2405 9 B. 4–6 13–15 18 leaf position, T. vaporariorum 8 , Moreover, the ultra- and the greenhouse B. tabaci and certain volatile com- 10–12 a 16 Furthermore, whiteflies can discrim- Bemisia tabaci, indicates an olfactory function. 7 using transcript analysis, and accessions. The whitefly olfactory system is so highly developed that 4 17 . Aleyrodes proletella Correspondence to: S Schlaeger, Biointeractionsment, and Rothamsted Crop Research, Harpenden Protection AL5 Depart- 2JQ, UK. E-mail: [email protected] Biointeractions and Crop Protection Department, Rothamsted Research,enden, Harp- UK School of Chemistry, University of Cardiff, Cardiff, UK B. tabaci In this review, we focus on plant-produced, volatile semiochem- and Michael A Birkett ∗ a b In behavioural bioassays,potential whitefly host plants preference and varies even between among host plant varieties, it can even differentiate between stereoisomers of VOCs. icals and their potential application inaim whitefly of management. this The review is toand identify encourage gaps in work whitefly olfaction onsively research this on topic. economically The important literature whitefly focuses species exclu- and biotypes cultivars colonization and virus infection. Odorant-binding and chemosensory proteins have been detected in pounds have been shown to bindtabaci to chemosensory proteins of structure of certain antennal sensilla of inate between differentfor qualitative example, differences conditions in nitrogen in fertilization, host plants, and b Cucumis published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Management of 1 ), particularly by act- published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. ), cucumber ( John A Pickett , are important economically in agriculture. Whiteflies are controlled mainly by synthetic and the greenhouse whitefly, a* new interventions are urgently 2 Citrullus lanatus , are common agricultural pests that Semiochemicals are detected by 3 Pest Management Science Bemisia tabaci, Solanum lycopersicum Pest Management Science whitefly; semiochemicals; volatile organic compounds; repellents; olfaction; pest control Trialeurodes vaporariorum

)andwatermelon(

© 2018 The Authors. This is an open access articlemedium, under provided the the terms original of work the is Creative properly Commons cited. Attribution License, which permits use, distribution and reproduction in any damage a widesuch range of as economically tomato important crop ( plants, Trialeurodes vaporariorum 1Whiteflies INTRODUCTION (: :the tobacco Aleyrodidae), whitefly, including sativus ing as vectors of devastating plant viruses. Abstract Whitefly (Hemiptera: Sternorrhyncha: Aleyrodidae) pests, including the tobacco whitefly, pests Stefanie Schlaeger, plant semiochemicals, compared with related (wileyonlinelibrary.com) DOI 10.1002/ps.5058 Prospects for management of whitefly using Review Received: 2 March 2018 Revised: 27 April 2018 Accepted article published: 2 May 2018 Published online in Wiley Online Library: 13 June 2018 olfactory organs, whichOlfaction are was not mostly thoughthost located plant to selection on play until a the theresearch beginning prior significant to of antennae. that role the focusing 21st in mainly on century,increasing whitefly whitefly numbers with vision. of studies However, have shown that whiteflyis behaviour affected by plant-emitted volatile organic compounds (VOCs). needed. Semiochemical-based approaches areronmentally benign considered alternatives to envi- the use ofsemiochemicals insecticides because act only as signalsdeployed. and are Semiochemicals not toxic also atrole have the and, levels an although essential theirselection for evolutionary use resistance, other related in semiochemicals would pestto need management evolve could in cause targeted. order to Newly fulfil evolvedand the chemicals used rationally crucial could to replace signalling semiochemicals be tohad role which readily previously resistance originally evolved. identified whitefly populations relies predominantly onbroad-spectrum the synthetic deployment insecticides, but of becauselution of rapid in evo- insecticide resistance, whitefly, insecticides but resistancealternative to to these theWhitefly is use behaviour evolving of is rapidly. insecticides, affectedsemiochemicals, by A by but differences in exploiting semiochemical-based in only naturalApplication plant management a of odour volatile few strategy antennal studies blends. signalling could preparation have Selected(Hemiptera: processes potential methods compounds provide Psyllidae), volatiles from to have may an been closely been help manipulate characterizedthe related suggested to by insect families, repellent facilitate as electrophysiology behaviour. the whitefly putative or or electroantennography. olfactometry. attractantto Behavioural (Hemiptera: be effect bioassays ) evaluated are of and in essential eachdemonstrated psyllids the to in semiochemical. respective identify the The cultivation field, system. relevancethe there Although olfactory of is system the of an semiochemicals value whiteflies emerging needs in of© range to 2018 whitefly semiochemicals be of The elucidated Authors. against management possible in more whiteflies field needs detail. has applications not and been some promising prospects.Keywords: Overall, Here, the 27 : 2405–2411 This method, biotypes, but 74 29 No absolute num- 2018; lasted longer with a 30 . B. tabaci 27 This technique can help to 23 Aphis fabae Pest Manag Sci Trioza apicalis The whole-insect preparation reduces the 28 was higher with a longer recovery time when using 