Chemical host-seeking cues of entomopathogenic nematodes
Xi Zhang
1, Lu Li
1, Lucie Kesner
2and Christelle Aure´lie Maud Robert
2,3Entomopathogenicnematodes(EPNs)areobligateparasites thatinfectabroadrangeofinsectspecies.Host-seekingisa crucialstepforEPNinfectionsuccessandsurvival.Yet,the identityandecologicalfunctionsofchemicalsinvolvedinhost- seekingbyEPNsremainoverlooked.Inthisreview,wereport knownCO2,plant-derivedandinsect-derivedcuesshaping EPNhost-seekingandrecognition.Despitespecies-specific responsetoenvironmentalcues,wehighlightahierarchical integrationofchemicalsbyEPNs.Wefurtheremphasizethe impactofEPNselectionpressure,age,andexperienceontheir responsivenesstoinfochemicals.Finally,wefeaturethatEPN chemicalecologycantranslateintopowerfulsustainable strategiestocontrolinsectherbivoresinagriculture.
Addresses
1KeyLaboratoryofPlantStressBiology,StateKeyLaboratoryofCotton Biology,SchoolofLifeSciences,HenanUniversity,Kaifeng475004, China
2InstituteofPlantSciences,UniversityofBern,Altenbergrain21, 3013Bern,Switzerland
3OeschgerCentreforClimateChangeResearch(OCCR),Universityof Bern,Falkenplatz16,3012Bern,Switzerland
Correspondingauthors:
Zhang,Xi(xizhang_2019@163.com),Robert,ChristelleAure´lieMaud (Christelle.robert@ips.unibe.ch)
CurrentOpinioninInsectScience2021,44:72–81
ThisreviewcomesfromathemedissueonParasites/parasitoids/
biologicalcontrol EditedbyFengZhu
https://doi.org/10.1016/j.cois.2021.03.011
2214-5745/ã2021TheAuthors.PublishedbyElsevierInc.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creative- commons.org/licenses/by-nc-nd/4.0/).
Introduction
Entomopathogenicnematodes(EPNs)areobligatepara- sitesthat infectandkill insects.Theirshort lifecycles, simplerearingrequirements,andstraightforwardmolec- ularmanipulationsrenderthemidealtostudyhost–para- siteinteractions[1].Additionally,theirefficacyinreduc- ingherbivoredamageinthefieldcontributedtotheiruse asbiologicalcontrolagentsinagriculture [2,3].
EPNscomprisethreegenera,Heterorhabditis,Steinernema, andOscheius [4].Infective juveniles(IJs) are third-stage free-livingnematodelarvae(iL3)thatlocate,select,and infectahostbyenteringthroughanatural orificeor by penetrating through the cuticle. Upon infection, IJs releasevenomproteinsandregurgitateanendosymbiotic entomopathogenicbacterium,leadingto afataltoxemia and septicemia of the host. Juveniles then undergo a transition from free-living to parasitic lifestyle and resume growth and development by feeding on the infected flesh. Adult nematodes reproduce inside the host generating several new generations of nematodes [5].Resourcedepletionandelevatednematodedensities inducetheproductionofascarosideC11ethanolamine,an ascaroside triggering the production of next generation IJs, often through Endotokia matricida [6]. The newly hatched IJs emerge from the resource-depleted host andsearchtoinfectnewhosts.
Juvenile host-seeking strategies are typically classified alongagradientrangingfromambushingtocruising[7].
Ambusher nematodes are stationary and infect mobile hosts. Attachment to a mobile host can be achieved through nictation, which corresponds to the nematode standingon itstail, curling,and propellingitselfin the air[8].Cruisernematodesdisperseinthesoilandlocate sedentaryhosts[9].Nematodeswithintermediatestrat- egies can ambush or disperse depending on the soil matrix and host presence [10,11]. Additionally, recent studies highlighted that EPNs can attract insects to infected cadavers just before emergence [12,13].
Being the first step of host–parasite interactions, host- seeking is critical in determining the success of a parasite.
The cues shaping host-seeking can be physical and chemical[14].Olfactorycuestriggerchemotaxisornicta- tioninalltestedEPNspecies,andincludecarbondiox- ide, as well as specific host-derived and plant-derived chemicals. EPNs mayuse CO2gradients to locatebio- logicalactivity,herbivore-inducedplantvolatilestolocate herbivore insects from a distance, and insect-derived chemicalsto accurately find a host. Finally, EPNs can assesstheirhostquality,includinginfectionstatusordiet, priorinfection.Yet,anddespitetheirpivotalroleinhost–
parasiteinteraction,theidentityandecologicalfunctions of thechemicalsinvolvedin host-seeking andhost-rec- ognitionbyEPNsremainpoorlyunderstood[15].
