Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection

Activation of innate immunity by membrane-localized receptors is conserved across eukaryotes. Plant genomes contain hundreds of such receptor-like genes and those encoding proteins with an extracellular leucine-rich repeat (LRR) domain represent the largest family. Here, we develop a high-throughput approach to study LRR receptor-like genes on a genome-wide scale. In total, 257 tobacco rattle virus-based constructs are generated to target 386 of the 403 identified LRR receptor-like genes in Nicotiana benthamiana for silencing. Using this toolkit, we identify the LRR receptor-like protein Response to XEG1 (RXEG1) that specifically recognizes the glycoside hydrolase 12 protein XEG1. RXEG1 associates with XEG1 via the LRR domain in the apoplast and forms a complex with the LRR receptor-like kinases BAK1 and SOBIR1 to transduce the XEG1-induced defense signal. Thus, this genome-wide silencing assay is demonstrated to be an efficient toolkit to pinpoint new immune receptors, which will contribute to developing durable disease resistance. The role of most plant leucine-rich repeat (LRR) receptors in innate immunity is unknown. Here, the authors develop virus-based constructs to silence LRR receptor-like genes in the Nicotiana benthamiana genome and identify Response to XEG1 that specifically recognizes the glycoside hydrolase 12 protein XEG1.

• Publication year

  2018

• Venue

  Nature Communications

• Publication date

  2018-02-09

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/s41467-018-03010-8PMID 29426870PMCID 5807360
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition[OPEN]

  2017cited by this paper
• Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate‐binding module 1

  2017cited by this paper
• New Insights on Leucine-Rich Repeats Receptor-Like Kinase Orthologous Relationships in Angiosperms

  2017cited by this paper
• PLANT SCIENCE: A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor

  2017cited by this paper
• A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae.

  2017cited by this paper
• Apoplastic recognition of multiple candidate effectors from the wheat pathogen Zymoseptoria tritici in the nonhost plant Nicotiana benthamiana

  2016cited by this paper
• Genomic screens identify a new phytobacterial microbe-associated molecular pattern and the cognate Arabidopsis receptor-like kinase that mediates its immune elicitation

  2016cited by this paper
• Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system

  2016cited by this paper
• Evolutionary Dynamics of the Leucine-Rich Repeat Receptor-Like Kinase (LRR-RLK) Subfamily in Angiosperms1[OPEN]

  2016cited by this paper
• NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana

  2016cited by this paper
• The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein

  2016cited by this paper
• L-type lectin receptor kinases in Nicotiana benthamiana and tomato and their role in Phytophthora resistance

  2015cited by this paper
• Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato

  2015cited by this paper
• A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana

  2015cited by this paper
• An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity

  2015cited by this paper
• The SGN VIGS tool: user-friendly software to design virus-induced gene silencing (VIGS) constructs for functional genomics.

  2015cited by this paper
• A Phytophthora sojae Glycoside Hydrolase 12 Protein Is a Major Virulence Factor during Soybean Infection and Is Recognized as a PAMP[OPEN]

  2015cited by this paper
• A Conserved Peptide Pattern from a Widespread Microbial Virulence Factor Triggers Pattern-Induced Immunity in Arabidopsis

  2014cited by this paper
• Tobacco rattle virus–based virus-induced gene silencing in Nicotiana benthamiana

  2014cited by this paper
• Genome analysis of poplar LRR-RLP gene clusters reveals RISP, a defense-related gene coding a candidate endogenous peptide elicitor

  2014cited by this paper
• Effector-triggered defence against apoplastic fungal pathogens

  2014cited by this paper
• Combining Transcriptome Assemblies from Multiple De Novo Assemblers in the Allo-Tetraploid Plant Nicotiana benthamiana

  2014cited by this paper
• Two for all: receptor-associated kinases SOBIR1 and BAK1.

  2014cited by this paper
• Phenotypic analyses of Arabidopsis T-DNA insertion lines and expression profiling reveal that multiple L-type lectin receptor kinases are involved in plant immunity.

  2014cited by this paper
• Receptor like proteins associate with SOBIR1-type of adaptors to form bimolecular receptor kinases.

