/regulatory
      partner rather than core EFR function."
- id: PMID:29320478
  title: An extracellular network of Arabidopsis leucine-rich repeat receptor kinases.
  findings: []
  reference_review:
    relevance: MEDIUM
    correctness: VERIFIED
    review_notes: "Full text available. Large-scale extracellular LRR-RK binary interaction
      network (Nature 2018); source of multiple EFR protein-binding (IPI) annotations
      (SERK5, BAK1, NIK1, etc.). High-throughput ectodomain interactions."
- id: PMID:29649442
  title: The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the Nucleus and Regulates
    Defense Hormone Expression during Plant Innate Immunity.
  findings: []
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "Full text available. EFR directly phosphorylates BIK1 to regulate
      JA/SA via a PRR-BIK1-WRKY axis; source of EFR Ser/Thr kinase (EXP), bacterial
      molecule response (IMP), and BIK1 protein-binding (IPI) annotations."
- id: file:ARATH/EFR/EFR-deep-research-falcon.md
  title: "Falcon/Edison deep research report: EFR"
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: "AI-generated (Falcon/Edison) deep-research synthesis used as supporting
      context; trace individual claims to primary literature before treating as definitive."
core_functions:
- description: Pattern-recognition receptor that perceives the bacterial PAMP elongation
    factor Tu (epitope elf18) as a transmembrane receptor serine/threonine protein
    kinase at the plasma membrane
  supported_by:
  - reference_id: PMID:16713565
    supporting_text: we used this finding in a targeted reverse-genetic approach to
      identify a receptor kinase essential for EF-Tu perception, which we called EFR
  - reference_id: PMID:16713565
    supporting_text: Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires
      EF-Tu binding sites and responsiveness upon transient expression of EFR
  - reference_id: file:ARATH/EFR/EFR-deep-research-falcon.md
    supporting_text: EFR is a prototypical Arabidopsis PRR for proteinaceous bacterial
      EF‑Tu epitopes (elf18/elf26).
  molecular_function:
    id: GO:0019199
    label: transmembrane receptor protein kinase activity
  directly_involved_in:
  - id: GO:0016045
    label: detection of bacterium
  - id: GO:0140426
    label: pathogen-associated molecular pattern receptor signaling pathway
  locations:
  - id: GO:0005886
    label: plasma membrane
- description: Ligand-activated protein serine/threonine kinase that autophosphorylates
    upon elf18 perception and directly phosphorylates the cytoplasmic kinase BIK1
    to propagate immune signaling
  supported_by:
  - reference_id: PMID:29649442
    supporting_text: EFR regulates the phytohormone jasmonic acid (JA) through direct
      phosphorylation of a receptor-like cytoplasmic kinase, BIK1
  - reference_id: PMID:24625928
    supporting_text: is activated upon ligand binding by phosphorylation on its tyrosine
      residues. Phosphorylation of a single tyrosine residue, Y836, is required for
      activation of EFR and downstream immunity
  molecular_function:
    id: GO:0106310
    label: protein serine kinase activity
  directly_involved_in:
  - id: GO:0140426
    label: pathogen-associated molecular pattern receptor signaling pathway
- description: Initiates PAMP-triggered immunity downstream of elf18 perception, including
    BAK1-dependent calcium-associated early signaling and activation of defense responses
  supported_by:
  - reference_id: PMID:20113440
    supporting_text: activation of FLS2 and EFR lead to BAK1-dependent, calcium-associated
      plasma membrane anion channel opening as an initial step in the pathogen defense
      pathway
  - reference_id: PMID:16713565
    supporting_text: flagellin and EF-Tu activate a common set of signaling events
      and defense responses
  - reference_id: file:ARATH/EFR/EFR-deep-research-falcon.md
    supporting_text: elf18 perception by EFR triggers canonical PTI outputs including
      ROS burst, MAPK activation, Ca2+-linked signaling, defense gene induction, callose
      deposition, and seedling growth inhibition.
  directly_involved_in:
  - id: GO:0140426
    label: pathogen-associated molecular pattern receptor signaling pathway
  - id: GO:0002237
    label: response to molecule of bacterial origin
existing_annotations:
- term:
    id: GO:0004672
    label: protein kinase activity
  evidence_type: IEA
  original_reference_id: GO_REF:0000120
  qualifier: enables
  review:
    summary: EFR is a protein kinase, so this term is correct, but it is a generic
      parent of the more specific (and experimentally supported) serine/threonine
      and serine kinase terms.
    action: KEEP_AS_NON_CORE
    reason: Correct but uninformative parent; the specific Ser/Thr kinase activity
      (GO:0106310/GO:0004674) is the core molecular function.
    supported_by:
    - reference_id: file:ARATH/EFR/EFR-notes.md
      supporting_text: EC 2.7.11.1; serine/threonine protein kinase.
