Insect Transmission of Plant Viruses: Multilayered Interactions Optimize Viral Propagation Beatriz Dader Alonso, Christiane Then, Edwige Berthelot, Marie Ducousso, J

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Insect transmission of plant viruses: multilayered interactions optimize viral propagation Beatriz Dader Alonso, Christiane Then, Edwige Berthelot, Marie Ducousso, J. C. K. Ng, Claus Martin Drucker

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Beatriz Dader Alonso, Christiane Then, Edwige Berthelot, Marie Ducousso, J. C. K. Ng, et al.. Insect transmission of plant viruses: multilayered interactions optimize viral propagation. Insect Science, Wiley, 2017, 24 (6), 10.1111/1744-7917.12470. hal-01602704

HAL Id: hal-01602704 https://hal.archives-ouvertes.fr/hal-01602704 Submitted on 26 May 2020

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect articleThis protectedis by copyright. All rights reserved. 10 Science but has yet to undergo copy This anis Accepted Article that has been peer from levels, organizational all integrating by transmission mediate plants host and viruses vectors, wa cell plant the by imposed impediment the and plants barrier separating spatial the overcome to strategies transmission sophisticated use Viruses viruses. plant Abstract Riverside, USA California, of University Research, Vector Disease for Center and Microbiology and Pathology Plant 1 and viral Dáder Beatriz optimize interactions multilayered viruses: plant propagation of transmission Insect REVIEW * Montpellier, France T Auhor running head: contributed equally INRA, UMR 385 BGPI (CIRAD BGPI 385 UMR INRA, itle itle .1111/1744 C

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By serving as vectors of transmission, insects play a key role in the infection cycle of many of cycle infection the in role key a play insects transmission, of vectors as serving By

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Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. fact, In host. new a of vessels and cells into directly viruses deliver can and parasites, feeding blood toward moving and seeking directionally and actively of capable are vectors water, or wind by distribution passive to contrary obvious: quite are toviruses help that entities biological vectors, on rely transmission horizontal of modes other All particles. solid other and dust on ride a hitching by dispersed are viruses other while hosts; new by inhaled s by produced aerosols within contained are viruses useinertsupportsvirusesreach infect to andhosts.new For example, humanrhinoviruses andother transmission, airborne In transmission. of category this to belongs also viruses, plant and fungal h animal, for reported as wounds, open through example for contact, indirect or direct by microbe among example, for (or medium new reach to matrix) extracellular the through movement Brownian by freely diffuse then and cells host lyse viruses case, simplest the In unrelated. potentially is that one even or species same the of another to host generation.Transmission behorizontal, canalso wherein istra the virus 1999) achiev is transmission, process, This host. another invade and reach to barriers spatial and physical cross to having of hurdle the overcome must viruses depleted, are resources host’s the and completed is th of spread applicable, where and encapsidation, multiplication, the for necessary infrastructures and energy the provide hosts The cycle. replication their of steps all for hosts eukaryotic or prokaryotic their on rely that parasites obligate are Viruses Introduction maig ht h ptoe pse fo a ifce poeio drcl t te next the to directly progenitor infected an from passes pathogen the that meaning , ed by using different but specific strategies. Transmission can be vertical be can Transmission strategies. specific but different using by ed bridge the distancethebetweentransmissionbridgesuccessThethe vectortwohosts.forof reasons Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

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Gutiérrez,2015;

ding to the vector and inoculation only by physical release from the latter, and the intermediate the and latter, the from release physical by only inoculation and vector the to ding et al.et - Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 like mouthparts of piercing of mouthparts like , 2016) - vector determinants of tra Drucker . Indeparture a from thesearchetypal reviews,presentwe here instead general a sts, leaving the punctured cells and tissues mostly intact and thus compatible forcompatible thus and intact mostly tissues andcellspunctured leaving the sts, (Overstreet Comment citer cedocument: &

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Zhou, 2015; Rosen . Recent reviews have provided thorough coverage thorough provided have reviews Recent .

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notwithstandi Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 - icltv tasiso (Kennedy transmission circulative (Watson g te nta epoaoy tgs f edn al nov sm fr o probing of form some involve all feeding of stages exploratory initial the ng, &

into the intestine. Virus particles (virions) contained in the ingested fluid are fluid ingested the in contained (virions) particles Virus intestine. the into

Comment citer cedocument: Roberts, 1939) or, to r to or, 1939) Roberts,

- referred to as the foregut. The advantage of binding to the stylets is that is stylets the to binding of advantage The foregut. the as to referred up to bind to the vector for retention and la andretention for the vector tobind to up - net neatos ht hav that interactions insect

t al. et eflect the fact that virions do not cycle through the through cycle not do virions that fact the eflect

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- Walker, sucking - Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. 2002) HC called phenomenon the enables This possible. is virions and HC of acquisition sequential virions, of independently vectors to bind HCs Since vector. the that shown been has it Furthermore, compl transmissible not. or HC the to complexed either forms, two in exist 2). (Table studied best caulim the and potyviruses various in identified (Pirone ligands vector to binding virion mediate to bridges molecular as HelperComponentscalled HCscontain (HCs). vector non encoded viral on this for relying indirectly, bind others directly, CMV non other for identified been also have ( interaction vector and/or stability capsid of determinants are CMV of protein coat the in regions specific example, For sites. binding vector specific as serve can proteins coat to unique epitopes that and mouthparts unfavorable including process transmission the throughout exist that dangers mouthparts mouthpa vector non that suggests species aphid 80 least at by transmitted family. insect another of members by not but family non a that in specificity vector no binding