In this review, we gather knowledge about chemical signals involvedin EPN host-seekingand host-recogni- tionbehavior.Wehighlighttheconnectionbetweenthe typeofchemicalsusedforforagingandEPNspecializa- tiondegree,foraging strategy,development,andexperi- ence.Finally,wefeaturehowEPNchemicalecologycan translate intosustainablepestmanagementstrategies.
Infochemicals shapingEPN host-seeking
Carbondioxide
EPNscanuseCO2,ubiquitouslyemittedbymostliving organisms, forhost location (forreview seeRef. [16]).
CO2triggersforagingbyEPNswithdivergentlifestrate- gies,forexample,generalists,specialists,ambushers,and cruisers,each ofthem exhibitingdifferentsensitivityto thiscue[17,18].TheCO2responseismediatedthrough thepairedBAGsensoryneuronsoftheheadinnematodes [18,19]. By elegantly combining BAG-neuron ablation and CO2-free attraction assays, Hallem et al. demon- strated thatH.and S.carpocapsaecanuseCO2solelyor incombinationwithinsectorplantodorstolocateahost [18,19].
Plant-derivedcues
EPNs have evolved the ability to use plant signals to locatepotentialherbivorehosts.Herbivore-infestedroots releaseaspecificblendofmoleculescomparedtohealthy plants [20–22]. The abundance and diffusion of these herbivore-induced plant volatiles (HIPVs) represent a detectable, albeit not reliable, indicator of herbivore presence.Belowgroundolfactometerassaysandreal-time observations of EPN behavior in Pluronic gel demon- stratethatEPNs aggregatein thevicinityof plantroots and preferentially orient towards wounded plants than towardshealthyplants[23–25].HIPVsfromvariousplant species, includingmaize,citrustrees, potato,sugarcane, carrot and vine, induce chemotaxisin EPNs [20,21,26–
32].TheattractiveeffectofHIPVswasobservedinboth cruiserandambusherEPNs,buttheresponsetodifferent volatiles was strain-specific rather than related to EPN foraging strategies[30–33].Forexample,onlyonestrain out of 3 tested strains of the ambusher S. carpocapsae exhibit chemotaxis towards linalool [32]. Furthermore, some HIPVs can triggerthe nictation of the ambusher [18].Anincreasingnumberofchemicalcompoundsmedi- ating EPN host-seeking behavior have been identified and aresummarizedin Table1.
Insectcues
EPNs canuse insect-specificcuestoefficientlylocate a host [34,35].Herbivoresconstantlyreleasechemicalsin theirenvironmentthroughpheromones,exudates,molt- ing skins (exuviae),or feces (frass). Insect-derivedche- micalsdiffusinginthesoilmatrixcantriggerEPNattrac- tion,repellence, or nictation(Table 2).Commoninsect cuestriggering chemotaxisornictationof EPNsinclude frass chemicalssuch asnitrogen metabolism,and waste
products, such as uric acid, hypoxanthine, xanthine, allantoin,urea,andammonia[36].Insectspecies-specific compounds,suchas sexpheromones,canattract EPNs.
For example, thefeces of the adult citrus weevil, Dia- prepes abbreviatus, contains [(E)-3-(2-hydroxyethyl)-4- methyl-2-pentenoate], a pheromone involvedin female attraction for mating [37].Intriguingly, this pheromone participatesintherecruitmentoftwointermediatecruiser EPNs, S. diaprepesi and H. indica [38]. Rivera et al.
hypothesizedthatthepheromone-containingfrasscould beusedasanindicatorofanear-futureeggdepositionand hostpresence[38].Thestrengthofchemotacticresponse to insect-derivedcuesmirrorsEPN host-seeking strate- gies:Ambusher EPNsareless responsiveto insectche- micals [17], except if the latter are associated with air movement or physical contact with the potential host [39,40].KnowninsectcuesmediatingEPNhost-seeking aresummarized inTable 2.
Infochemicals shapingEPNhost-recognition EPNs can use insect cues to recognize and assess the quality ofapotentialhost.EPNscandistinguishbetweeninsects fedondifferentplantspecies[41],althoughtheinvolved cues remain unidentified. EPNs may further recognize herbivoressequesteringtoxicplantsecondarymetabolites.
