PAMPs, MAMPs, DAMPs and others: an update on the … · understanding of the physiological and biological basis of these induced immunity mechanisms have greatly ... a huge potential

BASE Biotechnol. Agron. Soc. Environ.201216(2),257-268 Focus on:

PAMPs,MAMPs,DAMPsandothers:anupdateonthediversityofplantimmunityelicitorsGuillaumeHenry,PhilippeThonart,MarcOngenaUniv.Liege-GemblouxAgro-BioTech.WalloonCenterforIndustrialBiology.PassagedesDéportés,2.B-5030Gembloux(Belgium).E-mail:[email protected]

ReceivedonJuly25,2001;acceptedonNovember8,2011.

Plantspossessabroadarrayofdefensesthatcouldbeactivelyexpressedinresponseofpathogenicorganismsorparasitesbutalsofollowingbeneficialsaprophyticmicroorganismsrecognition.Specifically,therearecompoundsderivedfromtheseorganismsandcalledelicitorsthatareperceivedbytheplanttoinducealocallyorsystemicallyexpressedresistance.Theunderstandingofthephysiologicalandbiologicalbasisoftheseinducedimmunitymechanismshavegreatlyadvancedoverthepastyearsbutadeeperinvestigationofthemechanismsunderlyingtheperceptionofelicitorsisessentialtodevelopnovelstrategiesforpestcontrol.Theapplicationofchemicalandbiologicalstimulatorsofplantimmunedefensesinconventionalagricultureisexpectedtoincreasewithinthenextyears.Becauseoftheirorganicoriginandastheyprovidemeansforconferringplantprotectioninanon-transgenicmanner,elicitorsofplantimmunityhaveahugepotentialasbiocontrolproducts.Throughthisreview,wewanttoillustratethediversityofcompoundsidentifiedasstimulatorsoftheplantimmunesystemanddescribethemechanismsbywhichtheycouldberecognizedattheplasmamembranelevel.Keywords.Immunity,pestresistance,defensemechanisms,elicitors.

PAMPs, MAMPs, DAMPs et autres : mise à jour de la diversité des éliciteurs de l’immunité des plantes.Lesplantespossèdentunelargegammededéfensesquipeuventêtreexpriméesenréponseàlaperceptiondesorganismespathogènesouparasites,maisaussisuiteàlareconnaissancedecertainsmicro-organismessaprophytesbénéfiques.Plusprécisément,cesontdescomposésdérivésdecesorganismesetdénomméséliciteursquisontreconnusparlaplantepourstimulerunerésistanceexpriméedemanièrelocaleousystémique.Lacompréhensiondesbasesphysiologiquesetbiologiquesdesmécanismesdecesimmunitésabeaucoupprogressécesdernièresannées,maisuneconnaissanceplusapprofondiedesmécanismessous-jacentsà laperceptiondeceséliciteursestcependantessentiellepourdévelopperdenouveauxmoyensdecontrôledesnuisibles.L’applicationdeproduitsbiologiquesstimulateursdesdéfensesimmunitairesdesplantesdansl’agricultureconventionnelleestamenéeàcroîtredanslesprochainesannéesentantquestratégiephytosanitaire.Enraisondeleuroriginenaturelleetétantdonnéqu’ilsconfèrentuneprotectionsansmodificationgénétiquedesplantes,leséliciteursdel’immunitédesplantesrevêtentunénormepotentielentantqueproduitsdeluttebiologique.Autraversdecetterevue,nousvoulonsillustrerladiversitédescomposésidentifiésaujourd’huicommepouvantstimulerlesdéfensesimmunitairesdesplantesetlesmécanismesparlesquelsilspeuventêtreperçusauniveaudelamembraneplasmique.Mots-clés.Immunité,résistanceauxorganismesnuisibles,mécanismesdedéfense,éliciteurs.

I. BASIC CONCEPTS OF PLANT IMMUNITY

Astheyareconstantlyexposedtopathogensbutlackmobiledefendercellsandanadaptiveimmunesystem,plant defenses rely on the innate immunity of eachcellandonsystemicsignalsemanatingfrominfectionsites (Dangl et al., 2001;Ausubel, 2005).Theyhaveevolved a vast array of passive and active defensemechanismsthataremanifestedinthepest-colonizedorgan.Defensesignalscouldbesystemicallyemittedto activate a plethora of defense responses in thenon-colonizedorgansofaplant locally infectedbya

microbe, infestedbyanherbivoreorevenstimulatedbyachemicalcompound.Defensesignalscouldalsobeprimedforrapidactivationafteralocalizedperceptionofnon-pathogenicfungiorbacterialstrains.