  2014cited by this paper
• Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection

  2013cited by this paper
• Arabidopsis RECEPTOR-LIKE PROTEIN30 and Receptor-Like Kinase SUPPRESSOR OF BIR1-1/EVERSHED Mediate Innate Immunity to Necrotrophic Fungi[W][OPEN]

  2013cited by this paper
• De Novo Transcriptome Sequence Assembly and Analysis of RNA Silencing Genes of Nicotiana benthamiana

  2013cited by this paper
• Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex

  2013cited by this paper
• Fungal Endopolygalacturonases Are Recognized as Microbe-Associated Molecular Patterns by the Arabidopsis Receptor-Like Protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES11[W]

  2013cited by this paper
• The Receptor-Like Protein ReMAX of Arabidopsis Detects the Microbe-Associated Molecular Pattern eMax from Xanthomonas[W]

  2013cited by this paper
• Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing

  2012cited by this paper
• The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense

  2012cited by this paper
• Plant innate immunity: perception of conserved microbial signatures.

  2012cited by this paper
• A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research.

  2012cited by this paper
• The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death.

  2012cited by this paper
• Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity.

  2011cited by this paper
• Phosphorylation-Dependent Differential Regulation of Plant Growth, Cell Death, and Innate Immunity by the Regulatory Receptor-Like Kinase BAK1

  2011cited by this paper
• Leucine-Rich repeat receptor kinases are sporadically distributed in eukaryotic genomes

  2011cited by this paper
• Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots

  2010cited by this paper
• BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1.

  2010cited by this paper
• The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors

  2010cited by this paper
• PEPR2 Is a Second Receptor for the Pep1 and Pep2 Peptides and Contributes to Defense Responses in Arabidopsis[W]

  2010cited by this paper
• The ERECTA Receptor-Like Kinase Regulates Cell Wall-Mediated Resistance to Pathogens in Arabidopsis thaliana.

  2009cited by this paper
• AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants.

  2009cited by this paper
• Receptor-like kinases shape the plant

  2009cited by this paper
• A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.

  2009cited by this paper
• One for all: the receptor-associated kinase BAK1.

  2009cited by this paper
• A Genome-Wide Functional Investigation into the Roles of Receptor-Like Proteins in Arabidopsis1[W][OA]

  2008cited by this paper
• Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions.

  2008cited by this paper
• Malectin: a novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation.

  2008cited by this paper
• A Ligation-Independent Cloning Tobacco Rattle Virus Vector for High-Throughput Virus-Induced Gene Silencing Identifies Roles for NbMADS4-1 and -2 in Floral Development1[W][OA]

  2007cited by this paper
• The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants

  2007cited by this paper
• An endogenous peptide signal in Arabidopsis activates components of the innate immune response.

  2006cited by this paper
• The plant immune system

  2006cited by this paper
• Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.

  2006cited by this paper
• The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception[W]

  2005cited by this paper
• Phylogenomic Analysis of the Receptor-Like Proteins of Rice and Arabidopsis1[w]

  2005cited by this paper
• The Receptor for the Fungal Elicitor Ethylene-Inducing Xylanase Is a Member of a Resistance-Like Gene Family in Tomato

  2004cited by this paper
• Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice

  2004cited by this paper
• Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis1[w]

  2003cited by this paper
• Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

  2001cited by this paper
• FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis.

  2000cited by this paper
• Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids.

  1999cited by this paper
• A point mutation in the ethylene-inducing xylanase elicitor inhibits the beta-1-4-endoxylanase activity but not the elicitation activity.

  1999cited by this paper

• H3K27me3-Mediated Epigenetic Silencing of FgHMG1 Enables Fungal Host Immune Evasion.

  2026cites this paper
• The dual role of Xanthomonas effector XccXynB in plant cell wall deconstruction and immunity activation

  2026cites this paper
• A conserved extracellular LRR-only protein disrupts BAK1-mediated immune receptor formation to negatively regulate plant immunity.

  2026cites this paper
• The secreted elicitor protein VmHrp1 from Valsa mali activates plant immunity through RLP26 to enhance disease resistance.

  2025cites this paper
• Deciphering the complex signaling networks in phytophthora infected plants: Insights into microbiome interactions and plant defense mechanisms.