Forinstance,EPNsarerepelledbysix-methoxy-2-benzox- azolinoneN-glucoside (MBOA-Glc), aplant benzoxazinoid detoxification product, released by the benzoxazinoid sequesteringrootherbivore,Diabroticavirgifera[42].Sim- ilarly,EPNsarerepelledbyglucosinolatebreakdownpro- ducts[43].Althoughnumerousspecialistherbivoreshave evolvedtheabilitytosequesterand/orreleasetoxicplant metabolites, the impact of the latter on EPN foraging remainsoverlooked[41,44].Furthermore,EPNscandif- ferentiatebetweenhealthyandinfectedhosts[13,45–48], andevenbetweenhostsinfectedwithconspecificorhet- erospecific EPNs [49]. So far, only a few compounds, such as isoprenoidprenol(3-Methyl-2-buten-1-ol) andbutylated hydroxytoluene(BHT),havebeenimplicatedinlateinfec- tionrecognitioncues[12,13].Interestingly,bothprenol and BHT attract new, healthy, insects to late stage of infectioncadavers,aneffectthatenhancestheprobability of emerging EPNsto encounter new hosts[12,13].It shouldalsobenotedthat,whileprenolrepelsEPNs,BHT attracts IJs and enhance their predation success [12].
Known insect cuesmediatingEPN host-recognition are summarizedinTable2.
Interactive effectsand hierarchicalresponse to multiplecues
Although the most reliable cues for EPNsto forage would be cuesemanatingfrompotentialhosts,thelatterevolvedto emitbarely detectableamounts of signals[50]. On the other hand, attacked plants release large amounts, albeit less reliable,ofchemicalsthatdiffuseinthesoilmatrix[51].
This reliability-detectability dilemma may have driven EPNstointegrateacombinationofCO2,plant,andinsect
InfochemicalsinvolvedinEPNforagingZhangetal. 73
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Table1
Plant-derivedinfochemicalsinvolvedinentomopathogenicnematodeforaging
CompoundeffectonEPNs EPNspecies Chemicaltype Compound Plantspecies Ref.
Attractive H.bacteriophora Aromatic 2,4-Di-tert-butylphenol Carrot(Daucuscarota) [30]
Attractive H.bacteriophora Aldehyde Decanal Potato(Solanumtuberosum) [31]
Attractive H.bacteriophora Aldehyde Octanal Potato(Solanumtuberosum) [31]
Attractive H.bacteriophora Alcohol 1-Octanol ND [56]
Attractive H.bacteriophora Alcohol 1-Nonanol ND [56]
Attractive H.bacteriophora Alcohol 2-Heptanol ND [56]
Attractive H.bacteriophora Sesqui-terpene Humulene Beech(Fagussylvatica) [26]
Attractive H.bacteriophora Benzene p-Cymene ND [18]
Attractive H.bacteriophora Ester Methylsalicylate ND [18]
Attractive H.megidis Alcohol 1-Octen-3-ol Redfescue(Festucarubra) [28]
Attractive H.megidis Ketone 3-Octanone Redfescue(Festucarubra) [28]
Attractive H.megidis Hydro-carbon 1-Undecene Redfescue(Festucarubra) [28]
Attractive H.megidis Hydro-carbon Nonadecatriene Redfescue(Festucarubra) [28]
Attractive H.megidis Sesqui-terpene a-Curcumene Redfescue(Festucarubra) [28]
Attractive H.megidis Sesqui-terpene (E)-b-Caryophyllene Maize(Zeamays) [21]
Attractive H.megidis Disulfide Dimethyldisulfide Blackmustard(Brassicanapus) [52]
Attractive S.carpocapsae Alcohol Octanol ND [18]
Attractive S.carpocapsae Alcohol Nonanol ND [18]
Attractive S.carpocapsae Sesqui-terpene (E)-b-Caryophyllene Maize(Zeamays) [32]
Attractive S.carpocapsae Mono-terpene Linalool Maize(Zeamays) [32]
Attractive S.carpocapsae Mono-terpene Bornylacetate Carrot(Daucuscarota) [30]
Attractive S.carpocapsae Aldehyde Nonanal Potato(Solanumtuberosum) [31]
Attractive S.carpocapsae Aldehyde Octanal Potato(Solanumtuberosum) [31]
Attractive S.carpocapsae Aromatic 1,2,4-Trimethylbenzene Potato(Solanumtuberosum) [31]
Attractive S.carpocapsae Ketone 2-Nonanone ND [18]
Attractive S.carpocapsae Alcohol Heptanol ND [18]
Attractive S.carpocapsae Alcohol Pentanol ND [18]
