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Thirty years of resistance: Zig-zag through the plant immune system

Bruno Pok Man Ngou, Pingtao Ding, Jonathan D G Jones

The Plant Cell · 2022 · Review · CC BY

doi:10.1093/plcell/koac041

Abstract

Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 . Since then, many cell-surface pattern recognition receptors (PRRs) have been identified, and R genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) have been cloned. Here, we provide a list of characterized PRRs and NLRs. In addition to immune receptors, many components of immune signaling networks were discovered over the last 30 years. We review the signaling pathways, physiological responses, and molecular regulation of both PRR- and NLR-mediated immunity. Recent studies have reinforced the importance of interactions between the two immune systems. We provide an overview of interactions between PRR- and NLR-mediated immunity, highlighting challenges and perspectives for future research.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 16, 2026. Paragraph numbers are ours, so an answer can point at one.

The plant immune system

Plants are constantly challenged by diverse organisms, including viruses, bacteria, fungi, oomycetes, herbivores, and parasitic plants. Disease ensues when a plant is susceptible to any of these organisms. Plants carry powerful defense mechanisms. To cause disease, pathogens usually need to evade detection by the host and/or to suppress these immune responses. Cell-surface pattern recognition receptors (PRRs) in plants recognize conserved pathogen-/damage-/microbe-/herbivore-associated molecular patterns (PAMPs/DAMPs/MAMPs/HAMPs) and activate pattern-triggered immunity (PTI), which restricts pathogenicity. PRRs are plasma membrane (PM)-associated and are usually either receptor-like kinases (RLKs) or receptor-like proteins (RLPs) that lack a protein kinase domain. Pathogens have evolved to evade or suppress PTI through secreted effector molecules, which results in effector-triggered susceptibility (ETS). Plants, in turn, have evolved intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) to detect effectors, which are often encoded by Resistance (R) genes, and activate effector-triggered immunity (ETI) upon effector perception. Pathogens might then evolve or diversify or lose effectors to suppress or evade ETI. The interaction between PTI, ETS, and ETI was incorporated into the widely cited “zig-zag-zig” intellectual framework.

The alphabet soup digested: nomenclatures applied to the plant immune system

PTI was originally an abbreviation for “PAMP-triggered immunity”, mediated by PRRs such as Arabidopsis thaliana Flagellin-Sensing 2 (FLS2). ETI is an acronym for “effector-triggered immunity,” which is mostly mediated by NLRs, but can also involve RLP-mediated detection of apoplastic effectors. While the terms PTI and ETI are frequently used in the literature, there are limitations to their use in describing specific immune responses. For example, the apoplastic effector Avr4 from the tomato (Solanum lycopersicum) leaf mold pathogen Cladosporium fulvum binds to fungal chitin to retard cell wall degradation by host chitinases and thus the release of N-acetyl glucosamine oligomers that activate defense. Avr4 is recognized by the tomato cell-surface RLP Cf-4. Thus, while immunity activated by some PRRs can be classified as PTI, others can be classified as ETI, since cell-surface receptors can recognize both PAMPs and apoplastic effectors. Other terms have been introduced to classify immune responses based on receptors, such as PRR-mediated immunity and NLR-mediated immunity. Immune responses are best defined by the location of recognition by the initiating protein, such as extracellularly triggered immunity and intracellularly triggered immunity, or surface-receptor-mediated immunity and intracellular-receptor-mediated immunity. Each of these terms has its own advantages and should be used with caution (Figure 1A). In this review, we try to minimize the overuse of these acronyms and emphasize immune responses triggered by the corresponding receptors.

Structural and evolutionary overview of PRR proteins

Plant PRR proteins are either RLPs or RLKs. RLKs consist of an extracellular domain, a transmembrane domain, and cytoplasmic kinase domain. RLPs lack a cytoplasmic kinase domain, and both require co-receptors to transduce immune signals. PRRs are localized to the PM via a transmembrane α-helix or a glycophosphatidylinositol (GPI) anchor. Both RLPs and RLKs perceive ligands via a range of extracellular domains. These include leucine-rich repeat (LRR), lectin, malectin, lysin motif (LysM), and epidermal growth factor-like domains.

RLKs are found in Plasmodium, plants, and animals but not fungi. Conceivably, RLKs were present in the common ancestors of these organisms but were later lost in the fungi. Plant RLKs underwent remarkable expansion and constitute 60% of the kinases in the Arabidopsis genome. Arabidopsis RLKs can be classified into 44 subfamilies based on their kinase domains. The LRR–RLKs represent the largest subfamily of RLKs and are the best characterized RLKs in plants. A phylogenetic study of 33 plant species concluded that the average number of LRR–RLKs in angiosperms is approximately 250 per species (; Figure 1B). LRR–RLKs are further classified into 20 subgroups, with subgroup XII constituting genes involved in pathogen recognition, such as FLS2, EFR, and Xa21. Interestingly, the gene number in the LRR–RLK subgroup XII is highly variable across plant species, indicating that these genes underwent either expansion or contraction in particular lineages. Similarly, the LRR–RLPs represent the largest subfamily of RLPs in plants, and the size of this gene family is also highly variable across plant species (; Figure 1B).

Structural and evolutionary overview of NLR proteins

NLRs are grouped into three classes according to their N-terminal domains: coiled-coil (CC) NLRs (CNLs), Toll/Interleukin-1 receptor/Resistance (TIR) protein NLRs (TNLs), and RPW8-like CC domain (RPW8) NLRs (RNLs). Both CNLs and RNLs contain N-terminal CC-domains. Plant NLRs carry a nucleotide-binding (NB) domain shared by APAF-1, various plant R proteins and CED-4 (together, the NB-ARC domain), and LRR domains at their C-termini. These domains vary between NLRs, and additional noncanonical domains can be integrated into some NLRs (also known as NLR-integrated domains, or NLR-IDs; ). The functions of these domains also vary among NLRs. The LRR domain is involved in direct or indirect recognition of effectors. The NB-ARC domain exhibits ATP binding activity and acts as a switch for NLR activation (. The CC, TIR, and RPW8 domains function as signaling domains to downstream responses upon NLR activation. Some CC-domains are involved in effector recognition and interact directly with effectors (Avr-Pik) as well as a “guardee” protein (such as RIN4), which is a target of pathogen effectors. The α-helices in both the CC and RPW8 domains were recently shown to form cation channels required for defense signaling. TIR domains can also self-associate or associate with the TIR domains from paired TNLs, which is crucial for their activation. TIR domains, upon oligomerization, exhibit NADase activity, which leads to the production of variant-cyclic-ADP-ribose (v-cADPR;; ). TIR domains also exhibit 2′,3′-cAMP/cGMP synthetase activity. These small molecules produced by TIR domains likely function in signaling. The ID domain in NLR-IDs functions as a decoy, which enables the NLR to detect effectors targeting proteins with homology to the ID.

NLR genes are present in the genomes of all land plants. CNLs, TNLs, and RNLs are present in basal angiosperm species such as Amborella and Nymphaea. However, TNLs are absent from most monocot genomes, indicating that gene loss likely occurred before monocots diverged from dicots. The loss of TNLs was also accompanied by the loss of TNL-signaling components, such as ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), PHYTOALEXIN DEFICIENT 4 (PAD4), and SENESCENCE-ASSOCIATED GENE 101 (SAG101;; ). The loss of these signaling components may have driven the contraction of TNLs in some angiosperm lineages, or vice versa. Similar to the LRR–RLK-XII and LRR–RLP, the number of NLRs (or NB-ARC containing proteins) is also highly variable across the angiosperms. Furthermore, the LRR–RLK-XII, LRR–RLP, and NLR gene families have undergone lineage-specific co-expansion or co-contraction (; Figure 1B). The cause of these concerted expansions and/or contractions is currently unclear but has been proposed to be linked to pathogen pressure and ecological specialization.

PRRs involved in pathogen recognition

PRRs recognize PAMPs/MAMPs/HAMPs from bacteria, fungi, oomycetes, parasitic plants, and herbivores. Some PRRs also recognize self-molecules, such as DAMPs and other plant endogenous peptides (phytocytokines; ). Some PRRs are not involved in direct ligand recognition but function as PRR co-receptors and negative regulators of immune signaling. There are more than 60 characterized immunity-related PRRs with known elicitors, and we attempt here to list those PRRs with known elicitors that are involved in pathogen recognition (Figure 2). Due to space limitations, some PRR gene names are abbreviated: the full gene names can be found in Supplemental Data Set 1.

PRRs involved in bacterial recognition

Plants perceive a range of PAMPs from bacteria, including peptides, lipids, peptidoglycans (PGs), and polysaccharides. Arabidopsis perceives the bacteria-derived peptides flg22, elf18, and xup25 via the LRR–RLKs AtFLS2, AtEFR, and AtXPS1 and the proteinaceous eMAX and translation initiation factor 1 via the LRR–RLPs AtRLP1 and AtRLP32, respectively. Other bacterial peptides such as RaxX21, flgII-28, and csp22 are perceived by rice (Oryza sativa) OsXa21, tomato SlFLS3, and SlCORE/NbCSPR (from tomato and Nicotiana benthamiana), respectively. The bacterial lipid 3-hydroxydecanoic acid is perceived through the lectin receptor kinase AtLORE. PGs from bacterial cell walls are perceived by the LysM-containing RLP AtLYM1/3 and rice OsLYP4/6. Bacterial exopolysaccharides are perceived by the LysM-containing RLK LjEPR3 from Lotus japonicus to control rhizobium infections (; Figure 2A).

PRRs involved in fungal recognition

The fungal cell wall comprises chitin and oligo-galacturonides (OGs), which are perceived by multiple PRRs. Chitin is perceived by LysM-containing RLKs such as AtLYM2/4/5, OsLYP4/6, Medicago truncatula MtLYK4/9, grapevine (Vitis vinifera) VvLYK1-1/2, L. japonicus LjLYS6, and pea (Pisum sativum) PsLYK9. OGs are perceived by the cell wall-associated kinases AtWAK1/2. AtWAK1/2 also perceive pectin from the plant cell wall. The common wheat (Triticum aestivum) wall-associated kinase TaWAK perceives the protein SnTox1 from the necrotrophic fungal pathogen Parastagonospora nodorum and induces cell death. In addition to the fungal cell wall, apoplastic effectors from fungal pathogens are recognized by multiple LRR–RLPs. These include SlCf-2, SlCf-4, SlCf-5, SlCf-9, SlEIX2, SlVe1, SlHrc9-4E, SlI, SlI-3, and Brassica napus BnRLM2. A proteinaceous elicitor from the fungal pathogen Sclerotinia sclerotiorum, sclerotinia culture filtrate elicitor 1, is perceived by AtRLP30, and fungal endopolygalacturonases (endo-PGs) are perceived by the LRR–RLP AtRLP42 (,; Figure 2B).

PRRs involved in the recognition of oomycetes

The oomycete cell wall is also composed of chitin, endo-PGs, and OGs. Thus, plants also perceive oomycetes via PRRs described in the previous section. In addition, some PRRs recognize specific PAMPs from oomycetes. For example, the glycoside hydrolase XEG1 from Phytophthora sojae is recognized by the LRR–RLP NbRXEG1. INF1 elicitin from Phytophthora infestans is recognized by the LRR–RLP SmELR from Solanum microdontum. Arabidopsis AtRLP23 recognizes a conserved peptide (nlp20) in necrosis and ethylene (ET)-inducing peptide 1-like protein (NLP) from multiple pathogens, including Phytophthora parasitica. The Arabidopsis lectin-receptor kinase AtRDA2 was recently shown to recognize 9-methyl sphingoid base, a PAMP derived from oomycete ceramide (; Figure 2C).

PRRs involved in self-recognition

Plants perceive DAMPs and phytocytokines from damaged or infected tissues to amplify and modulate immune responses against pathogens. Damage-induced cytosolic calcium influx activates metacaspases, which cleave the DAMP precursor PROPEPs into PEPs. PEPs are then secreted and perceived by the LRR–RLKs AtPEPR1/2. Multiple phytocytokines are upregulated during immunity. The stress-induced plant signaling peptides CTNIPs are upregulated during PTI and are perceived by the Arabidopsis LRR–RLK AtHSL3. Another defense-induced secreted peptide, PIP1, is recognized by AtRLK7. The Arabidopsis LRR–RLK AtMIK2 perceives the phytocytokine SCOOP peptides and SCOOP-like peptides from Fusarium spp.. Thus, AtMIK2 is involved in both self and fungal recognition during immunity. Plant PRRs also perceive a range of extracellular (e) self-molecules, such as eH2O2, eATP, and eNAD. These molecules are perceived by AtHPCA1 (also known as AtCARD1), AtDORN1, and AtLecRK-1.8, respectively. In tomato, the hormone peptide systemin is perceived by SlSYR1/2 to enhance resistance against herbivores (; Figure 2D).

PRRs involved in the recognition of parasitic plants

In addition to eH2O2, AtCARD1 has also been shown to perceive the self-derived quinone compound 2,6-dimethoxy-1,4-benzoquinone (DMBQ; ). Perception of DMBQ induces AtCARD1-dependent immune responses. On the other hand, the parasitic plant Phtheirospermum japonicum perceives DMBQ via AtCARD1 homologs PjCADL1/2/3, which leads to development of haustoria for parasitic infection. Thus, CARD1 is involved in both immunity (for nonparasitic plants) and parasitic plant infection. Plants also perceive PAMPs from parasitic plants to restrict infection. The tomato LRR–RLP SlCuRe1 perceives the peptide Crip21 from the parasitic plant Cuscuta spp.. Crip21 is derived from a Cuscuta glycine-rich cell wall protein. Activation of SlCuRe1 by Crip21 elicits cell death and defense responses in tomato (; Figure 2E).

PRRs involved in viral recognition

While some PRRs, such as AtNIK1, have been shown to be required for viral resistance, no PRR has been reported to directly perceive viral particles. However, the Arabidopsis PRR co-receptor bak1 loss-of-function mutant exhibits enhanced susceptibility to multiple viruses. In addition, exogenous application of double-stranded RNAs and viral coat protein (CP) elicits PTI responses in plants. Conceivably, some uncharacterized PRR(s) are involved in the recognition of viral PAMPs (Figure 2F).

PRRs involved in the recognition of animals

In addition to eNAD+, AtLecRK-1.8 and AtLecRK-1.1 are involved in the perception of Pieris brassicae (cabbage moth) eggs. The ligand from P. brassicae eggs that activates AtLecRK-1.8 remains to be identified and characterized. The Arabidopsis LRR–RLK AtNILR1 is involved in the perception of Heterodera schachtii (sugarbeet nematode) extracts, and nilr1 mutants are hypersusceptible to nematode infection. The cowpea (Vigna unguiculata) LRR–RLP VuINR was shown to perceive inceptin, a proteolytic fragment of chloroplastic ATP synthase from the oral secretions of Lepidopteran herbivores (a HAMP; ). Whether PRRs can perceive ligands directly from herbivores remains to be determined (Figure 2G).

PRR co-receptors

Most, if not all, PRRs function with co-receptors to activate downstream immune responses. Multiple LRR–RLKs, such as FLS2, EFR, and PEPRs function with the co-receptors AtBAK1 and AtBKK1. LRR–RLPs function with the co-receptors SOBIR1 and BAK1, and the LysM-RLK LYKs and LysM-RLP LYMs function with the co-receptor CERK1. These co-receptors are highly conserved in land plants and are crucial for PRR-mediated immunity (Figure 2H).

NLRs involved in pathogen recognition

Sensor NLRs are involved in the recognition of effectors from viruses, bacteria, fungi, oomycetes, parasitic plants, and herbivores. Some NLRs act as helpers or co-receptors to transduce immune signals from sensor NLRs following effector recognition. Currently, there are more than 140 characterized NLRs with known recognized effectors. Here, we summarize a list of NLRs involved in effector recognition (Figure 3; Supplemental Data Set 2).

NLRs involved in bacterial recognition usually act by guarding host components

Bacterial effectors have been selected that target PRR signaling components and suppress host immunity. Plants have evolved multiple NLRs to guard host immune components, which indirectly detect bacteria and induce ETI. For example, the Pseudomonas syringae effector AvrPto suppresses PTI by inhibiting host kinase activity. The tomato decoy kinase Pto is guarded by the CNL Prf, which detects the perturbation of Pto kinase activity by AvrPto and activates ETI. Since plants have evolved multiple NLRs to guard central immune signaling pathways, some effectors from P. syringae are recognized by multiple NLRs from different plant species. Examples include the following: AvrB is recognized by AtTAO1, AtRPM1, and Glycine max GmRPG1b. AvrRpm1 from P. syringae pv. maculicola (Pma) is recognized by AtRPM1, AtRPS2, and GmRPG1r. AvrPphB is recognized by AtRPS5, Hordeum vulgare HvPbr1.b and HvPbr1.c. AvrRpt2 from P. syringae and RipBN from Ralstonia pseudosolanacearum are recognized by the CNL Ptr1 from multiple Solanaceous species. In addition, AvrRpt2 is recognized by the CNL AtRPS2, and AvrRpt2_EA from Erwinia amylovora is recognized by FB_MR5 from Malus × robusta 5. HopA1 is recognized by AtRPS6, and HopAI1 is recognized by both AtSUMM2 and AtRPS6.

On the other hand, central hubs of the immune system are targeted by multiple effectors. Correspondingly, NLRs, which guard central immune signaling components, can recognize multiple effectors. For example, the CNL AtZAR1 functions with the pseudokinase RKS1 to guard the receptor-like cytoplasmic kinase (RLCK) PBL2. By guarding RLCKs or decoy pseudokinases, AtZAR1 indirectly recognizes HopZ1a, HopF2, HopBA1, HopO1, HopX1, and AvrAC from P. syringae or Xanthomonas campestris, and potentially more effectors that target RLCKs. NbZAR1 is also required to recognize XopJ4 from Xanthomonas perforans via the pseudokinase JIM2. Other examples include the following: AvrRpm1Psa and AvrRpm1Psy from P. syringae pv. actinidiae biovar 3 (Psa) and P. syringae pv. syringae strain B728a (Psy) are recognized by Nicotiana tabacum NitabRPA1. AvrE and HopAA are both recognized by Arabidopsis CAR1. AvrRps4 from P. syringae pv. pisi and PopP2 from Ralstonia solanacearum are recognized by the paired-TNLs AtRRS1-R and AtRPS4. In addition, AvrRps4 can also be recognized by the paired-TNLs AtRRS1B and AtRPS4B. The TNL NbRoq1 recognizes HopQ1-1, XopQ, and RipB from P. syringae, Xanthomonas, and R. solanacearum, respectively. Multiple TRANSCRIPTION ACTIVATOR-LIKE (TAL) effectors from Xanthomonas oryzae are recognized by the CNLs OsXo1 and OsXa1.The tomato TNL SlBs4 also recognizes multiple Xanthomonas effectors. AvrRxo1-ORF1 from X. oryzae and Burkholderia andropogonis are recognized by the CNL ZmRxo1 from maize (Zea mays;; Figure 3A).

