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

The Plant Cell, Journal Year: 2022, Volume and Issue: 34(5), P. 1447 - 1478

Published: Feb. 10, 2022

Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate detection-and-response system. The first 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 (NLRs) cloned. Here, we provide list of characterized PRRs NLRs. In addition receptors, components signaling networks were discovered over last 30 years. We review pathways, physiological responses, molecular regulation both PRR- NLR-mediated immunity. Recent studies reinforced importance interactions between two systems. an overview immunity, highlighting challenges perspectives future research.

Language: Английский

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Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

Plant nucleotide-binding leucine-rich repeat-containing (NLR) receptors with an N-terminal Toll/interleukin-1 receptor (TIR) domain sense pathogen effectors to enable TIR-encoded nicotinamide adenine dinucleotide hydrolase (NADase) activity for immune signaling. TIR-NLR signaling requires the helper NLRs N requirement gene 1 (NRG1), Activated Disease Resistance (ADR1), and Enhanced Susceptibility (EDS1), which forms a heterodimer each of its paralogs Phytoalexin Deficient 4 (PAD4) Senescence-Associated Gene 101 (SAG101). Here, we show that TIR-containing proteins catalyze production 2'-(5''-phosphoribosyl)-5'-adenosine monophosphate (pRib-AMP) diphosphate (pRib-ADP) in vitro planta. Biochemical structural data demonstrate EDS1-PAD4 is complex pRib-AMP pRib-ADP, allosterically promote interaction ADR1-L1 but not NRG1A. Our study identifies TIR-catalyzed pRib-ADP as missing link TIR through likely second messengers plant immunity.

Language: Английский

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TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

Plant pathogen-activated immune signaling by nucleotide-binding leucine-rich repeat (NLR) receptors with an N-terminal Toll/interleukin-1 receptor (TIR) domain converges on Enhanced Disease Susceptibility 1 (EDS1) and its direct partners, Phytoalexin Deficient 4 (PAD4) or Senescence-Associated Gene 101 (SAG101). TIR-encoded nicotinamide adenine dinucleotide hydrolase (NADase) produces molecules to promote exclusive EDS1-PAD4 EDS1-SAG101 interactions helper NLR subclasses. In this work, we show that TIR-containing proteins catalyze adenosine diphosphate (ADP)-ribosylation of triphosphate (ATP) ADP ribose (ADPR) through ADPR polymerase-like NADase activity, forming ADP-ribosylated ATP (ADPr-ATP) ADPr-ADPR (di-ADPR), respectively. Specific binding ADPr-ATP di-ADPR allosterically promotes interaction N requirement gene 1A (NRG1A) in vitro planta. Our data reveal enzymatic activity TIRs enables specific activation the EDS1-SAG101-NRG1 immunity branch.

Language: Английский

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Ca ²⁺ signals in plant immunity

The EMBO Journal, Journal Year: 2022, Volume and Issue: 41(12)