The presence of infectious agents is detectedthrough the recognition of microbial signals. Allsignals that are perceived by plant cells and inducedefenseresponsesareconsideredaselicitors.Elicitorsmay be categorized in two classes: general (or non-specific)elicitors,whichdonotsignificantlydifferintheireffectondifferentcultivarswithinaplantspeciesandmay therefore be involved in general resistance,

258 Biotechnol. Agron. Soc. Environ. 201216(2),257-268 HenryG.,ThonartPh.&OngenaM.

andspecificelicitors,whichareformedbyspecializedpathogen races or strains and function only in plantcultivarscarryingthecorrespondingdiseaseresistancegene(Montesanoetal.,2003).

General elicitors are designated Pathogen-AssociatedMolecularPatterns(PAMPs)whenisolatedfrom infectious agentsbut theymayalso correspondto endogen plant-host derived signals resulting fromthe action of the pathogen agent called DAMPs(Damage-Associated Molecular Patterns), to signalsfrom non-pathogenic microorganisms referred hereasMAMPs(Microbe-AssociatedMolecularPatterns)

or to chemicals. The perception of general elicitorstriggers a broad array of reactions, which culminatein the activation of the so-called basal resistanceor PAMP-Triggered Immunity (PTI) (Nicaiseet al., 2009) (Figure 1A). This defensive reactionmay be strong enough to halt infection before theinvader microbe becomes established. However,some successful pathogenic microorganisms mayovercome basal resistance by delivering virulenceeffectorproteinsorDNAintohostcells.Thesespecificelicitorsinhibitsignalizationpathwaysorthesynthesisof defense compounds by the host plant and thus

Figure 1.Elicitorsmaybecategorizedintwoclasses—Les éliciteurs peuvent être classés en deux catégories.A:General(ornon-specific)elicitorsdonotsignificantlydifferintheireffectondifferentcultivarswithinaplantspeciesandareinvolvedinprimaryinnateimmunity.Theyincludechemicals,Microbes-AssociatedMolecularPatterns(MAMPs)fromnon-pathogenicmicroorganisms,Damage-AssociatedMolecularPatterns(DAMPs)fromplantsurfacesresultingfromtheactionoftheinvadingagentandPathogen-AssociatedMolecularPatterns(PAMPs)frompathogenicmicroorganisms.Evenifperceptionofelicitorsisoftendescribedasbeingreceptor-mediated,onlyfewbindingsiteshavebeencharacterizedtodate—Les éliciteurs généraux (non spécifiques) agissent de manière différente selon les cultivars au sein d’une espèce de plante et sont impliqués dans l’immunité innée primaire. Ils comprennent les produits phytopharmaceutiques, les profils moléculaires associés aux microbes (MAMPs) issus de micro-organismes non pathogènes, les profils moléculaires associés aux dommages (DAMPs) issus des surfaces de plante suite à l’action de l’envahisseur et les profils moléculaires associés aux pathogènes (PAMPs) issus de micro-organismes pathogènes. Même si la perception des éliciteurs est généralement récepteur-dépendante, très peu de sites de liaison ont été caractérisés à ce jour;B:Specificelicitors(oreffectors)areformedbyspecializedpathogensandfunctiononlyinplantcultivarscarryingthecorrespondingdiseaseresistancegene.Effectorstypicallyleadtothesecondaryinnateimmunityafteranintracellularreceptor-mediatedperception—Les éliciteurs spécifiques (ou effecteurs) sont formés par des pathogènes spécialisés et agissent uniquement chez les cultivars de plantes possédant le gène de résistance de maladie correspondant. Les effecteurs conduisent typiquement à l’immunité innée secondaire après une perception récepteur-dépendante intracellulaire.

A. General elicitors B. Specific elicitors

Primary innate immunity (basal resistance) Secondary innate immunity

Receptor

Receptor

Effector triggered immunity (ETI)PAMP triggered immunity (PTI)

?

Cellular signaling Cellular signalingCellular signaling

Immune response Immune response Immune response

MAMPs DAMPs PAMPs

Plant

Chemicals Pathogens PathogensNon pathogens Insects, herbivores

Effectors (Avr proteins)

Elicitorsofplantimmunity 259

suppress this first type of immunity. Such signalsarethespecificelicitorsandarelikelythecauseforsusceptibility of many crops to virulent microbialpathogens.Inresponse,plantshaveevolvedasecondline of defense through specific disease resistance(R)genes,theso-calledeffector-triggered-immunity(Pelletieretal.,2002;Jonesetal.,2006)(Figure 1B).Therecognizedeffectoristermedanavirulence(Avr)protein.Because the effector-Rprotein relationshipis highly specific, this R gene-mediated resistanceappears to be similar to adaptative immunity inmammals.However, asR gene-mediated resistanceis expressed through similar defense responses asthose that are active in basal resistance, but on amuch greater scale, ETI is considered as anotherform of plant innate immunity.Therefore, PTI andETIareconsideredasprimaryandsecondaryinnateimmunityrespectively.