NLRs involved in fungal recognition

Plant NLRs recognize multiple effectors and molecules from fungal pathogens. Victorin, a secondary metabolite from Cochliobolus victoriae, is recognized by LOV1 from Arabidopsis and Phaseolus vulgaris. AvrFom2 from Fusarium oxysporum is recognized by the CNL CmFom-2 from Cucumis melo. Hordeum vulgare RESISTANCE LOCUS A NLRs recognize a range of effectors from Blumeria graminis (;; and can even recognize races of wheat stripe rust. Multiple TNLs from Linum usitatissimum recognize effectors from Melampsora lini. Effectors from the rice blast fungus Magnaporthe oryzae are recognized by multiple CNLs from O. sativa (;,;,;;;;;;;;. Effectors from B. graminis, P. nodorum, Pyrenophora tritici-repentis, and Puccinia graminis are recognized by multiple CNLs from Triticum species. AvrSr50 from P. graminis is recognized by ScSr50 from Secale cereale. Avr2 from F. oxysporum is recognized by the CNL SlI2, and Pc-toxin from Periconia circinata is recognized by the CNL SbPc from Sorghum bicolor (;;; Figure 3B).

NLRs involved in the recognition of oomycetes

Multiple effectors from Hyaloperonospora arabidopsidis (Hpa) are recognized by Arabidopsis NLRs. ATR1, ATR4, ATR5, ATR13, and ATR39 are recognized by AtRPP1, AtRPP4, AtRPP5, AtRPP13, and AtRPP39, respectively. CX2CX5G effector-like proteins (CCG effectors) from Albugo candida are recognized by AtWRR4A and AtWRR4B.

The oomycete genus Phytophthora carries multiple phytopathogenic species that cause enormous crop losses worldwide. Identification of NLRs that recognize Phytophthora effectors provides resources for crop resistance. The P. sojae effectors Avr1k and Avr1b-1 are recognized by GmRps1-k. Effectors from P. infestans are also recognized by NLRs from multiple Solanaceae species. For example, the effectors Avramr1 and Avramr3, with homologs in many Phytophthora species, are recognized by Rpi-amr1 (from Solanum americanum) and Rpi-amr3, respectively. Avrblb1 is recognized by Rpi-blb1 (from Solanum bulbocastanum), Rpi-pta1, and Rpi-sto1 (from Solanum stoloniferum;; ). Avrblb2 is recognized by Rpi-blb2 and R9a (from S. bulbocastanum and Solanum demissum, respectively;; ). PexRD12 is recognized by Rpi-chc1 (from Solanum chacoense;; ). Avr1, Avr3b, and Avr8 are recognized by R1, R3b, and R8, respectively. PiAvr2 is recognized by multiple NLRs from Solanaceae. Avr3a is recognized by Rpi-sto2 and R3a (from Solanum tuberosum;;;; ). Avrvnt1 is recognized by Rpi-vnt1 from Solanum venturi (;; Figure 3C).

Apparent absence of NLRs involved in self-recognition in plants

In mammals, DAMPs can be indirectly recognized the intracellular NOD-, LRR-, and pyrin domain-containing protein 3-inflammasome in macrophages. However, no plant NLRs have been reported to detect self-molecules so far (Figure 3D).

NLRs involved in the recognition of parasitic plants

Virus-induced silencing of the CNL VuRSG3-301 from V. unguiculata leads to enhanced susceptibility to the parasitic plant Striga gesnerioides race 3. The effector recognized by VuRSG3-301 has not yet been identified (Figure 3E).

NLRs involved in viral recognition

The CPs from different viruses are recognized by pepper (Capsicum annuum) CaL1, CaL1a, Capsicum baccatum CbL2b, Capsicum chacoense CchaL4, Capsicum chinense CchiL1c, CchiL3, Capsicum frutescens CfL2, Nicotiana sylvestris NsN′, Solanum acaule Rx2, S. stoloniferum Rysto, and potato (S. tuberosum) Rx. Viral movement proteins are recognized by Tm2, SlTm22, and SlSw5-b. The RNA-dependent RNA Polymerase (NIb) of potyviruses is recognized by the Ca Pvr4. The RNA silencing suppressor protein NSs from tomato spotted wilt virus is recognized by CchiTsw. P3 cistrons from soybean mosaic virus are recognized by Gm3gG2. The helicase domain of the tobacco mosaic virus replicase (p50) is recognized by Nicotiana glutinosa N. Cucumber mosaic virus 2a protein is recognized by P. vulgaris PvRT4-4. To summarize, multiple components involved in the process of viral infection are recognized by NLRs (Figure 3F).

NLRs involved in the recognition of animals

Multiple NLRs were shown to be involved in resistance against herbivores. NLRs involved in nematode resistance include the TIR–NB–LRR pair AtDSC1 and AtWRKY19, Aegilops tauschii AtaCD3.1, CaMi, Prunus cerasifera PcMa, SlHero, StGpa-2, and StGro1-4. In addition, the tomato Mi gene confers resistance to multiple herbivores, such as nematodes, aphids, and whiteflies. Other NLRs have been shown to confer resistance against the arthropod Nilaparvata lugens (brown planthopper). These include the rice OsBph1/9 and OsBph14. While multiple NLRs are involved in herbivore resistance, more work is needed to identify the recognized effectors (Figure 3G).

Helper NLRs

While some sensor NLRs do not require helper NLRs, many NLRs function with helper NLRs to transduce immune signals. In Arabidopsis, some CNLs and/or most TNLs require the RNLs ACTIVATED DISEASE RESISTANCE 1 (collectively known as ADR1s, which includes AtADR1, AtADR1-L1, and AtADR1-L2) and/or N REQUIREMENT GENE 1 (collectively known as NRG1s, which includes AtNRG1A and AtNRG1B;;;; ). In Arabidopsis accession Col-0, the four RPW8 homologs, AtHR1, AtHR2, AtHR3, and AtHR4, also contribute to resistance against bacterial and fungal pathogens. In Solanaceous plants, the CNLs NB-LRR REQUIRED FOR HR-ASSOCIATED CELL DEATH-2 (NRC2), NRC3, and NRC4 function as helper NLRs for multiple sensor NLRs (; Figure 3H). The contribution of the NRC network to the functions of sensor NLRs has been extensively discussed.

The PRR signaling pathway

The extracellular domains of plant PRRs perceive diverse ligands. Binding of ligands leads to heterodimeric receptor complex formation between PRRs and their co-receptors, such as BAK1 and CERK1. On the other hand, RLPs constitutively interact with SOBIR1 and recruit BAK1 upon ligand recognition. In Arabidopsis, the bacterial flagellin peptide flg22 is perceived by the LRR–RLK FLS2. Flg22 acts as a “molecular glue” and interacts with and brings together the extracellular LRR domains of FLS2 and BAK1. Heterodimeric complex formation between the LRR domains of FLS2 and BAK1 brings their cytoplasmic kinase domains into close proximity, which leads to a series of auto- and trans-phosphorylation events. This activated receptor complex then phosphorylates RLCKs. RLCK subfamily VII members (collectively known as RLCK-VIIs) were first shown to be important for surface receptor-mediated immunity in tomato and tobacco and to be required for Cf-4 and Cf-9 to confer fungal resistance (. In Arabidopsis, RLCKs play particularly important roles during PRR-mediated immunity. BAK1 associates with and phosphorylates the RLCK-VII BIK1 at the Try243 and Try250 residues.

The activation of RLCK-VIIs promotes the phosphorylation of multiple signaling components, including the calcium channels CNGC2/4 and OSCA1.3, the NADPH oxidase respiratory burst oxidase protein D (RbohD), and the mitogen-activated protein kinase kinase kinase (MAPKKK5). The activation of multiple calcium channels by BIK1 leads to cytosolic calcium influx, which activates calcium-dependent protein kinases (CPKs). In Arabidopsis, CPK4/5/6/11, together with BIK1, phosphorylate and activate RbohD, which leads to reactive oxygen species (ROS) production. The phosphorylation of multiple ion channels by RLCKs also leads to stomatal closure in response to PAMPs. In parallel, MAPKKK3 and MAPKKK5 phosphorylate the MAPKKs MKK4 and MKK5, which then phosphorylate the MAPKs MPK3 and MPK6 in Arabidopsis. In parallel, MKK1/MKK2 also phosphorylate MPK4. RLCK-VIIs, CPKs, and MPKs phosphorylate and activate multiple defense-related transcription factors, such as WRKY transcription factors, resulting in the upregulation of defense-related genes. PTI-induced transcriptional reprogramming leads to the biosynthesis of antimicrobial compounds and defense-related hormones, such as ET and salicylic acid (SA;;;; ). Hydrogen peroxide (a type of ROS) promotes protein and phenolic cross-linking, which result in callose deposition and restricts fungal and oomycete infection (;; Figure 4A).

Signaling pathway of singleton NLRs

NLR-mediated immunity is triggered by the detection of effectors through intracellular NLRs. NLRs detect effectors either via direct interactions with effectors, guarding effector targets, or guarding decoy proteins. In Arabidopsis, CNLs and TNLs act as sensor NLRs that recognize effectors, while RNLs act as helper NLRs to transduce immune signals. While the majority of sensor NLRs in Arabidopsis require helper NLRs to mediate immunity, some CNLs mediate immune responses alone. These are known as singleton NLRs, such as ZAR1 and RPM1. ZAR1 recognizes a range of effectors by monitoring pseudokinases such as RKS1 and PBL2, which mimic authentic RLCK targets of effectors. The bacterial effector AvrAC from X. campestris uridylylates the RLCK PBL2. The ZAR1/RKS1 heterodimer associates with uridylylated PBL2 (PBL2UMP), which leads to conformational changes in the heterodimer. ADP in the NB-ARC domain in ZAR1 is ejected and replaced by ATP (. This results in the oligomerization of ZAR1/RKS1/PBL2UMP oligomers into pentameric resistosomes that localize to the PM to trigger downstream immune responses.

ZAR1 resistosomes were recently shown to exhibit cation channel activity. The N-terminal α-helices in ZAR1 form a funnel-shaped structure with a negatively charged carboxylate ring, which allows cations to pass through into the cytosol. Co-expression of ZAR1 with RKS1, PBL2, and AvrAC in plant protoplasts results in cytosolic calcium influx, ROS accumulation, and the perturbation of chloroplasts and vacuoles. Robust ROS accumulation during ZAR1 activation is likely caused by the activation of multiple downstream signaling components, such as the NADPH oxidases, since the CPKs are activated by cytosolic calcium influx. In addition, multiple CPKs and RbohD have been shown to be phosphorylated during RPS2 activation. Defense-related transcription factors are also likely activated by cytosolic calcium influx. The perturbation of chloroplasts and vacuoles is quickly followed by the loss of PM integrity and cellular rupture (; Figure 4B). How these processes are regulated by immune signaling components and their relationships to transcriptional reprogramming are currently unclear.

The signaling pathway of helper-NLR-dependent sensor NLRs

The majority of sensor NLRs requires helper NLRs to mediate immunity. In solanaceous plants, the NB-LRR REQUIRED FOR HR-ASSOCIATED CELL DEATH proteins (collectively known as NRCs) are required for immunity and hypersensitive cell death response (HR) mediated by multiple sensor NLRs. Interestingly, the N-terminal CC domain in ZAR1 contains a “MADA motif” that is also present in NRCs. This suggests that perhaps NRCs also form cation channels with α-helices following activation. In Arabidopsis, ADR1s and NRG1s are required for resistance and HR mediated by some CNLs and many TNLs. Following effector recognition, TNLs also oligomerize into resistosomes to mediate resistance. The Arabidopsis RPP1 recognizes the Hpa effector ATR1, and N. benthamiana ROQ1 recognizes the Xanthomonas effector XopQ. These effectors are recognized by the LRR and post-LRR domain, which likely leads to conformational changes and oligomerization of these TNLs into tetrameric resistosomes.

The TIR domains of TNLs are brought into close proximity following oligomerization, activating NADase activity and producing v-cADPR. TIR domains also exhibit 2′,3′-cAMP/cGMP synthetase activity by hydrolyzing RNA or DNA. v-cADPR and 2′,3′-cAMP/cGMP are proposed to be signaling molecules that activate downstream signaling components. Following the activation of TNLs, the EP-domain containing proteins (EP-proteins) SAG101 and EDS1 associate with NRG1. Similarly, the activation of TNLs also leads to the association of the EP-proteins PAD4 and EDS1 with ADR1. These associations lead to the activation of these signaling components, which in turn activate downstream immune responses, such as defense-related gene expression and HR. The RNLs ADR1 and NRG1 were also recently shown to function as calcium channels to activate immunity. It is conceivable that the association and activation of helper RNLs and EP-proteins induces calcium influx and triggers downstream immune responses (Figure 4C).

Physiological responses induced by RLKs

Following ligand perception, the PRR co-receptor BAK1 and the RLCK BIK1 are phosphorylated. This leads to the phosphorylation and activation of multiple signaling components. The activation of multiple calcium channels and NADPH oxidases leads to calcium influx, stomatal closure, ROS production, and callose deposition. The activation of CPKs and MAPKs leads to transcriptional reprograming and the biosynthesis of defense-related hormones. In Arabidopsis, MPK3/MPK6 activate 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID SYNTHASE (ACS) isoforms ACS2 and ACS6, which are involved in ET biosynthesis. The transcription factors SYSTEMIC-ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60 G (CBP60g) are required for PTI-induced upregulation of SA biosynthesis genes, such as ISOCHORISMATE SYNTHASE 1 (ICS1), EDS5, and AVRPPHB SUSCEPTIBLE 3 (PBS3;; ). SARD1 and CBP60g are also required for the upregulation of pipecolic acid (N-hydroxyl-pipecolic acid [NHP])-biosynthesis genes, such as FLAVIN-CONTAINING MONOOXYGENASE 1 (;; Figure 5).

Physiological responses induced by RLPs

Similar to RLKs, RLPs also require PRR co-receptors, RLCKs, CPKs, and MAPKs to transduce immune signals. In Arabidopsis, nlp20-induced immune responses mediated by RLP23 require the co-receptors BAK1, SOBIR1, and multiple RLCKs such as PBL19/20/30/31/32 (;;. The activation of RLP23 leads to changes in PM potential, an ROS burst, the phosphorylation of BIK1 and MAPKs, callose deposition, and SA and ET production, similar to the activation of FLS2. In addition, flg22 and nlp20 induce highly overlapping transcriptional reprogramming in Arabidopsis. Thus, RLKs and RLPs induce overlapping responses due to the activation of similar downstream signaling components. However, the individual activation of multiple RLPs, such as SlCf-4, SlCf-9, and AtRLP23, leads to the HR, perhaps due to the prolonged activation of downstream signaling components. PAD4, EDS1, and ADR1 are required for both RLK- and RLP-mediated immunity (;. Thus, EP-proteins and helper NLRs might also be activated during some PTI signaling, although it remains to be established whether EP proteins play a primary or secondary role in defense signaling (Figure 5).

Physiological responses induced by CNLs alone

Activation of the Arabidopsis CNL RPS2 in the absence of PTI leads to the phosphorylation of RbohD (in Ser343/347), CPKs, and MAPKs. RPS2-induced RbohD phosphorylation and ROS production are dependent on BAK1/BKK1 and BIK1. However, it is currently unclear whether BAK1/BKK1 and BIK1 are directly or indirectly activated by CNLs. While the ZAR1 resistosome directly triggers calcium influx, other calcium channels may also be activated by CNLs. The activation of RPM1, RPS2, and RPS5 leads to MAPK activation and the HR. In addition, the activation of many CNLs leads to the upregulation of SA- and NHP-biosynthesis genes. Thus, ET, SA, and NHP are likely to be produced during CNL activation (Figure 5).

Physiological responses induced by TNLs alone

Activation of the Arabidopsis TNL RRS1/RPS4 does not lead to the phosphorylation of BIK1, RbohD (in Ser39/343/347), MAPKs, calcium influx, ROS accumulation, or the HR. Thus, RLCKs, NADPH oxidases, calcium channels, or CPKs are unlikely to be activated by RRS1/RPS4 alone. Activation of RRS1/RPS4 induces weak callose deposition, perhaps via SA accumulation. Activation of TNLs leads to the association of EP-proteins with helper NLRs, which induces transcriptional reprogramming. Similar to CNLs, the activation of TNLs leads to the upregulation of SA- and NHP-biosynthesis genes. Thus, SA and NHP are likely to be produced during TNL activation (Figure 5).

Physiological responses induced by the co-activation of PRRs and NLRs

Co-activation of PRRs and NLRs (“PTI + ETI”) leads to the robust activation of BIK1, RbohD, and MPK3. This results in stronger calcium influx, ROS accumulation, and callose deposition compared to PTI or ETI alone. In addition, “PTI + ETI” leads to stronger accumulation of SA and NHP compared to PTI alone, which is likely due to the stronger expression of SA- and NHP-biosynthesis genes during ETI (;;;; Figure 5).

Regulation of PRR-mediated immunity

The PRR-signaling pathway is tightly regulated as the excessive activation of PRRs leads to autoimmunity and growth inhibition.

Regulation of PRRs

Both the transcript and protein levels of PRRs are regulated by multiple mechanisms. For example, the expression of FLS2 is regulated by the microRNA miR172b. The expression of FLS2 is also upregulated by ET. U-BOX DOMAIN-CONTAINING PROTEIN 12 (PUB12) and PUB13 mediate the polyubiquitination of FLS2, which leads to the endocytosis and degradation of this protein. Cf-4 also undergoes endocytosis upon Avr4 recognition. The activation of PRRs and their co-receptors must also be regulated. BAK1-INTERACTING RECEPTOR (BIR)-LIKE KINASE 1 is an RLK that associates with and sequesters BAK1 to prevent the auto-activation of BAK1-associated PRRs. Following PAMP perception, the peptide RAPID ALKALINIZATION FACTOR 23 (RALF23) is perceived by a PRR complex composed of the CrRLK1L FERONIA (FER) and the LORELEI-LIKE-GPI ANCHORED PROTEIN 1. The perception of RALF23 by FER negatively regulates the formation of the FLS2–BAK1 complex. FER regulates PM nanodomain organization to modulate PRR signaling. In addition, the phosphorylation status of PRRs is regulated by multiple protein phosphatases. In Arabidopsis, POLTERGEIST-LIKE 4 (PLL4) and PLL5 associate with EFR and negatively regulate elf18-induced responses. PROTEIN PHOSPHATASE 2A negatively regulates the phosphorylation status of BAK1 (; Figure 6).