Published: May 13, 2022

Review13 May 2022Open Access Ca2+ signals in plant immunity Philipp Köster orcid.org/0000-0002-1359-822X Institute of Plant and Microbial Biology Zürich-Basel Science Center, University Zürich, Switzerland Contribution: Visualization, Writing - original draft, review & editing Search for more papers by this author Thomas A DeFalco orcid.org/0000-0003-2897-1485 Cyril Zipfel Corresponding Author [email protected] orcid.org/0000-0003-4935-8583 The Sainsbury Laboratory, East Anglia, Norwich, UK Funding acquisition, Information Köster1, DeFalco1 *,1,2 1Institute 2The *Corresponding author. Tel: +41 044 63 48222; E-mail: EMBO Journal (2022)41:e110741https://doi.org/10.15252/embj.2022110741 PDFDownload PDF article text main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures Info Abstract Calcium ions function as a key second messenger ion eukaryotes. Spatially temporally defined cytoplasmic are shaped through the concerted activity channels, exchangers, pumps response diverse stimuli; these then decoded Ca2+-binding sensor proteins. In plants, signaling is central both pattern- effector-triggered immunity, with generation characteristic elevations potential pathogens being common both. However, despite their importance, long history scientific interest, transport proteins that shape integration remain poorly characterized. Here, we discuss recent work has shed light on deepened mysteries immunity. immune system All eukaryotes use systems protect themselves against pathogens. consists two characterized perception layers: one utilizes cell-surface pattern recognition receptors (PRRs) perceive extracellular immunogenic patterns, another relies intracellular nucleotide-binding leucine-rich repeat (NLR) recognize pathogenic effectors inside cell (Jones Dangl, 2006). first layer system, apoplastic elicitors such pathogen-, microbe-, damage-, or herbivore-associated molecular patterns (PAMPs, MAMPs, DAMPs, HAMPs, respectively) immune-modulating peptide phytocytokines recognized PRRs, which leads defense responses termed pattern-triggered (PTI) (Boller Felix, 2009; Yu et al, 2017; Zipfel, 2021). PRRs described date receptor kinases (RKs) (RPs) (Boutrot Albert 2020). RKs domain structure reminiscent metazoan tyrosine (RTKs) (DeFalco 2021); namely, ligand-binding (ECD), single-span transmembrane helix (TM) cytosolic protein kinase (Jamieson 2018), while RPs lack instead form functional bipartite adapter (Liebrand 2013; 2015; Postma 2016). Because architecture, plasma membrane (PM)-localized (or complexes) allow ligand binding be communicated across into events. nature varies, including proteins, lipids, carbohydrates, can derived from either pathogen herbivore (e.g., PAMPs, HAMPs) host plant, case macromolecules released upon damage (DAMPs) secreted (Gust 2017). PRR ECDs variety subdomains, (LRR), epidermal growth factor-like (EGF), lectin, lysin motif (LysM) domains best-studied to-date LRR-RKs FLAGELLIN-SENSING 2 (FLS2) EF-TU RECEPTOR (EFR), bacterial PAMPs flg22 elf18, respectively (Gómez-Gómez Boller, 2000; Both FLS2 EFR stable ligand-dependent complexes LRR-RK co-receptors SOMATIC EMBRYOGENESIS KINASE (SERK) family, BRASSINOSTEROID-INSENSITIVE 1-ASSOCIATED 1 (BAK1, also called SERK3) (Chinchilla 2007; Heese Roux 2011). Complex formation between phosphorylation events within activation receptor-like (RLCKs), directly phosphorylate regulate target order activate PTI (Liang Zhou, 2018; 2021) (Fig 1A). Figure 1. ETI induce residing at PM. They originating microbes, viruses, herbivores, parasitic damaged cells. turn, RLCKs activated downstream release few minutes after facet. Microbes introduce effector cells disturb overcome responses. Cytoplasmic NLRs sense presence ETI. To end, autoinhibition released, ADP changed ATP oligomerization occurs, leading finally (A). significant increase been reported occur Arabidopsis leaves starting 1.5 h peaking about infection avirulent bacteria (B). Schematic signatures plants induced Grant al (2000) RK: kinase; co-RK: coreceptor RP: protein; RLCK: like NLR: receptor; CC: coiled-coil; TIR: toll/interleukin-related; CNLs: CC-NLRs; TNLs: TIR-NLRs; RNLs: RPW8-NRLs; NBS: nucleotide site; LRR: repeats; PTI: immunity; ETI: c[Ca2+]: free concentration. Download figure PowerPoint Pathogens cytoplasm promote pathogenicity, often disturbing counteract this, rely NLR-type and/or activity, (ETI). Interestingly, share architecture those animals, featuring conserved (NBD) LRR domain, variable accessory N C termini (DeYoung Innes, 2006; Jones 2016; Baggs van Wersch categorized based N-terminal domains: coiled-coil (CC)-NLRs (CNLs), toll/interleukin-related (TIR)-NLRs (TNLs), RPW8-NLRs (RNLs). Of NLRs, CNLs TNLs sensors RNLs helpers (Baggs Wu Jubic 2019; Feehan present an inactive state, likely autoinhibitory, adenosine diphosphate (ADP) bound NBD (Williams 2011; Bernoux Upon activation, exchanged triphosphate (ATP) NLR via large multimeric structures (Danot 2009). similar mechanism hypothesized but only recently corroborated structural data discussed detail below. have traditionally viewed independent pathways; however, least some components shared layers (Thomma Activation triggers numerous overlapping events, fluxes, production reactive oxygen species (ROS), mitogen-activated (MAPK) cascades, transcriptional reprogramming, phytohormone biosynthesis (Cui Zhou Zhang, 2020; generally accompanied programmed death hypersensitive (HR) site 2006), although HR-like forms (Wang Recent further demonstrated linked levels (Ngou 2021; Pruitt Tian Yuan exact mechanisms governing linkage pathways remains elucidated fully. As changes intracelluar well documented thought (Seybold 2014; Moeder 2019). universal (Clapham, 2007). Owing its cytotoxicity, must maintained low (~10−8 10−7 M) living cells, thus sequestered stores (in primarily vacuole endoplasmatic reticulum, vesicular compartments, chloroplasts mitochondria) apoplast active transport, generating enormous electrochemical gradients membranes Edel Costa 2018). Ca2+-permeable channels therefore generate rapid, transient increases concentrations, turn interpreted suite cellular processes 2010). summarized three steps: encoding (via stimulus-triggered fluxes), decoding proteins), regulation processes). involved all aspects life, regulation, development, abiotic stress responses, reproduction (Kudla establishment beneficial plant-microbe interactions (Tian review, focus how encoded PM during signaling. influx oxidative burst (Doke, 1983, 1985; Apostol 1989; Keppler 1989) were among elicitor treatment (Atkinson 1996; Levine Zimmermann 1997; Lecourieux 2002). ROS was eventually attributed PM-localized NADPH oxidases RESPIRATORY BURST OXIDASE HOMOLOGUE (RBOH) family (Torres 2002); model thaliana (hereafter, Arabidopsis), single member, RBOHD, responsible (Nühse Zhang contrast, channel(s) remained comparably elusive many years 2014). Cytosolic evoked various measured culture using radioisotopes, Ca2+-sensitive dyes, electrophysiological approaches Gelli 1997). development genetically indicators (GECIs) greatly expanded possibilities real-time, kinetic analysis fluxes intact tissues treatment. GECI deployed aequorin (AEQ) Aequoria victoria (Knight 1991), holo-enzyme cofactor coelenterazine emits Ca2+-binding. When challenged virulent strains bacterium Pseudomonas syringae, expressing AEQ showed signal peak ~10 min. second, stronger, persistent seen 1.5–2 avirulent, ETI-activating P. syringae (Grant Kang 2010; Hung kinetics early elevation triggered (Blume 2002) biphasic ETI-inducing suggested may distinct 1B). Subsequent analyses AEQ-expressing shown elicitors, phytocytokines, sufficient elicit rapid (Ranf 2008, Vadassery Krol Such requires components, RLCK-VII/ AVRPPHB SUSCEPTIBLE (PBS1)-LIKE (PBL) members BOTRYTIS-INDUCED (BIK1) PBL1 (Li Ranf Monaghan 2015). More recently, deployment fluorescent GECIs allowed elicitor-induced level. include ratiometric yellow cameleons) intensiometric GCaMPs GECOs) (Grenzi 2021b; Waadt Flourescent utilized show oscillatory single-cell level (Thor Peiter, Keinath 2015) roots application laser ablation-induced lead transients (Keinath Marhavý Ca2+—tightly messengers There extensive interplay (Gilroy 2016); initial PTI-related mildly reduced oxidase inhibitor DPI catalase, there no effect longer-term, 2000). Similarly, rbohd mutants slight, quantitative defect elicitor-triggered when seedlings severely attenuated channel blockers Elicitor RBOHD BIK1 (Kadota Li 2014), suggesting complex relationship wherein, perception, PRR-mediated primes subsequent 2). not activates EF-hand indirectly Ca2+-regulated kinase-mediated (Ogasawara 2008; Dubiella 2013). CALCIUM DEPENDENT PROTEIN 5 (CPK5) sites (Dubiella Kadota While residues strictly required PTI-induced bursts 2007), individual contribution other impact certain uncovered. 