Ingeneral,basaldefenseisconsideredtobelessefficientthanETIinreducingplantdisease.However,studiesconductedonseveralplant-pathogensystemsinthelastdecadehaveshownthatbasaldefensesdoactuallyplayasignificantroleinpathogenrestrictionand disease resistance. Induction of primary innateimmunityisnowconsideredasakeycomponentofbiocontrol of pest in Integrated Pest Management.Thiswill be further illustrated belowwith selectedexamples.

2. SYSTEMIC PLANT IMMUNITY

When a resistance is established in the tissuesurrounding the site of initial infection, it is calledLocalized Acquired Resistance (LAR) (Kombrinket al.,2001)(Figure 2A).However,viaemissionof

Primary innate immunity (basal resistance)

A. Localized B. Systemic

MAMPPAMP/DAMP PAMP/DAMP/Chemical/Wounding

Localized Acquired Resistance(LAR)

Systemic Acquired Resistance(SAR)

Induced Systemic Resistance(ISR)

1. Perception

1. Perception

2. Signaling

2. Signaling3. Priming of defenses

4. Defenses induction

3. Defenses induction

Perception,signaling and defensesinduction

Figure 2. Theprimaryinnateimmunitycouldbelocalized(A)orsystemic(B)—L’immunité innée primaire peut être locale (A) ou systémique (B).

Systemicacquiredresistancecorrespondstoanenhancedstateofdefenseresponsesafterperceptionofpathogensorarangeofcompoundsandisinvariablyassociatedwithaccumulationofsalicylicacidandpathogenesis-relatedproteinsinresistanttissues.Besides,inducedsystemicresistanceistypicallystimulatedafterperceptionofbeneficialmicroorganismsbutalsoleadstotheestablishmentofanenhanceddefensepotential.Thisprimingstateallowsfasterdefenseresponsesinductionuponsubsequentpathogenattack—La résistance systémique acquise correspond à une augmentation des réponses de défense suite à la perception de pathogènes ou d’une large gamme de composés et est invariablement associée à une accumulation d’acide salicylique et de protéines PR (Pathogenesis-Related). Parallèlement, la résistance induite systémique est typiquement stimulée suite à la perception de micro-organismes bénéfiques, mais conduit également à l’augmentation du potentiel de défense. Cet état de sensibilisation permet l’induction plus rapide des réponses de défense en cas d’attaque ultérieure par un pathogène.


molecular signals, defense mechanisms can alsobe induced in distal organs of a plant that is locallyinfected by a pathogen. Such systemic resistancereactionrendersthehostlesssusceptibletosubsequentchallengebyapathogenoraparasiteindistaltissues.This long-lasting phenomenon was termed systemicacquiredresistance(Iritietal.,2010)(Figure 2B)andhasbeenextensivelyreviewedinthelastyears(Durrantetal.,2004).Recently,majoradvanceshavebeenmadeinidentifyingmetabolitesthatarecandidatesystemicsignals in plant defense against pathogens. Methylsalicylate, jasmonates, azelaic acid andaditerpenoidhavebeenproposedasmobilesignalsinvolvedintheactivationofSARwhichconfersenhancedresistanceagainst abroad spectrumofpathogens (Shah,2009).Conceptually, SAR has been associated with theperception of elicitors from avirulent pathogens butasimilarsystemicdefensemayalsobelightedonbyDAMPsorbyothercompoundsofbiologicalbutnotmicrobialoriginsandbychemicals.Another formofinducedresistancemayalsobetriggeredbymolecularpatterns isolated from beneficial non-pathogenicmicroorganisms(MAMPs),andisreferredasinducedsystemic resistance (Mishra et al., 2009). BestcharacterizedorganismsinducingISRaretheso-calledplantgrowthpromotingrhizobacteria(PGPR)amongwhich several species ofPseudomonas andBacillus(VanLoonetal.,1998;Lugtenbergetal.,2009).ISRis also phenotypically similar to SAR and both areeffectiveagainstabroadrangeofdiseasescausedbyviruses, bacteria and fungi (Vallad et al., 2004) andthereforepromisingtocontrolcroppests.Overthelast20years, researchonSARandISRhasconsiderablyimprovedourunderstandingofthemolecularbasisofsystemicresistance.Itappearedthat,fromamolecularpointofview,ISRdiffersfromSARanditmayexplainwhySARistypicallyeffectiveacrossawidearrayofplantspecies,whereasthereissomespecificityintheability of PGPR strains to elicit ISR in certain plantgenotypes (VanWees et al., 1997;Yan et al., 2002).Globally, local and systemic defense responsestriggered by microorganisms are controlled by asignalingnetworkinwhichtheplanthormonessalicylicacid (SA), jasmonic acid (JA), and ethylene (ET)play important rolesand thecorrespondingpathwayscrosscommunicate (Persello-Cartieaux et al., 2003).SAR triggered upon infection by necrosis-inducingpathogens is dependentonSA signaling (Park et al.,2008)whileISRtriggeredbybeneficialrhizobacteriatypically relies on the JA andET signaling pathway(Pieterse et al., 2002).However, both SAR and ISRphenomena converge downstream since they arecontrolledbythesametranscriptionalregulatorNPR1.