Regulation of PRR-signaling components

In addition to PRRs, downstream signaling components are also regulated to prevent prolonged activation. As a central signaling component in the PRR-signaling pathway, the Arabidopsis RLCK BIK1 is regulated by multiple mechanisms. EXTRA-LARGE G PROTEIN 2 (XLG2) functions with other heterotrimeric G proteins to attenuate proteasome-mediated degradation of BIK1. The turnover of BIK1 is regulated by CPK28, PUB4/25/26, and the E3 ubiquitin ligases RING-H2 FINGER A3A/B. The phosphorylation status of BIK1 is also negatively regulated by the protein phosphatase PP2C38. In addition to RLCKs, other PRR-signaling components must also be regulated. RbohD is ubiquitinated by the E3 ubiquitin ligase PIRE (PBL13 interacting RING domain E3 ligase), which leads to proteasome-mediated degradation. PHAGOCYTOSIS OXIDASE/ BEM1P (PB1) DOMAIN-CONTAINING PROTEIN negatively regulates ROS production by controlling the localization of RbohD. The PP2C phosphatases PP2C5 and AP2C1 negatively regulate the phosphorylation of MPK3 and MPK6 (; Figure 6).

Regulation of NLR-mediated immunity

Similar to PRRs, the prolonged activation of NLRs also leads to autoimmunity. Thus, the regulation of both NLRs and downstream signaling components is important to prevent autoimmunity.

Regulation of NLRs

The expression of NLRs is regulated at multiple levels. The transcription of NLRs is regulated by chromatin-remodeling proteins such as DECREASE IN DNA METHYLATION 1, SWI/SNF CHROMATIN REMODELER SYD, and multiple WRKY transcription factors. NLR transcript stability is also regulated by microRNAs and NONSENSE-MEDIATED mRNA DECAY factors, such as UP-FRAMESHIFT1/2/3. NLR transcripts also undergo alternative splicing, which is regulated by some MODIFIER OF SUPPRESSOR OF NPR1-1 (SNC1; MOS) proteins such as MOS4/12/14.

REQUIRED FOR MLA12 RESISTANCE 1 (RAR1), SUPPRESSOR OF THE G2 ALLELE OF SKP1 (SGT1), and HEAT SHOCK PROTEIN 90 (HSP90) function together as protein chaperones to regulate the folding, localization, and turnover of NLRs. In addition, NLR protein turnover is regulated by the SGT1-interacting protein SUPPRESSORS OF RPS4-RLD, multiple MUTANT SNC1-ENHANCING proteins, and the E3 ligases SNIPER1 and SNIPER2.

The localization of the ZAR1 resistosome to the PM is required for ZAR1-mediated resistance. In addition, the Arabidopsis importin-α nuclear transport receptor protein IMP-α3/MOS6 is required for SUPPRESSOR OF SNC1-mediated immunity. Thus, the localization of NLRs is important and is likely regulated by proteins involved in trafficking (Figure 6).

Regulation of NLR-signaling components

The correct localization of helper NLRs is likely important for signaling. For example, the helper NLR NRC4 accumulates at the extra-haustorial membrane following P. infestans infection. In addition, the balanced activity of both cytosolic- and nuclear-EDS1 is required for full immunity. Thus, the localization of helper NLRs and NLR-signaling components is important for defense. The activity of NLR signaling components is also negatively regulated. The Arabidopsis RNL NRG1C functions as a negative regulator in NLR-mediated immunity; overexpressing NRG1C compromised TNL-mediated HR and resistance. In addition, an atypical member of the NRC family, NRCX, negatively regulates other NRC members to modulate immunity. Posttranslational modifications (PTMs) are important for the functions of both PRRs and NLRs. For example, the phosphorylation of the C-terminus of the TNL RRS1-R is crucial for its recognition of the effector PopP2. It is currently unclear whether PTMs are important for the activation and/or stability of NLR-signaling components. Perhaps, EP-proteins and helper NLRs must also undergo PTMs in order to function properly. The additional regulation of NLR-signaling components pre-NLR activation and postNLR activation remains to be investigated (Figure 6).

Suppression of immunity by effectors

Multiple effectors have been shown to target both the PRR- and NLR-signaling pathways. Here, we summarize our knowledge of effectors reported to target PTI or ETI. Unless specified, the effectors mentioned in this section are from various P. syringae strains. AvrPtoB is an E3 ubiquitin ligase that induces the degradation of FLS2. HopB1 specifically degrades activated BAK1. AvrPto targets SOBIR1 and the FLS2–BAK1 complex by inhibiting their kinase activities. Similarly, the conserved Colletotrichum effector NIS1 also targets receptor kinase complexes. The tyrosine phosphatase HopAO1 directly dephosphorylates EFR. As RLCKs are central immune regulators, they are targeted by multiple effectors. AvrAC from X. campestris uridylylates BIK1 and PBL2. HopZ1a acetylates RLCKs, and AvrPphB is a cysteine protease that degrades RLCKs such as BIK1, PBS1, and PBL1. Other downstream PRR signaling components are also targeted by effectors. The ADP-ribosyltransferase HopF2 targets both BAK1 and MKK5 to suppress PTI signaling. HopAI1 inactivates MPK3, MPK4, and MPK6 via its phosphothreonine lyase activity. AvrRpt2 suppresses MPK4/11 activation. Interestingly, many parallel mechanisms are employed to suppress the same PRR-signaling node in different hosts by different pathogens (Figure 6).

Phosphorylation of SGT1 by MAPKs is required for NLR activation, implying that NLRs are regulated by SGT1 following PTI-induced MAPK activation. The R. solanacearum effector RipAC prevents MAPK-mediated phosphorylation of SGT1, which suppresses NLR-mediated immunity. Two effectors were recently shown to suppress NRC-mediated HR. The P. infestans effector AVRcap1b and the cyst nematode effector SPRYSEC15 can suppress autoimmunity induced by autoactive alleles of NRC2 and NRC3. Suppression of NRC2 and NRC3 by AVRcap1b is dependent on the membrane trafficking-associated protein TARGET OF MYB 1-LIKE PROTEIN 9A (NbTOL9a; ). AVRcap1b suppresses NRC2 and NRC3 by directly interacting with their NB-ARC domains. Another Phytophthora effector (from Phytophthora capsici), PcAvh103, suppresses immunity by promoting the disassociation of the EDS1–PAD4 complex. More studies are needed to identify pathogen effectors that target the NLR signaling pathway.

In Arabidopsis, the transcription factors CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 1/2/3 (CAMTA1/2/3) and CBP60a negatively regulate defense-induced transcriptional reprogramming. Pathogens also target defense-related transcription factors to suppress immunity. For example, the R. solanacearum effector PopP2 acetylates and inhibits WRKY transcription factors to suppress immunity. In addition, the Verticillium dahliae effector VdSCP41 inhibits SARD1 and CBP60g to facilitate its proliferation (; Figure 6).

The interactions between PTI and ETI

While PRR- and NLR-mediated immunity has been extensively studied for the last 20 years, it has not been clear how or if these defense mechanisms interact. NLR-mediated immunity is mostly activated in the presence of microbes or PAMPs. Most studies on NLR-mediated immunity have involved transient expression-based comparisons between PTI and “PTI + ETI.” The activation of NLRs in the absence of PTI has not been extensively studied until recently. There have been multiple reports on the different interactions between these two immune systems. Here, we describe three situations in which PTI and ETI interact with each other.

NLRs guard the PRR-signaling pathway

Many effectors target the PRR-signaling pathway. Plants have evolved multiple NLRs to detect these effectors via the guarding of PRR-signaling components or decoys. As a result, many PRRs and PRR-signaling loss-of-function mutants, such as the Arabidopsis mutants bak1-4 bkk1-1, bik1, cngc2/4, rbohd/f, mekk1, mkk1/2, mpk4, and camta3, exhibit autoimmune phenotypes (;;;;;;;. The autoimmunity observed in some of these mutants is caused by the activation of multiple NLRs. The TNL CONSTITUTIVE SHADE-AVOIDANCE 1 guards both BIR3 and BAK1. In addition, bak1-3 bkk-1-autoimmunity and HopB1-triggered immunity are dependent on ADR1s. RLCKs are targeted by multiple effectors. The CNL ZAR1 together with the RLCK RKS1 monitor PBL2, and the CNL RPS5 monitors PBS1, to reverse ETS. The CNL SUMM2 guards and senses the disruption of the MEKK1–MKK1/2–MPK4 kinase cascade via CALMODULIN-BINDING RECEPTOR-LIKE CYTOPLASMIC KINASE 3, a substrate protein of MPK4. SUMM2 also detects the P. syringae effector HopAI1, which inhibits MPK4 kinase activity. The TNL RPS6 also contributes to HopAI1-triggered immunity. Whether the autoimmunity in bik1, cgnc2/4, and rbohd/f is dependent on NLRs remains unclear. Other NLRs that guard the PRR-signaling pathway remain to be identified (Figure 7A).

Interdependency of signaling components between PRRs and NLRs

PRR co-receptors, RLCKs, NADPH oxidases, calcium channels, CPKs, and MAPKs are considered to be canonical PRR-signaling components, while EP proteins and helper NLRs are considered to be canonical NLR-signaling components. However, recent studies indicated that PRR-mediated resistance is dependent on canonical NLR-signaling components and vice versa (;;;; Figure 7B). As mentioned, flg22- and nlp20-induced resistance is partially dependent on EDS1, PAD4, SAG101, ADR1s, and NRG1s (;. proposed that EP-proteins and helper NLRs are activated by RLPs through interactions between RLP co-receptors (SOBIR1), EP-proteins, and helper NLRs, although it remains to be determined whether EP-proteins play a primary or secondary role in RLP defense signaling. Another report, however, suggested that the activation of PRRs leads to increased expression of multiple NLRs and other TIR-domain-containing proteins, promoting downstream signaling (. These two hypotheses are not mutually exclusive, and the exact mechanisms by which PRR-mediated immunity involves NLR-signaling components remain to be determined.

NLR-mediated immunity is also dependent on PRRs and multiple PRR-signaling components. In Arabidopsis, RPS2-, RPS5-, and RRS1/RPS4-mediated resistance is dependent on BAK1 and BKK1. RPS2-mediated resistance is also dependent on BIK1 and RbohD. Both RPM1- and RPS2-mediated resistance and the HR are dependent on CPK1/2/5/6. The activation of MPK3 and MPK6 is also required for the HR and resistance mediated by multiple NLRs including RPM1, RPS2, RPS5, and RRS1/RPS4. One of the proposed key mechanisms by which ETI halts pathogen infection is to potentiate and restore PTI from turnover and the action of pathogen effectors. As a result, PRRs and PRR-signaling components are required for NLR-mediated resistance. The molecular mechanisms by which ETI potentiates PTI will be discussed in the next section.

Mutual potentiation between PRR- and NLR-mediated immunity

Activation of the TNLs RRS1/RPS4 and RPP4 using an estradiol-inducible recognized effector (ETI without PTI) did not trigger the HR. The presence of PAMPs/MAMPs restored the HR induced by these TNLs. Similarly, the HR induced by the CNLs RPM1, RPS2, and RPS5 was also potentiated by the activation of PRRs. In addition, the HR and resistance induced by RPS2 are compromised in PRR mutants. There are a few possible mechanisms by which PRRs potentiate NLR-induced immunity. First, the activation of PRRs could induce the expression of NLRs and NLR-signaling components. A recent transcriptomics study suggested that the activation of different PRRs induces highly overlapping transcriptional changes. Indeed, the activation of six distinct PRRs led to the upregulation of genes encoding most TNLs, CNLs, EP-proteins, and helper NLRs in Arabidopsis (; Figure 7C; Supplemental Data Set 3). The increased abundance of these proteins might therefore “prime” the activation of NLRs upon effector recognition. Second, the activation of PRRs might prime NLR-mediated immunity via PTMs. Upon PAMP perception, SGT1 is phosphorylated by MAPKs, which is important for the stability of NLRs. In addition, nonsense-mediated decay of NLR transcripts is inhibited upon PAMP recognition. Thus, the stability of NLRs can be affected by both transcriptional and posttranscriptional modifications activated by PTI. Conceivably, EP proteins and helper NLRs might also be primed via PTMs induced by PTI. Flg22 treatment led to reduced polyubiquitination levels of EDS1. Whether and how PTI primes NLR-signaling components remain to be investigated.

The activation of NLRs potentiates PAMP-induced cellular responses, such as ROS production, callose deposition, and defense-related gene expression. The activation of multiple PRR signaling components, such as BIK1, RbohD, and MPK3, is also potentiated by ETI. ETI induces the transcript and protein accumulation of SOBIR1, BAK1, BIK1, RbohD, and MPK3. Transcriptomic analysis confirmed that multiple PRR signaling components are also upregulated upon the activation of RRS1/RPS4. These include CPK1/2/5/6, XLG2, and the calcium channels OSCA1.3, CNGC19/20, GLR2.7/2.8/2.9 (; Figure 7C; Supplemental Data Set 4). Interestingly, the transcript levels of BIK1, MPK3, and RbohD are only transiently upregulated during ETI. However, the protein levels of these genes remain upregulated for an extensive period of time. This implies that PTMs or other posttranscriptional mechanisms might also influence the stability of PRR-signaling components during ETI. The protein abundance of PRR signaling components, such as BAK1, BIK1, and RbohD, is tightly regulated by multiple processes (Figure 6). How ETI regulates or affects these processes remains unclear. In addition, calcium influx induced by NLRs might contribute to the potentiation of PTI through CPKs. To summarize, PTI and ETI mutually potentiate each other through multiple mechanisms to induce robust immunity against pathogens (Figure 7C).

Historic overview of research in PTI and future challenges

Researchers identified the first PRR-encoding gene, Cf-9, back in 1994. Multiple PRR genes, such as Xa21, Cf-2, Cf-4, FLS2, EFR, and RLP23, were subsequently identified and used as models to study PTI. Researchers then explored PRR-induced physiological responses and identified multiple signaling components. The activation of MAPKs by cell-surface receptors were reported back in 1997 and was verified for Cf- genes 2 years later. In tobacco (N. tabacum), the perception of PAMPs leads to the activation of wounding-induced protein kinase (WIPK) and SA-induced protein kinase (SIPK;; ). WIPKs and SIPKs are orthologs of the subsequently identified Arabidopsis MPK3 and MPK6, respectively. Accumulation of ROS and callose deposition during infection were also reported in 1997, and for Cf-initiated responses. Researchers identified the human Rbohs in Arabidopsis and showed that two of these (RbohD and RbohF) are required for ROS production during infection. It was unclear how these signaling components were activated by PRRs until the identification of the PRR co-receptors and RLCKs. BAK1 was identified as a co-receptor essential for FLS2-mediated resistance in 2007. In the same year, CERK1 was also shown to be essential for chitin-mediated immunity. In 2013, SOBIR1 was identified as a co-receptor of RLPs, and the structure of the FLS2/BAK1 receptor complex was also defined. In 2018, a genome-wide analysis of Arabidopsis LRR–RLKs interactions was reported, further supporting the theory that PRRs interact with each other to modulate and transduce signals. Tomato ACIK1 was the first RLCK shown to be an essential signaling component in PRR-mediated immunity (. The Arabidopsis ortholog BIK1 was subsequently shown to be a central PRR-signaling component. RbohD, MAPKKKs, and multiple calcium channels were shown to be phosphorylated by RLCKs, which leads to downstream immune responses (;;;;;;; Figure 8A).

More than 60 immunity-related PRRs with known ligands have now been identified. Arabidopsis EFR has been introduced into multiple plant species, such as tomato, rice, orange, and apple, providing broadspectrum resistance to many bacteria. Therefore, the identification of novel PRRs that recognize PAMPs or other elicitors would provide resources to engineer disease-resistant crops. Other challenges in PRR biology include trying to understand how PRRs activate downstream signaling components and physiological responses, how these processes are regulated and suppressed by effectors, and how resistance against pathogens is achieved (Figure 8B).

Historic overview of research in ETI and future challenges

Arabidopsis RPS2 and the tobacco N gene were the first reported NLR genes. Multiple NLRs, including RPM1 and L6, were subsequently identified. Understanding how NLRs detect effectors has led to multiple models. The guard hypothesis was proposed to explain how the protein kinase Pto confers Prf-dependent recognition of AvrPto. Many other examples have emerged that are consistent with this hypothesis, such as the requirement of the protease Rcr3 for Cf-2-mediated resistance. The decoy model was then proposed, which is further supported by the discovery of integrated decoy domains in NLRs. The discovery of NRCs led to the concept of NLR networks. Following the identification of multiple NLRs, researchers identified multiple genetic components required for NLR-mediated immunity. These include EDS1, NDR1, PAD4, RPW8, SGT1, RAR1, HSP90, SAG101, NRG1s, and ADR1s. EDS1 was later shown to co-function with SAG101 and PAD4 to mediate HR and resistance during ETI. Similarly, ADR1 and NRG1 have been shown to function downstream of multiple sensor NLRs to mediate the HR and resistance. How sensor NLRs activate these signaling components is currently under investigation. v-cADPR produced by TIR domains might contribute to the activation of EP-proteins and helper NLRs. NLRs were shown to oligomerize and trigger cytosolic calcium influx following effector recognition. The discovery of the structures of multiple NLR resistosomes proved that the oligomerization of NLRs is required for resistance, likely through the formation of cation channels. However, oligomerization of TIR domains imposed by an NLRC4 scaffold is sufficient to activate defense (; Figure 8A).

More than 140 NLRs with known recognized effectors have been identified. Cross-species transfer of NLR “stacks” provides durable resistance against pathogens. Identification of novel NLRs will provide resources to engineer crop resistance against multiple pathogens. Current challenges in NLR biology include understanding how NLRs activate downstream signaling components, how these signaling components then trigger immune responses, how these processes are regulated and suppressed by effectors, and how NLRs and PRRs co-function to achieve resistance against pathogens (Figure 8B).

Conclusion and perspectives

Plants respond to pathogens using a two-tier innate immune system activated by both cell-surface and intracellular immune receptors. The perception of PAMPs/MAMPs/DAMPs/HAMPs on the cell surface leads to PRR-mediated immunity, and the recognition of effectors leads to intracellular NLR-mediated immunity. The first plant Resistance (R) gene, Hm1, was cloned back in 1992. Many immune receptors have been identified since 1994, when the first PRR and NLRs were identified. Tremendous efforts have been made to understand the PRR- and NLR-signaling pathways. PRRs and NLRs utilize some overlapping but also unique signaling components to activate each of their downstream physiological responses, which thwart pathogen proliferation. Both signaling pathways are tightly regulated to prevent autoimmunity, while being suppressed by pathogen effectors. Recent studies have shown that PRR- and NLR-mediated immunity can be mutually potentiated and are dependent on each other. Great opportunities for novel discoveries remain in addressing the following challenges in the research of plant immunity: (1) identifying novel immune receptors; (2) understanding the signaling pathways and physiological responses triggered by both cell-surface and intracellular immune receptors; (3) understanding how immunity is intrinsically regulated and manipulated by external biotic and/or abiotic factors; (4) understanding the vastly diverse mechanisms by which plants resist pathogen infections; and (5) understanding how different immune systems function synergistically during infections. These challenges overlap with some of the “top 10 unanswered questions in molecular plant-microbe interactions” and will shape our understanding of plant immunity in the coming decades (Figure 8B).

Supplemental data

The following materials are available in the online version of this article.

Supplemental Data Set 1. PRRs involved in plant immunity.

Supplemental Data Set 2. NLRs involved in plant immunity.

