The plant immune system: From discovery to deployment

Cell, Journal Year: 2024, Volume and Issue: 187(9), P. 2095 - 2116

Published: April 1, 2024

Plant diseases cause famines, drive human migration, and present challenges to agricultural sustainability as pathogen ranges shift under climate change. breeders discovered Mendelian genetic loci conferring disease resistance specific isolates over 100 years ago. Subsequent breeding for underpins modern agriculture and, along with the emergence focus on model plants genetics genomics research, has provided rich resources molecular biological exploration last 50 years. These studies led identification of extracellular intracellular receptors that convert recognition microbe-encoded patterns or pathogen-delivered virulence effectors into defense activation. receptor systems, downstream responses, define plant immune systems have evolved since migration land ∼500 million Our current understanding provides platform development rational enhancement control many continue plague crop production.

Language: Английский

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Susceptibility reversed: modified plant susceptibility genes for resistance to bacteria

Trends in Plant Science, Journal Year: 2021, Volume and Issue: 27(1), P. 69 - 79

Published: Aug. 13, 2021

Plant pathogenic bacteria use host susceptibility (S) genes to promote disease development.Many bacterial species effector proteins target S genes, resulting in effector-triggered susceptibility.S are evolutionarily retained across plant species.S can be identified and precisely mutated through new genome engineering tools.Impairment of lead recessively inherited broad-spectrum resistance bacteria. Plants have evolved complex defence mechanisms avoid invasion potential pathogens. Despite this, adapted pathogens deploy manipulate rendering defences ineffective. The identification mutation exploited by important for the generation crops with durable resistance. Application mutant breeding resistant is limited because pleiotropy. New editing techniques open up possibilities modification genes. In this review, we focus on manipulated propose ways their precise modification. Finally, that coding transporter represent a group constantly exposed multitude pathogens, such as viruses, fungi, For microbes become pathogenic, high degree adaptation required overcome layers plants [1.Park J.M. Paek K.H. Recognition response plant-pathogen interactions.J. Biol. 2007; 50: 132-138Crossref Scopus (11) Google Scholar,2.Dodds P.N. Rathjen J.P. immunity: towards an integrated view plant–pathogen interactions.Nat. Rev. Genet. 2010; 11: 539-548Crossref PubMed (1883) Scholar]. possess ability fight off majority invading microbes, making exception interactions plants, two-layered system activated upon interaction microbial molecules extracellular intracellular immune receptors. first layer, pattern recognition receptors (see Glossary) cell surface perceive conserved elicitors called 'pathogen-associated molecular patterns' (PAMPs), leading PAMP-triggered immunity (PTI). Adapted PTI deploying proteins, (ETS). second layer defence, counteract ETS evolution (R) Inside cell, pathogen effectors directly or indirectly recognised products corresponding dominant R (ETI) [3.Jones J.D.G. Dangl J.L. system.Nature. 2006; 444: 323-329Crossref (7649) Scholar,4.Thomma B.P.H.J. et al.Of PAMPs effectors: blurred PTI-ETI dichotomy.Plant Cell. 2011; 23: 4-15Crossref (610) Effectors, however, rapidly evolve ETI avoiding once again To secure compatible interaction, factors encoded processes advantage. Suppression defences, nutrient acquisition, transport some cause (Figure 1) Scholar, 4.Thomma 5.Hui S. al.TALE-carrying trap nuclear import facilitation infection rice.Mol. Pathol. 