particular prerequisites (from either the virus or the vector). Yet there is a conspicuous degree of conspicuousdegree a is there Yet vector). the or virus the either prerequisites(from particular , where a HC acquired initially by the vector assists in the transmission of virions located in thein located virions oftransmission the in assists vector the by initiallyacquired HC a where ,

to vector mouthparts is often considered as being similar to contact transmission, requiringtransmission, contact to similar being as considered often is mouthparts vector to Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 . The reason for this is certainly that the capsid protects the viral genome from potentialfrom genome viral the protectscapsid the that certainlyis this forreason The . t. ay non Many rts. - icltv tasiso i nt h rsl o te non the of result the not is transmission circulative Perry exes can form in infected plant cells, before or at the time of acquisition, or in or acquisition, of time the at or before cells, plant infected in form can exes rmral faue f helper of feature remarkable A Comment citer cedocument: et al. et , - circulative virus can be transmitted by several species of one insect one of species several by transmitted be can virus circulative 1998; - icltv vrss s ter asd o bnig o h vector the to binding for capsid their use viruses circulative

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ovirus & Perry, 2013). Capsid determinants of transmission of determinants Capsid 2013). Perry,

Murphy, 2009) Murphy, - bindingvirion and

For example, For

Cauliflower - eitd rnmsin s ht iin may virions that is transmission mediated - transcomplementat , but by no whitefly species. This species. whitefly no by but ,

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ion CM) ae been have (CaMV) (Froissart tis so oteins, (CMV) is (CMV) et al. et - , Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. mid the in encouraged to refer to the workZhou by the in morea For canals.salivary the andfood the of junction to posterior way localized are virions the since viruses such of transmission the mediate to 2011; Ng, unpub foregut for understood well less virus (ingested) streaming inward (Uzest other each to parallel run that canals salivary the and food the of convergence the by formed tips) frame credible a provides theory This respectively. release, and binding virus favor saliva secreted and sapsaliva/plant ingested in composition) fluid potential,redox (pH, conditionsbiochemical different bin with compatible be must and inoculated, are virions which from sites the also are sites retention the that is problem conceptual The cycle. non feeding, accomplishing other steps inreplication the cyclethe rest theof time. wh HC vector. only units transmission forming by the resources cell economize to serve well as just might it However, by probed plantssites plant different from units transmission host of assembly favors it because other in even or inc to speculated transcomplementationbeen has cells, other in cell, same The second binding sites for acquired virions are located deeper in the vector’s digestive system, digestive vector’s the in deeper located are virions acquired for sites binding second The follow foreguts or stylets the in retaining and ligands unknown still to binding After en they are needed, i.e. when vectors probe on plants, leaving the virions and HCs available for available HCs and virions the leaving plants, on probe vectors when i.e. needed, are they en work for workfor explaininginoculation the virions of boundcommon the to canal (locatedthe stylet at et al. et -

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 and the hindgut the and , 2007). This common region is constantly expos constantly is region common This 2007). , - icltv iue ut e ncltd no nw ot o opee h transmission the complete to host new a into inoculated be must viruses circulative lished). It would seem lesslished).dependable It alternating for ingestion/salivation processes Comment citer cedocument: (Brault - - on vrss ie whitefly like viruses borne containing plant sap or outward streaming saliva. The situation is situation The saliva. streaming outward or sap plant containing et al. et

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(2017) ig n rlae Te urn hptei i that is hypothesis current The release. and ding . Here, available immobilization times can be much be can times immobilization available Here, . rease diversity of the transmitted virus populationvirustransmitted the of diversity rease

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et al. et , 2015) , (Brault Comment citer cedocument:

et al. et (Kennedy

- . Interestingly, this protein is also involved in endocytosis of animal of endocytosis in involved also is protein this Interestingly, . , 1992), suggesting that viruses infecting phyla as different as plants, as different as phyla infecting viruses that suggesting 1992), , et al. et mediated and receptor and mediated et al. et , 2007; Ammar 2007; ,

oh noyoi sses o gut for systems endocytosis both , 1962) , Shlas 2010) (Schelhaas, , because the viruses cycle through the vector and vector the through cycle viruses the because ,

et al. et -

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or protein of the of protein or - ad lo o te nenlzto of internalization the for also and , insect interactions. The viral capsid iscapsidinteractions. viral insect The

net ue ie nml besides animals like use Insects . For this to happen, virions must virions happen, to this For . mission ndocytosis for the uptake of uptake the for ndocytosis - eool n hemocoel and hemocoel (Watson - Pea associated proteins associated &

enation

Roberts,1939)

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n aias vle idpnety iia srtge fr nenlzto. polm that problem A internalization. for strategies similar independently evolved animals and iaavt lgn virus lugens Nilaparvata fr o cruaie rnmsin novs h poaain f iue, eerd o as to referred viruses, of propagation the involves transmission circulative of form e Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 erstanding. However, we are clear about some of the benefits that the viruses derive viruses the that benefits the of some about clear are we However, erstanding. - icltv aqiiinrtnin wie nrclua cmoet ae sd for used are components intracellular while acquisition/retention, circulative t the plant Comment citer cedocument: - circulative viruses, with the situation for foregut for situation the with viruses, circulative

eeto ad nclto fr oh non both for inoculation and retention (Nakashima

NR) ht a b insect be can that (NLRV)

Noda, 1995)

(Nault, 1997) (Nault, te hn, s novd n h iouain f all of inoculation the in involved is hand, other

- circulative viruses spend retaining in their in retainingspend viruses circulative .