13,30,31 . Overview of the technical set up of a gas chromatography–flame A. fabae Overall, research on whitefly olfaction would benefit from A further technique for investigating the olfactory response of receive antennal responses when there is a lowas number shown of sensilla, in the carrot psyllid more electrophysiological studies. GC–EAGcollection analysis can of a greatly volatile EAG-active facilitate VOCs are the detected by search insectaffect antennae for whitefly and semiochemicals. behaviour. most likely The EAGdose–response method tests can comparing also antennal bedoses responses used of at for the same different semiochemical.identify This the most investigation efficient can dose help for whitefly to management. towards semiochemicals utilizesings. single Here, sensillum record- the electricalrather than activity all sensilla of on one the antennal sensillum flagellum. is measured Figure 1. ionization detection coupled with electroantennography. study on the blackwhole-insect bean preparation aphid than with excised antennae. the whole-insect preparation technique. risk of drying antennae with the resistance increasinghigh to a for level measurements. too Another advantagelife of of the the antennal preparation longer is the usable option forery an extended recov- time between singleness of stimulations. The antennal responsive- aphid is immobilized using a copper wiresuccessful restraint. approach that A involved different fixing and insects within pipettewas tips used for psyllids, where whole-insectfor preparations GC–EAG were used and EAG. ber of antennal sensillathe was study presented indicates a in similar sparse sensillarT. apicalis set-up compared with alone and in combination withaphid GC, olfaction has research been and used more recently forcessfully has decades in been psyllid in applied olfaction suc- research. 4,23 The 21,22 5 adults © 2018 The Authors. 24 were puffed B. tabaci www.soci.org S Schlaeger, JA Pickett, MA Birkett The longevity of the published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. The technical set-up of 26 7 High-resolution gas chro- S. peruvianum 22 are extreme generalists and Thus, the method is not yet but here they are compared and 18 ght be repellent compounds. Fur- In these, excised antenna of The bioactive compounds are then further Pest Management Science T. vaporariorum 7,18 25 T. vaporariorum, An expedient approach to identifying whitefly and and 19,20 B. tabaci wileyonlinelibrary.com/journal/ps 2.2 Whitefly electrophysiologyUsually towards semiochemicals an extract of collectedand plant diverse volatiles includes range a oflikely complex compounds, to but have only a a semiochemical subset role. of them is Principal component analysis ofhelpful the to volatile identify collections putativeVarious may semiochemicals techniques for be within collecting plant a volatiles mixture. areas available, such solvent extraction, steam distillation or air entrainment. 2.1 Isolation ofBemisia putative semiochemicals tabaci 2 IDENTIFICATION ANDPLANT-EMITTED EVALUATION OF SEMIOCHEMICALS thus must be able to detect thehost different volatiles plants. specific to many of with other hemipterous pests in thecha, suborder the of the aphids Sternorrhyn- (Hemiptera:Psyllidae). Aphididae) All and adults psyllids of these (Hemiptera: plants families and are are phloem-feeders vectors on of host plant pathogens. matography (GC) coupled with electroantennographyand (GC–EAG) a detector (e.g. flamefor ionization the detector) identification is of apounds semiochemicals powerful (Fig. 1). within tool Here, a the blendat ability the of of olfactory com- a level compoundtion is to caused be indicated perceived by by a olfactoryon measured receptor the voltage neurones deflec- antennae. localized in sensilla EAG preparation might be increased by a differentration antennal prepa- technique, for example a whole-insect preparation. An EAG identified by GC-coupled mass spectrometry and/ornetic nuclear resonance mag- spectroscopy after purification by preparativeHowever, GC. no GC–EAG studyto with date. whiteflies Apparently, has EAG beenflies. is published Among not the a studies favouredEAG on measurements. technique whitefly for olfaction, white- only two include adapted sufficiently for whiteflies to identify activeGC–EAG. compounds by Whitefly electrophysiology might learnongoingresearchonaphidolfaction,inwhichGC–EAGandEAG from the longer are used widely to detect semiochemicals. were mounted on a custom-madeemitted holder and from volatile less-preferred terpenoids accessions ofSolanum the pennellii, wild S. tomato habrochaites plants individually over the antenna. Excisedremain whitefly viable antennae did for not thea duration collected plant of volatile a extract. GC–EAG experiment using thermore, it is important to includeproportions compounds that because differ in the their ratio of compounds can be crucial. semiochemicals is to compare the volatileent physiological collections conditions from of differ- the hostbehavioural plant responses that from whiteflies. evoke For example, different VOCs released from less-attractive plants mi latter is preferred because headspace collectionsreleased represent quantities actual of naturally occurring compounds. Inthis addition, non-destructive sampling methodcompounds formed does by damaged not plant tissue. riskleaf For extracting example, volatiles green aretomato detected plants after mechanical wounding. only in headspace collections from the sampling method, e.g. the choice of adsorbentto material, be needs investigated to achieve the best possible outcome.