- term:
    id: GO:0004674
    label: protein serine/threonine kinase activity
  evidence_type: IEA
  original_reference_id: GO_REF:0000003
  qualifier: enables
  review:
    summary: EFR is a serine/threonine protein kinase (EC 2.7.11.1) that autophosphorylates
      and phosphorylates BIK1. This EC-based mapping is correct and consistent with
      experimental kinase activity.
    action: ACCEPT
    reason: Accurate description of EFR catalytic activity, supported by experimental
      autophosphorylation and BIK1 phosphorylation.
    supported_by:
    - reference_id: PMID:29649442
      supporting_text: EFR regulates the phytohormone jasmonic acid (JA) through direct
        phosphorylation of a receptor-like cytoplasmic kinase, BIK1
- term:
    id: GO:0005524
    label: ATP binding
  evidence_type: IEA
  original_reference_id: GO_REF:0000002
  qualifier: enables
  review:
    summary: As a protein kinase EFR binds ATP; the cytoplasmic kinase domain has
      a defined ATP-binding region. Supportive molecular function consistent with
      its catalytic activity.
    action: ACCEPT
    reason: ATP binding is required for the kinase activity; consistent with the protein
      kinase ATP-binding site annotated in UniProt.
    supported_by:
    - reference_id: file:ARATH/EFR/EFR-notes.md
      supporting_text: kinase requires ATP (BINDING 718-726, 741)
- term:
    id: GO:0005886
    label: plasma membrane
  evidence_type: IEA
  original_reference_id: GO_REF:0000044
  qualifier: located_in
  review:
    summary: EFR is a single-pass type I plasma membrane protein and acts as a cell-surface
      PRR at the plasma membrane. This is a core localization.
    action: ACCEPT
    reason: Well-established plasma membrane localization of this cell-surface pattern-recognition
      receptor.
    supported_by:
    - reference_id: PMID:27317676
      supporting_text: Plasma membrane-localized pattern recognition receptors (PRRs)
        such as FLAGELLIN SENSING2 (FLS2), EF-TU RECEPTOR (EFR)
    - reference_id: file:ARATH/EFR/EFR-deep-research-falcon.md
      supporting_text: EFR is a surface-exposed transmembrane LRR-RK and the active
        signaling receptor functions at the plasma membrane.
- term:
    id: GO:0009617
    label: response to bacterium
  evidence_type: IEA
  original_reference_id: GO_REF:0000117
  qualifier: involved_in
  review:
    summary: EFR participates in the response to bacteria by perceiving bacterial
      EF-Tu, but this is a broad parent of the more specific experimentally supported
      terms (detection of bacterium, response to molecule of bacterial origin).
    action: KEEP_AS_NON_CORE
    reason: Correct but generic; more specific terms better capture EFR function.
    supported_by:
    - reference_id: PMID:16713565
      supporting_text: Arabidopsis plants detect a variety of PAMPs including conserved
        domains of bacterial flagellin and of bacterial EF-Tu
- term:
    id: GO:0012505
    label: endomembrane system
  evidence_type: IEA
  original_reference_id: GO_REF:0000044
  qualifier: located_in
  review:
    summary: EFR transits the secretory/endomembrane system during biogenesis (it
      is also annotated as single-pass type I endomembrane protein), but plasma membrane
      is the functionally relevant and more informative location.
    action: KEEP_AS_NON_CORE
    reason: True but broad; reflects ER transit/biogenesis rather than the site of
      receptor action.
    supported_by:
    - reference_id: PMID:19763087
      supporting_text: act in concert with STT3A-containing oligosaccharyltransferase
        complex in an N-glycosylation pathway in the endoplasmic reticulum
- term:
    id: GO:0031349
    label: positive regulation of defense response
  evidence_type: IEA
  original_reference_id: GO_REF:0000117
  qualifier: involved_in
  review:
    summary: EFR positively regulates plant defense; perception of EF-Tu/elf18 activates
      PTI defense responses and increases resistance, and loss of EFR enhances pathogen
      susceptibility.
    action: ACCEPT
    reason: EFR is a positive regulator of defense responses; consistent with experimental
      loss- and gain-of-function evidence.
    supported_by:
    - reference_id: PMID:16713565
      supporting_text: plant defense responses induced by PAMPs such as EF-Tu reduce
        transformation by Agrobacterium
    - reference_id: file:ARATH/EFR/EFR-deep-research-falcon.md
      supporting_text: EFR contributes to antibacterial immunity and induced resistance,
        including restriction of Pseudomonas syringae pv. tomato DC3000 growth after
        elf18 pretreatment.