Supplemental Data Set 3. Expression of ETI-related genes during PTI.

Supplemental Data Set 4. Expression of PTI-related genes during ETI.

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    Axtell MJ, Staskawicz BJ (2003 ) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369–377

    Not in our library10.1016/s0092-8674(03)00036-9

  16. 16.

    Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002 ) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295: 2073–2076

    Not in our library10.1126/science.1067554

  17. 17.

    Baggs E, Dagdas G, Krasileva KV (2017 ) NLR diversity, helpers and integrated domains: making sense of the NLR IDentity. Curr Opin Plant Biol 38: 59–67

    Not in our library10.1016/j.pbi.2017.04.012

  18. 18.

    Baggs EL, Monroe JG, Thanki AS, O’Grady R, Schudoma C, Haerty W, Krasileva KV (2020 ) Convergent loss of an EDS1/PAD4 signaling pathway in several plant lineages reveals coevolved components of plant immunity and drought response. Plant Cell 32: 2158–2177

    Not in our library10.1105/tpc.19.00903

  19. 19.

    Bailey K, Cevik V, Holton N, Byrne-Richardson J, Sohn KH, Coates M, Woods-Tör A, Aksoy HM, Hughes L, Baxter L, et al (2011 ) Molecular cloning of ATR5(Emoy2) from Hyaloperonospora arabidopsidis, an avirulence determinant that triggers RPP5-mediated defense in Arabidopsis. Mol Plant Microbe Interact 24: 827–838

    Not in our library10.1094/mpmi-12-10-0278

  20. 20.

    Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C (2002 ) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30: 361–371

    Not in our library10.1046/j.1365-313x.2001.01292.x

  21. 21.

    Barragan CA, Wu R, Kim ST, Xi W, Habring A, Hagmann J, Van de Weyer AL, Zaidem M, Ho WH, Wang G et al (2019 ) RPW8/HR repeats control NLR activation in Arabidopsis thaliana. PLoS Genet 15: e1008313

    Not in our library10.1371/journal.pgen.1008313

  22. 22.

    Bastedo DP, Khan M, Martel A, Seto D, Kireeva I, Zhang J, Masud W, Millar D, Lee JY, Lee AHY, et al (2019 ) Perturbations of the ZED1 pseudokinase activate plant immunity. PLoS Pathog 15: e1007900

    Not in our library10.1371/journal.ppat.1007900

  23. 23.

    Bendahmane A, Köhn BA, Dedi C, Baulcombe DC (1995 ) The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato. Plant J 8: 933–941

    Not in our library10.1046/j.1365-313x.1995.8060933.x

  24. 24.

    Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994 ) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1860

    Not in our library10.1126/science.8091210

  25. 25.

    Berzal-Herranz A, de la Cruz A, Tenllado F, Díaz-Ruíz JR, López L, Sanz AI, Vaquero C, Serra MT, García-Luque I (1995 ) The Capsicum L3 gene-mediated resistance against the tobamoviruses is elicited by the coat protein. Virology 209: 498–505

    Not in our library10.1006/viro.1995.1282

  26. 26.

    Bettgenhaeuser J, Hernández-Pinzón I, Dawson AM, Gardiner M, Green P, Taylor J, Smoker M, Ferguson JN, Emmrich P, Hubbard A, et al (2021 ) The barley immune receptor Mla recognizes multiple pathogens and contributes to host range dynamics. Nat Commun 12: 6915

    Not in our library10.1038/s41467-021-27288-3

  27. 27.

    Bi G, Su M, Li N, Liang Y, Dang S, Xu J, Hu M, Wang J, Zou M, Deng Y et al (2021 ) The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184: 3528–3541.e12

    Not in our library10.1016/j.cell.2021.05.003

  28. 28.

    Bi G, Zhou Z, Wang W, Li L, Rao S, Wu Y, Zhang X, Menke FLH, Chen S, Zhou JM (2018 ) Receptor-like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis. Plant Cell 30: 1543–1561

    Not in our library10.1105/tpc.17.00981

  29. 29.

    Bigeard J, Colcombet J, Hirt H (2015 ) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8: 521–539.

    Not in our library10.1016/j.molp.2014.12.022

  30. 30.

    Bjornson M, Pimprikar P, Nürnberger T, Zipfel C (2021 ) The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nat Plants 7: 579–586

    Not in our library10.1038/s41477-021-00874-5

  31. 31.
    A Conserved Peptide Pattern from a Widespread Microbial Virulence Factor Triggers Pattern-Induced Immunity in Arabidopsis · 2014
    No notice
  32. 32.

    Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL (2011 ) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci USA 108: 16463–16468

    Not in our library10.1073/pnas.1113726108

  33. 33.

    Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Zhendong T, Engelhardt S, Vetukuri RR, Harrower B, et al (2010 ) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci USA 107: 9909–9914

    Not in our library10.1073/pnas.0914408107

  34. 34.

    Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010 ) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464: 418–422

    Not in our library10.1038/nature08794

  35. 35.
    The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat · 2019
    No notice
  36. 36.

    Boutrot F, Zipfel C (2017 ) Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol 55: 257–286

    Not in our library10.1146/annurev-phyto-080614-120106

  37. 37.

    Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010 ) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107: 14502–14507

    Not in our library10.1073/pnas.1003347107

  38. 38.

    Bozsoki Z, Cheng J, Feng F, Gysel K, Vinther M, Andersen KR, Oldroyd G, Blaise M, Radutoiu S, Stougaard J (2017 ) Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception. Proc Natl Acad Sci USA 114: E8118–E8127

    Not in our library10.1073/pnas.1706795114

  39. 39.

    Brendolise C, Martinez-Sanchez M, Morel A, Chen R, Dinis R, Deroles S, Peeters N, Rikkerink EHA, Montefiori M (2018 ) NRG1-mediated recognition of HopQ1 reveals a link between PAMP and Effector-triggered Immunity. BioRxiv doi: 10.1101/293050

    Not in our library

  40. 40.

    Brock AK, Willmann R, Kolb D, Grefen L, Lajunen HM, Bethke G, Lee J, Nürnberger T, Gust AA (2010 ) The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol 153: 1098–1111

    Not in our library10.1104/pp.110.156109

  41. 41.

    Brulé D, Villano C, Davies LJ, Trdá L, Claverie J, Héloir MC, Chiltz A, Adrian M, Darblade B, Tornero P, et al (2019 ) The grapevine (Vitis vinifera) LysM receptor kinases VvLYK1-1 and VvLYK1-2 mediate chitooligosaccharide-triggered immunity. Plant Biotechnol J 17: 812–825

    Not in our library10.1111/pbi.13017

  42. 42.

    Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010 ) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107: 9452–9457

    Not in our library10.1073/pnas.1000675107

  43. 43.

    Cao Y, Aceti DJ, Sabat G, Song J, Makino SI, Fox BG, Bent AF (2013 ) Mutations in FLS2 Ser-938 dissect signaling activation in FLS2-mediated Arabidopsis immunity. PLoS Pathog 9: e1003313

    Not in our library10.1371/journal.ppat.1003313

  44. 44.
    The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1 · 2014
    No notice
  45. 45.

    Carter ME, Helm M, Chapman AVE, Wan E, Restrepo Sierra AM, Innes RW, Bogdanove AJ, Wise RP (2019 ) Convergent evolution of effector protease recognition by arabidopsis and barley. Mol Plant Microbe Interact 32: 550–565

    Not in our library10.1094/mpmi-07-18-0202-fi

  46. 46.

    Castel B, Ngou PM, Cevik V, Redkar A, Kim DS, Yang Y, Ding P, Jones JDG (2019a ) Diverse NLR immune receptors activate defence via the RPW8-NLR NRG1. New Phytol 222: 966–980

    Not in our library10.1111/nph.15659

  47. 47.

    Castel B, Wu Y, Xiao S, Jones JD (2019b ) An rpw8 quadruple mutant of Arabidopsis Col-0 is partially compromised in bacterial and fungal resistance. BioRxiv doi: 10.1101/839308

    Not in our library

  48. 48.
    The AvrM Effector from Flax Rust Has a Structured C-Terminal Domain and Interacts Directly with the M Resistance Protein · 2010
    Not checked
  49. 49.

    Catanzariti AM, Lim GTT, Jones DA (2015 ) The tomato I-3 gene: a novel gene for resistance to Fusarium wilt disease. New Phytol 207: 106–118

    Not in our library10.1111/nph.13348

  50. 50.

    Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997 ) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963–1965

    Not in our library10.1126/science.278.5345.1963

  51. 51.
    A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy†hypothesis · 2014
    No notice
  52. 52.

    Champouret N (2010 ) Functional genomics of Phytophthora infestans effectors and Solanum resistance genes. https://research.wur.nl/en/publications/functional-genomics-of-phytophthora-infestans-effectors-and-solan

    Not in our library

  53. 53.
    Detection of the virulent form of AVR3a from Phytophthora infestans following artificial evolution of potato resistance gene R3a. · 2014
    Not checked
  54. 54.
    Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture · 2017
    No notice
  55. 55.

    Chen J, Upadhyaya NM, Ortiz D, Sperschneider J, Li F, Bouton C, Breen S, Dong C, Xu B, Zhang X, et al (2017b ) Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science 358: 1607–1610

    Not in our library10.1126/science.aao4810

  56. 56.

    Chen R, Li H, Zhang L, Zhang J, Xiao J, Ye Z (2007 ) CaMi, a root-knot nematode resistance gene from hot pepper (Capsium annuum L.) confers nematode resistance in tomato. Plant Cell Rep 26: 895–905

    Not in our library10.1007/s00299-007-0304-0

  57. 57.

    Chen T, Bi K, He Z, Gao Z, Zhao Y, Fu Y, Cheng J, Xie J, Jiang D (2016 ) Arabidopsis mutant bik1 exhibits strong resistance to Plasmodiophora brassicae. Front Physiol 7: 402

    Not in our library10.3389/fphys.2016.00402

  58. 58.

    Chen T (2021 ) Identification and characterization of the LRR repeats in plant LRR-RLKs. BMC Mol and Cell Biol 22: 9

    Not in our library10.1186/s12860-021-00344-y

  59. 59.

    Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006 ) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465–476

    Not in our library10.1105/tpc.105.036574

  60. 60.

    Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007 ) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497–500

    Not in our library10.1038/nature05999

  61. 61.

    Claverie M, Dirlewanger E, Bosselut N, Van Ghelder C, Voisin R, Kleinhentz M, Lafargue B, Abad P, Rosso MN, Chalhoub B, et al (2011 ) The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge repeated C-terminal post-LRR region. Plant Physiol 156: 779–792

    Not in our library10.1104/pp.111.176230

  62. 62.

    Coleman AD, Maroschek J, Raasch L, Takken FLW, Ranf S, Hückelhoven R (2021 ) The Arabidopsis leucine-rich repeat receptor-like kinase MIK2 is a crucial component of early immune responses to a fungal-derived elicitor. New Phytol 229: 3453–3466

    Not in our library10.1111/nph.17122

  63. 63.
    The Arabidopsis Protein Phosphatase PP2C38 Negatively Regulates the Central Immune Kinase BIK1 · 2016
    No notice
  64. 64.

    Dangl JL, Jones JD (2001 ) Plant pathogens and integrated defence responses to infection. Nature 411: 826–833

    Not in our library10.1038/35081161

  65. 65.

    de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, et al (2012 ) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109: 5110–5115

    Not in our library10.1073/pnas.1119623109

  66. 66.

    de Ronde D, Butterbach P, Lohuis D, Hedil M, van Lent JWM, Kormelink R (2013 ) Tsw gene-based resistance is triggered by a functional RNA silencing suppressor protein of the Tomato spotted wilt virus. Mol. Plant Pathol 14: 405–415

    Not in our library10.1111/mpp.12016

  67. 67.
    Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network. · 2021
    Not checked
  68. 68.

    Derkacheva M, Yu G, Rufian JS, Jiang S, Derbyshire P, Morcillo RJL, Stransfeld L, Wei Y, Menke FLH, Zipfel C, et al (2020 ) The Arabidopsis E3 ubiquitin ligase PUB4 regulates BIK1 homeostasis and is targeted by a bacterial type-III effector. BioRxiv doi: 10.1101/2020.10.25.354514

    Not in our library

  69. 69.

    Devanna NB, Vijayan J, Sharma TR (2014 ) The blast resistance gene Pi54of cloned from Oryza officinalis interacts with Avr-Pi54 through its novel non-LRR domains. PLoS One 9: e104840

    Not in our library10.1371/journal.pone.0104840

  70. 70.

    DeYoung BJ, Qi D, Kim SH, Burke TP, Innes RW (2012 ) Activation of a plant nucleotide binding-leucine rich repeat disease resistance protein by a modified self protein. Cell Microbiol 14: 1071–1084

    Not in our library10.1111/j.1462-5822.2012.01779.x

  71. 71.

    Ding P, Sakai T, Shrestha RK, Perez NM, Guo W, Ngou BPM, He S, Liu C, Feng X, Zhang R, et al (2020 ) Chromatin accessibility landscapes activated by cell surface and intracellular immune receptors. J Exp Bot 72: 7927–7941

    Not in our library10.1093/jxb/erab373

  72. 72.

    Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JD (1998 ) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10: 1915–1925

    Not in our library10.1105/tpc.10.11.1915

  73. 73.

    Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JD (1996 ) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451–459

    Not in our library10.1016/s0092-8674(00)81290-8

  74. 74.

    Dodds P, Thrall P (2009 ) Recognition events and host-pathogen co-evolution in gene-for-gene resistance to flax rust. Funct Plant Biol 36: 395–408

    Not in our library10.1071/fp08320

  75. 75.

    Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG (2004 ) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16: 755–768

    Not in our library10.1105/tpc.020040

  76. 76.

    Domazakis E, Wouters D, Lochman J, Visser R, Joosten MHAJ, Vleeshouwers VGAA (2020 ) ELR is a true pattern recognition receptor that associates with elicitins from diverse Phytophthora species. BioRxiv doi: 10.1101/2020.09.21.305813

    Not in our library

  77. 77.

    Dong OX, Ao K, Xu F, Johnson KCM, Wu Y, Li L, Xia S, Liu Y, Huang Y, Rodriguez E, et al (2018 ) Individual components of paired typical NLR immune receptors are regulated by distinct E3 ligases. Nat Plants 4: 699–710

    Not in our library10.1038/s41477-018-0216-8

  78. 78.

    Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, et al (2009 ) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106: 22163–22168

    Not in our library10.1073/pnas.0912139106

  79. 79.

    Du Y, Berg J, Govers F, Bouwmeester K (2015a ) Immune activation mediated by the late blight resistance protein R1 requires nuclear localization of R1 and the effector AVR1. New Phytol 207: 735–747

    Not in our library10.1111/nph.13355

  80. 80.

    Du J, Verzaux E Chaparro-Garcia A, Bijsterbosch G, Keizer LCP, Zhou J, Liebrand TWH, Xie C, Govers F, Robatzek S, et al (2015b ) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat Plants 1: 15034

    Not in our library10.1038/nplants.2015.34

  81. 81.

    Dufayard JF, Bettembourg M, Fischer I, Droc G, Guiderdoni E, Périn C, Chantret N, Diévart A (2017 ) New insights on leucine-rich repeats receptor-like kinase orthologous relationships in angiosperms. Front Plant Sci 8: 381

    Not in our library10.3389/fpls.2017.00381

  82. 82.

    Duggan C, Moratto E, Savage Z, Hamilton E, Adachi H, Wu CH, Leary AY, Tumtas Y, Rothery S, Maqbool A, et al (2021 ) Dynamic accumulation of a helper NLR at the plant-pathogen interface underpins pathogen recognition. BioRxiv doi: 10.1101/2021.03.15.435521

    Not in our library10.1073/pnas.2104997118

  83. 83.

    Duxbury Z, Wang S, MacKenzie CI, Tenthorey JL, Zhang X, Huh SU, Hu L, Hill L, Ngou PM, Ding P, et al (2020 ) Induced proximity of a TIR signaling domain on a plant-mammalian NLR chimera activates defense in plants. Proc Natl Acad Sci USA 117: 18832–18839

    Not in our library10.1073/pnas.2001185117

  84. 84.

    Duxbury Z, Wu CH, Ding P (2021 ) A comparative overview of the intracellular guardians of plants and animals: nlrs in innate immunity and beyond. Annu Rev Plant Biol 72: 155–184

    Not in our library10.1146/annurev-arplant-080620-104948

  85. 85.

    Eitas TK, Nimchuk ZL, Dangl JL (2008 ) Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB. Proc Natl Acad Sci USA 105: 6475–6480

    Not in our library10.1073/pnas.0802157105

  86. 86.

    Erickson FL, Holzberg S, Calderon-Urrea A, Handley V, Axtell M, Corr C, Baker B (1999 ) The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. Plant J 18: 67–75

    Not in our library10.1046/j.1365-313x.1999.00426.x

  87. 87.

    Eschen-Lippold L, Jiang X, Elmore JM, Mackey D, Shan L, Coaker G, Scheel D, Lee J (2016 ) Bacterial AvrRpt2-like cysteine proteases block activation of the Arabidopsis mitogen-activated protein kinases, MPK4 and MPK11. Plant Physiol 171: 2223–2238

    Not in our library10.1104/pp.16.00336

  88. 88.
    EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases · 1999
    Not checked
  89. 89.
    Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1 · 2022
    Not checked
  90. 90.

    Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ (2013 ) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci USA 110: 9166–9170

    Not in our library10.1073/pnas.1203458110

  91. 91.

    Feehan JM, Castel B, Bentham AR, Jones JD (2020 ) Plant NLRs get by with a little help from their friends. Curr Opin Plant Biol 56: 99–108

    Not in our library10.1016/j.pbi.2020.04.006

  92. 92.

    Felix G, Duran JD, Volko S, Boller T (1999 ) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265–276

    Not in our library10.1046/j.1365-313x.1999.00265.x

  93. 93.

    Feng F, Yang F, Rong W, Wu X, Zhang J, Chen S, He C, Zhou JM (2012 ) A Xanthomonas uridine 5’-monophosphate transferase inhibits plant immune kinases. Nature 485: 114–118

    Not in our library10.1038/nature10962

  94. 94.

    Feys BJ, Moisan LJ, Newman MA, Parker JE (2001 ) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J 20: 5400–5411

    Not in our library10.1093/emboj/20.19.5400

  95. 95.

    Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE (2005 ) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17: 2601–2613

    Not in our library10.1105/tpc.105.033910

  96. 96.

    Foster SJ, Park TH, Pel M, Brigneti G, Sliwka J, Jagger L, van der Vossen E, Jones JDG (2009 ) Rpi-vnt1.1, a Tm-2(2) homolog from Solanum venturii, confers resistance to potato late blight. Mol Plant Microbe Interact 22: 589–600

    Not in our library10.1094/mpmi-22-5-0589

  97. 97.

    Gabriëls SHEJ, Vossen JH, Ekengren SK, van Ooijen G, Abd-El-Haliem AM, van den Berg GCM, Rainey DY, Martin GB, Takken FLW, de Wit PJGM, et al (2007 ) An NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins. Plant J 50: 14–28

    Not in our library10.1111/j.1365-313x.2007.03027.x

  98. 98.

    Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng YT, Chen S, Li X, et al (2009 ) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6: 34–44

    Not in our library10.1016/j.chom.2009.05.019

  99. 99.
    Bifurcation of Arabidopsis NLR Immune Signaling via Ca2+-Dependent Protein Kinases · 2013
    No notice
  100. 100.

    Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han GZ (2018 ) Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177: 82–89

    Not in our library10.1104/pp.18.00185

  101. 101.
    Balanced Nuclear and Cytoplasmic Activities of EDS1 Are Required for a Complete Plant Innate Immune Response · 2010
    No notice
  102. 102.

    Ghislain M, Byarugaba AA, Magembe E, Njoroge A, Rivera C, Román ML, Tovar JC, Gamboa S, Forbes GA, Kreuze JF, et al (2019 ) Stacking three late blight resistance genes from wild species directly into African highland potato varieties confers complete field resistance to local blight races. Plant Biotechnol J 17: 1119–1129

    Not in our library10.1111/pbi.13042

  103. 103.

    Gilardi P, García-Luque I, Serra MT (2004 ) The coat protein of tobamovirus acts as elicitor of both L2 and L4 gene-mediated resistance in Capsicum. J Gen Virol 85: 2077–2085

    Not in our library10.1099/vir.0.80017-0

  104. 104.

    Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S (2008 ) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18: 1824–1832

    Not in our library10.1016/j.cub.2008.10.063

  105. 105.

    Gómez-Gómez L, Boller T (2000 ) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003–1011

    Not in our library10.1016/s1097-2765(00)80265-8

  106. 106.

    González-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JDG (2006 ) The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18: 1067–1083

    Not in our library10.1105/tpc.106.040998

  107. 107.

    Goritschnig S, Krasileva KV, Dahlbeck D, Staskawicz BJ (2012 ) Computational prediction and molecular characterization of an oomycete effector and the cognate Arabidopsis resistance gene. PLoS Genet 8: e1002502

    Not in our library10.1371/journal.pgen.1002502

  108. 108.

    Goto Y, Maki N, Sklenar J, Derbyshire P, Menke FLH, Zipfel C, Kadota Y, Shirasu K (2020 ) The phagocytosis oxidase/Bem1p (PB1) domain-containing protein PB1CP negatively regulates the NADPH oxidase RBOHD in plant immunity. BioRxiv doi: 10.1101/2020.12.28.423414

    Not in our library10.1111/nph.19302

  109. 109.

    Gouhier-Darimont C, Stahl E, Glauser G, Reymond P (2019 ) The Arabidopsis lectin receptor kinase LecRK-I.8 is involved in insect egg perception. Front Plant Sci 10: 623

    Not in our library10.3389/fpls.2019.00623

  110. 110.

    Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000 ) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23: 441–450

    Not in our library10.1046/j.1365-313x.2000.00804.x

  111. 111.

    Grant M.R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R.W., Dangl J.L. (1995 ) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843–846.

    Not in our library10.1126/science.7638602

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    Grech-Baran M, Witek K, Poznański J, Grupa-Urbańska A, Malinowski T, Lichocka M, Jones JD, Hennig J (2021 ) The Rysto immune receptor recognizes a broadly conserved feature of potyviral coat proteins. BioRxiv

    Not in our library10.1111/nph.18183

  113. 113.

    Gronnier J, Franck CM, Stegmann M, DeFalco TA, Cifuentes AA, Dünser K, Lin W, Yang Z, Kleine-Vehn J, Ringli C, Zipfel C (2020 ) FERONIA regulates FLS2 plasma membrane nanoscale dynamics to modulate plant immune signaling. BioRxiv

    Not in our library

  114. 114.

    Groux R, Stahl E, Gouhier-Darimont C, Kerdaffrec E, Jimenez-Sandoval P, Santiago J, Reymond P (2021 ) Arabidopsis natural variation in insect egg-induced cell death reveals a role for LECTIN RECEPTOR KINASE-I.1. Plant Physiol 185: 240–255

    Not in our library10.1093/plphys/kiaa022

  115. 115.

    Grubb LE, Derbyshire P, Dunning KE, Zipfel C, Menke FLH, Monaghan J (2021 ) Large-scale identification of ubiquitination sites on membrane-associated proteins in Arabidopsis thaliana seedlings. Plant Physiol 185: 1483–1488

    Not in our library10.1093/plphys/kiab023

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    Guan R, Su J, Meng X, Li S, Liu Y, Xu J, Zhang S (2015 ) Multilayered regulation of ethylene induction plays a positive role in Arabidopsis resistance against Pseudomonas syringae. Plant Physiol 169: 299–312

    Not in our library10.1104/pp.15.00659

  117. 117.

    Guo H, Ahn HK, Sklenar J, Huang J, Ma Y, Ding P, Menke FLH, Jones JDG (2020 ) Phosphorylation-regulated activation of the Arabidopsis RRS1-R/RPS4 immune receptor complex reveals two distinct effector recognition mechanisms. Cell Host Microbe 27: 769–781.e6

    Not in our library10.1016/j.chom.2020.03.008

  118. 118.

    Hall TJ (1980 ) Resistance at the TM-2 locus in the tomato to tomato mosaic virus. Euphytica 29: 189–197

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  119. 119.

    Han L, Li GJ, Yang KY, Mao G, Wang R, Liu Y, Zhang S (2010 ) Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J 64: 114–127

    Not in our library10.1111/j.1365-313x.2010.04318.x

  120. 120.

    Hander T, Fernández-Fernández AD, Kumpf RP, Willems P, Schatowitz H, Rombaut D, Staes A, Nolf J, Pottie R, Yao P, et al (2019 ) Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides. Science 363: eaar7486

    Not in our library10.1126/science.aar7486

  121. 121.
    What are the Top 10 Unanswered Questions in Molecular Plant-Microbe Interactions? · 2020
    Not checked
  122. 122.

    He P, Shan L, Lin NC, Martin GB, Kemmerling B, Nürnberger T, Sheen J (2006 ) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563–575

    Not in our library10.1016/j.cell.2006.02.047

  123. 123.
    The tomato receptor CuRe1 senses a cell wall protein to identify Cuscuta as a pathogen · 2020
    Not checked
  124. 124.

    Hind SR, Strickler SR, Boyle PC, Dunham DM, Bao Z, O'Doherty IM, Baccile JA, Hoki JS, Viox EG, Clarke CR, et al (2016 ) Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nat Plants 2: 16128

    Not in our library10.1038/nplants.2016.128

  125. 125.

    Hohmann U, Lau K, Hothorn M (2017 ) The structural basis of ligand perception and signal activation by receptor kinases. Annu Rev Plant Biol 68: 109–137

    Not in our library10.1146/annurev-arplant-042916-040957

  126. 126.

    Hohmann U, Nicolet J, Moretti A, Hothorn LA, Hothorn M (2018 ) Mechanistic analysis of the SERK3 elongated allele defines a role for BIR ectodomains in brassinosteroid signaling. BioRxiv doi: 10.1101/257543

    Not in our library10.1038/s41477-018-0150-9

  127. 127.

    Holton N, Nekrasov V, Ronald PC, Zipfel C (2015 ) The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLoS Pathog 11: e1004602

    Not in our library10.1371/journal.ppat.1004602

  128. 128.

    Horsefield S, Burdett H, Zhang X, Manik MK, Shi Y, Chen J, Qi T, Gilley J, Lai JS, Rank MX et al (2019 ) NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. Science 365: 793–799

    Not in our library10.1126/science.aax1911

  129. 129.

    Hoser R, Zurczak M, Lichocka M, Zuzga S, Dadlez M, Samuel MA, Ellis BE, Stuttmann J, Parker JE, Hennig J, et al (2013 ) Nucleocytoplasmic partitioning of tobacco N receptor is modulated by SGT1. New Phytol 200: 158–171

    Not in our library10.1111/nph.12347

  130. 130.

    Hou S, Liu D, He P (2021 ) Phytocytokines function as immunological modulators of plant immunity. Stress Biol 1: 8

    Not in our library10.1007/s44154-021-00009-y

  131. 131.
    The Secreted Peptide PIP1 Amplifies Immunity through Receptor-Like Kinase 7 · 2014
    Corrected
  132. 132.
    Suppression of Plant Resistance Gene-Based Immunity by a Fungal Effector · 2008
    No notice
  133. 133.

    Houterman PM, Ma L, van Ooijen G, de Vroomen MJ, Cornelissen BJC, Takken FLW, Rep M (2009 ) The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. Plant J 58: 970–978

    Not in our library10.1111/j.1365-313x.2009.03838.x

  134. 134.

    Huang S, Chen X, Zhong X, Li M, Ao K, Huang J, Li X (2016 ) Plant TRAF proteins regulate NLR immune receptor turnover. Cell Host Microbe 19: 204–215

    Not in our library10.1016/j.chom.2016.01.005

  135. 135.

    Huot B, Yao J, Montgomery BL, He SY (2014 ) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7: 1267–1287

    Not in our library10.1093/mp/ssu049

  136. 136.

    Irieda H, Inoue Y, Mori M, Yamada K, Oshikawa Y, Saitoh H, Uemura A, Terauchi R, Kitakura S, Kosaka A, et al (2019 ) Conserved fungal effector suppresses PAMP-triggered immunity by targeting plant immune kinases. Proc Natl Acad Sci USA 116: 496–505

    Not in our library10.1073/pnas.1807297116

  137. 137.

    Jacob F, Kracher B, Mine A, Seyfferth C, Blanvillain-Baufumé S, Parker JE, Tsuda K, Schulze-Lefert P, Maekawa T (2018 ) A dominant-interfering camta3 mutation compromises primary transcriptional outputs mediated by both cell surface and intracellular immune receptors in Arabidopsis thaliana. New Phytol 217: 1667–1680

    Not in our library10.1111/nph.14943

  138. 138.

    Jacob P, Kim NH, Wu F, El-Kasmi F, Chi Y, Walton WG, Furzer OJ, Lietzan AD, Sunil S, Kempthorn K, et al (2021 ) Plant “helper” immune receptors are Ca2+-permeable nonselective cation channels. Science 373: 420–425

    Not in our library10.1126/science.abg7917

  139. 139.

    Jehle AK, Lipschis M, Albert M, Fallahzadeh-Mamaghani V, Fürst U, Mueller K, Felix G (2013 ) The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25: 2330–2340

    Not in our library10.1105/tpc.113.110833

  140. 140.

    Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000 ) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19: 4004–4014

    Not in our library10.1093/emboj/19.15.4004

  141. 141.

    Jo KR (2013 ) Unveiling and deploying durability of late blight resistance in potato: from natural stacking to cisgenic stacking.

    Not in our library

  142. 142.

    Johal GS, Briggs SP (1992 ) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258: 985–987

    Not in our library10.1126/science.1359642

  143. 143.

    Johnson KCM, Xia S, Feng X, Li X (2015 ) The chromatin remodeler SPLAYED negatively regulates SNC1-mediated immunity. Plant Cell Physiol 56: 1616–1623

    Not in our library10.1093/pcp/pcv087

  144. 144.

    Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG (1994 ) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789–793

    Not in our library10.1126/science.7973631

  145. 145.

    Jones JDG, Dangl JL (2006 ) The plant immune system. Nature 444: 323–329

    Not in our library10.1038/nature05286

  146. 146.

    Jones JDG, Brigneti G, Smilde D (2003 ) Putting plant disease resistance genes to work. In Vasil IK, ed, Plant Biotechnology 2002 and Beyond, Springer Netherlands, Dordrecht, the Netherlands, pp 10–17

    Not in our library

  147. 147.

    Joosten MH, Cozijnsen TJ, De Wit PJ (1994 ) Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367: 384–386

    Not in our library10.1038/367384a0

  148. 148.

    Jung HW, Panigrahi GK, Jung GY, Lee YJ, Shin KH, Sahoo A, Choi ES, Lee E, Kim KM, Yang SH, et al (2020 ) Pathogen-associated molecular pattern-triggered immunity involves proteolytic degradation of core nonsense-mediated mRNA decay factors during the early defense response. Plant Cell 32: 1081–1101

    Not in our library10.1105/tpc.19.00631

  149. 149.

    Kadota Y, Liebrand TWH, Goto Y, Sklenar J, Derbyshire P, Menke FLH, Torres MA, Molina A, Zipfel C, Coaker G, et al (2019 ) Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. New Phytol 221: 2160–2175

    Not in our library10.1111/nph.15523

  150. 150.

    Kadota Y, Shirasu K, Zipfel C (2015 ) Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56: 1472–1480

    Not in our library10.1093/pcp/pcv063

  151. 151.

    Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones JDG, Shirasu K, Menke F, Jones A, et al (2014 ) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54: 43–55

    Not in our library10.1016/j.molcel.2014.02.021

  152. 152.

    Kaloshian I, Lange WH, Williamson VM (1995 ) An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proc Natl Acad Sci USA 92: 622–625

    Not in our library10.1073/pnas.92.2.622

  153. 153.

    Kamoun S, van West P, de Jong AJ, de Groot KE, Vleeshouwers V, Govers F (1997 ) A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol. Plant Microbe Interact 10: 13–20

    Not in our library10.1094/mpmi.1997.10.1.13

  154. 154.

    Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E, Tharreau D, Terauchi R (2012 ) Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J 72: 894–907

    Not in our library10.1111/j.1365-313x.2012.05110.x

  155. 155.

    Kato H, Nemoto K, Shimizu M, Abe A, Asai S, Ishihama N, Daimon T, Ojika M, Kawakita K, Onai K, et al (2021 ) Pathogen-derived 9-methyl sphingoid base is perceived by a lectin receptor kinase in Arabidopsis. BioRxiv doi: 10.1101/2021.10.18.464766

    Not in our library

  156. 156.

    Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszyński A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH, et al (2015 ) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523: 308–312

    Not in our library10.1038/nature14611

  157. 157.

    Khan M, Subramaniam R, Desveaux D (2016 ) Of guards, decoys, baits and traps: pathogen perception in plants by type III effector sensors. Curr Opin Microbiol 29: 49–55

    Not in our library10.1016/j.mib.2015.10.006

  158. 158.

    Kim MG, Geng X, Lee SY, Mackey D (2009a ) The Pseudomonas syringae type III effector AvrRpm1 induces significant defenses by activating the Arabidopsis nucleotide-binding leucine-rich repeat protein RPS2. Plant J 57: 645–653

    Not in our library10.1111/j.1365-313x.2008.03716.x

  159. 159.

    Kim SB, Lee HY, Seo S, Lee JH, Choi D (2015 ) RNA-dependent RNA polymerase (NIb) of the potyviruses is an avirulence factor for the broad-spectrum resistance gene Pvr4 in Capsicum annuum cv. CM334. PLoS One 10: e0119639

    Not in our library10.1371/journal.pone.0119639

  160. 160.

    Kim SH, Kwon SI, Saha D, Anyanwu NC, Gassmann W (2009b ) Resistance to the Pseudomonas syringae effector HopA1 is governed by the TIR-NBS-LRR protein RPS6 and is enhanced by mutations in SRFR1. Plant Physiol 150: 1723–1732

    Not in our library10.1104/pp.109.139238

  161. 161.

    Kim Y, Gilmour SJ, Chao L, Park S, Thomashow MF (2020 ) Arabidopsis CAMTA transcription factors regulate pipecolic acid biosynthesis and priming of immunity genes. Mol Plant 13: 157–168

    Not in our library10.1016/j.molp.2019.11.001

  162. 162.
    The Cell Wall Associated Kinases, WAKs, As Pectin Receptors · 2012
    Not checked
  163. 163.

    Kørner CJ, Klauser D, Niehl A, Domínguez-Ferreras A, Chinchilla D, Boller T, Heinlein M, Hann DR (2013 ) The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol Plant Microbe Interact 26: 1271–1280

    Not in our library10.1094/mpmi-06-13-0179-r

  164. 164.
    RefPlantNLR is a comprehensive collection of experimentally validated plant disease resistance proteins from the NLR family · 2021
    No notice
  165. 165.

    Krasileva KV, Dahlbeck D, Staskawicz BJ (2010 ) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22: 2444–2458

    Not in our library10.1105/tpc.110.075358

  166. 166.

    Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JDG (2002 ) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296: 744–747

    Not in our library10.1126/science.1069288

  167. 167.

    Kutschera A, Dawid C, Gisch N, Schmid C, Raasch L, Gerster T, Schäffer M, Smakowska-Luzan E, Belkhadir Y, Vlot AC, et al (2019 ) Bacterial medium-chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364: 178–181

    Not in our library10.1126/science.aau1279

  168. 168.

    Lacaze A, Joly DL (2020 ) Structural specificity in plant-filamentous pathogen interactions. Mol Plant Pathol 21: 1513–1525

    Not in our library10.1111/mpp.12983

  169. 169.

    Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma BPHJ, Staskawicz B, et al (2010 ) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28: 365–369

    Not in our library10.1038/nbt.1613

  170. 170.

    Laflamme B, Dillon MM, Martel A, Almeida RND, Desveaux D, Guttman DS (2020 ) The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science 367: 763–768

    Not in our library10.1126/science.aax4079

  171. 171.

    Lagudah ES, Moullet O, Appels R (1997 ) Map-based cloning of a gene sequence encoding a nucleotide-binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome 40: 659–665

    Not in our library10.1139/g97-087

  172. 172.

    Lai Y, Eulgem T (2018 ) Transcript-level expression control of plant NLR genes. Mol Plant Pathol 19: 1267–1281

    Not in our library10.1111/mpp.12607

  173. 173.

    Lal NK, Nagalakshmi U, Hurlburt NK, Flores R, Bak A, Sone P, Ma X, Song G, Walley J, Shan L, et al (2018 ) The receptor-like cytoplasmic kinase BIK1 localizes to the nucleus and regulates defense hormone expression during plant innate immunity. Cell Host Microbe 23: 485–497.e5

    Not in our library10.1016/j.chom.2018.03.010

  174. 174.

    Laohavisit A, Wakatake T, Ishihama N, Mulvey H, Takizawa K, Suzuki T, Shirasu K (2020 ) Quinone perception in plants via leucine-rich-repeat receptor-like kinases. Nature 587: 92–97

    Not in our library10.1038/s41586-020-2655-4

  175. 175.

    Lapin D, Kovacova V, Sun X, Dongus JA, Bhandari D, von Born P, Bautor J, Guarneri N, Rzemieniewski J, Stuttmann J, et al (2019 ) A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell 31: 2430–2455

    Not in our library10.1105/tpc.19.00118

  176. 176.

    Larkan NJ, Lydiate DJ, Parkin IAP, Nelson MN, Epp DJ, Cowling WA, Rimmer SR, Borhan MH (2013 ) The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol 197: 595–605

    Not in our library10.1111/nph.12043

  177. 177.

    Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995 ) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195–1206

    Not in our library10.1105/tpc.7.8.1195

  178. 178.

    Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D, Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H, et al (2015 ) A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161: 1074–1088

    Not in our library10.1016/j.cell.2015.04.025

  179. 179.
    Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD · 2020
    No notice
  180. 180.