. Thus, there are a few insect viruses insect few a are there Thus, . - to - insect ve viruses are insect viruses that viruses insect are viruses ve - - associated proteins are involved are proteins associated icltv ad icltv virus circulative and circulative missibility. In addition, unlike addition, In missibility. - rnmte truh plant through transmitted - - borne viruses being less being viruses borne etr eemnns of determinants vector - cir uaie and culative Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. review will focus both,on beginning wi and body, vector’s the vector Ingwell by proposed (VMH) Hypothesis Manipulation Vector transmission. virus enhance that ways in phenotypes plant host p havestudies many Indeed, insects. by selection host change also principle, in can, it physiology, plant changes infection viral sinceand plant, the statusof physiological the influencedby be can steps these of Each sap. phloem surface, leaf the steps: four specie other to applies and stimuli different involving process responses complex a is insects by selection plant Host selection. vecinsectalterplants in virusinfectionhow well asconsider They host. plant and vector, virus, the between contacts molecular mere the beyond extends 2015) T Viruses modify vector performance and behavior to enhance transmission specialist strategies,respectively. non Thus, vector. suitable non of specificity vector lower much he continuum of processes occurring during insect during occurring processes of continuum he

- host interactions in two different manners: two ininteractions host (Fereres Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 ( 1) visual and chemical attraction to a host plant, host a to attraction chemical and visual ( ) rbn o eiems n mspyl ise, and tissues, mesophyll and epidermis on probing 3) &

oeo 2009) Moreno, s of the orders the of s ( 2) indirect effects mediated by viral interference with the host plant. This plant. host the with interference viral by mediated effects indirect 2) Comment citer cedocument: - icltv ad icltv tasiso mgt ersn gnrls and generalist represent might transmission circulative and circulative rovided evidence that viruses themselves might alter specific aspects ofaspects specific alter mightthemselves viruses that evidencerovided

Ti poes s best is process This . th the latter.th the - icltv vrss nacs hi cacs o none a encounter to chances their enhances viruses circulative Hemiptera

( or

1) direct effects due to the presence of virions invirions presenceof the to due effects direct 1) - mediated plant virus transmission (Ng transmission virus plant mediated Thysanoptera

tor behaviors associated with host planthostbehaviors associated with tor - ecie fr pis bt t basically it but aphids, for described ( t al. et 2) alighting and initial assessment of assessment initial and alighting 2)

This has been conceptualized in the in conceptualized been has This

as well as (2012 )

( . . ) sustained 4)

The process comprises process The ln viruse Plant influence s feeding &

Zhou,

of Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect their This articleis protected by copyright. All rightsreserved. and aphids viruliferous these of migration the by followed aphids, by plants infected sett andbehavior their changed aphids later but release, insect after minutes 30 to up plants inoculated (Hodge preferentiallyleafdisks with infected on free In manipulation? vector on plants) (in for slower be should quality circulativevirus plant in decline the Therefore, longer. considerably are periods 2008) plants infected on probing after periods brief for only ability transmission the featurenon becauseone of non For plant. deteriorating the from long discourage would plants of quality nutrition mediate to vectors insect their in behaviors and periods arrestment feeding different require would viruses circulative non that surmise to reasonable is it attracted, once However, efficiency. acquisition hos plant infected to attraction vector enhance would viruses non both that suggest considerationsTheoretical leave. or colonizing, and ali after initialattractivenessthe altervectorsinfectedtheplantsturn, to of Indirect vector manipulation What evidenceexistsrefutesWhat supportsthatnon modelsthe or of in and, infection virus by modified be both can (VOC) compounds organic volatile and color Plant led on healthy plants. This behavior can be correlated with the initial acquisition of virions from virions of acquisition initial the with correlated be can behavior This plants. healthy on led I cnrs, hs ol clea would this contrast, In . & ghting, insects probe the infected plants for quality as hosts and either commit to staying to commit either and hosts as quality for plants infected the probe insects ghting,

Powell, 2008) Powell, Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 - infected plantsto favor sustained feedinginfected the on host pia ptoe spread pathogen optimal . Aphis gossypiiAphis Comment citer cedocument: -

circulative transmissioncirculativeacquireretainisthat vectorsquickly, virusesbut l b a iavnae o cruaie iue wee acquisition where viruses circulative for disadvantage a be rly -

circulative viruses, this would increase trans increase would this viruses, circulative

Glover alates preferred plants infected with CMV over mock over CMV infectedwith plants preferredalates Glover Bean - choice assays, choice yellow mosaic virusyellow mosaic (Mauck - term settlement and induce quick vector dispersal vector quick induce and settlement term

t al. et Acyrthosiphon pisum Acyrthosiphon 2012) , s s srtg t ipoe virus improve to strategy a as ts

(BYMV)healthydiskscomparedto - circulativevirus (Fereres Rpd erdto ad low and degradation Rapid . - circulative and circulativeand circulative &

Moreno, 2009) (Mauck

Harris aphids settled aphids Harris (Hodge mission efficiency mission - induced changesinduced - circulative and circulative

et al.et & , 2

Powell, .Then, 012) .

- Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. other for found also was Werner 2007; plants the by released VOCs to correlated was and release, non over leaves and tests X virus Potato virus plants on marked more significantly was leaves potato on non of these that than cohesive more from be to appears gathered studies picture emerging The 3B). (Table Luteoviridae family the from viruses on transmission. plant specific of complexity the on reflect clearly (Fereres the increases potentially virus the of This transmissibility loses vector off. the before host healthy taking another on probing before of probability plants infected the on period shorter a for aphids attract not SMV like viruses circulative moc on than so more (Peñaflor with infected plants to attracted was Matsumura plants healthy to virions of inoculation Evidence of aphid attraction to circulative virus circulative to attraction aphid of Evidence

(PLRV) than on plants infected by the non the by infected plants on than (PLRV)

t al. et emigration bioassays showed again the preference of bioassaysemigrationtheagainshowed et al. et Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

1999) , et al. et , 2016). Within this period, aphids initiated sustained feeding on SMV on feeding sustained initiated aphids period, this Within 2016). , (PVX), or on virus on or (PVX), - infected ones. The attraction increased over time for up to 60 minutes after aphid after minutes 60 to up for time over increased attraction The ones. infected Myzus persicae Myzus , 2009; Rajabaskar 2009; , Tee n ohr xmls (T examples other and These . k - Comment citer cedocument: ncltd lns a eair iavnaeu t tasiso o non of transmission to disadvantageous behavior a plants, inoculated Luteoviridae (Hodge - free plants free

Sulzer and Sulzer &

- Powell, 2008) Powell, aphid pathosystems (Table 3B), strongly suggesting that this that suggesting strongly 3B), (Table pathosystems aphid (Carmo et al. et , 2013) , (Castle - Rhopalosiphum maidis Rhopalosiphum Sousa - - virus circulative -

Soybean mosaic virus mosaic Soybean infected plants was mostly obtained from st from obtained mostly was plants infected . Attraction to infected to Attraction .

. By contrast, SMV contrast, By . et al. et et al. et be A mgt em otoesa, u they but controversial, seem might 3A) able - - vector interactions and their impacts on virus on impacts their andinteractions vector circulative viruses. Thus, viruses. circulative

, 1998) ,

, 20 , infected by the circulative the by infected ( Y virus Potato Eigenbr 14) M. persicaeM. . In separate studies, olfactometer studies, separate In . . The soybean aphidsoybean The . ode ode

Fitch, but the latter the but Fitch, -

infected soybean plants did plants soybean infected (SMV) for up to 60 minutes 60 to up for (SMV) et al. et

forPLRV (PVY), the non the (PVY), plants, assisted by VOC, by assisted plants, , 2002; , M. persicae M. - - infected potatoinfected infected plants infected Potato Aphis glycines Aphis Alvarez

remained - vectored

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M. persicaeM. ern, 1992) Perring, Brevicoryne , and of of and , was A. . Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. short a with plants Arabidopsis infected Hily fitness. vector on role a play can that parameter such one of non impact greatly might models general the by considered not usually are that parameters interaction other and specific, less and transient are Non transmission. controlling parameters the of variations large a not might which vectors, their and virusescirculative betweenrelationships specific/sustained non do than vectors of fitness transmit with infected chew the for infected alwaysmightapathosystem,notbespecificforplants sinceincreasedfitness beenreported hasalso on vectors of performance better that noted be should It hemipterans. phytophagous surprising not is which vectors, aphid of those with line in all are 3B) (Table reports available few the in provided results The vectors. hemipteran other for available are fitness vector on plants) (in infection virus of influences the on data Less vect aphid of case the in least at fitness, vector increase viruses circulative that notion general the support results most Thus, impact. negative the neutralizes possibly this forms, wingless than inf the on developed insects alate more affected negatively Fiebig well. as reported been have results Contrasting 3B). (Table 1993) Berger, PLRV on increase natural of rates intrinsic Taken together, it seems that circulativ that seems it together, Taken ) (Musser Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 ing Te ae epne ie bte vco ftes hs en rep been has fitness, vector better i.e. response, same The . Southern bean mosaic virus mosaic bean Southern - biting Mexican bean beetle ( beetle bean Mexican biting et al.et Sitobion avenae Sitobion , 2003) Comment citer cedocument: - .

circulative viruses. This could be attributed to the intimate and more and intimate the to attributed be could This viruses. circulative

Fabricius development. However, that study also showed that showed also study that However, development. Fabricius

- ce pat. ic aae ptnily ped YV better BYDV spread potentially alates Since plants. ected ie gntp spotd larger supported genotype lived - (SBMV, which it vectors) or with BPMV (which it does not does it (which BPMV with or vectors) it which (SBMV, e viruses show more consistent effects on attraction and attraction on effects consistent more show viruses e infected potato plants than on uninfected ones uninfected on than plants potato infected - cir Epilachna varivestis Epilachna culative transmission. Plant longevity is an example an is longevity Plant transmission. culative ie te iiaiis n edn bhvos among behaviors feeding in similarities the given

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did not not did lectrical (2014) o (2014) - restricted circulative viruses. . Similar results were obtained in other pathosystems (Table pathosystems other in obtained were results Similar . otato plants suggested a reduction in plant resistance to stylet penetration on penetration stylet to resistance plant in reduction a suggested plants otato

odn ahd o BYDV on aphids Rondani

probed more frequently on PVY on frequently more probed Comment citer cedocument: (Montllor P enetration bserved that bserved &

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made more intracellular probing punctures on punctures probing intracellular more made

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Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 (Medina /PLRV - mediated indirect modification of insect behaviors and performance, studies have studies performance, and behaviors insect of modification indirect mediated ( Rajabaskar ( - Ngumbi Ortega Comment citer cedocument: - netd ha pat, hl non while plants, wheat infected et al.et t al. et et al.et , 2009; Ingwell

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(1997) who reported that viruliferous aphids transmitting PVY from infected pepper plants hadplants infectedpepper from aphidstransmitting PVYviruliferous reported that (1997)who , 2017) Cucurbit chlorotic yellows virus yellows chlorotic Cucurbit Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 - related pathways involved in virus transmission .