Attractive S.carpocapsae Sesqui-terpene (E)-b-Caryophyllene* Hempvarieties(Cannabissativa) [29]
Attractive S.carpocapsae Alcohol Hexanol ND [18]
Attractive S.carpocapsae Ester Octylacetate ND [18]
Attractive S.diaprepesi Sesqui-terpene Geijerene Citrus(CitrusparadisiPoncirustrifoliata) [20]
Attractive S.diaprepesi Sesqui-terpene Pregeijerene Citrus(CitrusparadisiPoncirustrifoliata) [20]
Attractive S.diaprepesi Sesqui-terpene a-Santalene Citrus(CitrusparadisiPoncirustrifoliata) [20]
Attractive S.diaprepesi Mono-terpene a-cis-Bergamotene Citrus(CitrusparadisiPoncirustrifoliata) [20]
Attractive S.diaprepesi Mono-terpene Limonene Citrus(CitrusparadisiPoncirustrifoliata) [27]
Attractive S.feltiae Aromatic 1,2,4-Trimethylbenzene Potato(Solanumtuberosum) [31]
Attractive S.feltiae Canna-binoid Cannabidiol* Medicalcannabis(Cannabissativa) [29]
Attractive S.kraussei Aldehyde Decanal Potato(Solanumtuberosum) [31]
Repellent H.bacteriophora Mono-terpene a-Pinene Carrot(Daucuscarota) [30]
Repellent H.bacteriophora Mono-terpene Terpinolene Carrot(Daucuscarota) [30]
Repellent H.bacteriophora Alcohol Hexanol ND [18]
Repellent H.bacteriophora Alcohol Heptanol ND [18]
Repellent H.bacteriophora Alcohol Nonanol ND [18]
Repellent H.bacteriophora Alcohol Octanol ND [18]
Repellent H.bacteriophora Aromatic Belzaldehyde ND [18]
Repellent H.bacteriophora Mono-terpene 3-Carene ND [18]
Repellent H.bacteriophora Mono-terpene Limonene ND [18]
Repellent H.megidis Hydro-carbon Decane Redfescue(Festucarubra) [28]
Repellent S.carpocapsae Mono-terpene Terpinolene Carrot(Daucuscarota) [30]
Repellent S.carpocapsae Mono-terpene a-Pinene Carrot(Daucuscarota) [30]
Repellent S.carpocapsae Alcohol 2-Ethylhexanol Carrot(Daucuscarota) [30]
Repellent S.carpocapsae Mono-terpene Bornylacetate Carrot(Daucuscarota) [30]
Repellent S.carpocapsae Alcohol 2-Ethyl-1-hexanol Potato(Solanumtuberosum) [31]
Repellent S.carpocapsae Mono-terpene Limonene ND [18]
Repellent S.feltiae Aldehyde Decanal Potato(Solanumtuberosum) [33]
Repellent S.feltiae Sulfide Dimethylsulfide Blackmustard(Brassicanapus) [43]
Repellent S.feltiae Aldehyde Octanal Potato(Solanumtuberosum) [32]
Repellent S.feltiae Mono-terpene Terpinolene Carrot(Daucuscarota) [30]
Repellent S.feltiae Aldehyde Octanal Potato(Solanumtuberosum) [30]
Repellent S.feltiae Hydro-carbon Undecane Potato(Solanumtuberosum) [31]
Repellent S.kraussei Sulfide Dimethylsulfide Blackmustard(Brassicanapus) [43]
Repellent S.kraussei Disulfide Dimethyldisulfide Blackmustard(Brassicanapus) [43]
Repellent S.kraussei Trisulfide Dimethyltrisulfide Blackmustard(Brassicanapus) [43]
Repellent S.kraussei Isothio-cyanate Allylisothio-cyanate Blackmustard(Brassicanapus) [43]
signalswhenforaging[50](Figure1).Yet,itwouldnotbe surprisingif specialistEPNsrespond tolowerdetection thresholdforinsectcuesandalmostexclusivelyrelyonthe latter, but this hypothesis remains to be tested. Some evidence points towards a hierarchical order of EPN responsetospecificstimuliduringforaging.CruiserEPNs preferentiallyorient towardsacombination of CO2with plant or insect signals than towards individual signals [17,52]. Similarly, they preferentially navigate towards plantandinsectvolatilecombinationratherthantowards oneofthesignalsalone[53].Interestingly,EPNspreferen- tiallyfollowplantvolatilecuesratherthanherbivoreodor- ants alone [17,20,53–56] although they prefer infested plantcuesratherthanhealthyplantcues[25,57].Finally, EPNspreferentiallyfollowhost-specificcuesratherthan CO2alone [17,56] (Figure 1). Ambusher EPNs also follow a hierarchicalorderofresponsetoenvironmentalcues,but the required activation step may be physical (air movement, attachmenttotheinsectcuticle)andnotchemical[8,39].