2. tightly interconnected PTI, signals. NADPH-oxidase EF-hands, terminus (indicated grey arrows targeting p-sites). addition, thereby black Reactive perceived cysteine pairs RK HPCA1/CARD1. This H2O2 Arabidopsis, pathway HPCA1 known. AEQ-based screen impaired H2O2-induced identified LRR-RK, HYDROGEN PEROXIDE INDUCED INCREASE (HPCA1), putative (Wu 2020a). independently CANNOT RESPOND TO DMBQ (CARD1), loss quinone compound 2,6-dimethoxy-1,4-benzoquinone (DMBQ), regulates HPCA1/CARD1-dependent (Laohavisit regulated HPCA1/CARD1, role regulating sensor(s) unclear. AEQ-measured calcium cngc2 cngc4 2019), perception. Shaping efflux generated coordinated action transporters involve (Spalding Harper, Resentini possess major families mediate out cytosol: Ca2+/H+ exchangers (CAXs), autoinhibited Ca2+-ATPases (ACAs) ER (Geisler Shigaki Hirschi, García Bossi ACA relieved Ca2+/CaM-binding, allows feedback ACA8 homolog ACA10 interactors FLS2, aca8 aca10 displayed defects flg22-induced compromised resistance (Frei dit Frey 2012), disturbed stomatal closure PAMP (Yang 2017), shapes PTI. Two tonoplast-localized ACAs, ACA4 ACA11, implicated aca4 aca11 display autoimmune phenotypes spontaneous (Boursiac Although wildtype total content 2010), revealed basal elevated (Hilleary Elicitor-induced peaks 3), rescued mis-localization ACAs tonoplast 2020), indicating critical maintain homeostasis modulate 3. Disturbance machinery impairs (CAX) Ca2+-ATPase reside establish concentrations termination export vacuolar lumen mutants, consequently phenotype lines, slower onset signal, higher concentration retarded reduction Hilleary (2020) (C). Plasma membrane-localized Extensive require PM-localized, Gd3+ La3+ abolishes 2002; Kwaaitaal Maintz studies clearly implicate signaling, hidden. started decipher defense-related roles several classes begun Below, immunity-related candidates phylogenetic groups rather than following chronological identification strict PTI/ETI dichotomy. CNGCs—from strong One tetrameric cyclic nucleotide-gated (CNGCs) (Köhler Neuhaus, 1998). CNGCs comprise gene 20 Arabidopsis) (Mäser 2001) named topology organization, mammalian (CNG) hyperpolarization-activated nucleotide-modulated (HCN) (Kaupp Seifert, Matulef Zagotta, 2003). Individual six helices termini, (CNBD) located CNGC (Kaplan previous reports indicated CNBDs bind nucleotides (Baxter 2008), cAMP cGMP (Leng Gao 2014, Meena it unclear whether bona fide agonists planta. Furthermore, existence guanylate adenylate cyclases (GCs ACs) proteomes still under debate will here. Indeed, suggest multiple RKs, GC (Qi Turek Irving, 2021), determined vitro activities GCs position argues physiological relevance (Ashton, Bojar Nevertheless, over past decades Ca2+-permeable, non-selective cation (Jarratt-Barnham calmodulin (CaM), CaM-binding (CaMBDs) found examined (Arazi 1999; Köhler Hua 2003; Fischer 2013, 2016a) isoforms 2016a). Ca2+/CaM 2016b) Ca2+-independent IQ CaMBD C-terminal end essential 2016a; Pan additional Ca2+-dependent CaMBDs providing negative (feedback) divided four subfamilies phylogeny, group IV IVa IVb 2001). members, CNGC2 CNGC4, isolated defense, (dnd) lesion mimic (hlm) dnd1 dnd2/hlm1 (null (Clough Balagué Jurkowski 2004). dnd initially defective induction HR, able carry (Yu These phenotypic defects, dwarf morphology, delayed flowering, salicylic acid (SA), death, dis-regulated auxin Chan 2004; Chin Chakraborty keeping immune-related dnd1/cngc2 mediator molecule nitric oxide (NO) compared WT lipopolysaccharide (LPS) (Ali same study used pharmacological inhibitors CaM, NO synthase (NOS)-type process. Given mammalian-type NOS enzymes land (Santolini 2017) myriad functions CaM results however cautiously. reporter lines full (Ma 2012). convergence (Couto Bjornson specificity achieved. virus-induced silencing (VIGS) tomato flg22, positively (Saand Recently, loss-of-function each forward genetic exhibited syringae. Remarkably, dependent high media, indistinguishable plants. bik1, do conditional Detailed characterization heterologously expressed Xenopus laevis oocytes subunits inactive, CNGC2-CNGC4 heteromers produce currents wherein together (Chin inhibited CaM; experiments CNGC4 partially 2019) 4A). highlights subject, phosphorylation, and, potentially, 4. fulfil homo- heterotertramers homotetramers heterotetramers cytosol. Ca2+-bound Calmodulin (CAM) inhibits loop. initiation phosphorylates CAM-mediated inhibition rice, RLCK185 OsCNGC9. If OsCNGC9 containing tetramer homomeric heteromeric known resolved pathways. CNGC19 CNGC20 PM, phosphorylated BAK1, initiates degradation channels. bak1/bkk1 coRK accumulation CNGC19/CNGC20 influx, ultimately causing death. media (Chan 2013),