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et al. et ß C1 protein intera . In another example, Casteelexample, another In . - Tomato yellow leaf curl China virus China curl leaf Tomatoyellow , 2010) , Pro - triggered immunity (PTI), and on that of highly specific pathogen moleculespathogen specific highly of that on and (PTI), immunitytriggered Comment citer cedocument: - - associatedinterferencedefenseplants the of triggered immunity (ETI). They drive fast defense responses like reactiveresponsesdefensefastlikedrive They (ETI). immunitytriggered (Casteel

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a Bel van t al. et Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 Thangamani (Nuttall & 2017) ,

il 2016) Will,

et tube clogging; it is tempting to speculate that this or other factorsalso mightother or this thatspeculate temptingto is it clogging; tube n w ae oeu ta seii gp i kolde ih so b filled. be soon might knowledge in gaps specific that hopeful are we and Jaouan Comment citer cedocument: et al. et al. - activatedtransmission used to facilitate virusinoculation. Several studies 2000) ,

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- 2016; , coated mostly Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. Acknowledgments virus and insectcontrol str and pathways these identify to developnewto willhelpknowledge becausetheir futurealso scientificpleasures butpure for mechanisms, the for challenge a is It revealed. be to beginning only o especially determinants, molecular the transmission, to related could i by insects 1), directly, (Fig. cycle performance the complete to vector And, transmission. modify guide to may factors, vector with viruses interacting Finally, host. new a out seek to vector determin to altered be may behaviors and virus of influences the with again Subsequently, step. acquisition the control may morphs transmission of formation transmission viral then vectors, attract/deter virus beginning, the In 1). the is Transmission Outlook of plantdefense against aphids aresomehow deviated by these viruses to enable these reactions. defensesplant of inhibition correlateswith TuMV on probe aphids when vacuoles to transiently relocalizes protein insects the by acquired are that vectors and plants infected in changes documenting evidence of body large the Despite nteract with plantdefenses during plantprobing and infestation to facilitate viral infection.

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

- oiid ln prmtr (hom opsto, oaie, t) vco fitness vector etc), volatiles, composition, (phloem parameters plant modified result of multi of result ( Comment citer cedocument: Bak ategies. - t al. et oiid ln prmtr (oaie, oo, uret, t) may etc) nutrients, color, (volatiles, parameters plant modified -

layered interactions at each step of the transmission process (Fig.process transmission the of step each at interactionslayered 2013; ,

e the duration of virus acquisition and to encourage the encourage to and acquisition virus of duration the e Martinière (Bak - pcfc rtis n, n oe c some in and, proteins specific et al. et

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2013) , . It has been suggested that early stepsearly suggestedthat been has It . te ln ad etr ie are sides vector and plant the n Lkws, h ptvrl NIa potyviral the Likewise, . - netd evs n this and leaves infected ss vector ases, - induced -

Pro Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. M.S. Vernerey, E., Malouvet, J.L., Macia, D., Gargani, A., Bak, C.L. Casteel, and S.A. Whitham, C., Yang, A.L., Cheung, A., Bak, T.P. Pirone, and D.W. Thornbury, P.L., Atreya, C.D., Atreya, S.A. Hogenhout, and M.G. Redinbaugh, A.E., Whitfield, C.W., Tsai, E.D., Ammar, W.F. Tjallingii, and M. Dicke, B., Vosman, M., Verbeek, E., Garzo, A.E., Alvarez, References authorsThe havedeclared that no competing interests exist. Disclosure FP7 N° agreement grant under Program Framework Seventh EU’s the from funding received has which program fellowship AgreenSkills the by supported is B.D. J.C.K.N.). (to NSF the from (#1146797) cri on Studies J.C.K.N.). and M.D. (to 12 grant ANR the M.D.), (to department SPE INRA by supported is work Our criticism. constructive for reviewers the to Thanks - 609398 (A the presence of the expression ininfected tobacco plants. P Entomology hosts. plant and insect with interactions rhabdovirus of aspects molecular persicae with plants potato otyvirus

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 .

Entomologia Experimentaliset Applicata greenSkills+ contract), and E.B. acknowledgesa CIFRE fellowship (No. 1115/2015). HC ,

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Pérez, N.A.,Berger,Pérez, P.H.,Zemetra,R.S.,Ding, Eigenbrode,H. andS.D. Pérez, N.A., Berger, P.H. and Zemetra,R.S. and Berger, N.A.,P.H. Pérez, 21) eitrn n dpea pest dipteran and Hemipteran (2016) –

Infected ,

London.

(1962) and oao pi slvr effector salivary aphid potato rngnc n utasomd whea untransformed and transgenic

requires the viral PIII protein.PIII requiresviralthe Frankliniella fusca. Frankliniella B

re ylo daf viru dwarf yellow arley A conspectus of aphids as vectors of plant viruses plant of vectors as aphids of conspectus A of

Rhopalosiphumpadi Hmpea Ahdde, n rngnc and transgenic on Aphididae), (Homoptera:

, Neohydatothripsvariabilis ,

(2016) Effects of of Effects (2016) 58 Nature and ,

350

Journal of Journal eut, M. Cerutti, – ,

361. 444 s: s: , (Homoptera: Aphididae) to(Homoptera: Aphididae)

. 323 (2004a) Life history of thehistoryof Life (2004a) e Me47 s EMBO J EMBO Frontiers inPlantScience fcos n pat host plant and ffectors .

Economic Entomology Economic – Soybean ora o Economic of Journal

329. t al. et is ournal t.

a , and Environmental

glu 19) Aphid (1999) v ein , tathione evaluation 18 n ,

ecrosis 7077 - S – - , .

Weldegergis 5 Tc slvr csai saottn 2 upess F rsoss n os dnrtc cells. dendritic mouse in responses IFN suppresses L2 sialostatin cystatin salivary Tick 15)

benefits population grow population benefits .