  2025cites this paper
• A conserved Phytophthora apoplastic trypsin-like serine protease targets the receptor-like kinase BAK1 to dampen plant immunity

  2025cites this paper
• Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens, 20 Years Later: What Has Changed?

  2025cites this paper
• The receptor‐like protein RXEG1 confers broad‐spectrum resistance in soybean and cotton by recognizing microbial glycoside hydrolase 12 proteins

  2025influential citation
• Fighting Enemies in Every Which Way.

  2025cites this paper
• Reciprocal phosphorylation between SOAK1 and SOBIR1 fine-tunes receptor-like protein (RLP)–mediated plant immunity

  2025cites this paper
• Exploring the infection strategy of Colletotrichum fructicola in pecan and two effectors Cf-ID1 and Cf-ID2 were characterized using unique molecular identifier-RNA sequencing technology

  2025cites this paper
• A Necrotrophic Phytopathogen‐Derived GPI‐Anchored Protein Functions as an Elicitor to Activate Plant Immunity and Enhance Resistance

  2025cites this paper
• Proteomic Analysis of the Fusarium graminearum Secretory Proteins in Wheat Apoplast Reveals a Cell-Death-Inducing M43 Peptidase

  2025cites this paper
• Endophytic strategies decoded by genome and transcriptome analysis of Fusarium nematophilum strain NQ8GII4

  2025cites this paper
• A Fusarium pseudograminearum secreted protein Fp00392 is a major virulence factor during infection and is recognized as a PAMP1

  2025cites this paper
• Glucuronoyl Esterase of Pathogenic Phanerochaete carnosa Induces Immune Responses in Aspen Independently of Its Enzymatic Activity

  2025cites this paper
• StBPA1 attenuates surface receptor activation and finely regulates immune responses against bacterial and oomycete pathogens in potato.

  2025cites this paper
• The apoplastic protein OsCPIP8 confers dual protection by inhibiting pathogenic protease and activating rice immunity

  2025cites this paper
• Unraveling plant immunity: from pathogen perception to resistance engineering.

  2025cites this paper
• Genome-Wide Identification and Functional Characterization Reveal Four LRR-RLPs Mediating Valsa Canker Resistance in Apple (Malus domestica)

  2025cites this paper
• Cell-surface pattern recognition receptors: Emerging players in plant-oomycete interactions.

  2025cites this paper
• Oomycete plant pathogens: biology, pathogenesis and emerging control strategies.

  2025cites this paper
• Uncovering Convergent Pattern Recognition Receptors Recognising Phytophthora Across Plant Lineages

  2025cites this paper
• A GmNRF5a–GmCERK1–GmCAK1 module mediates chitin/chitosan‐triggered immune response in soybean

  2025cites this paper
• Temporally-coordinated bivalent histone modifications of BCG1 enable fungal invasion and immune evasion

  2024cites this paper
• Novel structural insights at the extracellular plant-pathogen interface.

  2024cites this paper
• A conserved protein family in mirid bug Riptortus pedestris plays dual roles in regulating plant immunity.

  2024cites this paper
• Profiling of Phakopsora pachyrhizi transcriptome revealed co-expressed virulence effectors as prospective RNA interference targets for soybean rust management.

  2024cites this paper
• Ss4368: Pathogen-Associated Molecular Pattern for Inducing Plant Cell Death and Resistance to Phytophthora capsici

  2024cites this paper
• Genomic and culture-based analysis of Cyclaneusma minus in New Zealand provides evidence for multiple morphotypes

  2024cites this paper
• AlphaFold-guided redesign of a plant pectin methylesterase inhibitor for broad-spectrum disease resistance.

  2024cites this paper
• A novel xylanase from a myxobacterium triggers a plant immune response in Nicotiana benthamiana

  2024cites this paper
• Receptor-like cytoplasmic kinases of different subfamilies differentially regulate SOBIR1/BAK1-mediated immune responses in Nicotiana benthamiana

  2024cites this paper
• Molecular characterization revealed the role of thaumatin-like proteins of Rhizoctonia solani AG4-JY in inducing maize disease resistance

  2024cites this paper
• Plant immunity suppression by an β-1,3-glucanase of the maize anthracnose pathogen Colletotrichum graminicola

  2024cites this paper
• Immune signaling: receptor-like proteins make the difference.