2406 2407 The four-arm 10,41 In this experimental set-up, 39,40 wileyonlinelibrary.com/journal/ps published to date. These investigate the B. tabaci Designs of different dual-choice olfactometers. The directions for (A) (B) (C) The four-arm olfactometer (Fig. 3) is a different device in insect Figure 2. the whitefly’s choices and the locations of the stimuli/control are illustrated. and attractancy shouldcontext. be used with cautionolfactometry and and always a standard in either bioassay repellents in and attractants. aphid studies used for olfactometer might have received little considerationbioassays for because whitefly its designall requires insects arms. to Whiteflies actively areFor explore example, known they to fly up fly thethey host over plant may even when actively disturbed. short However, walk(Schlaeger distances. S, in personal a observation). four-arm or Y-shaped olfactometer the insect can move freely withinwith an respective airstreams. arena There divided have been into 2 four four-armter areas olfactome- tests with effect of odour masking of non-host plantsvolatiles or aphid-induced plant rather than selected semiochemicals. 38 This might 38 The terms repellency published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. 5,6 However, none of the stud- the junction into one of the 36,37 actants are evaluated based on via : 2405–2411 © 2018 The Authors. Pest Management Science 74 2018; branches. Their choice is evaluated by the numbereach of of individuals in the decision chambers. Thesay Y-shaped is performed olfactometer using bioas- a directed, charcoal-filtered andairstream humidified (Fig. 2C). Here, whiteflies are alsothe released olfactometer. at They the need base of tochoice. walk Their to preference the is junction evaluatedindividuals by and that counting make entered the a the number respective(e.g. of moving channel at in least a one third defined intolency way olfactometer the tests respective predominate channel). because of Repel- the greaterest inter- in preventing the settlement ofplants viruliferous (Table whiteflies 1). on Two types crop been of olfactory-mediated defined repellents depending have on their effect on insect behaviour. Pest Manag Sci So-called true repellentsfrom cause the odour source, insects whereas odour-masking to repellentsor reduce actively disrupt the move attractivenesstrue away repellents of using the a hostbecause Y-shaped whiteflies plant. olfactometer may Investigation might not be of enter difficult the choice region. Management of whitefly using plant semiochemicals2.3 Evaluationsemiochemicals of whitefly behaviour towards EAG studies do notfied reveal plant-emitted the semiochemical, i.e. behavioural whether activityan it of attractant. is an a For repellent identi- this, or needs to insect be evaluated, for behaviour example in towards antometers olfactometer assay. olfactory Olfac- are cues sealed deviceswithout directed with airstreams providing different a odour sources. The systeminsect of www.soci.org is channels released with intodecide or the between channels system permeated with where the test it odourthe and can solvent with move or with freely airsemiochemicals and alone. to A the solvent is releaseserves often as device needed a (usually to control. apply filter Evaluationon of paper) the insect and choice behaviour canchannel. of be It channel based is or expectedchannels on that containing the the insect an time will attractantvent/air, spent respond and stimulus in positively positively compared to a to withpared particular channels with sol- a containing repellent stimulus. solvent/air Therecedure is com- wide for variation measuring in whitefly the pro- responsesthe to number semiochemicals (e.g. of whitefliestometer released, or the the dimensions evaluationcompare of studies. method the However, olfac- used), dual-choice makingwhich olfactometers it the (Fig. 2), difficult insect in to choosesing the between stimulus two and one channels containingbeen only (one used the contain- solvent in or air),VOCs all have (Table tests 1). A with tubularwhiteflies whiteflies olfactometer are is responding released a into to linear the devicefreely individual middle in in of either which the direction (Fig. tube 2A). and Theducted can behavioural without bioassay move airflow. is The con- tested airbornebeen semiochemicals have considered as repellentsevaluation using method the (Table avoidance 1). index Thisflies