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 irpin f w dfnie inln ptwy b a ia RA iecn suppressor. silencing RNA viral a by pathways signaling defensive two of Disruption Viruses ,

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and 21) A (2017) v itro t al. et Tavella, L. Tavella,

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(Gennadius) (Hemiptera: (Gennadius) Campos Chagas, A. Chagas, Campos and Tomato

eec ad volatile and defence et al. et aaly K. Macaulay, ector.

(2014) The NSs The (2014) y ellow

ln virus plant ora of Journal leaf curl leaf

t al. et et al. et -

infected oats. 2 Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 , hplspu padi Rhopalosiphum

De Moraes, C.M. and Mescher, M.C. Mescher, and C.M. Moraes, De e00183. Functional Ecology Southwestern Entomologist Plant,Cell & Environment - ée, .. Egnrd, .. D Mre, .. n Mshr M.C. Mescher, and C.M. Moraes, De S.D., Eigenbrode, N.A., Pérez,

- infected wheat. Entomologia Experimentalis Applicataet Comment citer cedocument: Cucumber mosaic virus mosaic Cucumber - . ee, .. Nub, . Jimenez E., Ngumbi, N.A., Perez, Journal ofVirology

(1986) Feeding responses of two grain aphids to aphids grain two of responses Feeding (1986)

neto o wne wet n rebg Hmpea Aphididae) (Homoptera: greenbug on wheat winter of infection Hmpea Ahdde rsoss o oaie us from cues volatile to responses Aphididae) (Hemiptera: vecto - ereg RL ad edl G.B. Heidel, and R.L. Deerberg, ,

26 Environmental Entomology ,

r 1162 Frankliniella occidentalis ,

37 , –

19 1175. , ,

1427

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109 CurrentOpinion inPlantBiology ,

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– – 1439.

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Doumayrou, J. Doumayrou, 42 , . Phytopathology

38 ,

, 19) De (1994)

836 – 69. –

8 45.

et al. et eeiu efcs of effects leterious arley yellow arley ieboe S.D. Eigenbrode, , ,

32 94

(2013) A virus A (2013) , ,

53 706 - mediated – infection

61. – (2012) 711. Barley dwarf

phs.

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 & . 19) rhoo tasiso o pat iue: nw synthesis. new a viruses: plant of transmission Arthropod (1997)

, Molecular Plant

St. Paul 15 plantvirus vector ,

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(2015) Insect vector Insect (2015)

p Comment citer cedocument: . 510.

(1995) Nonpathogenic (1995)

– (2000)

M - (2 netd evs y h mxcn en beetle, bean mexican the by leaves infected MN, USA icrobe Interactions 1) htfy edn bhvo ad t rltosi wt non with relationship its and behavior feeding Whitefly 016) . Journal ofInsect Behavior Cucumber mosaic virus ,

, 90 Vector

79 . ,

, 521

13587 Virology - plant virus intera virus plant - M – 541. Virology ediated –

13593. :

Nilaparvata lugens reovirus lugens Nilaparvata

, MPMI

207

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303 ransmission ,

, mutantswith altered physical properties

16 , –

, ctions associated with non with associated ctions 395

307. 854 (2013) A plant virus manipulates the manipulates virus plant A (2013) , 247 – – 403. 861.

– 20) Increased (2003) 256. of

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21) An (2016) is transmitted to theto transmitted is plcn varivestis Epilachna P urn Oiin in Opinion Current athogens Annals larval growth larval P transmitting L - circulative, oS O oS

immuno (eds f the of NE J.K. ,

8 - - ,

242 ucchini yellow mosaic potyvirus mosaic yellow ucchini dvanc on. on. ,

Journal of Molecular Microbiology and Biotechnology 204 Journal ofGeneral Virology , D., Gal D., , es in es

(1999) Role of Role (1999)

– (1996)Helper – 210.

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V Palukaitis, P. Palukaitis, - irus On, A., Huet, H., Wang, Y. and Raccah, B. Raccah, andY.Wang, H., Huet, A., On,

R esearch

Bean pod mottle virus mottle pod Bean outer capsid proteins in transmission of transmission in proteins capsid outer - - Pérez, N.A., Ding, H. and Rodriguez, A. dependenttransmissi vector

, K.J., De Moraes, C.M. and Mescher, M.C. Mescher, and C.M. Moraes, De K.J., ,

(1998) Amino acid changes in the coat protein of cucumber of protein coat the in changes acid Amino (1998) ,

Integrative & Comparative Biology 79

( 33 ed

, (2009)Parasitic crustaceansas ofan with vectors viruses,

, 897 s

Functional Ecology 1733 . : effects on aphid transmission and binding to purified to binding and transmission aphid on effects :

, K

89 . –

Maramorosch, F Maramorosch, 904. – ,

(2008) 2037 1747.

–

20) Vector (2000) 2045. Small deletions in the potato leafroll virus leafroll potato the in deletions Small

and

Soybean mosaic virus mosaic Soybean 30 Myzus persicae Myzus . on of plantviruses. of on A. Murphy A. ,

1648

(1998) Mutations in the (1998)inMutations - , ot neatos n disease in interactions host

2 – , 1659.

, 381

49 (2007) (2007)

P & hytoreovirus , –

127 A 386.

. and J. Shatkin J.

Myzuspersicae – 21) fet of Effects (2016)

141. AnnualReview gossypii Aphis on host on

) by insect by - , infected

pp.15 HC - plant - Pro

is – .