The two main types of systemic resistance SARand ISRcanbebothgloballyviewedas a three-stepprocessinvolvingsequentially:

– theperceptionbyplantcellsofelicitorsproducedby theinducingagentsthatinitiatesthephenomenon,– signal transduction that isneeded topropagate the inducedstatesystemicallythroughtheplant,– expressionofdefensemechanismssensu strictothat limitorinhibitfurtherpathogenpenetrationintothe hosttissues.

In this review, we focus on the early moleculardialogue and provide an overview of microbialelicitorsofSAR,ISRbutalsoLARthatareperceivedbyplantsat theplasmamembrane level.WewillnotconsiderthoseactingintracellularlyaseffectorsoftheETI. Some excellent review papers are available tothereaderforfurtherupdatedinformationabouttheseeffectors (Sheen et al., 2007; Katagiri et al., 2010;Zhouetal.,2010).

3. THE MULTIPLE PAMPs AND THEIR PERCEPTION BY PLANT CELLS

PAMPs represent structures that are essential formicrobial life and that are typically harbored byinvading pathogens. These include cell surfaceconstituents but may also be secreted enzymes orproteins normally located in the cytoplasm.A broadarrayofstructurallydiversePAMPshasbeendescribedoriginating from fungal, oomycete and bacterialpathogens.MostofthesePAMPsareoligosaccharides,glycopeptides, and peptides. Some of these patternssuch as Pep-13, xylanase and cold-shock protein areonly perceived by a narrow range of plant speciesbelongingtoonlyoneplantfamily(Felixetal.,2003;Ronetal.,2004).Arepresentativeexample isEF-Tuin the family Brassicaceae (Kunze et al., 2004). Bycontrast,otherPAMPssuchaschitin,LPSandflagellintrigger defense responses inmany host species evenif there is some degree of specificity and perceptionefficacyforaplantfamilyorspeciesasinthecaseofflagellin(Zipfeletal.,2006).

PAMPs are perceived at the plant cell surfaceby high-affinity receptors typically consisting in anextracellular ligand-bindingdomainwith leucine-richrepeats (LRR), a single transmembrane domain andan intracellular serine/threonine kinase-signalingdomain.Theyare referred toas receptor-likekinases(RLK). Receptor-like proteins (RLPs) are similarlystructured, but lack the cytoplasmic kinase domain.In Arabidopsis, 610RLKs and 56RLPs have beenidentified(Shiuet al.,2001;Fritz-Laylinetal.,2005).A large number of genes encoding RLKs and RLPsare transcriptionally induced upon PAMP treatment,illustrating the large diversity of such perceptionsystemsandsuggestingtheirpotentialroleindefense(Zipfeletal.,2004;Zipfeletal.,2006).


4. INDIRECT PERCEPTION OF PATHOGENS VIA DAMPs

In a more indirect way, plants can also detect thepresence of pathogens through the perception ofendogenouscompoundsthathavebeenreleasedfromstructural barriers or from other macromolecules bylyticenzymesproducedbytheinvaderorbythehostitself. SuchDAMPs typically appear in the apoplastand may thus, like PAMPs, play the role of signalfor danger to induce innate immunity. For instance,oligogalacturonidesarereleasedbymicrobialenzymesand putatively recognized by the receptor WAK1(D’Ovidioetal.,2004).Emissionoftheseendogenoussignalsallowsdisruptedorinjuredcellstocommunicatetheirdamagetothetissueorsystemicallytoallorgans.Systemin is formed in damaged tomato leaves andis further perceived as primary signal for systemicdefense induction (Ryan et al., 2003). Similarly, the23-residuepeptideAtPep1isreleasedfromprecursorproteinsinresponsetowoundingandtriggersaninnateimmuneresponseinArabidopsisviarecognitionbythePEPR1receptor(Yamaguchietal.,2006).

5. A PANOPLY OF MAMPs TO RENDER PLANTS MORE RESISTANT

5.1. Elicitors from beneficial rhizobacteria

ComparedtoPAMPsfrompathogens,lessinformationareavailableonthedeterminantsfromnon-pathogenicrhizobacteria that trigger ISR. Nevertheless, thecharacterization of compounds and/or sub-structuresof rhizobacteria recognized by plant cells hasconsiderably improved these last decades allowing abetterunderstandingof themolecular talksoccurringin this kind of interaction (DeVleesschauwer et al.,2009).