as index in the is the repellent the zone numberflies subtracted in of from the white- control the zone number dividedcounted. of by Bioassays white- the in total number the ofwithout T-shaped whiteflies an olfactometer airstream are (Fig. 2B). conducted of Whiteflies are the released device at and the need base to move ies has addressed whitefly behaviourevaluating towards an a true oriented repellent movement by Overall, away whitefly from repellents the or odour attr the source. proportion ofvent responding used or whiteflies clean in air. Thewhitefly relation behaviour degree is of also dose-dependent. to the semiochemical the effect on sol- be resolved by including the response(responders rate for vs. all non-responders) tested whiteflies or excludingset responses minimum from below the a evaluation. 43 Phaseo- Synthetic : 2405–2411 plants emit 42 Encarsia for- 74 )-4,8-dimethyl- E 2018; than the In a Y-shaped olfactometer, 43 . E. formosa -infested bean plants, )-3-hexen-1ol, ( Arabidopsis thaliana Pest Manag Sci Z B. tabaci towards plant-produced, individual volatile organic T. vaporariorum plants attracted more , than from plants that are not infested. in wind tunnel bioassays. Bemisia tabaci An indirect but important approach to control whiteflies is lus vulgaris 1,3,7-nonatriene (DMNT) and 3-octanonequantities are from emitted in higher whitefly behaviour. For instance, thecrop plant might visual override the attractiveness effect of a of hostlent. odour-masking the In repel- general, all potential semiochemicals mustrespective be cultivation tested system for in their the relevance in whitefly control. Under field conditions, whitefly semiochemicals are exposedtypes to all of odorants from thesemiochemical environment. might be The diminished effect in of a a mixture of whitefly VOCs. to identifyural plant-mediated enemies. semiochemicals For that example, attract ( nat- 3 POSSIBLESEMIOCHEMICALS APPLICATION OF TO WHITEFLY MANAGEMENT Keeping whitefly infestation onthreshold crop level is plants part below of an an integratedThe pest economic management settlement strategy. and feedingenough of for one virus transmission individual because the on vectored a virus diseases crop plant is odour of plants that were not treated with the semiochemical. application of syntheticA. myrcene thaliana to the odour of non-infested versions of these VOCs, when presented individuallyincreased or the in a attractancy blend, ofmosa, the whitefly , myrcenewhenattackedby © 2018 The Authors. www.soci.org S Schlaeger, JA Pickett, MA Birkett published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. )-Limonene)-Limonene)-Limonene Attractancy Repellency Repellency Preference Avoidance index Avoidance index 5 6 )-Limonene 32 Repellency Response 37 )-Caryophyllene)-Ocimene Attractancy Repellency Preference Avoidance index)-2-Hexenal 5 6 Attractancy Response/attraction rate 36 -Pinene*-Pinene* Repellency Repellency Avoidance index Preference 32 33 R E R E R E R 𝛼 𝛼 Pest Management Science Overview of olfactometer tests evaluating the behavioural response of Design of a four-arm olfactometer. The four areas of the arena for In contrast to evaluation of a true repellent, experimental set-ups compounds Type of olfactometer Compound Stated effect Evaluation method Reference *Isomeric composition not given. T-shapedTubularTubularTubularTubularTubular ( Tubular TubularY-tube MyrceneY-tube ( Y-tubeY-tube Limonene*Y-tube CitronellalY-tube CitralY-tubeY-tube Geranyl Repellency nitrileY-tube 2-Ethyl-1-hexanol* o-Xylene Repellency Phenol RepellencyY-tube Salicylic Attractancy acid Repellency Avoidance index Repellency Limonene* 1,8-Cineole Avoidance Linalool* index ( Repellency Avoidance index Attractancy Preference Repellency Avoidance index Avoidance index Repellency Geranyl nitrile Repellency 6 Preference Attractancy 32 Preference Preference 32 Preference Repellency Residence time 32 32 33 Residence time Response 33 33 34 35 34 35 37 T-shaped ( TubularTubular ( ( Y-tubeY-tubeY-tube 3-Hexen-1-ol* Limonene* ( Attractancy Repellency Response/attraction rate Response/attraction rate 36 36 Table 1. for host odour-masking repellents shouldted by include the volatiles host emit- plant.that In might also addition, interfere the with crop the plant effect has of visual the cues semiochemical on wileyonlinelibrary.com/journal/ps Figure 3. the whitefly’s choices and the locations of the stimuli/control are illustrated.