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108 (2010) Come in and take your coat off coat your take and in Come (2010) Entomologia Experimentaliset Applicata ,

Myzus persicae 9350 - specific mannerto promote virulence. P , L - -

, rceig o te ainl cdm o Sine o th of Sciences of Academy National the of Proceedings – oS ée, .. n Egnrd, S.D. Eigenbrode, and N.A. Pérez, 34 J. Bos, and C. Martinez, 15 Comment citer cedocument: 9355. , O , 227

- 1 NE transmitted – -

8. , Pérez, N.A. and Eigenbrode, S.D. Eigenbrode, and N.A. Pérez, –

, 5 247.

12 . ,

Journal ofGeneral Virology e12137. ,

1378

oao efol virus leafroll Potato

C –

iugna virus hikungunya 1388. -

Graff, V., Gonçalves, M.C. Gonçalves, V., Graff, 21) neto wt a ln vrs oiis vector modifies virus plant a with Infection (2011)

(2017) An aphid effector targets trafficking protein trafficking targets effector aphid An (2017)

VirusResearch - how

B., Farich, B.A. Farich, B.,

(1999) - 148 21) rfrne y vrs etr for vector virus a by Preference (2014) Plant

netd oao lns uig disease during plants potato infected host cells provide endocytosis for virus for endocytosis provide cells host

, ifr fo ta eiie b needle by elicited that from differs

, 82

172

(2013) Dynamics of Myzus persicae Myzus of Dynamics (2013) Physiology , Lettuce infectious yellows virus yellows infectious Lettuce

1 – 995 , 181.

186 and – 2007.

and ,

32 , Santana

pp.01458.2016. – van Den Heuvel, J.F. Heuvel, Den van

37. Beet western yellows western Beet

(2010) Host immune Host (2010) Uie Sae of States United e

- Magal, N. Magal,

Current

et al. et :

et in

acquisition analysis using partially purified virions and the whitefly the and virions purified partially using analysis acquisition Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 Journal ofGeneral Virology Virology ,

104 Environmental Macrosiphum gei Macrosiphum ,

, 10536

479

n ccme vrs y h vector the by virus cucumber and ,

Comment citer cedocument: 80 – 480 ,

–

oao pte wl virus wilt spotted Tomato 1111 10541. Proceedings of the National Academy of Sciences of the United States United the of Sciences of Academy National the of Proceedings Frankliniella occidentalis , -

278 component activity correlate with non with correlate activity component Entomology (1939) A comparative study of the transmission of of transmission the of study comparativeA (1939) – 1117. –

- ée, .. Dn, . n Egnrd, S.D. Eigenbrode, and H. Ding, N.A., Pérez,

289. (Koch).

P , otato leafroll virus leafroll otato

861 ,

Proceedings of the Ro the of Proceedings 38

21) net vector Insect (2015) – ,

86 - 1429 Moya, J.J. and Pirone, T.P. Pirone, and J.J. Moya,

. –

Phytopathology 1438.

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104 - induced volatiles emitted during disease during emitted volatiles induced and

yu persicae Myzus

17959 20) Molecul (2007) Candresse, T. Candresse, - yal Society of London of Society yal eitd rnmsin f plant of transmission mediated – 17964. - ,

retention of virions in aphid in virions of retention 98 and Proceedings of the National the Proceedingsof ,

(1996) Loss of (1996)Loss Zietlow, C. Zietlow,

(Sulz),

Bemisia tabaci Bemisia et al. et – r aoae f plant of sabotage ar 50.

(2009)

H (2007) A protein A (2007) . circumflexus M. yocyamus virusyocyamus

et al et

, hne in Changes -

) inhibits S) 127

P . otyvirus . Journal

(2008) ,

543 –

- Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 T 0518 . , , Li ,

Scientific Reports 160 ,

- W 01. ,

246 . region of region X

. , Tian ,

– ,

251. 21 Comment citer cedocument: ,

1294

(2009) Cucumber mosaic.(2009)

H and its 2b RNA silencing suppressor modify plant modify suppressor silencing RNA 2b its and

Cauliflower . , Gao , ,

1 – ,

1304. 187.

ss effects.

and (2014) Aphid behavioral responses to virus to responses behavioral Aphid (2014) mosaic Wang - EntomologiaApplicataetExperimentalis and virus

J . Cell Research et al. et Zhou, X.P. Zhou,

The g

ene Plant Health InstrHealth Plant

(2017) Viral effector protein manipulates protein effector Viral (2017) - 2

responsible for aphid transmissibility aphid for responsible

et al. et ,

27 y vrs ahgnct factor. pathogenicity virus a by and ,

(2012) Begomovirus (2012) 402 Lewsey, M.G. Lewsey, – uctor 415

- aphid interactions aphid 18) oain and Location (1987) .

DOI: 10.1094/PHI DOI: - infected plants infected

et al. et ,

153 - whitefly

(2011) ,

246

in – - .

Banerjee, 1999; Acquisition from Multiplication in Inoculation time Acquisition time Inoculation into Transmission to Retention time Latency period Virus retained Transmission Transmission

Particularity the progeny Characteristics of thedifferent viral transmission strategies by vectors (with datafrom inoculation the vector after molt Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 strategy mode

Brault

Epidermis, mesophyll, sometimes (non et al. Comment citer cedocument: Epidermis, mesophyll, phloem Capsid Minutes to hours - persistent, semi , 2010; Whitfield Seconds to minutes Seconds to minutes Stylets and foregut Non

- xylem None circulative

No No No transcomplementa Allows

- or daysor persistent) Helper etal.

, 2015).