Language: Английский

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Viruses inhibit TIR gcADPR signalling to overcome bacterial defence

Nature, Journal Year: 2022, Volume and Issue: 611(7935), P. 326 - 331

Published: Sept. 29, 2022

Language: Английский

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Shared TIR enzymatic functions regulate cell death and immunity across the tree of life

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

In the 20th century, researchers studying animal and plant signaling pathways discovered a protein domain that is shared across diverse innate immune systems: Toll/interleukin-1/resistance gene (TIR) domain. The TIR found in several architectures was defined as an adaptor mediates protein-protein interactions immunity developmental pathways. However, studies of nerve degeneration animals-and subsequent breakthroughs plant, bacterial, archaeal systems-revealed domains possess enzymatic activities. We provide synthesis functions role various related products evolutionarily systems. These may ultimately guide interventions would span tree life, from treating human neurodegenerative disorders bacterial infections to preventing diseases.

Language: Английский

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Cyclic ADP ribose isomers: Production, chemical structures, and immune signaling

Science, Journal Year: 2022, Volume and Issue: 377(6614)

Published: Sept. 1, 2022

Cyclic adenosine diphosphate (ADP)–ribose (cADPR) isomers are signaling molecules produced by bacterial and plant Toll/interleukin-1 receptor (TIR) domains via nicotinamide adenine dinucleotide (oxidized form) (NAD + ) hydrolysis. We show that v-cADPR (2′cADPR) v2-cADPR (3′cADPR) cyclized O-glycosidic bond formation between the ribose moieties in ADPR. Structures of 2′cADPR-producing TIR reveal conformational changes lead to an active assembly resembles those Toll-like adaptor domains. Mutagenesis reveals a conserved tryptophan is essential for cyclization. 3′cADPR activator ThsA effector proteins from antiphage defense system termed Thoeris suppressor immunity when HopAM1. Collectively, our results molecular basis cADPR isomer production establish bacteria as antiviral immunity–suppressing molecule.

Language: Английский

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The molecular basis of heat stress responses in plants

Molecular Plant, Journal Year: 2023, Volume and Issue: 16(10), P. 1612 - 1634

Published: Sept. 22, 2023

Language: Английский

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Oligomerization of a plant helper NLR requires cell-surface and intracellular immune receptor activation

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(11)

Published: March 6, 2023

Plant disease resistance involves both detection of microbial molecular patterns by cell-surface pattern recognition receptors and pathogen effectors intracellular NLR immune receptors. NLRs are classified as sensor NLRs, involved in effector detection, or helper required for signaling. TIR-domain-containing (TNLs) require NRG1 ADR1 resistance, activation defense requires the lipase-domain proteins EDS1, SAG101, PAD4. Previously, we found that associates with EDS1 SAG101 a TNL activation-dependent manner [X. Sun et al. , Nat. Commun. 12 3335 (2021)]. We report here how itself during TNL-initiated immunity. Full immunity coactivation mutual potentiation receptor-initiated signaling [B. P. M. Ngou, H.-K. Ahn, Ding, J. D. G. Jones, Nature 592 110–115 (2021), Yuan 105–109 find while TNLs is sufficient to promote NRG1–EDS1–SAG101 interaction, formation an oligomeric resistosome additional defense. These data suggest vivo part mechanism links receptor pathways.

Language: Английский

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Stress-related biomolecular condensates in plants

The Plant Cell, Journal Year: 2023, Volume and Issue: 35(9), P. 3187 - 3204

Published: May 10, 2023

Biomolecular condensates are membraneless organelle-like structures that can concentrate molecules and often form through liquid-liquid phase separation. condensate assembly is tightly regulated by developmental environmental cues. Although research on biomolecular has intensified in the past 10 years, our current understanding of molecular mechanisms components underlying their formation remains its infancy, especially plants. However, recent studies have shown may be central to plant acclimation stress conditions. Here, we describe mechanism, regulation, properties stress-related plants, focusing granules processing bodies, 2 most well-characterized condensates. In this regard, showcase proteomes bodies an attempt suggest methods for elucidating composition function Finally, discuss how modulate responses they might used as targets biotechnological efforts improve tolerance.

Language: Английский

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