2019; 20: 519-532Crossref (16) Although disease, durable, inherited, potentially [6.Pavan al.Loss novel strategy resistance.Mol. Breed. 25: 1-12Crossref (202) More than 200 infect diseases [7.Buttimer C. al.Bacteriophages diseases.Front. Microbiol. 2017; 8: 34Crossref (171) So far, management has been based mainly chemicals [8.Sundin G.W. al.Bacterial management: challenges, experience, innovation future prospects.Mol. 2016; 17: 1506-1518Crossref (78) decades, successfully relied introgression major recognise confer crops. Bacterial under strong negative selection when fast breakdown [9.Pitman A.R. al.Exposure drives virulence plants.Curr. 2005; 15: 2230-2235Abstract Full Text PDF (95) Scholar,10.Bent A.F. Mackey D. Elicitors, effectors, genes: paradigm lifetime supply questions.Annu. Phytopathol. 45: 399-436Crossref (561) addition, bactericide horizontal gene transfer between Scholar,11.Sundin Wang N. Antibiotic plant-pathogenic bacteria.Annu. 2018; 56: 161-180Crossref (102) Therefore, strategies, control needed. Here, review different pathosystems, but specifically recently shown involved (Table 1). We which modified gain suggest category genes.Table 1Identified bacteria, function, interacting speciesSusceptibility geneEffectorPathogenPlant speciesS categoryRefsBIK1XopRXanthomonas oryzae pv. (Xoo)ArabidopsisSuppression defences/entry host[38.Wang al.A Xanthomonas effector, XopR, associates receptor-like cytoplasmic kinases suppresses stomatal closure.Sci. China Life Sci. 59: 897-905Crossref (22) Scholar]TaNCED_5BS, TaNCED_5DStal8Xanthomonas translucens undulosa XtuWheatSuppression defences[44.Peng Z. al.Xanthomonas commandeers rate-limiting step ABA biosynthesis susceptibility.Proc. Natl. Acad. U. A. 116: 20938-20946Crossref (27) Scholar]SAM-MT1,SAM-MT2AvrXccBXanthomonas campestris (Xcc)ArabidopsisSuppression defences[41.Liu L. al.The type III AvrXccB targets putative methyltransferases innate Arabidopsis.Mol. 18: 768-782Crossref (17) Scholar]HIPMHrpNErwinia amylovoraAppleSuppression defences[40.Campa M. al.HIPMIs Malus spp.: reduced expression reduces Erwinia amylovora.Mol. Microbe Interact. 32: 167-175Crossref (13) Scholar,62.Oh C.S. Beer S.V. AtHIPM, ortholog apple HrpN-interacting protein, regulator growth mediates growth-enhancing effect HrpN Arabidopsis.Plant Physiol. 145: 426-436Crossref (44) Scholar]SWEET11PthXo1Xanthomonas (Xoo)RiceNutrient acquisition[18.Streubel J. al.Five phylogenetically close rice SWEET TAL effector-mediated oryzae.New Phytol. 2013; 200: 808-819Crossref (219) Scholar,48.Oliva R. al.Broad-spectrum blight using editing.Nat. Biotechnol. 37: 1344-1350Crossref (211) Scholar]SWEET13PthXo2Xanthomonas Scholar]SWEET14AvrXa7PthXo3TalCTalFXanthomonas Scholar]GhSWEET10Avrb6Xanthomonas citri malvacearum (Xcm)CottonNutrient acquisition/symptom development[17.Cox K.L. al.TAL driven induction confers cotton.Nat. Commun. 815588Crossref (92) Scholar]MeSWEET10aTAL20xam668Xanthomonas axonopodis manihotis (Xam)CassavaNutrient acquisition[49.Cohn promoted transcription activator-like effector–mediated sugar cassava.Mol. Plant-Microbe 2014; 27: 1186-1198Crossref (128) Scholar]CsLOB1,CsLOB2,CsLOB3Any Xcc Xfa,PtXa4Xanthomonas (Xcc),Xanthomonas fuscans aurantifolii (Xfa)Sweet orange,GrapefruitSymptom development[53.Jia H. al.Genome CsLOB1 citrus canker.Plant 817-823Crossref (215) 54.Peng al.Engineering canker-resistant CRISPR/Cas9-targeted geneCsLOB1promoter citrus.Plant 1509-1519Crossref (265) 55.Zhang al.Homologues function canker.Mol. 798-810Crossref (25) Scholar]OsPIP;3Hpa1Xanthomonas (Xoo)RiceTranslocation effectors[57.Zhang al.Silencing aquaporin diminishes rice.Australas. 