- term:
    id: GO:0106310
    label: protein serine kinase activity
  evidence_type: IEA
  original_reference_id: GO_REF:0000116
  qualifier: enables
  review:
    summary: EFR is a protein serine kinase (Rhea/EC mapping). Same activity is also
      experimentally supported (EXP annotations below). Core molecular function.
    action: ACCEPT
    reason: Accurate; the same activity is corroborated by experimental EXP annotations.
    supported_by:
    - reference_id: PMID:18158241
      supporting_text: AvrPto binds receptor kinases, including Arabidopsis FLS2 and
        EFR
- term:
    id: GO:0005515
    label: protein binding
  evidence_type: IPI
  original_reference_id: PMID:23395902
  qualifier: enables
  review:
    summary: GRP7/RBG7 associates with EFR at the plasma membrane and binds EFR mRNA;
      this is a real interaction but the bare protein binding term is uninformative
      about EFR's function. The biologically meaningful relationship is regulatory
      (RNA-binding-protein co-association).
    action: MARK_AS_OVER_ANNOTATED
    reason: Bare protein binding is not informative as a core molecular function;
      per curation guidance more specific terms should capture the relationship.
    supported_by:
    - reference_id: PMID:23395902
      supporting_text: GRP7 directly interacts in vivo with the PRRs FLS2 and EFR
        in a specific manner
- term:
    id: GO:0005515
    label: protein binding
  evidence_type: IPI
  original_reference_id: PMID:24625928
  qualifier: enables
  review:
    summary: This IPI captures EFR interactions with BAK1 and with the bacterial effector
      HopAO1/hopD2 (effector that dephosphorylates EFR). Real interactions but the
      bare protein binding term is uninformative.
    action: MARK_AS_OVER_ANNOTATED
    reason: Generic protein binding; the meaningful co-receptor and effector-targeting
      relationships are better captured by specific terms.
    supported_by:
    - reference_id: PMID:24625928
      supporting_text: A tyrosine phosphatase, HopAO1, secreted by P. syringae, reduces
        EFR phosphorylation
- term:
    id: GO:0005515
    label: protein binding
  evidence_type: IPI
  original_reference_id: PMID:29320478
  qualifier: enables
  review:
    summary: From a large-scale extracellular LRR-RK binary interaction network; multiple
      EFR ectodomain interactions (SERK5, BAK1, NIK1, etc.). Real high-throughput
      interactions but the bare protein binding term is uninformative.
    action: MARK_AS_OVER_ANNOTATED
    reason: Generic protein binding from a high-throughput screen; uninformative as
      a core function.
    supported_by:
    - reference_id: PMID:29320478
      supporting_text: An extracellular network of Arabidopsis leucine-rich repeat
        receptor kinases
- term:
    id: GO:0106310
    label: protein serine kinase activity
  evidence_type: EXP
  original_reference_id: PMID:18158241
  qualifier: enables
  review:
    summary: Experimental evidence for EFR protein serine kinase activity (autophosphorylation
      and catalytic activity; UniProt cites this PMID for EC 2.7.11.1). Core molecular
      function.
    action: ACCEPT
    reason: Experimentally supported core kinase activity of EFR.
    supported_by:
    - reference_id: file:ARATH/EFR/EFR-notes.md
      supporting_text: EC 2.7.11.1; serine/threonine protein kinase. CATALYTIC ACTIVITY
        records cite PubMed:18158241 and PubMed:29649442.
- term:
    id: GO:0106310
    label: protein serine kinase activity
  evidence_type: EXP
  original_reference_id: PMID:29649442
  qualifier: enables
  review:
    summary: Experimental evidence that EFR directly phosphorylates BIK1, demonstrating
      its protein serine kinase activity. Core molecular function.
    action: ACCEPT
    reason: "Experimentally supported; EFR directly phosphorylates the substrate BIK1.