Ithasbeendemonstratedthatflagellinfromtheplantbeneficial rhizobacteriumPseudomonas putida strainWCS358canactaselicitorof systemic resistance inArabidopsisagainstP. syringae(Mezianeetal.,2005).However,additionalexperimentswithotherbacterialisolatesandonmultiplepathosystemsarerequiredtoaccurately evaluate towhat extendflagellinsmaybeconsideredasgeneraldeterminantsoftherhizobacteria-mediated ISR. Lipopolysaccharides (LPS) are cellsurface components of Gram- bacteria associatedwith theoutermembraneof thecellenvelope.Thesecompounds have also been occasionally reported asPAMPs. They are tripartite amphipathic moleculescomprising a lipidA moiety which is embedded intheouterleafletofthephospholipid/proteinbilayer,acoreoligosaccharideandaO-antigensidechain.Thislast part is immunologically dominant and can show

considerablestructuralvariation.InvolvementofLPSin the elicitation of ISR by beneficial bacteria wasreported in various pathosystems withP. fluorescens(Vanpeeretal.,1992;Leemanetal.,1996;Duijffetal.,1997;Tangetal.,2005)andP. putidastrains(Mezianeetal.,2005)butalsowithBurkholderia cepaciainthetobacco/Phytophthora nicotianeae pathosystem andRhizobium eltiG12oncystnematode-infectedpotato(Reitzetal.,2002).ItwasevidencedbytestingpurifiedLPS,heat-killedcells,crudecellenvelopeextractsormutantswithmodifiedLPS. Inmany cases,mutantsthat lack the O-antigen side chain are not inducers,suggestingacrucialroleofthissub-structure.ThereforetheobserveddegreeofspecificityshouldberelatedtothecompositionofpseudomonadLPSthatarealmoststrain-specific regarding the structure of the O-sidechainandtheirelicitingactivityseemstobedependentontheisolatestudied.

Toensuretheirgrowthiniron-limitedenvironments,microorganisms have evolved powerful Fe3+-acquisition systems based on the excretion of high-affinity iron-chelatingmolecules termedsiderophores(Loper et al., 1991). Pyoverdines are siderophorestypically synthesized by fluorescent Pseudomonas(Budzikiewicz,2004)andfromexperimentsinvolvingpyoverdin-non-producingmutantsoradditionofpurepyoverdines,thesecompoundswerealsodemonstratedas potential ISR elicitors (Hofte et al., 2007;De Vleesschauweretal.,2009).Forinstance,WCS358can elicit ISR in several plants such asArabidopsis,bean, tomato andEucalyptus through its siderophore(Bakkeretal.,2003;Mezianeetal.,2005;Ranetal.,2005). SA is produced by some of the rhizobacteriathat induce systemic resistance under iron-limitedconditions.Itsrole in theISRelicitationprocesswasdemonstratedinthecaseofPseudomonas aeruginosaKMPCH (Demeyer et al., 1997; De Meyer et al.,1999). Nevertheless, several reports showed that SAproductionbyotherstrainswasnotassociatedwithISR(Leemanetal.,1996;Pressetal.,1997).SAisalsoanintermediateinthebiosynthesisofothersiderophoressuchaspyochelininPseudomonas aeruginosa(Serinoet al., 1997) and a role for pyochelin was proposedin ISR triggered in tomato byP. aeruginosa 7NSK2(Audenaertetal.,2002).

In our laboratory, searching for moleculardeterminants of P. putida BTP1 responsible for ISRelicitationledtotheisolationofanexcretedcompoundconsistingofatri-N-alkylatedbenzylaminederivative(NABD)(Ongenaetal.,2005).Theelicitorpropertieswere mainly established on the basis of treatmentof bean roots with the pure compound NABD thatmimickedtheprotectiveeffectoftheproducingstrainand by showing that a BTP1 derivative affected inNABDsynthesiswasalso impaired in its efficacy tostimulateISR.


Some Pseudomonas products known fortheir antibiotic activities such as pyocyanine and2,4-diacetylphloroglucinol (DAPG) may also act aselicitors of systemic resistance (Iavicoli et al., 2003;Siddiquietal.,2003b).Thephenazine-typemoleculepyocyanine was proposed to act synergisticallywith pyochelin to trigger ISR in tomato treatedwithP. aeruginosa7NSK2(Audenaertetal.,2002).DAPGisanotherantibioticproducedbyP. fluorescensCHA0that also retains some ability to stimulate defense-relatedreactionsinthehostplantasit isanessentialcomponentof theISR-mediateddiseasereductionbythis strain inArabidopsis and tomato plants infectedrespectively by Peronospora parasitica and thenematodeMeloidogyne javanica(Iavicolietal.,2003;Siddiquietal.,2003a).

AnotherclassofcompoundsthatrecentlyemergedasISRelicitorsarebiosurfactantssuchasrhamnolipidsand lipopeptides. The potential of LPs as plantresistanceinducerswasdemonstratedin2007fortwodifferentmoleculessynthesizedbyPseudomonasandBacillus.Tranetal.(2007)showedthatmassetolideAproduced by Pseudomonas fluorescens retains ISR-eliciting activity in tomato plants for the control ofPhytophthora infestans,thecausalagentoflateblight.Pure fengycins and surfactins from Bacillus subtilisprovidedasignificantinducedprotectiveeffectsimilartotheoneinducedbylivingcellsoftheproducingstrain.Inacomplementaryapproach,experimentsconductedon bean and tomato showed that overexpression ofbothsurfactinandfengycinbiosyntheticgenes in thenaturally poor producer B. subtilis strain168 wasassociatedwitha significant increase in thepotentialofthederivativestoinduceresistance(Ongenaetal.,2007). Until recently, volatile organic compoundsand more particularly 2,3-butendiol were the soledeterminants for elicitation identified from Bacillusspp.(Ryuetal.,2004).