48: 143-158Crossref (9) Scholar,59.Li P. al.Rice PIP1;3 harpin Hpa1 cooperate translocation.J. Exp. Bot. 70: 3057-3073Crossref (28) Scholar,60.Wang X. al.Hpa1 translocator oryzae.BMC 105Crossref Scholar]OsImpα1a,OsImpα1bTALEs Xoo XocXanthomonas (Xoo), oryzicola (Xoc)RiceTranslocation effectors[5.Hui Scholar]Osaba1UnknownXanthomonas (Xoc)Rice(Entry host)Suppression defences[36.Zhang al.Postinvasive conferred stomata 255-266Crossref Scholar]LPT3, LPT4UnknownPseudomonas syringaeArabidopsisSuppression defences[45.Gao al.LTP3 contributes Arabidopsis enhancing abscisic acid (ABA) biosynthesis.Mol. 412-426Crossref Scholar]WAT1UnknownRalstonia solanacearumArabidopsisSuppression defences[25.Denance al.Arabidopsis wat1 (walls thin1)-mediated vascular pathogen, Ralstonia solanacearum, accompanied cross-regulation salicylic tryptophan metabolism.Plant 73: 225-239Crossref (88) Scholar,26.Tang Y. al.Cotton WATs modulate SA local lignin deposition participating against Verticillium dahliae.Front. 10: 526Crossref (26) Scholar]Upa20AvrBs3Xanthomonas vesicatoriaPepperNutrient development[51.Kay acts factor induces size regulator.Science. 318: 648-651Crossref (408) Scholar]CaMLO6UnknownRalstonia solanacearumPepperSuppression defences[46.Yang al.Pepper CaMLO6 negatively regulates solanacearum positively temperature humidity responses.Plant Cell 2020; 61: 1223-1238Crossref Scholar]AtGAD1, AtGAD2, AtGAD4, NdGAD4, SlGAD2RipIRalstonia solanacearumArabidopsis, tobacco, tomatoNutrient acquisition[50.Xian protein hijacks metabolism support nutrition.Cell Host Microbe. 28 (e7): 548-557Abstract Scholar] Open table tab Any facilitates considered [12.Van Schie C.C.N. Takken F.L.W. Susceptibility 101: how good host.Annu. 52: 551-581Crossref (239) Scholar,13.Gawehns F. effector-target immunity.Microb. 6: 223-229Crossref (39) belong diverse families widely functions A categorisation suggests they largely fall into three categories includes entry. well-known example powdery mildew Mildew Locus O (MLO). Inactivation MLO prevents fungal penetration cells [14.Appiano al.Identification candidate cultivated Solanaceae functional characterization tobacco NtMLO1.Transgenic Res. 2015; 24: 847-858Crossref (43) Genes act regulators category. An Downey Resistance6 (DMR6), 2(OG)-Fe(II) oxygenase catalysis defence-associated hormone (SA). Loss DMR6 leads via levels [15.van Damme encodes 2OG-Fe(II) defense-associated downy mildew.Plant 2008; 54: 785-793Crossref (126) Scholar,16.Zhang al.S5H/DMR6 5-hydroxylase fine-tunes homeostasis.Plant 175: 1082-1093Crossref (80) third allow sustained compatibility host, assist nutrition metabolic pathogen. instance, Sugars Will Eventually Be Exported Transporter (SWEET) targets, apoplast, where reside. During infection, upregulated (TALEs) provide nutrients [17.Cox Scholar,18.Streubel As researched further, it becoming clear more susceptibility. discussed 'To translocate effectors' subsection was targeted translocation effectors. Thus, It might seem counterintuitive retained. Many physiological plants. OsSWEET11 pollen development grain filling (Oryza sativa). upregulation also supports bacterium (Xoo) planta [19.Chu Promoter mutations essential result rice.Genes Dev. 1250-1255Crossref (362) Scholar,20.Ma al.Essential role during early stage filling.Plant 58: 863-873Crossref (90) Due dual susceptibility, inactivation along pleiotropic effects. Yet, extent fitness costs dependent growing conditions. mlo barley (Hordeum vulgare L.) mutants exhibit