Understandingtheorderandcombinationsofstimuliused by EPNs during foraging is crucial to correctlyidentify involvedinfochemicals.
EPN species-specificresponseto infochemicals
EPNsexhibitspecies-specificresponsetoCO2,plantand insect cues. The relative importance of CO2 is highly variableamongspecies[16].Itshouldbenotedthatthe specialist EPN, S. scapterisci, relies less on CO2 than generalist EPNs in the presence of host cues [17,58].
Different EPN species exhibit strong preferences for different plant species [25,54,55], but whether these preferencescorrelatewiththepresenceoftheirpreferred hostsremainstobeelucidated.Similarly,EPNresponse toinsectcuesvariesconsiderablybetweenEPNspecies.
Inacomprehensivechemotaxisandnictationstudy,Dill- man et al.[17] demonstratedthat4 outofthe6 tested species displayed specific responses to insect-derived cues[17].Thespecificityofresponseisapivotalfactor to account for when introducing EPNs for biological control.Severalstudiesreportedtheinadequacyofintro- ducingnewEPNspeciestocontrolherbivorepests[59], but understanding EPN-hostspecificity would allow to better definetheappropriatedstrainsto use.
Ecosystem-specific selectionpressure, age, and experience shapeEPNresponseto infochemicals
Oneofthechallengesassociatedwiththeidentification of chemical cuesinvolved inEPNhost-seekingbehav- ior is the variability of response within strains. EPN response depends on their selection pressure, age,and experience.ArtificialselectionincreasesEPNhost-find- ingefficacywithinafewgenerations[60–62].Thisrapid geneticadaptationofEPNstoenvironmentalinfochem- icalstogetherwithlowmobilitysuggestprobablystrong variations in chemotaxis between EPN populations [63].
Additionally,EPN age(referringhereto thetimesince emergencefromthenatalcadaver)isimplicatedinbehav- ioral shifts. For instance, CO2 repels S. scapterisci IJs immediately after emergence but attracts them over thefollowing weeks[64].Similarly,therepellent effect of prenol was age-dependent in 3 outof 5 testedEPN species[65].
EPNexperience,throughpriorexposuretovolatiles,can primeEPNsinacompound-specificmanner[63],result- ing in increased EPN efficacy [66,67,68]. Persistent exposureresults inincreasedpreferencesandlong-term memory [63].Intriguingly, primed EPNs can influence thebehaviorandchemotaxisofco-occurringEPNspecies [63].Thespecificityofresponsetochemicalcuesempha- sizesthecrucialneedforstandardizedassaystoelucidate theroleof infochemicalsin host-seeking.
Chemically mediated interactions among EPNsand soil-living organisms
Except for herbivores, EPNs will also encounter and interactwithvariousorganismsinsoil.EPNsmayinfect non-herbivore preys, such as fungivorous insects. It is probablethatEPNshaveevolvedtorecognizeandorient towardsfungalchemicals,andmaybeeventowardsfun- givore-inducedfungalcues.Recently,1-octen-3-ol(octe- nol)and1-pentanolhavebeenidentifiedfromthefungus Fusarium solanivolatiles,which areattractivefor botha fungivorousinsectandforEPNs[18,69–71].Otherfungi, suchasF.oxysporum,producecaryophyllene,whichmay
InfochemicalsinvolvedinEPNforagingZhangetal. 75
Table1(Continued)
CompoundeffectonEPNs EPNspecies Chemicaltype Compound Plantspecies Ref.