    Leppyanen IV, Shakhnazarova VY, Shtark OY, Vishnevskaya NA, Tikhonovich IA, Dolgikh EA (2017 ) Receptor-like kinase LYK9 in Pisum sativum L. Is the CERK1-like receptor that controls both plant immunity and AM symbiosis development. Int J Mol Sci 19: 8

    Not in our library10.3390/ijms19010008

  181. 181.

    Li G, Huang S, Guo X, Li Y, Yang Y, Guo Z, Kuang H, Rietman H, Bergervoet M, Vleeshouwers VGGA, et al (2011 ) Cloning and characterization of r3b; members of the r3 superfamily of late blight resistance genes show sequence and functional divergence. Mol Plant Microbe Interact 24: 1132–1142

    Not in our library10.1094/mpmi-11-10-0276

  182. 182.

    Li J, Timko MP (2009 ) Gene-for-gene resistance in Striga-cowpea associations. Science 325: 1094

    Not in our library10.1126/science.1174754

  183. 183.

    Li J, Wang Q, Li C, Bi Y, Fu X, Wang R (2019 ) Novel haplotypes and networks of AVR-Pik alleles in Magnaporthe oryzae. BMC Plant Biol 19: 204

    Not in our library10.1186/s12870-019-1817-8

  184. 184.

    Li L, Kim P, Yu L, Cai G, Chen S, Alfano JR, Zhou JM (2016 ) Activation-dependent destruction of a co-receptor by a Pseudomonas syringae effector dampens plant immunity. Cell Host Microbe 20: 504–514

    Not in our library10.1016/j.chom.2016.09.007

  185. 185.

    Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, et al (2014 ) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15: 329–338

    Not in our library10.1016/j.chom.2014.02.009

  186. 186.

    Li Q, Wang J, Bai T, Zhang M, Jia Y, Shen D, Zhang M, Dou D (2020 ) A Phytophthora capsici effector suppresses plant immunity via interaction with EDS1. Mol Plant Pathol 21: 502–511

    Not in our library10.1111/mpp.12912

  187. 187.

    Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, Zhang Z, Zhao Q, Feng Q, Zhang H, et al (2009 ) The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant Microbe Interact 22: 411–420

    Not in our library10.1094/mpmi-22-4-0411

  188. 188.

    Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou JM (2005 ) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA 102: 12990–12995

    Not in our library10.1073/pnas.0502425102

  189. 189.

    Li Y, Li S, Bi D, Cheng YT, Li X, Zhang Y (2010a ) SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathog 6: e1001111

    Not in our library10.1371/journal.ppat.1001111

  190. 190.

    Li Y, Tessaro MJ, Li X, Zhang Y (2010b ) Regulation of the expression of plant resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol 153: 1425–1434

    Not in our library10.1104/pp.110.156240

  191. 191.

    Liang X, Zhou JM (2018 ) Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol 69: 267–299

    Not in our library10.1146/annurev-arplant-042817-040540

  192. 192.
    Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor · 2016
    No notice
  193. 193.

    Liebrand TWH, van den Berg GCM, Zhang Z, Smit P, Cordewener JHG, America AHP, Sklenar J, Jones AME, Tameling WIL, Robatzek S, et al (2013 ) Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci USA 110: 10010–10015

    Not in our library10.1073/pnas.1220015110

  194. 194.

    Ligterink W, Kroj T, zur Nieden U, Hirt H, Scheel D (1997 ) Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276: 2054–2057

    Not in our library10.1126/science.276.5321.2054

  195. 195.

    Lin W, Li B, Lu D, Chen S, Zhu N, He P, Shan L (2014 ) Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc Natl Acad Sci USA 111: 3632–3637

    Not in our library10.1073/pnas.1318817111

  196. 196.

    Lin W, Lu D, Gao X, Jiang S, Ma X, Wang Z, Mengiste T, He P, Shan L (2013 ) Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. Proc Natl Acad Sci USA 110: 12114–12119

    Not in our library10.1073/pnas.1302154110

  197. 197.

    Lin X, Olave-Achury A, Heal R, Witek K, Karki HS, Song T, Wu C, Adachi H, Kamoun S, Vleeshouwers VGAA, et al (2021 ) Rpi-amr3 confers resistance to multiple Phytophthora species by recognizing a conserved RXLR effector. BioRxiv doi: 10.1101/2021.06.10.447899

    Not in our library10.1016/j.molp.2022.07.012

  198. 198.

    Lin X, Song T, Fairhead S, Witek K, Jouet A, Jupe F, Witek AI, Karki HS, Vleeshouwers VGAA, Hein I, et al (2020 ). Identification of Avramr1 from Phytophthora infestans using long read and cDNA pathogen-enrichment sequencing (PenSeq). Mol Plant Pathol 21: 1502–1512

    Not in our library10.1111/mpp.12987

  199. 199.

    Liu B, Li JF, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K, et al (2012 ) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24: 3406–3419

    Not in our library10.1105/tpc.112.102475

  200. 200.

    Liu J, Chen S, Chen L, Zhou Q, Wang M, Feng D, Li JF, Wang J, Wang HB, Liu B (2017 ) BIK1 cooperates with BAK1 to regulate constitutive immunity and cell death in Arabidopsis. J Integr Plant Biol 59: 234–239

    Not in our library10.1111/jipb.12529

  201. 201.

    Liu Y, Zhang S (2004 ) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16: 3386–3399

    Not in our library10.1105/tpc.104.026609

  202. 202.

    Liu Y, Maierhofer T, Rybak K, Sklenar J, Breakspear A, Johnston MG, Fliegmann J, Huang S, Roelfsema MRG, Felix G, et al (2019 ) Anion channel SLAH3 is a regulatory target of chitin receptor-associated kinase PBL27 in microbial stomatal closure. eLife 8: e44474

    Not in our library10.7554/elife.44474

  203. 203.

    Liu Y, Sun T, Sun Y, Zhang Y, Radojičić A, Ding Y, Tian H, Huang X, Lan J, Chen S, et al (2020 ) Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. Plant Cell 32: 4002–4016

    Not in our library10.1105/tpc.20.00499

  204. 204.

    Liu Y, Zeng Z, Zhang YM, Li Q, Jiang XM, Jiang Z, Tang JH, Chen D, Wang Q, Chen JQ, et al (2021 ) An angiosperm NLR Atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion. Mol. Plant 14: 2015–2031

    Not in our library10.1016/j.molp.2021.08.001

  205. 205.

    Liu Z, Friesen TL, Ling H, Meinhardt SW, Oliver RP, Rasmussen JB, Faris JD (2006 ) The Tsn1-ToxA interaction in the wheat-Stagonospora nodorum pathosystem parallels that of the wheat-tan spot system. Genome 49: 1265–1273

    Not in our library10.1139/g06-088

  206. 206.

    Lokossou AA, Park T, van Arkel G, Arens M, Ruyter-Spira C, Morales J, Whisson SC, Birch PRJ, Visser RGF, Jacobsen E, et al (2009 ) Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Mol Plant Microbe Interact 22: 630–641

    Not in our library10.1094/mpmi-22-6-0630

  207. 207.

    Lolle S, Greeff C, Petersen K, Roux M, Jensen MK, Bressendorff S, Rodriguez E, Sømark K, Mundy J, Petersen M (2017 ) Matching NLR immune receptors to autoimmunity in camta3 mutants using antimorphic NLR alleles. Cell Host Microbe 21: 518–529.e4

    Not in our library10.1016/j.chom.2017.03.005

  208. 208.

    Lorang JM, Hagerty CH, Lee R, McClean PE, Wolpert TJ (2018 ) Genetic analysis of victorin sensitivity and identification of a causal nucleotide-binding site leucine-rich repeat gene in Phaseolus vulgaris. Mol Plant Microbe Interact 31: 1069–1074

    Not in our library10.1094/mpmi-12-17-0328-r

  209. 209.

    Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011 ) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439–1442

    Not in our library10.1126/science.1204903

  210. 210.

    Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010 ) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107: 496–501

    Not in our library10.1073/pnas.0909705107

  211. 211.

    Lu X, Kracher B, Saur IML, Bauer S, Ellwood SR, Wise R, Yaeno T, Maekawa T, Schulze-Lefert P (2016 ) Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proc Natl Acad Sci USA 113: E6486–E6495

    Not in our library10.1073/pnas.1612947113

  212. 212.

    Lüdke D, Roth C, Kamrad SA, Messerschmidt J, Hartken D, Appel J, Hörnich BF, Yan Q, Kusch S, Klenke M, et al (2021 ) Functional requirement of the Arabidopsis importin-α nuclear transport receptor family in autoimmunity mediated by the NLR protein SNC1. Plant J 105: 994–1009

    Not in our library10.1111/tpj.15082

  213. 213.

    Lukasik E, Takken FLW (2009 ) STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol 12: 427–436

    Not in our library10.1016/j.pbi.2009.03.001

  214. 214.
    Callose Deposition: A Multifaceted Plant Defense Response · 2011
    Not checked
  215. 215.

    Luo M, Xie L, Chakraborty S, Wang A, Matny O, Jugovich M, Kolmer JA, Richardson T, Bhatt D, Hoque M, et al (2021 ) A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat. Biotechnol 39: 1–6

    Not in our library10.1038/s41587-020-00770-x

  216. 216.

    Luu DD, Joe A, Chen Y, Parys K, Bahar O, Pruitt R, Chan LJG, Petzold CJ, Long K, Adamchak C, et al (2019 ) Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor. Proc Natl Acad Sci USA 116: 8525–8534

    Not in our library10.1073/pnas.1818275116

  217. 217.

    Ma C, Liu Y, Bai B, Han Z, Tang J, Zhang H, Yaghmaiean H, Zhang Y, Chai J (2017 ) Structural basis for BIR1-mediated negative regulation of plant immunity. Cell Res 27: 1521–1524

    Not in our library10.1038/cr.2017.123

  218. 218.

    Ma S, Lapin D, Liu L, Sun Y, Song W, Zhang X, Logemann E, Yu D, Wang J, Jirschitzka J, et al (2020a ) Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370: eabe3069

    Not in our library10.1126/science.abe3069

  219. 219.

    Ma X, Claus LAN, Leslie ME, Tao K, Wu Z, Liu J, Yu X, Li B, Zhou J, Savatin DV, et al (2020b ) Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581: 199–203

    Not in our library10.1038/s41586-020-2210-3

  220. 220.

    Ma X, Xu G, He P, Shan L (2016 ) SERKing coreceptors for receptors. Trends Plant Sci 21: 1017–1033

    Not in our library10.1016/j.tplants.2016.08.014

  221. 221.

    Ma X, Zhang C, Kim DY, Huang Y, Chatt E, He P, Vierstra RD, Shan L (2021 ) Ubiquitylome analysis reveals a central role for the ubiquitin-proteasome system in plant innate immunity. Plant Physiol 185: 1943–1965

    Not in our library10.1093/plphys/kiab011

  222. 222.

    Ma Y, Walker RK, Zhao Y, Berkowitz GA (2012 ) Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. Proc Natl Acad Sci USA 109: 19852–19857

    Not in our library10.1073/pnas.1205448109

  223. 223.

    Macho AP, Zipfel C (2014 ) Plant PRRs and the activation of innate immune signaling. Mol Cell 54: 263–272

    Not in our library10.1016/j.molcel.2014.03.028

  224. 224.

    Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C, Roy S, Kadota Y, Oh M-H, Sklenar J, Derbyshire P, et al (2014 ) A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343: 1509–1512

    Not in our library10.1126/science.1248849

  225. 225.

    Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003 ) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379–389

    Not in our library10.1016/s0092-8674(03)00040-0

  226. 226.

    Manser B, Koller T, Praz CR, Roulin AC, Zbinden H, Arora S, Steuernagel B, Wulff BBH, Keller B, Sánchez-Martín J (2021 ) Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2. Plant J 106: 993–1007

    Not in our library10.1111/tpj.15214

  227. 227.

    Martin R, Qi T, Zhang H, Liu F, King M, Toth C, Nogales E, Staskawicz BJ (2020 ) Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science 370: eabd9993

    Not in our library10.1126/science.abd9993

  228. 228.

    Matsumoto K, Sawada H, Matsumoto K, Hamada H, Yoshimoto E, Ito T, Takeuchi S, Tsuda S, Suzuki K, Kobayashi K, et al (2008 ) The coat protein gene of tobamovirus P 0 pathotype is a determinant for activation of temperature-insensitive L 1a-gene-mediated resistance in Capsicum plants. Arch Virol 153: 645–650

    Not in our library10.1007/s00705-008-0032-y

  229. 229.

    Mazo-Molina C, Mainiero S, Haefner BJ, Bednarek R, Zhang J, Feder A, Shi K, Strickler SR, Martin GB (2020 ) Ptr1 evolved convergently with RPS2 and Mr5 to mediate recognition of AvrRpt2 in diverse solanaceous species. Plant J 103: 1433–1445

    Not in our library10.1111/tpj.14810

  230. 230.
    Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes · 2017
    No notice
  231. 231.

    Meng X, Zhang S (2013 ) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51: 245–266

    Not in our library10.1146/annurev-phyto-082712-102314

  232. 232.

    Mestre P, Baulcombe DC (2006 ) Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18: 491–501

    Not in our library10.1105/tpc.105.037234

  233. 233.

    Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998 ) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10: 1307–1319

    Not in our library10.1105/tpc.10.8.1307

  234. 234.

    Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994 ) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089–1099

    Not in our library10.1016/0092-8674(94)90282-8

  235. 235.

    Mitre LK, Teixeira-Silva NS, Rybak K, Magalhães DM, de Souza-Neto RR, Robatzek S, Zipfel C, de Souza AA (2021 ) The Arabidopsis immune receptor EFR increases resistance to the bacterial pathogens Xanthomonas and Xylella in transgenic sweet orange. Plant Biotechnol J 19: 1294–1296

    Not in our library10.1111/pbi.13629

  236. 236.

    Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007 ) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613–19618

    Not in our library10.1073/pnas.0705147104

  237. 237.

    Mizumoto H, Nakamura I, Shimomoto Y, Sawada H, Tomita R, Sekine KT, Kiba A, Nishiguchi M, Kobayashi K, Hikichi Y (2012 ) Amino acids in Tobamovirus coat protein controlling pepper L(1a)' ' gene-mediated resistance. Mol Plant Pathol 13: 915–922

    Not in our library10.1111/j.1364-3703.2012.00801.x

  238. 238.

    Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A, Segonzac C, Malinovsky FG, Rathjen JP, MacLean D, Romeis T, et al (2014 ) The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16: 605–615

    Not in our library10.1016/j.chom.2014.10.007

  239. 239.

    Monino-Lopez D, Nijenhuis M, Kodde L, Kamoun S, Salehian H, Schentsnyi K, Stam R Lokossou A, Abd-El-Haliem A, Visser RGF, et al (2021 ) Allelic variants of the NLR protein Rpi-chc1 differentially recognize members of the Phytophthora infestans PexRD12/31 effector superfamily through the leucine-rich repeat domain. Plant J 107: 182–197

    Not in our library10.1111/tpj.15284

  240. 240.

    Mott GA, Thakur S, Smakowska E, Wang PW, Belkhadir Y, Desveaux D, Guttman DS (2016 ) Genomic screens identify a new phytobacterial microbe-associated molecular pattern and the cognate Arabidopsis receptor-like kinase that mediates its immune elicitation. Genome Biol 17: 98

    Not in our library10.1186/s13059-016-0955-7

  241. 241.

    Mucyn TS, Clemente A, Andriotis VME, Balmuth AL, Oldroyd GED, Staskawicz BJ, Rathjen JP (2006 ) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18: 2792–2806

    Not in our library10.1105/tpc.106.044016

  242. 242.

    Mukhtar MS (2013 ) Engineering NLR immune receptors for broad-spectrum disease resistance. Trends Plant Sci 18: 469–472

    Not in our library10.1016/j.tplants.2013.08.005

  243. 243.

    Nagy ED, Bennetzen JL (2008 ) Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res 18: 1918–1923

    Not in our library10.1101/gr.078766.108

  244. 244.

    Nagy ED, Lee TC, Ramakrishna W, Xu Z, Klein PE, SanMiguel P, Cheng CP, Li J, Devos KM, Schertz K, et al (2007 ) Fine mapping of the Pc locus of Sorghum bicolor, a gene controlling the reaction to a fungal pathogen and its host-selective toxin. Theor Appl Genet 114: 961–970

    Not in our library10.1007/s00122-006-0481-1

  245. 245.

    Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y (2009 ) RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J 60: 218–226

    Not in our library10.1111/j.1365-313x.2009.03949.x

  246. 246.

    Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006 ) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436–439

    Not in our library10.1126/science.1126088

  247. 247.

    Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JDG (2004 ) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135: 1113–1128

    Not in our library10.1104/pp.103.036749

  248. 248.

    Navathe S, Yadav PS, Chand R, Mishra VK, Vasistha NK, Meher PK, Joshi AK, Gupta PK (2020 ) ToxA-Tsn1 interaction for spot blotch susceptibility in Indian wheat: an example of inverse gene-for-gene relationship. Plant Dis 104: 71–81

    Not in our library10.1094/pdis-05-19-1066-re

  249. 249.

    Neiva IP, Silva AA da, Resende JF, Carvalho R, de C, Oliveira AMS, de, Maluf WR (2019 ) Tomato genotype resistance to whitefly mediated by allelochemicals and Mi gene. Chilean J Agric Res 79: 124–130

    Not in our library

  250. 250.

    Ngou BPM, Ahn HK, Ding P, Jones JDG (2021a ) Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592: 110–115

    Not in our library10.1038/s41586-021-03315-7

  251. 251.

    Ngou BPM, Ahn HK, Ding P, Redkar A, Brown H, Ma Y, Youles M, Tomlinson L, Jones JDG (2020 ) Estradiol-inducible AvrRps4 expression reveals distinct properties of TIR-NLR-mediated effector-triggered immunity. J Exp Bot 71: 2186–2197

    Not in our library10.1093/jxb/erz571

  252. 252.

    Ngou BPM, Ding P, Jones JDG (2021b ) Channeling plant immunity. Cell 184: 3358–3360

    Not in our library10.1016/j.cell.2021.05.035

  253. 253.

    Ngou BPM, Heal R, Wyler M, Schmid MW, Jones JD (2022 ) Concerted expansion and contraction of immune receptor gene repertoires in plant genomes. BioRxiv doi: 10.1101/2022.01.01.474684

    Not in our library10.1038/s41477-022-01260-5

  254. 254.

    Ngou BPM, Jones JDG, Ding P (2021c ) Plant immune networks. Trends Plant Sci 27: 255–273

    Not in our library10.1016/j.tplants.2021.08.012

  255. 255.

    Niehl A, Wyrsch I, Boller T, Heinlein M (2016 ) Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211: 1008–1019

    Not in our library10.1111/nph.13944

  256. 256.
    The tomato Prf complex is a molecular trap for bacterial effectors based on Pto transphosphorylation. · 2013
    Not checked
  257. 257.

    Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, Cano LM, Win J, Bos JIB, Liu H-Y, van Damme M, et al (2009 ) In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21: 2928–2947

    Not in our library10.1105/tpc.109.068247

  258. 258.