2408 2409 T. adults in Wild tomato 54 is of particular B. tabaci A promising attempt 53 This approach is now A. proletella 55 . Few studies deal with The repellent property against Application of 7-epizingiberene 54 7,18 , feeding primarily on cruciferous wileyonlinelibrary.com/journal/ps although B. tabaci Introduction of the biosynthetic path- 18 )-germacrene D and has led to the rational S A. proletella 3 accession PI127826 is naturally less attractive to -farnesene from the plant (emitted continuously) T. vaporariorum or 𝛽 )- species could be more advantageous because of the E and releases distinct quantities of the sesquiterpene and was not investigated with the transgenic lines in this For a better general understanding, it might be useful to broaden Semiochemicals can be expensive to synthesize and may be release of ( and release from the aphidlar (sudden trichomes are burst sources release). of semiochemicals, Plant makingfor glandu- them genetic targets engineering in pest resistance. to cultivated tomatoa reduced free-choice settlement bioassay. of interest because it is a specialist in comparisonB. with the generalists tabaci vaporariorum ACKNOWLEDGEMENTS This review was supportedwork by at BBSRC Rothamsted grant(SCP) BB/M023729/1. forms strategic The part programme (BBS/OS/CP/000001) of funded the through Smart Crop Protection 4 CONCLUSION Plant-produced VOCs can alter whitefly behaviour, but fewhave studies investigated the effects ofcals the through electrophysiology actual and putative behavioural semiochemi- workflies. with More white- information about theneeded, olfactory for system of example whiteflies which is sensillaThis knowledge are is responsible necessary for to identify olfaction. semiochemicalsquent for use subse- in whitefly management. the research on whiteflyimportance olfaction to in other addition species of to economic B. tabaci study. chemically unstable, which isA unfavourable possible for approach to field overcome application. thesedesign challenges of is the analogues rational ofsynthesis. semiochemicals In using chemoenzymatic thisstrate by method, the acceptance specificallyto responsible of analogues biosynthesis enzyme of the leads properties. the unnatural natural Successful sub- product usehas that of recently might this have beensemiochemical synthetic superior demonstrated ( biology for approach the aphid sesquiterpene being tested with theand whitefly its semiochemical biosynthesis 7-epizingiberene thetic enzyme, pathways epizingiberene for production synthase.potential of Biosyn- of the new beingthe analogues engineered have library into the of cropwidened. plants The semiochemical availability and tools ofopportunity therefore for a to wide mitigate whitefly range thesemiochemicals. management of evolution tools of provides whitefly an resistance to way of 7-epizingiberene into the glandularvated trichomes tomato of with the trichome culti- specific promotorsof led to this production whitefly semiochemical. to modify semiochemical biosynthesismanagement has in been shown trichomes in cultivated for tomato. whitefly S. habrochaites B. tabaci hydrocarbon 7-epizingiberene. plant species. In addition,Trialeurodes semiochemical interventions against higher value of glasshouseproduction. products in comparison with arable discovery of novel semiochemicals. 44 In 48 ,the D. citri ) or Greek The most , for up to , reduced 51 It has been Cymbopogon Furthermore, 47 49 . and sweet C. sinensis citri published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. , the causative agent settlement on tomato Psidium guajava C. sinensis , because of the confined Coriandrum sativum However, the repellent effect This mode of direct pest man- -farnesene or methyl salicylate 52 50 -farnesene, which has been con- ) field centred on a wheat–pea )-limonene, citral and, as a slow 𝛽 𝛽 R )- B. tabaci )- E ) strip intercropping system reduced sprays or slow-release dispensers. E ) plants, or a citronella grass ( via , Murraya paniculata , in a four-arm olfactometer bioassay. T. vaporariorum infestation of tomato plants was reduced by : 2405–2411 © 2018 The Authors. Pest Management Science 74 Where economically viable, another possibility 44 2018; 45 Triticum aestivum Application of the sesquiterpene hydrocarbon and B. tabaci The potential of using a push–pull strategy for 32 Candidatus asiaticus Citrus sinensis This strategy is especially suited to the control of green- 46 Ocimum minimum 44 )-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT). A synthetic Semiochemicals can be integrated into a cropping system using Semiochemicals are