Someothermoleculesfrombeneficialrhizobacteriaretain plant defense eliciting activity such asexopolysaccharides (Ipper et al., 2008) or quorumsensing signal molecules (N-acyl-L-homoserinelactone)(Schuheggeretal.,2006)againillustratingthevarietyinstructureandnatureofthatkindofMAMPs.

5.2. Elicitors from beneficial fungi and from yeast

MAMPs involved in systemic resistance triggeredby beneficial fungi are not so well characterizedcompared to rhizobacteria. Djonovic et al. (2006)recently demonstrated that the hydrophobin-likeelicitor Sm1 of the beneficial soil-borne fungusTrichoderma virens induces systemic resistance inmaize.MaizeplantsgrownwithSM1-deletionstrainsor SM1-overexpressing strains displayed decreasedor enhanced levels of systemic disease protection,

respectively,demonstrating its role in triggeringhostdefense. Peptaibols are linear peptide antibioticsproduced by Trichoderma and other fungal genera.In the biocontrol agent and inducer of plant defenseresponses Trichoderma virens, enzymes formingpeptaibolsareencodedbytex1anddisruptionofthesegenesledtoasignificantlyreducedsystemicresistanceresponseincucumberplantsagainsttheleafpathogenPseudomonas syringae pv. lachrymans as comparedwith plants grown in presence of the wild-type(Viterbo et al., 2007). Two synthetic 18-amino-acidpeptaibol isoforms induce systemic protection whenapplied to cucumber seedlings suggesting that thesepeptides are critical in the chemical communicationbetweenTrichodermaandplantsastriggersofdefenseresponses.However,thepeptaibolalamethicininducedaformofactivecelldeathinArabidopsis thalianacellculturesandcausedlesionsinleavesofplantsafterafewdaysshowingthatthesemoleculesmayalsoretainsome phytotoxicity on certain plant species (Rippaet al., 2010). It has also recently been demonstratedthat some other secondary metabolites of plantbeneficialTrichodermaspp.suchasharzianolideandpentyl-pyranonemayhavearoleinactivationofplantdefenseresponses(Vinaleetal.,2008).

5.3. Still searching for receptors

The molecular basis of defense activation followingPAMPs,DAMPs,MAMPs and chemicals perceptionremain elusive but some aspects have just recentlybeendisclosed(Conrath,2011).IthasbeenspeculatedthatMAMPsofbeneficialmicrobesandPAMPsfrompathogensarerecognizedinasimilarway,ultimatelyresultinginanenhanceddefensivecapacityoftheplant.Howeverthereshouldbedifferencesinthemoleculartalk since thehostplant tolerates thenon-pathogenicassociated microbes while it tries to antagonizepathogen populations. Also, in plant–beneficialmicrobe interactions, MAMP-triggered immunityrelies on priming for enhanced defense with almostno transcriptional re-programming and fitness costpriortoinfection.Thisiscontrastingwithotherformsof systemic resistance involving direct activationof the defense arsenal. So, mechanistically, plantperceptionofMAMPsshouldretainsomespecificity.Intriguingly, no specific proteinaceous binding siteshave been identified forMAMPs perceptionwhile afewplasmamembranereceptorsforPAMPshavebeencharacterized(Gressentetal.,1999;Fliegmannetal.,2004;Kunzeetal.,2004;Ronetal.,2004;Chinchillaetal.,2006;Kakuetal.,2006;Leeetal.,2009).

Recognition of different parts in thelipopolysaccharide structuremayallowplant cells todiscriminate symbiotic and infectiousGram-bacteriaandthisstronglysuggeststhatasomewhatspecialized


perception system is involved at the plant cell walllevel.However,thishasyettobedemonstrated.

Thestrain-specificeffectofpyoverdinsinISRmaybeexplainedasfarasthepeptidechainisinvolvedintheperceptionprocessbyplantcellsbecauseofthestructuraldifferences between naturally occuring pyoverdines.Actually, there is nopartial sequence sharedby threeactivepyoverdinsfromWCS358,WCS374andCHA0.Testingawiderrangeofheterogeneouspyoverdinsonthe same plant is required to evaluate whether someaminoacidsequencesmayrepresentepitopesperceivedby specific receptors in the membrane of root cells.An alternative to direct recognition of pyoverdins bytheplant is the indirect perceptionof rhizobacteriallyinduced alterations in the plant’s immediateenvironment i.e. the rhizosphere. Given the scarcityofbioavailableironandthehighaffinityofpyoverdinfor the ferric ion, pyoverdin-producing rhizobacteriaare thought to interfere with the iron acquisition byothersoilorganisms,includingthehostplant(Vansuytet al.,2007).Amodelimplyingpyoverdin-inducedironstressontherootsasaprimaryeventintheactivationofrhizobacteriamediatedresistancehasbeenproposed(DeVleesschauweretal.,2009).