    Paal J, Henselewski H, Muth J, Meksem K, Menéndez CM, Salamini F, Ballvora A, Gebhardt C (2004 ) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38: 285–297

    Not in our library10.1111/j.1365-313x.2004.02047.x

  259. 259.

    Park TH, Vleeshouwers VGAA, Huigen DJ, van der Vossen EAG, van Eck HJ, Visser RGF (2005 ) Characterization and high-resolution mapping of a late blight resistance locus similar to R2 in potato. Theor Appl Genet 111: 591–597

    Not in our library10.1007/s00122-005-2050-4

  260. 260.

    Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniels MJ (1996 ) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8: 2033–2046

    Not in our library10.1105/tpc.8.11.2033

  261. 261.

    Peart JR, Lu R, Sadanandom A, Malcuit I, Moffett P, Brice DC, Schauser L, Jaggard DAW, Xiao S, Coleman MJ, et al (2002 ) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc Natl Acad Sci USA 99: 10865–10869

    Not in our library10.1073/pnas.152330599

  262. 262.

    Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005 ) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 15: 968–973

    Not in our library10.1016/j.cub.2005.04.053

  263. 263.

    Peil A, Hübert C, Wensing A, Horner M, Emeriewen OF, Richter K, Wöhner T, Chagné D, Orellana-Torrejon C, Saeed M, et al (2019 ) Mapping of fire blight resistance in Malus ×robusta 5 flowers following artificial inoculation. BMC Plant Biol 19: 532

    Not in our library10.1186/s12870-019-2154-7

  264. 264.

    Peiró A, Cañizares MC, Rubio L, López C, Moriones E, Aramburu J, Sánchez-Navarro J (2014 ) The movement protein (NSm) of Tomato spotted wilt virus is the avirulence determinant in the tomato Sw-5 gene-based resistance. Mol Plant Pathol 15: 802–813

    Not in our library10.1111/mpp.12142

  265. 265.

    Pel M (2010 ) Mapping, isolation and characterization of genes responsible for late blight resistance in potato.

    Not in our library

  266. 266.

    Pelham J (1966 ) Resistance in tomato to tobacco mosaic virus. Euphytica 15: 258–267

    Not in our library

  267. 267.

    Perraki A, DeFalco TA, Derbyshire P, Avila J, Séré D, Sklenar J, Qi X, Stransfeld L, Schwessinger B, Kadota Y, et al (2018 ) Phosphocode-dependent functional dichotomy of a common co-receptor in plant signalling. Nature 561: 248–252

    Not in our library10.1038/s41586-018-0471-x

  268. 268.

    Petre B, Contreras MP, Bozkurt TO, Schattat MH, Sklenar J, Schornack S, Abd-El-Haliem A, Castells-Graells R, Lozano-Duran R, Dagdas YF, et al (2021 ) Host-interactor screens of Phytophthora infestans RXLR proteins reveal vesicle trafficking as a major effector-targeted process. Plant Cell 33: 1447–1471

    Not in our library10.1093/plcell/koab069

  269. 269.

    Piazza S, Campa M, Pompili V, Costa LD, Salvagnin U, Nekrasov V, Zipfel C, Malnoy M (2021 ) The Arabidopsis pattern recognition receptor EFR enhances fire blight resistance in apple. BioRxiv doi: 10.1101/2021.01.22.427734

    Not in our library10.1038/s41438-021-00639-3

  270. 270.

    Piedras P, Hammond-Kosack KE, Harrison K, Jones JDG (1998 ) Rapid, Cf-9 - and Avr9-dependent production of active oxygen species in tobacco suspension cultures. Mol Plant Microbe Interact 11: 1155–1166

    Not in our library

  271. 271.
    Oak genome reveals facets of long lifespan · 2018
    No notice
  272. 272.

    Postma J, Liebrand TWH, Bi G, Evrard A, Bye RR, Mbengue M, Kuhn H, Joosten MHAJ, Robatzek S (2016 ) Avr4 promotes Cf-4 receptor-like protein association with the BAK1/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol 210: 627–642

    Not in our library10.1111/nph.13802

  273. 273.

    Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, Albert M, Robinson MR, Chan LJG, Luu DD, Chen H, et al (2015 ) The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci Adv 1: e1500245

    Not in our library10.1126/sciadv.1500245

  274. 274.

    Pruitt RN, Zhang L, Saile SC, Karelina D, Fröhlich K, Wan W-L, Rao S, Gust AA, Locci F, Joosten MHAJ, et al (2020 ) Arabidopsis cell surface LRR immune receptor signaling through the EDS1-PAD4-ADR1 node. BioRxiv doi: 10.1101/2020.11.23.391516

    Not in our library

  275. 275.

    Pruitt RN, Locci F, Wanke F, Zhang L, Saile SC, Joe A, Karelina D, Hua C, Fröhlich K, Wan W-L, et al (2021 ) The EDS1-PAD4-ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature 598: 495–499

    Not in our library10.1038/s41586-021-03829-0

  276. 276.
    The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity · 2018
    No notice
  277. 277.

    Rai AK, Kumar SP, Gupta SK, Gautam N, Singh NK, Sharma TR (2011 ) Functional complementation of rice blast resistance gene Pi-k h (Pi54) conferring resistance to diverse strains of Magnaporthe oryzae. J Plant Biochem Biotechnol 20: 55–65

    Not in our library

  278. 278.

    Rao S, Zhou Z, Miao P, Bi G, Hu M, Wu Y, Feng F, Zhang X, Zhou JM (2018 ) Roles of receptor-like cytoplasmic kinase VII members in pattern-triggered immune signaling. Plant Physiol 177: 1679–1690

    Not in our library10.1104/pp.18.00486

  279. 279.
    MAP Kinase Cascades in Arabidopsis Innate Immunity · 2012
    No notice
  280. 280.

    Read AC, Hutin M, Moscou MJ, Rinaldi FC, Bogdanove AJ (2020a ) Cloning of the rice Xo1 resistance gene and interaction of the Xo1 protein with the defense-suppressing xanthomonas effector Tal2h. Mol Plant Microbe Interact 33: 1189–1195

    Not in our library10.1094/mpmi-05-20-0131-sc

  281. 281.

    Read AC, Moscou MJ, Zimin AV, Pertea G, Meyer RS, Purugganan MD, Leach JE, Triplett LR, Salzberg SL, Bogdanove AJ (2020b ) Genome assembly and characterization of a complex zfBED-NLR gene-containing disease resistance locus in Carolina Gold Select rice with Nanopore sequencing. PLoS Genet 16: e1008571

    Not in our library10.1371/journal.pgen.1008571

  282. 282.

    Redkar A, Cevik V, Bailey K, Furzer OJ, Fairhead S, Borhan MH, Holub EB, Jones JDG (2021 ) The Arabidopsis WRR4A and WRR4B paralogous NLR proteins both confer recognition of multiple Albugo candida effectors. BioRxiv doi: 10.1101/2021.03.29.436918

    Not in our library10.1111/nph.18378

  283. 283.

    Rentel MC, Leonelli L, Dahlbeck D, Zhao B, Staskawicz BJ (2008 ) Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proc Natl Acad Sci USA 105: 1091–1096

    Not in our library10.1073/pnas.0711215105

  284. 284.

    Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM, Dekker HL, de Koster CG, Cornelissen BJC (2004 ) A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol Microbiol 53: 1373–1383

    Not in our library10.1111/j.1365-2958.2004.04177.x

  285. 285.
    Perception of a conserved family of plant signalling peptides by the receptor kinase HSL3 · 2022
    Not checked
  286. 286.
    Perception of a divergent family of phytocytokines by the Arabidopsis receptor kinase MIK2 · 2021
    No notice
  287. 287.

    Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JDG, Brown JKM (2006 ) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18: 2402–2414

    Not in our library10.1105/tpc.106.043307

  288. 288.

    Romeis T, Piedras P, Jones JD (2000 ) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12: 803–816

    Not in our library10.1105/tpc.12.5.803

  289. 289.

    Romeis T, Piedras P, Zhang S, Klessig DF, Hirt H, Jones JD (1999 ) Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11: 273–287

    Not in our library10.1105/tpc.11.2.273

  290. 290.

    Ron M, Avni A (2004 ) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16: 1604–1615

    Not in our library10.1105/tpc.022475

  291. 291.

    Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998 ) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95: 9750–9754

    Not in our library10.1073/pnas.95.17.9750

  292. 292.

    Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tör M, de Vries S, Zipfel C (2011 ) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23: 2440–2455

    Not in our library10.1105/tpc.111.084301

  293. 293.

    Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE, Durrant WE, Fritz-Laylin L, Nekrasov V, Sjölander K, Yoshioka H, et al (2005 ) Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell 17: 295–310

    Not in our library10.1105/tpc.104.026013

  294. 294.
    Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions · 2020
    No notice
  295. 295.

    Saito T, Meshi T, Takamatsu N, Okada Y (1987 ) Coat protein gene sequence of tobacco mosaic virus encodes a host response determinant. Proc Natl Acad Sci USA 84: 6074–6077

    Not in our library10.1073/pnas.84.17.6074

  296. 296.
    Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99 · 2017
    No notice
  297. 297.

    Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J, Derbyshire P, Cevik V, Rallapalli G, Saucet SB, et al (2015 ) A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161: 1089–1100

    Not in our library10.1016/j.cell.2015.04.024

  298. 298.
    Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens · 2016
    No notice
  299. 299.

    Saucet SB, Ma Y, Sarris PF, Furzer OJ, Sohn KH, Jones JDG (2015 ) Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4. Nat Commun 6: 6338

    Not in our library10.1038/ncomms7338

  300. 300.

    Saur IM, Bauer S, Kracher B, Lu X, Franzeskakis L, Müller MC, Sabelleck B, Kümmel F, Panstruga R, Maekawa T, et al (2019 ) Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. eLife 8: e44471

    Not in our library10.7554/elife.44471

  301. 301.

    Saur IML, Kadota Y, Sklenar J, Holton NJ, Smakowska E, Belkhadir Y, Zipfel C, Rathjen JP (2016 ) NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana. Proc Natl Acad Sci USA 113: 3389–3394

    Not in our library10.1073/pnas.1511847113

  302. 302.

    Schmidt SM, Lukasiewicz J, Farrer R, van Dam P, Bertoldo C, Rep M (2016 ) Comparative genomics of Fusarium oxysporum f. sp. melonis reveals the secreted protein recognized by the Fom-2 resistance gene in melon. New Phytol 209: 307–318

    Not in our library10.1111/nph.13584

  303. 303.

    Schornack S, Ballvora A, Gürlebeck D, Peart J, Baulcombe D, Ganal M, Baker B, Bonas U, Lahaye T (2004 ) The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37: 46–60

    Not in our library10.1046/j.1365-313x.2003.01937.x

  304. 304.
    Expression Levels of avrBs3-Like Genes Affect Recognition Specificity in Tomato Bs4- But Not in Pepper Bs3-Mediated Perception · 2005
    Not checked
  305. 305.

    Schultink A, Qi T, Bally J, Staskawicz B (2019 ) Using forward genetics in Nicotiana benthamiana to uncover the immune signaling pathway mediating recognition of the Xanthomonas perforans effector XopJ4. New Phytol 221: 1001–1009

    Not in our library10.1111/nph.15411

  306. 306.

    Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B (2017 ) Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J 92: 787–795

    Not in our library10.1111/tpj.13715

  307. 307.

    Schulze S, Yu L, Ehinger A, Kolb D, Saile S, Stahl M, Franz-Wachtel M, Li L, El Kasmi F, Cevik V, et al (2021 ) The TIR-NBS-LRR protein CSA1 is required for autoimmune cell death in Arabidopsis pattern recognition co-receptor bak1 and bir3 mutants. BioRxiv doi: 10.1101/2021.04.11.438637

    Not in our library

  308. 308.

    Schwessinger B, Bahar O, Thomas N, Holton N, Nekrasov V, Ruan D, Canlas PE, Daudi A, Petzold CJ, Singan VR, et al (2015 ) Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLoS Pathog 11: e1004809

    Not in our library10.1371/journal.ppat.1004809

  309. 309.
    Phosphorylation-Dependent Differential Regulation of Plant Growth, Cell Death, and Innate Immunity by the Regulatory Receptor-Like Kinase BAK1 · 2011
    No notice
  310. 310.

    Segonzac C, Macho AP, Sanmartín M, Ntoukakis V, Sánchez-Serrano JJ, Zipfel C (2014 ) Negative control of BAK1 by protein phosphatase 2A during plant innate immunity. EMBO J 33: 2069–2079

    Not in our library10.15252/embj.201488698

  311. 311.

    Seo YS, Rojas MR, Lee JY, Lee SW, Jeon JS, Ronald P, Lucas WJ, Gilbertson RL (2006 ) A viral resistance gene from common bean functions across plant families and is up-regulated in a non-virus-specific manner. Proc Natl Acad Sci USA 103: 11856–11861

    Not in our library10.1073/pnas.0604815103

  312. 312.

    Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J (2008 ) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4: 17–27

    Not in our library10.1016/j.chom.2008.05.017

  313. 313.

    Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003 ) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301: 1230–1233

    Not in our library10.1126/science.1085671

  314. 314.

    Shi G, Zhang Z, Friesen TL, Raats D, Fahima T, Brueggeman RS, Lu S, Trick HN, Liu Z, Chao W, et al (2016 ) The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci Adv 2: e1600822

    Not in our library10.1126/sciadv.1600822

  315. 315.

    Shirasu K (2009 ) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60: 139–164

    Not in our library10.1146/annurev.arplant.59.032607.092906

  316. 316.

    Shiu SH, Bleecker AB (2003 ) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132: 530–543

    Not in our library10.1104/pp.103.021964

  317. 317.

    Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BACM, Baulcombe DC (2012 ) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24: 859–874

    Not in our library10.1105/tpc.111.095380

  318. 318.

    Smakowska-Luzan E, Mott GA, Parys K, Stegmann M, Howton TC, Layeghifard M, Neuhold J, Lehner A, Kong J, Grünwald K, et al (2018 ) An extracellular network of Arabidopsis leucine-rich repeat receptor kinases. Nature 553: 342–346

    Not in our library10.1038/nature25184

  319. 319.
    Characterization of Susceptibility and Resistance Responses to Potato Cyst Nematode (Globodera spp.) Infection of Tomato Lines in the Absence and Presence of the Broad-Spectrum Nematode Resistance Hero Gene · 2005
    Not checked
  320. 320.

    Sone T, Takeuchi S, Miki S, Satoh Y, Ohtsuka K, Abe A, Asano K (2013 ) Homologous recombination causes the spontaneous deletion of AVR-Pia in Magnaporthe oryzae. FEMS Microbiol Lett 339: 102–109

    Not in our library10.1111/1574-6968.12058

  321. 321.
    Two RxLR Avirulence Genes in Phytophthora sojae Determine Soybean Rps1k-Mediated Disease Resistance · 2013
    Not checked
  322. 322.

    Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, et al (1995 ) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804–1806

    Not in our library10.1126/science.270.5243.1804

  323. 323.

    Srichumpa P, Brunner S, Keller B, Yahiaoui N (2005 ) Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat. Plant Physiol 139: 885–895

    Not in our library10.1104/pp.105.062406

  324. 324.

    Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel C (2017 ) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355: 287–289

    Not in our library10.1126/science.aal2541

  325. 325.

    Steinbrenner AD, Munoz-Amatriain M, Venegas JMA, Lo S, Shi D, Holton N, Zipfel C, Abagyan R, Huffaker A, Close TJ, et al (2019 ) A receptor for herbivore-associated molecular patterns mediates plant immunity. BioRxiv doi: 10.1101/679803

    Not in our library

  326. 326.
    Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity · 2018
    No notice
  327. 327.

    Sun T, Huang J, Xu Y, Verma V, Jing B, Sun Y, Ruiz Orduna A, Tian H, Huang X, Xia S, et al (2020 ) Redundant CAMTA transcription factors negatively regulate the biosynthesis of salicylic acid and N-hydroxypipecolic acid by modulating the expression of SARD1 and CBP60g. Mol Plant 13: 144–156

    Not in our library10.1016/j.molp.2019.10.016

  328. 328.
    ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity · 2015
    No notice
  329. 329.
    Pathogen effector recognition-dependent association of NRG1 with EDS1 and SAG101 in TNL receptor immunity · 2021
    No notice
  330. 330.

    Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J (2013 ) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342: 624–628

    Not in our library10.1126/science.1243825

  331. 331.

    Swanson KV, Deng M, Ting JPY (2019 ) The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol 19: 477–489

    Not in our library10.1038/s41577-019-0165-0

  332. 332.

    Sweat TA, Lorang JM, Bakker EG, Wolpert TJ (2008 ) Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis. Mol Plant Microbe Interact 21: 7–19

    Not in our library10.1094/mpmi-21-1-0007

  333. 333.

    Takagi M, Hamano K, Takagi H, Morimoto T, Akimitsu K, Terauchi R, Shirasu K, Ichimura K (2019 ) Disruption of the MAMP-induced MEKK1-MKK1/MKK2-MPK4 pathway activates the TNL immune receptor SMN1/RPS6. Plant Cell Physiol 60: 778–787

    Not in our library10.1093/pcp/pcy243

  334. 334.

    Takahashi A, Casais C, Ichimura K, Shirasu K (2003 ) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100: 11777–11782

    Not in our library10.1073/pnas.2033934100

  335. 335.

    Tameling WIL, Baulcombe DC (2007 ) Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19: 1682–1694

    Not in our library10.1105/tpc.107.050880

  336. 336.

    Tarr DEK, Alexander HM (2009 ) TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders. BMC Res Notes 2: 197

    Not in our library10.1186/1756-0500-2-197

  337. 337.

    Tateda C, Zhang Z, Shrestha J, Jelenska J, Chinchilla D, Greenberg JT (2014 ) Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell 26: 4171–4187

    Not in our library10.1105/tpc.114.131938

  338. 338.

    Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JD (1997 ) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9: 2209–2224

    Not in our library10.1105/tpc.9.12.2209

  339. 339.

    Thomas NC, Hendrich CG, Gill US, Allen C, Hutton SF, Schultink A (2020 ) The immune receptor Roq1 confers resistance to the bacterial pathogens xanthomonas, Pseudomonas syringae, and ralstonia in tomato. Front Plant Sci 11: 463

    Not in our library10.3389/fpls.2020.00463

  340. 340.

    Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011 ) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4–15

    Not in our library10.1105/tpc.110.082602

  341. 341.

    Thor K, et al (2020 ) The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity. Nature 585: 569–573

    Not in our library10.1038/s41586-020-2702-1

  342. 342.

    Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997 ) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11: 1187–1194

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    Tian H, Chen S, Wu Z, Ao K, Yaghmaiean H, Sun T, Huang W, Xu F, Zhang Y, Wang S, et al (2020 ) Activation of TIR signaling is required for pattern-triggered immunity. BioRxiv doi: 10.1101/2020.12.27.424494

    Not in our library

  344. 344.