an important component of push–pull A different approach to the deployment of semiochemicals is to T. aestivum–Pisum sativum E,E plants was reducedtles in with a a 1% greenhouse mixture experiment of using ( bot- aphid infestationaphids. and increased the number of parasitized Pera D6, mixture of DMNThosts and TMTT orange reduced jasmine the attractiveness of the for field application ofof active semiochemicals synthesized is the VOCs deployment cultural practices, e.g. intercropping with semiochemical-emitting plants. Adult intercropping with either coriander ( basil ( spec.) mulch. space involved. house pests, such as Pest Manag Sci release agent and antioxidant,as olive the oil (in ‘push’treatment. a treatment, ratio and of 63 yellow : 7 sticky : 30) traps as the pull No field studiesbeen with reported. selected whitefly However, semiochemicals have Management of whitefly using plant semiochemicalsare systemic, affecting the whole plant. Thus, theold economic thresh- is very low. Consequently, the odour-maskinglent effect is of a not repel- sufficient, because whitefliesplant. may To still control land whitefly on virus thevents crop vectors, whitefly colonization a almost true completely is repellent preferred. that pre- technology that combines repellentssame and cropping attractants system. within The the pest(push)andatthesametimeluredtoamoreattractivesource www.soci.org is deterred from the(pull). crop plant dimethyl disulfide released from polyethylene vials reduced infestation in an orchard of Valencia4 weeks. oranges, modify the emitted VOCs of the crop plantsuch by genetic that engineering, the plant ismasking) either or not becomes attractive repellent. to pest insects (odour management of the Asian citrus psyllid agement can be supplementednatural with enemies the for attraction of conservation beneficial biological control. in a paraffinin oil a formulation wheat released ( from a rubber septum aphid alarm pheromone ( ( on aphids could noteffect be in confirmed the in fielding field might the trial. be studies. Another explanation due might The be to the missing difference bad between weather conditions dur- stated that moreneeds knowledge to about beperformed. generated psyllid–host However, before interactions been potential more identified, applied psyllid for( studies semiochemicals example, can have the be homoterpenes DMNT and firmed in laboratory bioassays. prominent example of thisof strategy elite to wheat date to is release the ( engineering Y-shaped and four-arm olfactometeridentified assays, from dimethyl the disulfide, non-host guava, of citrus greening disease, has been reviewed. vector of the attractiveness of volatiles from Ento- Chem ,Iden- JInsect :85–92 JChem Crop Prot :373–391 35 . , Reducing et al. (Hemiptera: :1605–1611 58 Chem Senses : 2405–2411 , The salicylic Bemisia tabaci 72 74 et al. et al. , Odor, not perfor- :164–173 (2010). 2018; :238–254 (1998). et al. -Plant Interact 136 81 Bemisia tabaci :9329–9334 (2000). :709–716 (2017). Phytochemistry 97 Arthropod Struct Dev Oikos Annu Rev Entomol :269–274 (2005). 11 to three maize, potato, and wheat :19–27 (2014). 10 :22140 (2016). Pheromone Signaling: Methods and :127–142 (2016). 6 :146 (2017). ’s selection between healthy and virus Pest Manag Sci :1048 (2016). 150 (Homoptera: ) antennae – an 26 8 17 :183–190 (2014). Entomol Exp Appl 8 Sci Rep -jasmone as an insect semiochemical and in Chem cis :2–9 (2012). Trends Plant Sci :241–253 (2015). 37 Front Physiol Bemisia tabaci Int J Mol Sci Proc Natl Acad Sci USA biotype B. Trioza apicalis . 157 Rhopalosiphum padi Entomol Exp Appl :919–928 (1998). :325–338 (2016). Arthropod–Plant Interact , ed. by Touhara K. Humana Press, Totowa, NJ, pp. 157–177 44 :1589–1600 (2003). ,Newrolesfor 41 , Aspects of insect chemical ecology: exploitation of reception , Prospects for repellent in pest control: current developments 29 :709–723 (2001). :759–769 (2008). et al. :393–403 (2015). (2013). et al. (2011). smells better than citrusLiviidae). to females of and collaborative research20 projects for volatile situation. orous insects – finding the right mix. volatiles: a comparison of methods. proteins, and degrading enzymes. Physiol Formic and acetic acidselicit in olfactory and degradation behavioral responses products from an of insectSenses vector. plant volatiles recording in insect antennae, in Protocols (2013). istics of ator tiny neurons but of carrot specialized33 psyllids olfactory (Homoptera: system: Triozidae). olfactory recep- sillar array on cultivars and the selection ofmol prospective Exp Appl crop border plants. of tomato volatiles