  2024cites this paper
• Structural Insights into Ligand Recognition and Receptor Activation of Plant Leucine-Rich Repeat (LRR) Transmembrane Receptors

  2024cites this paper
• Bioinformatics-based identification of GH12 endoxyloglucanases in citrus-pathogenic Penicillium spp.

  2024cites this paper
• The conserved GOLD domain in the Plasmodiophora brassicae effector Pb257 is required for triggering cell death and root swelling

  2024cites this paper
• Dual activation of soybean resistance against Phytophthora sojae by pectin lyase and degraded pectin oligosaccharides

  2024influential citation
• Enhancing Fruit Resistance against Fungal Pathogens Using a Pathogen-Associated Molecular Pattern PdEIX.

  2024cites this paper
• MaSMG7-Mediated Degradation of MaERF12 Facilitates Fusarium oxysporum f. sp. cubense Tropical Race 4 Infection in Musa acuminata

  2024cites this paper
• Receptor-like proteins: decision-makers of plant immunity

  2024cites this paper
• A novel protein elicitor (Cs08297) from Ciboria shiraiana enhances plant disease resistance

  2024cites this paper
• A receptor kinase senses sterol by coupling with elicitins in auxotrophic Phytophthora

  2024cites this paper
• A conserved extracellular effector protein Ssh1296 from Scleromitrula shiraiana triggers cell death and regulates plant immunity.

  2024cites this paper
• A novel LRR receptor-like kinase BRAK reciprocally phosphorylates PSKR1 to enhance growth and defense in tomato

  2024cites this paper
• A pair of soybean malectin-like domain-containing receptor-like kinases jointly regulate pattern-triggered immunity by forming hetero-oligomers

  2024influential citation
• PTI‐ETI synergistic signal mechanisms in plant immunity

  2024cites this paper
• SsdchA is a novel secretory cellobiohydrolase driving pathogenicity in Sclerotinia sclerotiorum

  2024cites this paper
• Plant Biostimulant as an Environmentally Friendly Alternative to Modern Agriculture.

  2024cites this paper
• Plant genes related to Phytophthora pathogens resistance

  2024cites this paper
• The receptor-like kinase ETI-dependent receptor-like kinase 1 positively regulates effector-triggered immunity by stabilizing NLR-required for cell death 4 in Nicotiana benthamiana.

  2024cites this paper
• A pair of G-type lectin receptor-like kinases modulate nlp20-mediated immune responses by coupling to RLP23 receptor complex.

  2023cites this paper
• A Nicotiana benthamiana receptor-like kinase regulates Phytophthora resistance by coupling with BAK1 to enhance elicitin-triggered immunity.

  2023cites this paper
• Resistance strategies for defense against Albugo candida causing white rust disease.

  2023cites this paper
• Plant Receptor-like proteins (RLPs): Structural features enabling versatile immune recognition

  2023cites this paper
• The effector Fg62 contributes to Fusarium graminearum virulence and induces plant cell death

  2023cites this paper
• A Pythium myriotylum Small Cysteine-Rich Protein Triggers Immune Responses in Diverse Plant Hosts.

  2023cites this paper
• Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS

  2023cites this paper
• Genomic, effector protein and culture-based analysis of Cyclaneusma minus in New Zealand provides evidence for multiple morphotypes

  2023cites this paper
• Stripe Rust Effector Pst_9302 Inhibits Wheat Immunity to Promote Susceptibility

  2023cites this paper
• Life and death: the destiny of Phytophthora sojae determined by a receptor-like kinase

  2023cites this paper
• Oomycete pathogen pectin acetylesterase targets host lipid transfer protein to reduce salicylic acid signaling.

  2023cites this paper
• A new spider mite elicitor triggers plant defenses and promotes resistance to herbivores.

  2023cites this paper
• Plasmopara viticola effector PvCRN11 induces disease resistance to downy mildew in grapevine.

  2023cites this paper
• Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities.