Repellent S.kraussei Isothio-cyanate Phenylethylisothiocyanate Blackmustard(Brassicanapus) [43]
Repellent S.kraussei Aromatic Benzonitrile Blackmustard(Brassicanapus) [43]
Repellent S.kraussei Aromatic 2,4-Di-tert-butylphenol Carrot(Daucuscarota) [30]
Repellent S.kraussei Mono-terpene a-Pinene Carrot(Daucuscarota) [30]
Repellent S.kraussei Mono-terpene Terpinolene Carrot(Daucuscarota) [30]
H.:Heterorhabditis;S.:Steinernema;O.:Oscheius.Ref.:reference.ND:Nondetermined,theauthorsusedsyntheticcompoundsthatareknowntobe releasedbyplants.Astarindicatesaputativeeffect,astheeffectofthepurecompoundwasnottested.
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s/parasitoids/biologicalcontrol
Compound effect on EPNs EPN species Chemical type Compound Insect species Ref.
Attractive H. bacteriophora Alcohol Propanol Acheta domesticus(Orthoptera) [17,18]
Attractive H. bacteriophora Thiazole 4,5 Dimethyl-thiazole Zophobas morio(Coleoptera) [18]
Attractive H. bacteriophora Oxide Carbon dioxide ND [56]
Attractive H. bacteriophora Aromatic Butylated hydroxytoluene Diabrotica virgifera(Coleoptera) [12]
Attractive H. indica Ester (E)-3-(2-Hydroxyethyl)-4-methyl-2-pentenoate Diaprepes abbreviatus(Coleoptera) [38]
Attractive O. carolinensis Amine Trimethylamine Acheta domesticus(Orthoptera) [17]
Attractive O. carolinensis Mono-terpene g-Terpinene Acheta domesticus(Orthoptera) [17]
Attractive O. carolinensis Amine Trimethylamine Armadillidium vulgare(Isopoda) [17]
Attractive O. carolinensis Aldehyde Hexanal Galleria mellonella(Lepidoptera) [17]
Attractive S. carpocapsae Ketone 2-Propanone Armadillidium vulgare(Isopoda) [17]
Attractive S. carpocapsae Hydro-carbon Tetradecane Armadillidium vulgare(Isopoda) [17]
Attractive S. carpocapsae Ketone 2-Propanone Chrysobothris mali(Coleoptera) [17]
Attractive S. carpocapsae Ether Tetrahydrofuran Euborellia femoralis(Dermaptera) [17]
Attractive S. carpocapsae Mono-terpene a-Pinene Galleria mellonella(Lepidoptera) [17]
Attractive S. carpocapsae Aromatic 4-Methylphenol Scapteriscus borellii(Orthoptera) [17]
Attractive S. carpocapsae Quinone p-Benzoquinone Scapteriscus borellii(Orthoptera) [17]
Attractive S. carpocapsae Alcohol Hexanol Galleria mellonella(Lepidoptera) [18]
Attractive S. carpocapsae Oxide Carbon dioxide Tenebrio molitor(Coleoptera) [18]
Attractive S. carpocapsae Thiazole 4,5-Dimethylthiazole Zophobas morio(Coleoptera) [18]
Attractive S. diaprepesi Ester (E)-3-(2-Hydroxyethyl)-4-methyl-2-pentenoate Diaprepes abbreviatus(Coleoptera) [38]
Attractive S. feltiae Diureide Allantoin Galleria mellonella(Lepidoptera) [36]
Attractive S. feltiae Hydride Ammonia Galleria mellonella(Lepidoptera) [36]
Attractive S. feltiae Amino acid Arginine Galleria mellonella(Lepidoptera) [36]
Attractive S. feltiae Purine Uric acid Galleria mellonella(Lepidoptera) [36]
Attractive S. feltiae Purine Xanthine Galleria mellonella(Lepidoptera) [36]
Attractive S. glaseri Amine Trimethylamine Acheta domesticus(Orthoptera) [17]
Attractive S. glaseri Amine Trimethylamine Armadillidium vulgare(Isopoda) [17]
Attractive S. glaseri Quinone p-Benzoquinone Scapteriscus borellii(Orthoptera) [17]
Attractive S. glaseri Hemi-terpene Isoprenol Plodia interpunctella(Lepidoptera) [47]
Attractive S. scapterisci Hydroxy ketone 3-Hydroxy-2-butanone Acheta domesticus(Orthoptera) [17]
Attractive S. scapterisci Sulfone Dimethyl sulfone Acheta domesticus(Orthoptera) [17]
Attractive/Repellent H. bacteriophora Hydride Ammonia Galleria mellonella(Lepidoptera) [48]
Repellent H. bacteriophora Benzoxa-zolinone MBOA-Glucose Diabrotica virgifera(Coleoptera) [42]
Repellent H. bacteriophora Aldehyde Hexanal ND [18]
Repellent H. bacteriophora Mono-terpene a-Pinene ND [18]
Repellent H. bacteriophora Ketone 2,4-Butanedione ND [18]
Repellent S. carpocapsae Aldehyde Hexanal ND [18]
Repellent S. carpocapsae Ketone 2,3-Butanedione ND [18]
Repellent S. feltiae Diureide Allantoic acid Galleria mellonella(Lepidoptera) [36]
Repellent S. glaseri Hemi-terpene Prenol Galleria mellonella(Lepidoptera) [13]
Repellent S. riobrave Hemi-terpene Prenol Galleria mellonella(Lepidoptera) [13]
H.:Heterorhabditis;S.:Steinernema;O.:Oscheius.Ref.:reference. ND: Non determined, the authors used synthetic compounds known to be released by insects.