by corianderBemisia volatiles tabaci in host plant selection of and detection as tools for deceptionPhysiol of Entomol pests and beneficial insects. adaptation to high stimulus levels? (2006). of plant volatiles(Gennadius) as on tomato. repellents to control whitefly and Yasudahost-locating T, response in Volatiles theEcol parasitoid, from Encarsia formosa. whitefly-infested plants elicit a mance, dictates acid-mediated release of plantBemisia volatiles tabaci affects the host choice of Volatile organic compounds emitted bythe behaviour bottlebrush of species the sweet affect potato9 whitefly. infected plants. tification of plantArthropod-Plant Interact chemicals attracting and repelling whiteflies. whiteflies on cucumbervegetables. using intercropping with less preferred et al. and future challenges. JL plant defense. responses of 26 Pickett JA, Aradottir GI, Birkett MA, Bruce TJA, Chamberlain K, Khan ZR 23 Beloti VH, Santos F, Alves GR, Bento JMS and Yamamoto PT, Curry leaf 20 Oliveira MRV, Henneberry TJ and Anderson P, History, current status, 21 Bruce TJA, Wadhams LJ and22 Woodcock CM, Bruce TJA and Insect Pickett JA, host Perception of location: plant volatile a blends by herbiv- 24 Raguso RA and Pellmyr25 O, Leal Dynamic WS, headspace Odorant analysis reception in of insects: floral roles of receptors, binding 28 George J, Robbins PS, Alessandro RT, Stelinski LL and Lapointe SL, 29 Olsson SB and Hansson BS, Electroantennogram and single sensillum 30 Kristoffersen L, Larsson MC and Anderbrant O, Functional character- 31 Kristoffersen L, Hallberg E, Wallén R and Anderbrant O, Sparse sen- 41 Togni PHB, Laumann RA, Medeiros MA and Sujii ER, Odour masking 27 Park KC and Hardie J, An improved aphid electroantennogram. 32 DuWX,HanXQ,WangYBandQinYC,Aprimaryscreeningandapplying 42 Birkett MA, Chamberlain K, Guerrieri E, Pickett JA, Wadhams LJ 33 Chen G, Su Q, Shi X, Liu X, Peng Z, Zheng H 35 Sacchetti P, Rossi E, Bellini L, Vernieri P, Cioni PL and Flamini G, 34 Shi XB, Chen G, Tian LX, Peng ZK, Xie W, Wu QJ 36LiYF,ZhongST,QinYC,ZhangSQ,GaoZL,DangZH 37 Zhao Q, Zhu JWJ, Qin YC, Pan PL, Tu HT, Du WX 38DeletreE,SchatzB,BourguetD,ChandreF,WilliamsL,RatnadassA 39 Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin 40 Schroder ML, Glinwood R, Webster B, Ignell R and Kruger K, Olfactory , et al. Bemisia (Genna- © 2018 The Authors. Ann Appl Aleyrodes :145–160 :e0177483 Front Plant ,Identifica- New Phytol Trialeurodes Trialeurodes Trialeurodes (Hemiptera: L.) is associ- 24 :1285 (2017). Ecol Entomol 12 8 Aleyrodes pro- . J Econ Entomol et al. www.soci.org S Schlaeger, JA Pickett, MA Birkett -curcumene act as MED by head tran- , Biotype character- :133–143 (1995). R Appl Entomol Zoolog 24 PLoS One Bemisia tabaci and associated natural et al. published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. :68–73 (2011). Trialeurodes vaporariorum Bemisia tabaci 72 Front Plant Sci Bemisia tabaci Bemisia tabaci Rosmarinus officinialis :225 (2016). :259–269 (2014). (Hemiptera: Aleyrodidae). 8 Bemisia tabaci chemosensory proteins: role of CSP in :e0154706 (2016). Int J Insect Morphol Embryol 151 11 Phytochemistry (MEAM1; B biotype): a Neotropical scenario. :e0171739 (2017). Viruses :13697 (2015). 5 12 (Homoptera: Aleyrodidae). :e0121820 (2015). :88–99 (2018). Int J Insect Morphol Embryol :925–935 (2009). 10 Pest Management Science Bemisia tabaci PLoS One (Hemiptera: Aleyrodidae) biotype Q. (Westwood), the glasshouse whitefly, and (Westwood), the glasshouse whitefly, to tomato and eggplant. Sci Rep 172 151 Bemisia tabaci PLoS One (Linnaeus), the cabbage whitefly, (Homoptera: Aleyrodi- Entomol Exp Appl , Tomato infection by whitefly-transmitted circulative and Bemisia tabaci :155–171 (2014). PLoS One (Linnaeus), the cabbage whitefly, and . et al. :466 (2017). , Tomato-produced 7-epizingiberene and Bemisia tabaci 165 :856–870 (2016). :1307–1316 (2017). 8 :260–267 (1999). :561–570 (2014). repellents to whiteflies. vore: experiments with24 the whitefly, letella insect defense. et al. proletella dae).Part2:ultrastructure. dius), the tobacco whitefly (Homoptera:nal Aleyrodidae). morphology. Part 1: exter- tion and expression profile analysischemosensory of odorant protein binding genes protein in and (1995). vaporariorum vaporariorum RNA viruses that affectBiol intensive vegetable production. scriptome. ization, developmental profiling, insecticide responseproperty and of binding Ann Appl Biol RNC, Insecticide resistancewhitefly and control failure likelihood of the application in agriculture:212 successes and challenges. Volatile-mediated attraction ofvaporariorum greenhouse whitefly