      Note from the Falcon deep-research synthesis - a more recent allosteric-activation
      model (Muhlenbeck/Bender/Zipfel 2024) proposes that EFR catalytic activity can
      be partly dispensable in vivo and that BIK1 trans-phosphorylation is driven largely
      by EFR-activated BAK1; the direct EFR->BIK1 kinase-substrate annotation is retained
      but this mechanistic nuance should be considered when interpreting EFR's catalytic
      role."
    supported_by:
    - reference_id: PMID:29649442
      supporting_text: EFR regulates the phytohormone jasmonic acid (JA) through direct
        phosphorylation of a receptor-like cytoplasmic kinase, BIK1
- term:
    id: GO:0140426
    label: pathogen-associated molecular pattern receptor signaling pathway
  evidence_type: IMP
  original_reference_id: PMID:20113440
  qualifier: acts_upstream_of_or_within
  review:
    summary: EFR initiates PAMP-triggered immune signaling upon elf18 perception,
      including BAK1-dependent calcium-associated early signaling. This is the defining
      biological process for EFR.
    action: ACCEPT
    reason: Core biological process; EFR is the PRR that initiates the PAMP receptor
      signaling pathway.
    supported_by:
    - reference_id: PMID:20113440
      supporting_text: activation of FLS2 and EFR lead to BAK1-dependent, calcium-associated
        plasma membrane anion channel opening as an initial step in the pathogen defense
        pathway
    - reference_id: file:ARATH/EFR/EFR-deep-research-falcon.md
      supporting_text: elf18 perception by EFR triggers canonical PTI outputs including
        ROS burst, MAPK activation, Ca2+-linked signaling, defense gene induction,
        callose deposition, and seedling growth inhibition.
- term:
    id: GO:0002237
    label: response to molecule of bacterial origin
  evidence_type: IMP
  original_reference_id: PMID:29649442
  qualifier: involved_in
  review:
    summary: EFR responds to the bacterial molecule EF-Tu (elf18) to activate immune
      signaling. Core function consistent with its identity as the EF-Tu receptor.
    action: ACCEPT
    reason: EFR perceives bacterial EF-Tu/elf18; well-supported core process.
    supported_by:
    - reference_id: PMID:29649442
      supporting_text: EFR is a PRR that recognizes bacterial EF-Tu and
        activates immune signaling
- term:
    id: GO:0005515
    label: protein binding
  evidence_type: IPI
  original_reference_id: PMID:29649442
  qualifier: enables
  review:
    summary: EFR binds the cytoplasmic kinase BIK1 (associates in absence of ligand,
      dissociates upon PAMP perception, and phosphorylates it). A real and functionally
      important interaction, but the bare protein binding term is uninformative; the
      kinase-substrate relationship is captured by the Ser/Thr kinase activity terms.
    action: MARK_AS_OVER_ANNOTATED
    reason: Bare protein binding; the meaningful EFR-BIK1 kinase-substrate relationship
      is better represented by the kinase activity annotations.
    supported_by:
    - reference_id: PMID:29649442
      supporting_text: direct phosphorylation of a receptor-like cytoplasmic kinase,
        BIK1
- term:
    id: GO:0005886
    label: plasma membrane
  evidence_type: ISM
  original_reference_id: GO_REF:0000122
  qualifier: located_in
  review:
    summary: Predicted (AtSubP) plasma membrane localization, consistent with the
      experimentally and structurally supported plasma membrane location of this cell-surface
      PRR. Core localization.
    action: ACCEPT
    reason: Consistent with established plasma membrane localization of EFR.
    supported_by:
    - reference_id: PMID:27317676
      supporting_text: Plasma membrane-localized pattern recognition receptors (PRRs)
        such as FLAGELLIN SENSING2 (FLS2), EF-TU RECEPTOR (EFR)
- term:
    id: GO:0005515
    label: protein binding
  evidence_type: IPI
  original_reference_id: PMID:27317676
  qualifier: enables
  review:
    summary: EFR forms a complex with the malectin-like LRR-RLK IOS1, which primes
      PTI. Real interaction, but the bare protein binding term is uninformative about
      EFR function.
    action: MARK_AS_OVER_ANNOTATED
    reason: Generic protein binding with a regulatory partner; uninformative as a
      core molecular function.
    supported_by:
    - reference_id: PMID:27317676
      supporting_text: complexes between the membrane-localized IOS1 and
        BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1)-dependent PRRs
        FLS2 and EFR
- term:
    id: GO:0005515
    label: protein binding
  evidence_type: IPI
  original_reference_id: PMID:18158241
  qualifier: enables
  review:
    summary: EFR binds the Pseudomonas effector AvrPto, which inhibits receptor kinase
      activity. Real interaction, but the bare protein binding term is uninformative;
      the relevant biology (effector targeting) is not captured by this generic term.
    action: MARK_AS_OVER_ANNOTATED
    reason: Generic protein binding (effector interaction); uninformative as core
      function.