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therefore attract EPNs [72]. Orienting towards fungal cues mayenhance theinfection success ofEPNs when fungivorousinsectsarepresent.Theidentityandroleof fungalvolatilesinEPNforagingisreceivinganincreased attentionandwillfurthercontributetobetterunderstand EPN foragingstrategiesin soil.
EPNsalsointeractwithplantpathogens,suchasphyto- pathogenic nematodes (PPNs). Terpenoid volatiles, known to be attractive for EPNs, also attract PPNs to therootvicinity[33].Thebenefitforaplanttoemitsuch terpenoids can therefore be counterbalanced,and even reversed, depending on the presence of PPNs in the environment. Yet, it is generally accepted that, during the infection process, EPNs produce nematicidal and repellent compounds,suchasammonia,indoleand stil- bene derivatives, that kill or deter PPNs [73–75] and thereafter,maylimittheimpactofPPNsontheplantand EPN success.
EPNs maycompete for resources with other herbivore enemies, including different EPN species, arthropods, parasitoids,entomopathogenicfungiorfree-livingbacter- ivorousnematodes[69,76–82].Forexample,likeEPNs, the predatory mites and Acrobeloides–group (free-living bacterivorous nematodes) can also be attracted to
chemical cues from rust mite-infested tulip bulbs [83,84]. However, some synergistic effects on infection rateshavealso been reportedbetweenEPNsandento- mopathogenicfungi[85–87].
Finally, EPNs also have a myriad of enemies, such as fungi,bacteria,protozoaandothermicroaphropodsinsoil [88,89].Interestingly,someoftheseenemiesareableto eitherhighjackEPN-attractantsignalsortolureEPNsin their vicinity. For instance, the nematophagous fungi Pochonia clamydosporia can produce 1-octen-3-ol, which is also produced by plants and attractive to EPNs [28,36,90,91] These potential risks of EPN chemotaxis shouldalso betakenintoaccountduringapplicationfor insect pestbiologicalcontrol.
ThesoilmatrixasmodulatorofEPNresponse Thesoilisacomplexmatrix,whosephysical,biological, and chemical properties can considerably influence chemical emission,stability, diffusion,and degradation.
Forinstance,soilmoisture,pH,andtexturecaninfluence therootHIPVprofilesanddiffusion [92,93].Soilmicro- organisms use plant volatiles as source of carbon, and thereforemodulatetheirabundanceanddispersion[94].
Root architecture also influences EPN foraging, with higher root density being negatively correlated with
InfochemicalsinvolvedinEPNforagingZhangetal. 77
Figure1
?
HIPVs Plant cues
EPN-infected cadaver Species
specific
+
Host specificity
Plant/Host quality
HIPVs specificity
Chemically driven foraging decisions in Entomopathogenic Nematodes Sp. 1 - Healthy
None
Sp. 1 - Infested Non-host insect Plant:
Insect:
Sp. 1 - Infested Host insect
Sp. 2 - Infested Host insect
CO2
Current Opinion in Insect Science
ChemicallydrivenforagingdecisionsinEntomopathogenicNematodes(EPNs).ArrowsrepresentpossibleEPNchoices.Thewidersideofthe trianglesindicateEPNpreferences.Yellow:Carbondioxide(CO2),Green/greenspheres:Healthyplantvolatilesandexudates,Orange/orange spheres:Herbivore-InducedPlantVolatiles(HIPVs)andexudates,Red:Insect-derivedcues.Sp.:species.Interrogationmarksindicateunknown differenciationbyEPNs.Theplantspecies2enhancestheherbivorequalityasahost(e.g.Lowerconcentrationsofsecondarymetabolites).