Whitefly attraction to rosemary ( ated with volatile composition and quantity. (2017). Bemisia tabaci 110 The role of specific tomato volatilesPlant in Physiol tomato–whitefly interaction. level of nitrogen makesattracting tomato more plants releasing lessSci volatiles and tion of tomato leaflets byand two whiteflies, 49 tiveness of tomato plantsenemies. to in chilli affect preferences of the whitefly, Aleyrodidae). non-circulative viruses induce contrasting changes in plantand volatiles vector behaviour. the antennal sensilla ultrastructure of two cryptic species in NKP tabaci 1 Navas-Castillo J, Lopez-Moya JJ and Aranda MA, Whitefly-transmitted 2 Dângelo RAC, Michereff-Filho M, Campos MR, da Silva P and Guedes 3 Pickett JA and Khan ZR, Plant volatile-mediated signalling and its 4 Darshanee HLC, Ren H, Ahmed N,5 Zhang ZF, Sadeh D, Liu Nitzan N, Shachter YH A, Chaimovitsh and D, Dudai N Liu and Ghanim TX, M, 6 Tu HT and Qin YC, Repellent effects of different celery varieties in 7 Bleeker PM, Diergaarde PJ, Ament K, Guerra J, Weidner M, Schutz S 9 Tsueda H, Tsuduki T and Tsuchida K, Factors that affect the selec- 8 Islam MN, Hasanuzzaman ATM, Zhang Z-F, Zhang Y and Liu T-X, High 19 Bernays EA, When host choice is a problem for a generalist herbi- 18 Bleeker PM, Diergaarde PJ, Ament K, Schutz S, Johne B, Dijkink J 16 Wang R, Li FQ, Zhang W, Zhang XM, Qu C, Tetreau G 15 Mellor HE and Anderson M, Antennal sensilla of whiteflies: wileyonlinelibrary.com/journal/ps REFERENCES Biotechnology and Biological Sciences Researchtrial Strategy Council’s Challenge Indus- Fund. 17 Liu GX, Ma HM, Xie HY, Xuan N, Guo X, Fan ZX 10 Tan X-L and Liu T-X, Aphid-induced plant volatiles affect the attrac- 11 Saad KA, Roff MNM, Hallett RH and Idris AB, Aphid-induced defences 13 Zhang XM, Wang S, Li S, Luo C,14 Li YX Mellor and HE and Zhang Anderson M, F, Antennal sensilla Comparison of whiteflies: of 12 Fereres A, Penaflor M, Favaro CF, Azevedo KEX, Landi CH, Maluta

2410 2411 Proc Natl :404–414 Chem Com- 35 Curr Opin Biotechnol :17077–17103 (2012). :59–67 (2014). J Appl Entomol 13 19 :11183 (2015). 5 wileyonlinelibrary.com/journal/ps Int J Mol Sci Sci Rep Curr Opin Plant Biol :20124–20129 (2012). 109 :7550–7553 (2015). , Novel olfactory ligands via terpene synthases. 51 , The first crop plant genetically engineered to release an insect , Improved herbivore resistance in cultivated tomato with the Kuwayama to host plant volatiles. et al. :169–176 (2003). (2011). insect resistance. friends to feast on foes: engineeringplants terpene emission more to make attractive crop to14 herbivore enemies. et al. pheromone for defence. MR, Plant glandular trichomes as targets for breedingof or engineering resistance to herbivores. et al. sesquiterpene biosynthetic pathway from aAcad Sci wild USA relative. citri JA mun 50 Birkett MA and Pickett JA, Prospects of genetic51 engineering for robust Degenhardt J, Gershenzon J, Baldwin IT and Kessler A,52 Attracting Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC, Doherty A 53 Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC and Kant 54 Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR 55 Touchet S, Chamberlain K, Woodcock CM, Miller DJ, Birkett MA, Pickett Funct :375–400 biotype B. Diaphorina 52 , Phloem-feeding , A push–pull strat- et al. et al. :397 (2018). https://doi published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. , is reduced by terpenoids Bemisia tabaci 44 Annu Rev Entomol :893–896 (2015). 71 JChemEcol Diaphorina citri :86–92 (2017). :93–103 (2018). 91 : 2405–2411 © 2018 The Authors. 162 Pest Management Science Pest Manag Sci 74 JPestSci 2018; :1304–1312 (2013). 27 Entomol Exp Appl egy to control aphids combinesreleases. intercropping with semiochemical psyllid control. Blassioli-Moraes MC, Attractiveness ofto the host Asian citrus plant psyllid, volatile extracts from the non-host cashew. .org/10.1007/s10886-018-0937-1. volatiles and dimethyl disulphide inhibit response of whiteflies can fool their hostEcol plants, but not their parasitoids. in integrated pest(2007). management. the selection of host tomato plants by 46 Xu Q, Hatt S, Lopes T, Zhang Y, Bodson B, Chen J 47 Yan HX, Zeng JW and Zhong GY, The push–pull strategy for citrus 48 Fancelli M, Borges M, Laumann RA, Pickett JA, Birkett MA and 49 Onagbola EO, Rouseff RL, Smoot JM and Stelinski LL, Guava leaf 45 Carvalho MG, Bortolotto OC and Ventura MU, Aromatic plants affect 44 Cook SM, Khan ZR and Pickett JA, The use of push–pull strategies Pest Manag Sci Management of whitefly using plant semiochemicals43 Zhang PJ, Xu CX, Zhang JM, Lu YB, Wei JN, Liu YQ www.soci.org