autonecrosis leaf senescence. tomato (Solanum lycopersicum), naturally occurring ol-2 mutant, MLO, without any observed [21.Bai al.Naturally Central American accession caused loss Mlo function.Mol. 21: 30-39Crossref (213) Downregulation Defence No Death1 (DND1) results severe stunting tomato. potato tuberosum), silencing causes only mild conditions [22.Sun K. al.Down-regulation DND1 orthologs late mildew.Transgenic 123-138Crossref (24) Orthologs often present species, most probably due involvement biological seed arabidopsis (Arabidopsis thaliana), rice, soybean (Glycine max) [20.Ma Scholar,23.Wang GmSWEET15 sucrose export from endosperm embryo.Plant 180: 2133-2141Crossref (45) Scholar,24.Chen L.Q. cascade sequentially expressed transporters coat provides 607-619Crossref (199) auxin Walls Are Thin1 (WAT1), secondary wall biosynthesis, cotton (Gossypium hirsutum) [25.Denance Since its discovery barley, arabidopsis, tomato, pea (Pisum sativum), cucumber (Cucumis sativus L.), eggplant melongena), (Nicotiana benthamiana), grapevine (Vitis vinifera), (Malus domestica) Scholar,21.Bai Scholar,27.Acevedo-Garcia mildew-resistant mlo2 mlo6 mlo12 triple displays altered phenotypes types phytopathogens.Sci. Rep. 7: 9319Crossref 28.Pavan al.Pea er1 associated loss-of-function at homologous locus.Theor. Appl. 123: 1425-1431Crossref (104) 29.Berg J.A. al.Functional clade V genes.BMC 80Crossref (20) 30.Pessina al.Characterization family Rosaceae analysis domestica.BMC Genomics. 618Crossref (64) 31.Pessina al.Knockdown grapevine.Hortic. 3: 16016Crossref DMR1, DMR6, Powdery Resistance4 (PMR4), PMR6, Cellulose Synthase catalytic subunit 3 (CESA3), DND1, functionally characterised [32.Huibers R.P. al.Powdery impairment SlPMR4 SlDMR1.PLoS One. 8e67467Crossref (53) 33.Sun six resistance.Transgenic 731-742Crossref (51) 34.Santillán Martínez M.I. al.CRISPR/Cas9-targeted mutagenesis PMR4 mildew.BMC 284Crossref (36) conservation feature applicability breeding. postgenomics era, model makes characterisation relatively easy rather straightforward task 2). Entry critical infections. Natural openings hydathodes entry portals [35.Panchal Melotto Stomate-based defense environmental cues.Plant Signal. Behav. 12e1362517Crossref (18) Stomata closure challenge basal mechanism limits Scholar,36.Zhang RPM1-interacting protein4 (RIN4) together H+-ATPases AHA1 AHA2 reopening Pseudomonas syringae DC3000 [37.Liu al.RIN4 plasma membrane regulate apertures attack.PLoS 2009; 7e1000139Crossref (195) Similarly, XopR Botrytis-induced Kinase1 (BIK1) suppress PAMP-induced [38.Wang insights stomata-regulated transpiration restricting spread. spread appear favoured water soaking leaves. Osaba1 exhibits Xoo. remain after higher [36.Zhang activate responses, reactive oxygen (ROS), modifications, production antimicrobial compounds contribution these responses lifestyle example, ROS hypersensitive limit (hemi)biotrophs. Inversely, necrotrophs stimulate induce susceptibility-associated death [39.Mengiste T. necrotrophs.Annu. 2012; 267-294Crossref (333) apple, necrogenic amylovora HIPM (HrpN-interacting spp.) establish [40.Campa contrast, (Xcc) methyltransferase SAM-MT1/SAM-MT2 callose [41.Liu further tightly regulated networks hormones [42.Ma K.W. Ma W. Phytohormone pathways facilitate infection.Plant Mol. 91: 713-725Crossref (81) relationships hormonal antagonistic synergistic [43.Bürger Chory Stressed out about hormones: orchestrate immunity.Cell 26: 163-172Abstract changes balance prime TaNCED_5BS TaNCED_5DS, ABA, (Xtu) wheat. ABA-induced Lipid Transfer Protein (LPT) LPT3 LPT4 infection. both cases, antagonism [44.Peng Scholar,45.Gao