    Tian H, Wu Z, Chen S, Ao K, Huang W, Yaghmaiean H, Sun T, Xu F, Zhang Y, Wang S, et al (2021 ) Activation of TIR signalling boosts pattern-triggered immunity. Nature 598: 500–503

    Not in our library10.1038/s41586-021-03987-1

  345. 345.

    Tian W, Hou C, Ren Z, Wang C, Zhao F, Dahlbeck D, Hu S, Zhang L, Niu Q, Li L, et al (2019 ) A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572: 131–135

    Not in our library10.1038/s41586-019-1413-y

  346. 346.

    Tomita R, Sekine KT, Mizumoto H, Sakamoto M, Murai J, Kiba A, Hikichi Y, Suzuki K, Kobayashi K (2011 ) Genetic basis for the hierarchical interaction between Tobamovirus spp. and L resistance gene alleles from different pepper species. Mol Plant Microbe Interact 24: 108–117

    Not in our library10.1094/mpmi-06-10-0127

  347. 347.

    Torres MA, Dangl JL, Jones JDG (2002 ) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99: 517–522

    Not in our library10.1073/pnas.012452499

  348. 348.

    Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998 ) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J 14: 365–370

    Not in our library10.1046/j.1365-313x.1998.00136.x

  349. 349.

    Triplett LR, Cohen SP, Heffelfinger C, Schmidt CL, Huerta AI, Tekete C, Verdier V, Bogdanove AJ, Leach JE (2016 ) A resistance locus in the American heirloom rice variety Carolina Gold Select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola. Plant J 87: 472–483

    Not in our library10.1111/tpj.13212

  350. 350.

    Truman W, Sreekanta S, Lu Y, Bethke G, Tsuda K, Katagiri F, Glazebrook J (2013 ) The CALMODULIN-BINDING PROTEIN60 family includes both negative and positive regulators of plant immunity. Plant Physiol 163: 1741–1751

    Not in our library10.1104/pp.113.227108

  351. 351.
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    No notice
  352. 352.

    van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, de Wit PJGM (2006 ) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19: 1420–1430

    Not in our library10.1094/mpmi-19-1420

  353. 353.

    van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, Maclean D, Takken FLW, Jones JDG (2008 ) The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20: 697–719

    Not in our library10.1105/tpc.107.056978

  354. 354.

    Van der Biezen EA, Jones JD (1998 ) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23: 454–456

    Not in our library10.1016/s0968-0004(98)01311-5

  355. 355.

    van der Burgh AM, Joosten MHAJ (2019 ) Plant immunity: thinking outside and inside the box. Trends Plant Sci 24: 587–601

    Not in our library10.1016/j.tplants.2019.04.009

  356. 356.

    van der Hoorn RAL, Kamoun S (2008 ) From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 20: 2009–2017

    Not in our library10.1105/tpc.108.060194

  357. 357.

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  358. 358.
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    Not checked
  359. 359.
    Effector Genomics Accelerates Discovery and Functional Profiling of Potato Disease Resistance and Phytophthora Infestans Avirulence Genes · 2008
    No notice
  360. 360.

    Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME, Rietman H, Cano LM, Lokossou A, Kessel G, et al (2011 ) Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol 49: 507–531

    Not in our library10.1146/annurev-phyto-072910-095326

  361. 361.

    Vo KTX, Lee SK, Halane MK, Song MY, Hoang TV, Kim CY, Park SY, Jeon J, Kim ST, Sohn KH, et al (2019 ) Pi5 and pii paired nlrs are functionally exchangeable and confer similar disease resistance specificity. Mol Cells 42: 637–645

    Not in our library10.14348/molcells.2019.0070

  362. 362.
    Callose-mediated resistance to pathogenic intruders in plant defense-related papillae · 2014
    No notice
  363. 363.

    Vossen JH, van Arkel G, Bergervoet M, Jo KR, Jacobsen E, Visser RGF (2016 ) The Solanum demissum R8 late blight resistance gene is an Sw-5 homologue that has been deployed worldwide in late blight resistant varieties. Theor Appl Genet 129: 1785–1796

    Not in our library10.1007/s00122-016-2740-0

  364. 364.

    Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E, Bautor J, Niefind K, Parker JE (2013 ) Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe 14: 619–630

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  365. 365.

    Wan J, Tanaka K, Zhang XC, Son GH, Brechenmacher L, Nguyen THN, Stacey G (2012 ) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 160: 396–406

    Not in our library10.1104/pp.112.201699

  366. 366.

    Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008 ) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471–481

    Not in our library10.1105/tpc.107.056754

  367. 367.

    Wan L, Essuman K, Anderson RG, Sasaki Y, Monteiro F, Chung EH, Osborne Nishimura E, DiAntonio A, Milbrandt J, Dangl JL, et al (2019a ) TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. Science 365: 799–803

    Not in our library10.1126/science.aax1771

  368. 368.

    Wan WL, Zhang L, Pruitt R, Zaidem M, Brugman R, Ma X, Krol E, Perraki A, Kilian J, Grossmann G, et al (2019b ) Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences. New Phytol 221: 2080–2095

    Not in our library10.1111/nph.15497

  369. 369.
    A lectin receptor kinase as a potential sensor for extracellular nicotinamide adenine dinucleotide in Arabidopsis thaliana · 2017
    Not checked
  370. 370.

    Wang G, Roux B, Feng F, Guy E, Li L, Li N, Zhang X, Lautier M, Jardinaud M-F, Chabannes M, et al (2015 ) The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18: 285–295

    Not in our library10.1016/j.chom.2015.08.004

  371. 371.

    Wang J, Grubb LE, Wang J, Liang X, Li L, Gao C, Ma M, Feng F, Li M, Li L, et al (2018a ) A regulatory module controlling homeostasis of a plant immune kinase. Mol Cell 69: 493–504.e6

    Not in our library10.1016/j.molcel.2017.12.026

  372. 372.

    Wang J, Hu M, Wang J, Qi J, Han Z, Wang G, Qi Y, Wang HW, Zhou JM, Chai J (2019a ) Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364: eaav5870

    Not in our library10.1126/science.aav5870

  373. 373.

    Wang J, Wang J, Hu M, Wu S, Qi J, Wang G, Han Z, Qi Y, Gao N, Wang HW, et al (2019b ) Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364: eaav5868

    Not in our library10.1126/science.aav5868

  374. 374.

    Wang L, Albert M, Einig E, Fürst U, Krust D, Felix G (2016 ) The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein. Nat Plants 2: 16185

    Not in our library10.1038/nplants.2016.185

  375. 375.

    Wang L, Einig E, Almeida-Trapp M, Albert M, Fliegmann J, Mithöfer A, Kalbacher H, Felix G (2018b ) The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nat Plants 4: 152–156

    Not in our library10.1038/s41477-018-0106-0

  376. 376.

    Wang Y, Li J, Hou S, Wang X, Li Y, Ren D, Chen S, Tang X, Zhou JM (2010 ) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22: 2033–2044

    Not in our library10.1105/tpc.110.075697

  377. 377.

    Wang Y, Schuck S, Wu J, Yang P, Döring AC, Zeier J, Tsuda K (2018c ) A MPK3/6-WRKY33-ALD1-pipecolic acid regulatory loop contributes to systemic acquired resistance. Plant Cell 30: 2480–2494

    Not in our library10.1105/tpc.18.00547

  378. 378.
    Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection · 2018
    No notice
  379. 379.
    The TIR-NB-LRR pair DSC1 and WRKY19 contributes to basal immunity of Arabidopsis to the root-knot nematode Meloidogyne incognita · 2020
    Not checked
  380. 380.

    Weber H, Pfitzner AJ (1998 ) Tm-2(2) resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Mol Plant Microbe Interact 11: 498–503

    Not in our library10.1094/mpmi.1998.11.6.498

  381. 381.

    Wen RH, Khatabi B, Ashfield T, Saghai Maroof MA, Hajimorad MR (2013 ) The HC-Pro and P3 cistrons of an avirulent Soybean mosaic virus are recognized by different resistance genes at the complex Rsv1 locus. Mol Plant Microbe Interact 26: 203–215

    Not in our library10.1094/mpmi-06-12-0156-r

  382. 382.

    Westerink N, Brandwagt BF, de Wit PJGM, Joosten MHAJ (2004 ) Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol Microbiol 54: 533–545

    Not in our library10.1111/j.1365-2958.2004.04288.x

  383. 383.

    Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994 ) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78: 1101–1115

    Not in our library10.1016/0092-8674(94)90283-6

  384. 384.

    Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF, Segonzac C, Ve T, Ma Y, Saucet SB, Ericsson DJ, et al (2014 ) Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344: 299–303

    Not in our library10.1126/science.1247357

  385. 385.

    Willmann R, Lajunen HM, Erbs G, Newman M-A, Kolb D, Tsuda K, Katagiri F, Fliegmann J, Bono J-J, Cullimore JV, et al (2011 ) Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci USA 108: 19824–19829

    Not in our library10.1073/pnas.1112862108

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    Witek K, Lin X, Karki HS, Jupe F, Witek AI, Steuernagel B, Stam R, van Oosterhout C, Fairhead S, Heal R, et al (2021 ) A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector. Nat Plants 7: 198–208

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  387. 387.

    Wu AJ, Andriotis VME, Durrant MC, Rathjen JP (2004 ) A patch of surface-exposed residues mediates negative regulation of immune signaling by tomato Pto kinase. Plant Cell 16: 2809–2821

    Not in our library10.1105/tpc.104.024141

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    Wu CH, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R, Vossen JH, Kamoun S (2017a ) NLR network mediates immunity to diverse plant pathogens. Proc Natl Acad Sci USA 114: 8113–8118

    Not in our library10.1073/pnas.1702041114

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    Wu CH, Derevnina L, Kamoun S (2018 ) Receptor networks underpin plant immunity. Science 360: 1300–1301

    Not in our library10.1126/science.aat2623

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    Not in our library10.1038/s41586-020-2032-3

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    Not in our library10.1111/nph.13310

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    Wu J, van der Burgh A, Bi G, Zhang L, Alfano JR, Martin GB, Joosten MHAJ (2017b ) The bacterial effector AvrPto targets the regulatory co-receptor SOBIR1 and suppresses defence signalling mediated by the receptor-like protein Cf-4. Mol Plant Microbe Interact 31: 75–85

    Not in our library10.1094/mpmi-08-17-0203-fi

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    Wu Y, Gao Y, Zhan Y, Kui H, Liu H, Yan L, Kemmerling B, Zhou JM, He K, Li J (2020b ) Loss of the common immune coreceptor BAK1 leads to NLR-dependent cell death. Proc Natl Acad Sci USA 117: 27044–27053

    Not in our library10.1073/pnas.1915339117

  394. 394.

    Wu Z, Li M, Dong OX, Xia S, Liang W, Bao Y, Wasteneys G, Li X (2019 ) Differential regulation of TNL-mediated immune signaling by redundant helper CNLs. New Phytol 222: 938–953

    Not in our library10.1111/nph.15665

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    Wu Z, Tian L, Li X (2021a ) N-terminally truncated helper NLR NRG1C antagonizes immunity mediated by its full-length neighbors NRG1A and NRG1B. BioRxiv doi: 10.1101/2021.01.27.428547

    Not in our library10.1093/plcell/koab285

  396. 396.

    Wu Z, Tian L, Liu X, Zhang Y, Li X (2021b ) TIR signaling promotes the interactions between EDS1/PAD4 and ADR1-L1 and oligomerization of ADR1-L1. BioRxiv doi: 10.1101/2021.05.23.445317

    Not in our library

  397. 397.

    Wu Z, Tong M, Tian L, Zhu C, Liu X, Zhang Y, Li X (2020c ) Plant E3 ligases SNIPER1 and SNIPER2 broadly regulate the homeostasis of sensor NLR immune receptors. EMBO J 39: e104915

    Not in our library10.15252/embj.2020104915

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    Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, et al (2008 ) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18: 74–80

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  399. 399.

    Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001 ) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291: 118–120

    Not in our library10.1126/science.291.5501.118

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    Xiao Y, Stegmann M, Han Z, DeFalco TA, Parys K, Xu L, Belkhadir Y, Zipfel C, Chai J (2019 ) Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572: 270–274

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    Xing W, Zou Y, Liu Q, Liu J, Luo X, Huang Q, Chen S, Zhu L, Bi R, Hao Q, et al (2007 ) The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449: 243–247

    Not in our library10.1038/nature06109

  402. 402.

    Xu F, Xu S, Wiermer M, Zhang Y, Li X (2012 ) The cyclin L homolog MOS12 and the MOS4-associated complex are required for the proper splicing of plant resistance genes. Plant J 70: 916–928

    Not in our library10.1111/j.1365-313x.2012.04906.x

  403. 403.

    Xu S, Zhang Z, Jing B, Gannon P, Ding J, Xu F, Li X, Zhang Y (2011 ) Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLoS Genet 7: e1002159

    Not in our library10.1371/journal.pgen.1002159

  404. 404.

    Yamada K, Yamaguchi K, Shirakawa T, Nakagami H, Mine A, Ishikawa K, Fujiwara M, Narusaka M, Narusaka Y, Ichimura K, et al (2016 ) The Arabidopsis CERK1-associated kinase PBL27 connects chitin perception to MAPK activation. EMBO J 35: 2468–2483

    Not in our library10.15252/embj.201694248

  405. 405.

    Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010 ) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22: 508–522

    Not in our library10.1105/tpc.109.068874

  406. 406.

    Yamaguchi Y, Pearce G, Ryan CA (2006 ) The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA 103: 10104–10109

    Not in our library10.1073/pnas.0603729103

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    Yang CW, González-Lamothe R, Ewan RA, Rowland O, Yoshioka H, Shenton M, Ye H, O’Donnell E, Jones JDG, Sadanandom A (2006 ) The E3 ubiquitin ligase activity of arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. Plant Cell 18: 1084–1098

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    Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco · 2001
    Not checked
  409. 409.

    Yoon M, Rikkerink EHA (2020 ) Rpa1 mediates an immune response to avrRpm1Psa and confers resistance against Pseudomonas syringae pv. actinidiae. Plant J 102: 688–702

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    Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation · 1998
    Not checked
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    Yu D, Song W, Tan EYJ, Liu L, Cao Y, Jirschitzka J, Li E, Logemann E, Xu C, Huang S, et al (2021 ) TIR domains of plant immune receptors are 2’,3'-cAMP/cGMP synthetases mediating cell death. BioRxiv doi: 10.1101/2021.11.09.467869

    Not in our library10.1016/j.cell.2022.04.032

  412. 412.

    Yu G, Xian L, Xue H, Yu W, Rufian JS, Sang Y, Morcillo RJL, Wang Y, Macho AP (2020 ) A bacterial effector protein prevents MAPK-mediated phosphorylation of SGT1 to suppress plant immunity. PLoS Pathog 16: e1008933

    Not in our library10.1371/journal.ppat.1008933

  413. 413.

    Yuan M, Jiang Z, Bi G, Nomura K, Liu M, Wang Y, Cai B, Zhou JM, He SY, Xin XF (2021 ) Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592: 1–5

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  414. 414.

    Zeng X, Yang X, Zhao Z, Lin F, Wang L, Pan Q (2011 ) Characterization and fine mapping of the rice blast resistance gene Pia. Sci China Life Sci 54: 372–378

    Not in our library10.1007/s11427-011-4154-1

  415. 415.

    Zhai C, Zhang Y, Yao N, Lin F, Liu Z, Dong Z, Wang L, Pan Q (2014 ) Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PLoS One 9: e98067

    Not in our library10.1371/journal.pone.0098067

  416. 416.

    Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, et al (2007 ) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1: 175–185

    Not in our library10.1016/j.chom.2007.03.006

  417. 417.

    Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, et al (2010a ) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7: 290–301

    Not in our library10.1016/j.chom.2010.03.007

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    Zhang L, Kars I, Essenstam B, Liebrand TWH, Wagemakers L, Elberse J, Tagkalaki P, Tjoitang D, van den Ackerveken G, et al (2014 ) Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol 164: 352–364

    Not in our library10.1104/pp.113.230698

  419. 419.

    Zhang S, Klessig DF (1998 ) Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc Natl Acad Sci USA 95: 7433–7438

    Not in our library10.1073/pnas.95.13.7433

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    Zhang S, Wang L, Wu W, He L, Yang X, Pan Q (2015 ) Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Sci Rep 5: 11642

    Not in our library10.1038/srep11642

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    Zhang W, Fraiture M, Kolb D, Löffelhardt B, Desaki Y, Boutrot FFG, Tör M, Zipfel C, Gust AA, Brunner F (2013 ) Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25: 4227–4241

    Not in our library10.1105/tpc.113.117010

  422. 422.

    Zhang XC, Gassmann W (2007 ) Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. Plant Physiol 145: 1577–1587

    Not in our library10.1104/pp.107.108720

  423. 423.

    Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z, et al (2010b ) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci USA 107: 18220–18225

    Not in our library10.1073/pnas.1005225107

  424. 424.

    Zhang Z, Liu Y, Huang H, Gao M, Wu D, Kong Q, Zhang Y (2017a ) The NLR protein SUMM2 senses the disruption of an immune signaling MAP kinase cascade via CRCK3. EMBO Rep 18: 292–302

    Not in our library10.15252/embr.201642704

  425. 425.

    Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Ba H, Zhou J, Zhang Y (2012 ) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11: 253–263

    Not in our library10.1016/j.chom.2012.01.015

  426. 426.

    Zhang ZM, Ma KW, Gao L, Hu Z, Schwizer S, Ma W, Song J (2017b ) Mechanism of host substrate acetylation by a YopJ family effector. Nat Plants 3: 17115

    Not in our library10.1038/nplants.2017.115

  427. 427.

    Zhao B, Ardales EY, Raymundo A, Bai J, Trick HN, Leach JE, Hulbert SH (2004 ) The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Mol Plant Microbe Interact 17: 771–779

    Not in our library10.1094/mpmi.2004.17.7.771

  428. 428.

    Zhao Y, Huang J, Wang Z, Jing S, Wang Y, Ouyang Y, Cai B, Xin X-F, Liu X, Zhang C, et al (2016 ) Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proc Natl Acad Sci USA 113: 12850–12855

    Not in our library10.1073/pnas.1614862113

  429. 429.

    Zhou J, Wu S, Chen X, Liu C, Sheen J, Shan L, He P (2014 ) The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1. Plant J 77: 235–245

    Not in our library10.1111/tpj.12381

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    Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998 ) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10: 1021–1030

    Not in our library10.1105/tpc.10.6.1021

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    Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006 ) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749–760

    Not in our library10.1016/j.cell.2006.03.037

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    Zorzatto C, Machado JPB, Lopes KVG, Nascimento KJT, Pereira WA, Brustolini OJB, Reis PAB, Calil IP, Deguchi M, Sachetto-Martins G, et al (2015 ) NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature 520: 679–682

    Not in our library10.1038/nature14171

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    Zou Y, Wang S, Zhou Y, Bai J, Huang G, Liu X, Zhang Y, Tang D, Lu D (2018 ) Transcriptional regulation of the immune receptor FLS2 controls the ontogeny of plant innate immunity. Plant Cell 30: 2779–2794

    Not in our library10.1105/tpc.18.00297

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