Structural similarities are neither obvious in otherbacterialproductsidentifiedsofarasISRdeterminantslike NABD, SA, DAPG, pyocyanin or volatile2,3-butanediol. Results obtained by comparing theactivity of pure benzylamine with that of NABD inISR assayswith bean and cucumber suggest that thearomatic amino part of themolecule is important forits biological activity (Ongena et al., 2008b).SAandDAPG also contain an aromatic phenolic group andthus such phenyl-derived moieties could constitutea general motif widely recognized by specific plantcell receptors.Additional experiments are required toappreciate the relative importance of such structuraltraits by testing multiple naturally co-produced orchemicallysynthesizedderivatives.

Lipopeptidesmaybesensitizedbyplanttissuesviaa less specific mechanism than high-affinity proteicreceptor. Due to their amphiphilic nature and theirputative surfactantproperties, thesemolecules readilyinsertintophospholipidbilayertherebycreatingsomedisturbance or channeling in the plasma membrane.This may, in turn, activate a cascade of moleculareventsleadingtodefensiveresponses.Itisnoteworthythatsuchmembraneperturbationshouldremainlimitedsincethepurecompoundshadnotoxiceffectonplanthealthattheconcentrationused(Jourdanetal.,2009).

6. NON-MICROBIAL ELICITORS

As stated above, some compounds that are not frommicrobial origin have also been reported as efficient

plant defense inducers. Biotic elicitors were isolatedfrom algae or shrimp and crab walls. The linearhepta-β-glucoside laminarin elicitor from the brownalga Laminaria digitata elicits defense responses invariousplantsandabindingsitehasbeenidentifiedinmembranesofthemodellegumesMedicago truncatulaandLotus japonicasaswellasinmembranefractionsfromsoybean(Fliegmannetal.,2004;Klarzynskietal.,2000).Apparent Kd values range from 5 to 200nMand elicitor effects observed in tobacco are specificto linear β-1,3 linkages, with laminaripentaose beingthe smallest elicitor-active structure. But contrary tobranched glucans, no receptor has been yet isolated.Chitosan is a deacylated derivative of chitin usuallyprepared from crab shells and serves as a molecularpattern which stimulates the innate immune systemsofplants(Nurnbergeretal.,2004).Althoughaplasmamembrane receptor for chitin fragments has beencharacterized(Iritietal.,2010),thesignaltransductionpathwayactivatedbychitosanisnotwelldefined.

Besides pathogenic microbes, there are certainchemicalswhichuponapplicationtoplantsmimicthehost-pathogen interaction leading to SAR (Gullinoet al.,2000;Oostendorpetal.,2001).Naturalsignalingmolecules like SA, JA and systemin are componentsof the biological induction and are able to induce asystemicprotection(Cohenetal.,1993;Holleyetal.,2003; Mayers et al., 2005). Chemical elicitors likeDL-β-aminobutyricacid(BABA)(Hongetal.,1999),oxalic acid (Mucharromah et al., 1991), 2,6-dichloroisonicotinic acid (INA) and its derivatives (Qianet al., 2006), benzo[1,2,3]thiadiazole (BTH) (Kunzet al., 1997) and derivatives S-methyl benzo[1,2,3]thiadiazole-7-carbothiate (acibenzolar-S-methyl)(Cools et al., 2002) have also been shown to beeffectiveelicitorsforinducingthebiosynthesisofplantsecondarymetabolites.However,plantsexposedtohighconcentrationsofBTHorINAmayalsoexhibitsignsofphytotoxicity,butthiseffectseemstobeindependentoftheinducedresistanceresponse(Louwsetal.,2001).

7. PRACTICAL APPLICATIONS OF PLANT IMMUNITY TRIGGERING COMPOUNDS

Recentprogressesinourunderstandingofprinciplesofplantsystemicimmunityhasbeenthedrivingforcetosetupfieldandgreenhousecropprotectionexperimentsbased on these phenomena. Based on the promisingresults obtained with beneficial ISR-inducing micro-organisms,thedevelopmentofmicrobialformulationswaspromotedforapplicationinconventionalagriculture.Rhizobacterial-orfungal-mediatedISRdoesnotconferatotalprotectionagainstpathogeninfectionbutasthephenomenon is long-lasting (VanLoonet al.,1998),effective against a broad range of diseases and in


multipleplantspecies(seebelow)andnotconducivefordevelopmentofpathogenresistance(multiplicityandvarietyofinduceddefensestrategies,seebelow),ISR-based biocontrol strategies are promising andsome trialswere successfully performed under fieldconditions (Wei et al., 1996; Zehnder et al., 2001).Also,somechemicalsarestronginducersofaSAR-like response. Compounds such as 2,6-dichloroisonicotinicacid,benzothiadiazoleanditsderivativeacibenzolar-S-methyl, or β-amino butyric acid, arenowadayssuccessfullyemployed tocontroldiseasesofvariouscropplants(Valladetal.,2004).