  2023cites this paper
• Structural insights of cell wall integrity signaling during development and immunity.

  2023cites this paper
• Stacking of PRRs in potato to achieve enhanced resistance against Phytophthora infestans

  2023cites this paper
• The CAP superfamily protein PsCAP1 secreted by Phytophthora triggers immune responses in Nicotiana benthamiana through a leucine-rich repeat receptor-like protein.

  2023cites this paper
• Divergent sequences of tetraspanins enable plants to specifically recognize microbe-derived extracellular vesicles

  2023cites this paper
• The power of patterns: new insights into pattern-triggered immunity.

  2023cites this paper
• A glycoside hydrolase 12 protein from Cytospora chrysosperma triggers plant immunity but is not essential to virulence

  2023cites this paper
• An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP

  2023cites this paper
• BAK1 protects the receptor-like kinase BIR2 from degradation to promote pattern-triggered immunity in Nicotiana benthamiana.

  2023cites this paper
• Plant immunity in soybean: progress, strategies, and perspectives

  2023cites this paper
• Convergent evolution of immune receptors underpins distinct elicitin recognition in closely related Solanaceous plants.

  2023cites this paper
• Recognition of Pep-13/25 MAMPs of Phytophthora localizes to an RLK locus in Solanum microdontum

  2023cites this paper
• Structural basis of RLP activation by a pathogen glycoside hydrolase.

  2022cites this paper
• A fungal microRNA-like RNA subverts host immunity and facilitates pathogen infection by silencing two host receptor-like kinase genes.

  2022cites this paper
• The novel leucine-rich repeat receptor-like kinase MRK1 regulates resistance to multiple stresses in tomato

  2022cites this paper
• Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector.

  2022cites this paper
• Thirty years of resistance: Zig-zag through the plant immune system

  2022influential citation
• Nep1-Like Proteins From the Biocontrol Agent Pythium oligandrum Enhance Plant Disease Resistance Independent of Cell Death and Reactive Oxygen Species

  2022cites this paper
• Secreted Glycoside Hydrolase Proteins as Effectors and Invasion Patterns of Plant-Associated Fungi and Oomycetes

  2022cites this paper
• Unraveling Plant Cell Death during Phytophthora Infection

  2022cites this paper
• Characterization of two conserved cell death elicitor families from the Dothideomycete fungal pathogens Dothistroma septosporum and Fulvia fulva (syn. Cladosporium fulvum)

  2022influential citation
• Development of Designer Transcription Activator-Like Effector-Based Plant Growth Regulator for Higher Yield in Rice

  2022cites this paper
• From plant immunity to crop disease resistance.

  2022cites this paper
• Functional Diversification Analysis of Soybean Malectin/Malectin-Like Domain-Containing Receptor-Like Kinases in Immunity by Transient Expression Assays

  2022cites this paper
• The Secreted Ribonuclease SRE1 Contributes to Setosphaeria turcica Virulence and Activates Plant Immunity

  2022cites this paper
• Co-evolved ascorbate oxidases of plant and the blast fungus orchestrate host apoplast redox state to modulate rice immunity.

  2022cites this paper
• Research Progress and Prospect of Alfalfa Resistance to Pathogens and Pests

  2022cites this paper
• Microbe-derived non-necrotic glycoside hydrolase family 12 proteins act as immunogenic signatures triggering plant defenses.

  2022cites this paper
• Two divergent immune receptors of the allopolyploid Nicotiana benthamiana reinforce the recognition of a fungal microbe-associated molecular pattern VdEIX3

  2022cites this paper
• Pathogenic strategies and immune mechanisms to necrotrophs: Differences and similarities to biotrophs and hemibiotrophs.

  2022cites this paper
• CC-type glutaredoxin gene CsGRX4 in cucumber responds to Botrytis cinerea via JA signaling pathway

  2022cites this paper
• Plant receptor-like protein activation by a microbial glycoside hydrolase

  2022cites this paper
• An F-box protein attenuates fungal xylanase-triggered immunity by destabilizing LRR-RLP NbEIX2 in a SOBIR1-dependent manner.

  2022cites this paper
• New insights from a plant immune receptor may help design of disease resistant crops

  2022cites this paper