Language: Английский

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Natural variation in the pattern‐triggered immunity response in plants: Investigations, implications and applications

Molecular Plant Pathology, Journal Year: 2024, Volume and Issue: 25(3)

Published: March 1, 2024

Abstract The pattern‐triggered immunity (PTI) response is triggered at the plant cell surface by recognition of microbe‐derived molecules known as microbe‐ or pathogen‐associated molecular patterns derived from compromised host cells called damage‐associated patterns. Membrane‐localized receptor proteins, pattern receptors, are responsible for this recognition. Although much machinery PTI conserved, natural variation exists within and across species with respect to components recognition, activation response, strength induced. This review describes what about variation. We discuss how in can be measured knowledge might utilized control disease developing varieties enhanced resistance.

Language: Английский

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Status, Gaps and Perspectives of Powdery Mildew Resistance Research and Breeding in Cucurbits

Critical Reviews in Plant Sciences, Journal Year: 2024, Volume and Issue: 43(4), P. 211 - 290

Published: March 6, 2024

Cucurbitaceae, the gourd family of flowering plants, is a very large and diverse family, order Cucurbitales, contains 95 genera 950–980 species food ornamental wild weedy mostly with high genetic diversity. This review focused on most important cucurbit crops (Cucumis sativus, Cucumis melo, Cucurbita spp., Citrullus lanatus, Momordica charantia, Lagenaria siceraria, Luffa acutangula) some their relatives as hosts powdery mildews (CPM). Powdery (PM) (Ascomycota, Erysiphales) are one frequently encountered easily visible groups plant pathogenic fungi > 900 species. They obligate biotrophs, they colonize above-ground tissues, leaves, though may also stems, petioles, flowers fruits, usually debilitators, not killers. These parasitic have been problematic cucurbits for long time world-wide, causing serious economic losses in yield quality. All economically host CPM. Seven PM different taxonomic positions, ranges, geographic distributions ecological requirements known cucurbits. CPM taxonomy denomination rapidly changed during last few decades through detailed analyses clarifications. At least three parasitize cucurbits: endoparasite Leveillula taurica (Lt) marginal importance; two ectoparasitic species, Golovinomyces orontii (Go), Podosphaera xanthii (Px), which world-wide. The pathogens differ distribution, occur together mixed infections. highly variable at population level virulence, race identities, fast adaptation pathogens. Cucurbit-CPM interactions complicated, between respective pathogen Here we present critical overview obstacles, gaps recent progress these matters six respect to resistance resources, genetics resistance, mapping development molecular markers, physiology mechanisms developments mlo-mediated patents, breeding.

Language: Английский

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The barley immune receptor Mla recognizes multiple pathogens and contributes to host range dynamics

Nature Communications, Journal Year: 2021, Volume and Issue: 12(1)

Published: Nov. 25, 2021

Abstract Crop losses caused by plant pathogens are a primary threat to stable food production. Stripe rust ( Puccinia striiformis ) is fungal pathogen of cereal crops that causes significant, persistent yield loss. exhibits host species specificity, with lineages have adapted infect wheat and barley. While stripe barley commonly restricted their corresponding hosts, the genes underlying this specificity remain unknown. Here, we show three resistance genes, Rps6 , Rps7 Rps8 contribute immunity in rust. cosegregates powdery mildew at Mla locus. Using transgenic complementation different alleles, confirm allele-specific recognition . Our results major on shared genetic architecture underlies non-adapted

Language: Английский

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Parasitic Plants: An Overview of Mechanisms by Which Plants Perceive and Respond to Parasites

Annual Review of Plant Biology, Journal Year: 2022, Volume and Issue: 73(1), P. 433 - 455

Published: April 1, 2022

In contrast to most autotrophic plants, which produce carbohydrates from carbon dioxide using photosynthesis, parasitic plants obtain water and nutrients by parasitizing host plants. Many important crop are infested these heterotrophic leading severe agricultural loss reduced food security. Understanding how perceive resist provides insight into underlying defense mechanisms the potential for applications. this review, we offer a comprehensive overview of current understanding perception pre-attachment post-attachment responses mounted host. Since research overlooks role organ specificity in resistance responses, also summarize cases cross-organ parasitism, indicates nonconventional haustorial connections on other organs, example, when stem form haustoria their roots. different tissue types respond could provide developing universal mechanism crops against both root