    supported_by:
    - reference_id: PMID:18158241
      supporting_text: AvrPto binds receptor kinases, including Arabidopsis FLS2 and
        EFR
- term:
    id: GO:0002764
    label: immune response-regulating signaling pathway
  evidence_type: IMP
  original_reference_id: PMID:19763087
  qualifier: acts_upstream_of_or_within
  review:
    summary: EFR signaling regulates plant immune responses; this paper studies EFR
      function and its ER quality-control dependence (EFR accumulation and signalling
      impaired in psl/stt3a mutants). Consistent with EFR's role in immune signaling.
    action: ACCEPT
    reason: EFR initiates and regulates immune response signaling; supported by EFR
      functional/quality-control studies.
    supported_by:
    - reference_id: PMID:19763087
      supporting_text: EFR accumulation and signalling, but not of FLS2, are impaired
        in psl1, psl2, and stt3a plants
- term:
    id: GO:0009626
    label: plant-type hypersensitive response
  evidence_type: IMP
  original_reference_id: PMID:19763087
  qualifier: acts_upstream_of_or_within
  review:
    summary: This paper concerns ER quality control of EFR and elf18-triggered (PTI)
      responses (anthocyanin de-repression, SA-dependent defense), not a classical
      EFR-dependent hypersensitive response (programmed cell death). Surface PRRs
      like EFR drive PTI and generally do not by themselves trigger HR, which is the
      hallmark of NLR-mediated effector-triggered immunity. The abstract does not
      mention hypersensitive response.
    action: MARK_AS_OVER_ANNOTATED
    reason: HR/programmed cell death is not a core EFR (surface PRR) output; this
      IMP annotation likely over-propagates a general defense role to the specific
      HR term. Retained (not removed) as an experimental TAIR annotation whose full
      reasoning cannot be fully verified from the cached text.
    supported_by:
    - reference_id: file:ARATH/EFR/EFR-notes.md
      supporting_text: PTI by surface PRRs like EFR generally does NOT trigger
        HR/cell death (that is the hallmark of ETI/intracellular NLRs)
- term:
    id: GO:0019199
    label: transmembrane receptor protein kinase activity
  evidence_type: TAS
  original_reference_id: PMID:19763087
  qualifier: enables
  review:
    summary: EFR is a single-pass transmembrane receptor that combines elf18 ligand
      perception (ectodomain) with intracellular serine/threonine kinase signaling.
      This is the most informative molecular function term for EFR, capturing both
      the receptor and catalytic activities.
    action: ACCEPT
    reason: Most informative MF term; matches the GO definition (combining with a
      signal and transmitting it across the membrane to initiate change via protein
      phosphorylation). Core function.
    supported_by:
    - reference_id: PMID:16713565
      supporting_text: a receptor kinase essential for EF-Tu perception, which we
        called EFR
- term:
    id: GO:0016045
    label: detection of bacterium
  evidence_type: IDA
  original_reference_id: PMID:16713565
  qualifier: acts_upstream_of_or_within
  review:
    summary: EFR detects the bacterial PAMP EF-Tu; transient expression in N. benthamiana
      confers EF-Tu binding and responsiveness, and efr mutants are altered in bacterial
      interaction. Core biological process.
    action: ACCEPT
    reason: Direct experimental evidence that EFR detects bacterial EF-Tu; core to
      its function as the EF-Tu receptor.
    supported_by:
    - reference_id: PMID:16713565
      supporting_text: Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires
        EF-Tu binding sites and responsiveness upon transient expression of EFR
proposed_new_terms: []
suggested_questions:
- question: Does EFR-mediated PTI ever contribute to localized cell death/hypersensitive-response-like
    outputs, or is the GO:0009626 annotation an over-extension of a general defense
    role?
  experts:
  - Plant immunity researchers
- question: What is the complete set of direct EFR kinase substrates beyond BIK1,
    and how does tyrosine phosphorylation (e.g. Y836) shape substrate selection?
  experts:
  - Plant receptor kinase signaling researchers
suggested_experiments:
- hypothesis: EFR-dependent PTI does not require a hypersensitive-response/programmed
    cell death module
  description: Compare elf18-triggered responses (ROS, MAPK, callose, defense gene
    induction) versus cell-death markers in wild-type and efr mutants, and test whether
    HR-associated readouts are EFR-independent.
- hypothesis: Tyrosine phosphorylation of EFR (Y836) gates substrate phosphorylation
    of BIK1 and downstream hormone outputs
  description: Use EFR Y836F and kinase-dead (D849N) variants to measure BIK1 phosphorylation,
    JA/SA accumulation, and resistance to P. syringae, dissecting the contribution
    of tyrosine versus serine/threonine phosphorylation.