www.sciencedirect.com CurrentOpinioninInsectScience2021,44:72–81
EPNperformance[95].Rootcolonizedwithmicrobescan alterHIPVemissions,andthereafter,alteredEPNattrac- tion[96].Therefore,thesoilcharacteristicscanconsid- erablymodulateEPNsignalperceptionandhost-seeking behavior.Thisphenomenonshouldbecarefullyconsid- eredwhenidentifyingmoleculesinvolvedinEPNhost- seeking.
Applicationinagriculture
Despite the considerable potential of EPNs in pest control, inconsistencies in efficacy have impaired the developmentofEPN-basedpestmanagementprograms [2,59].AsEPNefficacylargelyreliesonhost-findingand infectivity, exploiting infochemical pathways shaping theirforagingbehaviormayallowthetailoringofpower- ful strategies to control herbivore pests in agriculture.
Severalavenues, basedonEPNchemicalecology,have beenproposed.First,cropscouldbeselected orgeneti- cally modified to constitutively emit attractive HIPVs [97].Yet,thisapproachrequiresathoroughinvestigation ofpleiotropiceffects.Forinstance,anddespiteproviding abetterprotectionagainstrootherbivores,transforming maize plants to constitutively release (E)–b–- caryophyllene compromises plant development, appa- rencyto leaf herbivores, andyield [98].Furthermore,a constitutivereleaseofEPNattractantmaydisturbEPN host location. A second approach yielding promising results is the release of EPN-infected cadavers in the field.Theuseofcadaversconfersseveraladvantagessuch as enhanced EPN protection against unfavorable envi- ronmentalconditions[99],betterdispersalandvirulence [100,101],attraction of herbivores [12,13],andinduc- tion of plant defenses [102,103]. The effect of EPN- infectedcadaversonplantsremainstobefurtherinvesti- gatedtoassesspossiblefitnesscostsontheplants,asthe volatilesorchemicalsreleasedfromcadaversmayinduce unnecessary and costlyplant defenses. Third, encapsu- latingEPNsinashellcoveredwithherbivoreattractants andfeeding stimulantssuccessfullyincreasedherbivore control in the field [104,105]. Fourth, EPN selective breeding can increase EPN responsiveness to specific cues[62].Despiteminortrade-offsbetweenresponsive- nessandinfectiveness,selectedEPNstrainsweremore effective than original strains in controlling herbivore pests in thefield [62]. Finally,EPN previous exposure to insect cues or EPN pheromone increases their host- findingandinfectivity[66,67,68].Thesestudiesprovide promising strategies to develop potent biocontrol strategies.
Conclusion
The effortof the research community in characterizing thecues involved in EPN host-seeking hasresulted in considerableprogressinthefieldandhassetsolidfoun- dations for future research. The identification of info- chemicalsshapingEPNforagingbehaviorisinitsyoung
age but already demonstrated the large variability of responseamongandwithinEPNstrains.Werecommend a thorough and concerted effort in standardizing and reporting experimental conditions. For example, some factorssuchas EPN origin,age, or previousexperience (rearing conditions) should be reported in all studies.
Such endeavor will not only allow theidentification of furtherkey infochemicals for EPN foragingbut also of modulators of EPN response. Possible modulators highlightedin thisreview include hierarchicalorders of signalintegration, EPN specialization degree, selective pressure,age,andexperience.Understandingthechem- icalecologyofentomopathogenicnematodesispivotalto developpowerful,sustainable,strategiestocontrolinsect herbivoresin agriculture.
Authorcontributions
X.Z. and CAM.R. wrote the first draft, reviewed, and edited the manuscript. L.L. and L.K. edited and reviewedthemanuscript.
Conflictofintereststatement Nothingdeclared.
Acknowledgements
WethankPierreMate´oforhiscommentsonapreviousversionofthis manuscript.TheworkofX.Z.andL.L.issupportedbytheProgramof IntroducingTalentsofDisciplinetoUniversities(111Project,number D16014)ofHenanUniversity.TheworkofCAM.R.andL.K.issupported bytheSwissNationalScienceFoundation(projects310030_189071and 310030_192564).
Referencesand recommendedreading
Papersofparticularinterest,publishedwithintheperiodofreview, havebeenhighlightedas:
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