Language: Английский

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Exploiting breakdown in nonhost effector–target interactions to boost host disease resistance

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(35)

Published: Aug. 22, 2022

Plants are resistant to most microbial species due nonhost resistance (NHR), providing broad-spectrum and durable immunity. However, the molecular components contributing NHR poorly characterised. We address question of whether failure pathogen effectors manipulate plants plays a critical role in NHR. RxLR (Arg-any amino acid-Leu-Arg) from two oomycete pathogens,

Language: Английский

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How Do Pathogens Evolve Novel Virulence Activities?

Molecular Plant-Microbe Interactions, Journal Year: 2021, Volume and Issue: 34(6), P. 576 - 586

Published: Feb. 1, 2021

This article is part of the Top 10 Unanswered Questions in MPMI invited review series. We consider state knowledge on pathogen evolution novel virulence activities, broadly defined as anything that increases fitness with consequence causing disease either qualitative or quantitative senses, including adaptation pathogens to host immunity and physiology, species, genotypes, tissues, environment. The activities an adaptive trait based selection exerted by hosts variants have been generated de novo arrived from elsewhere. In addition, biotic abiotic environment a experiences beyond may influence activities. host-pathogen evolution, range expansion, external factors can mediate evolution. then discuss mechanisms which generate recombine genetic variation leads DNA point mutation, transposable element activity, gene duplication neofunctionalization, exchange. summary, if there (epi)genetic mechanism create genome, it will be used evolve factors. Our has biased response major resistance, leaving other underexplored. Understanding key driving forces give rise integration evolutionary concepts methods mechanistic research plant-microbe interactions help inform crop protection. [Formula: see text] Copyright © 2021 Author(s). open access distributed under CC BY-NC-ND 4.0 International license .

Language: Английский

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Effector loss drives adaptation of Pseudomonas syringae pv. actinidiae biovar 3 to Actinidia arguta

PLoS Pathogens, Journal Year: 2022, Volume and Issue: 18(5), P. e1010542 - e1010542

Published: May 27, 2022

A pandemic isolate of Pseudomonas syringae pv. actinidiae biovar 3 (Psa3) has devastated kiwifruit orchards growing cultivars Actinidia chinensis . In contrast, arguta (kiwiberry) is not a host Psa3. Resistance mediated via effector-triggered immunity, as demonstrated by induction the hypersensitive response in infected leaves, observed microscopy and quantified ion-leakage assays. Isolates Psa3 that cause disease have been isolated analyzed, revealing 51 kb deletion exchangeable effector locus (EEL). This natural EEL-mutant strains with synthetic knockouts EEL were more virulent plantlets than wild-type Screening complete library knockout identified increased growth planta for four effectors–AvrRpm1a, HopF1c, HopZ5a, HopAW1a –suggesting resistance Hypersensitive (HR) assays indicate three these effectors trigger species-specific HR. strain all knocked out escaped recognition, but cumulative increase bacterial pathogenicity virulence was observed. These avirulence can be used turn to identify first cognate genes breeding durable into future cultivars.

Language: Английский

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Contrasting patterns of microbial dominance in the Arabidopsis thaliana phyllosphere

Proceedings of the National Academy of Sciences, Journal Year: 2022, Volume and Issue: 119(52)

Published: Dec. 20, 2022

Sphingomonas is one of the most abundant bacterial genera in phyllosphere wild Arabidopsis thaliana , but relative to Pseudomonas ecology and its interaction with plants poorly described. We analyzed genomic features over 400 isolates collected from local A. populations, which revealed much higher intergenomic diversity than for considerably more uniform found same host populations. Variation plasmid complements additional suggest high adaptability this genus, widespread presence protein secretion systems hints at frequent biotic interactions. While some showed plant-protective phenotypes lab tests, was a rare trait. To begin understand extent strain sharing across alternate hosts, we employed amplicon sequencing bulk-culturing metagenomics approach on both neighboring plants. Our data reveal that thrive other diverse plant poor competitor dying or dead leaves.

Language: Английский

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