On another hand, the continuous discovery ofnew PAMPs and MAMPs contributes to enlargeour reservoirofveryefficient structuralpatterns forboosting plant immunity. The most active of thesecompoundsmaybeproducedbiotechnologicallyandpurified to the required level for commercialization.Alternatively they may serve as molecular basisfor the development of new structural derivativeswith higher activity and/or lower susceptibility todegradation and/or lower lateral toxicity. Even ifneither SAR nor ISR will become a stand-alonemethod for pest control, it is now clear that theywill be further integrated into pest managementsystems.

Interfering with themolecular dialogue betweenPAMPsandtheircognateplasmamembrane,sensingsystems may also be the basis of novel strategiesto engineer durable plant disease resistance. Forinstance, enhancement of the potential of plant torecognize a broader range of PAMPs and thereforeresist to a broader range of pathogens has beensuccessfully achieved via heterologuous expressionor overexpression of PRR/LRR-RK receptors insome plants (Gust et al., 2007). Another approachto improve disease resistance is overexpression ofantibodies fused with antimicrobial peptides andthatrecognizespecificpathogensurfacecomponents(Li etal., 2008). Enhancing the expression of keyregulators of systemic resistance such as NPR1whichcontrolsimmunity-associatedgenesisalsoanalternativestrategytoboostthedefensereactioninitsentirety(Makandaretal.,2006).

8. CONCLUSION

Considering the large and still increasing numberof molecular patterns and effectors harbored bypathogens, it is clear that plants have evolved tomountveryefficientnon-selfrecognitionsystems.AstheyalsodevelopperformingandspecificreceptorstodetectendogenousDAMPs,theconceptof“stranger”recognitioncouldbeextendedto“danger”recognition.Theperceptionofallthesesignalsappearstotrigger

the same stereotypical defense program even if itvariesintermsofkineticandstrengthoftheresponsebetweenPTIandETI(Bolleretal.,2009).

Elicitors of SAR and ISR could potentiallyrevolutionize pest management in conventionalagriculture.AlotofnewmoleculesactingasPAMPsand MAMPs will most probably be discovered inthecomingyearsbutwearestillfarfromadetailedunderstanding of the fascinating mechanisms bywhich non-pathogenic microorganisms induceresistance inplants. In support to thecomplexityofthisinteractionistheplethoraofstructurallydistinctelicitorsactiveattriggeringplantdefenseresponses.Suchdiversity is reminiscent of the largevarietyofpathogen-derived elicitors with immune-stimulatingactivity (Schreiber et al., 2008). Some high-affinityproteic receptormay be involved in the recognitionof thoseISRelicitorsactiveatconcentrations in thepico-tonanomolarrangewithoutanydose-responserelationship (flagellin, SA, pyocyanin, DAPG).However, theperceptionof thosecompoundsactingat micromolar concentrations or even more shouldrelyonanotherlessspecificmechanismbasedeitheron low-affinity receptororonsome interactionwithothercellmembranecomponentssuchaslipidbilayeras was suggested for lipopeptides (Ongena et al.,2008a). It isbecomingclearer that the lipid fractionof eukaryotic plasma membranes may act as veryefficientsensorofvariousabioticandbioticexternalsignals.Itmaythusrepresentanalternativemodeofmicrobe sensing and intimately cooperate togetherwith specialized proteic receptors to optimize non-selfrecognitionbyplants.

Abbreviations

BABA:DL-β-aminobutyricacidBTH:Benzo[1,2,3]thiadiazoleDAMP:Damage-AssociatedMolecularPatternDAPG:2,4-diacetylphloroglucinolET:EthyleneETI:Effector-TriggeredImmunityISR:InducedSystemicResistanceJA:JasmonicAcidLAR:LocalizedAcquiredResistanceLPS:LipopolysaccharidesLRR:Leucine-RichRepeatsMAMP:Microbe-AssociatedMolecularPatternPAMP:Pathogen-AssociatedMolecularPatternPGPR:PlantGrowthPromotingRhizobacteriaPTI:PAMP-TriggeredImmunityRLK:Receptor-LikeKinaseRLP:Receptor-LikeProteinSA:SalicylicAcidSAR:SystemicAcquiredResistance


Acknowledgements

GuillaumeHenryisbeneficialofagrantfromtheFormationàlaRecherchedansl’Industrieetl’Agriculture(F.R.I.A.)andMarcOngenaisresearchassociateattheFondsNationaldelaRechercheScientifique(F.R.S-FNRS).

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