Non Days to lifetime Hours to days Epidermis, mesophyll, phloem - propagative (Accessory)salivary glands No

Minutes to hours Hours to days (persiste Sometimes Circulative Phloem

Yes Days to months are virus hosts andInsects plants

nt)

Propagative

Lifetime

Yes

Gray

circulative viruses Virus

Examples of proteins viral involved in vector interaction. Only proteins for which virus

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

e Caulimovirida Potyviridae e Closterovirida Bromoviridae Poleroviridae

Poleroviridae

Aphids, whiteflies, Family

Cucumovirus, planthoppers Alfamovirus, Comment citer cedocument: Crinivirus

Aphids Aphids s Whiteflie Aphids Aphids

Aphids Vector

tion Aphids, whiteflies, Caulimovirus, Helper leafhoppers Waïkavirus

Potyvirus, Yes Yes No No No No

Coat protein protein Readthrough Coat protein, P2 HC protein Minor coat

Coat protein, Readthrough

Interaction Pro protein Vector

Aphids, whiteflies, Begomovirus Polerovirus, Luteovirus,

beetles

Chen al. Reinbold Chay et al Woolston al. 1996; Blanc Atreya 2011 Tian al ., 1998; Ng , 2008 , 1998

., 2005; Leh et al.

et al. &

et al

Francki, 1990; Perry

et al. , 1999; Chen et al , 1996 Reference ., 1992; Wang et al Phytoreovirus, planthoppers, et al. , 2001; Peter ., 1987; Moreno Oryzavirus Fijivirus, Aphids, et al ., 1998; Peng

thrips , 2000 .,

1999 et al -

vector

et .,

et al.

et , Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect Cucumber mosaic virus Soybean Vector arrestment mosaic virus Soybean virus Turnip mosaic mosaic virus Cucumber mosaic virus Bean yellow

This articleis protected by copyright. All rightsreserved. Table 3 viruswilt Tomato spotted virus Wound tumor Rice dwarfvirus, dwarfvirus Potato yellow virus Abuliton mosaic interaction domains have been characterized arelisted. Table 2

Virus Virus

Indirectand direct effects of viruses behavioron and performance of insectvectors. Examples of proteins viral involved in vector interaction. Only proteins for which virus

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

Vector settlement ( Bromoviridae Potyviridae Potyviridae Potyviridae Bromoviridae Potyviridae A) Indirect effects of non Bunyaviridae Reoviridae e Rhabdovirida Geminiviridae

Family Family Comment citer cedocument:

A. glycines persicaeM. A. gossypii A. pisum A. gossypii R. maidis

Thrips per Leafhop per Leafhop s Whiteflie

Vector Vector

circulative viruses Helper C. sativus G. max G. max benthamiana N. C. sativus V. faba Yes Yes Yes No

Host

protein NSs Non Coat protein G Psn4 structural protein and P8, non Coat proteins P2 Coat protein G Coat protein

Interaction -

structural

Vector response

+, up+, to up+, to 60 60 min 30 min Vector – – + +

N ,

Carmo Fereres Peñaflor Casteel Carmo Hodge et al. Whitfield 2015 Omura Gaedigk Höhnle

, 2014 - - & Sousa Sousa & et al.et et al. et al.et

et al. et al Powell, 2008

Reference Yan, 1999; Chen et al. Reference

, 2001 , 2015 , 1999 ., 2016 , 1986 et al.et al.et , 2008; Margaria

, 2014 , 2014

- vector

al. , Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect dwarf virus Barley yellow virus leafPotato roll Vector settlement ( mosaic virus Cucumber VirusPotato Y Vector feeding behavior mosaic virus Southern bean mottle virus Bean pod mosaic virus Soybean mottle virus Bean pod virus Alfalfa mosaic mosaic virus Wheatstreak virus Turnip mosaic virus Turnip mosaic virus Turnip mosaic mosaic virus Zucchini yellow virus Turnip mosaic Vector fitness mosaic Soybean mosaic virus This articleis protected by copyright. All rightsreserved. B) Indirecteffects of circulative viruses

virus

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

Potyviridae Poleroviridae Poleroviridae Bromoviridae Potyviridae Sobemovirus Secoviridae Potyviridae Secoviridae Bromoviridae Potyviridae Potyviridae Potyviridae Potyviridae Potyviridae Potyviridae

Comment citer cedocument:

M. persicaeM. A. gossypii persicaeM. E. varivestis E. varivestis A. glycines (non A. glycines A. glycines graminumS. B. brassicae persicaeM. persicaeM. A. gossypii persicaeM. persicaeM. R. padi - vector)

G. max G. max T. aestivum B. rapa benthamiana N. A. thaliana C. pepo B. rapa G. max T. aestivum tuberosumS. C. sativus C. annuum vulgarisP. vulgarisP. G. max

– – – – + + + + 0 + + + + + + –

Donaldson Donaldson Michels Hodgson, 1981 Casteel Casteel Blua Hodgson, 1981 Fereres 2004b Jiménez 2013 alet Alvarez Eigenbrode Castle Carmo Collar Musser Musser Peñaflor ., 2009; Rajabaskar &

etal

- etal Perring, 1992 Sousa et al.et al.et etal et alet al.et et alet - et al.et Martínez et al. ., 1997 ., 1998; & & et al.et ., 2007; Werner ., 2003 ., 1999 , 2015 , 2014, 2015

, 2003 , 1994 Gratton, 2007 Gratton, 2007 et alet , 2016

, 2002;

., 2014 etal

., et al

., Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect Vector settlement ( dwarf virus Barley yellow virus borne yellows Cucurbit aphid virus leafPotato roll dwarf virus Barley yellow Vector feeding behavior dwarf virus Barley yellow leaf curlvirus Tomato yellow virus Bean leaf roll virus spotted wilt Tomato dwarf virus Barley yellow dwarf virus Barley dwarf virus Barley yellow virus leafPotato roll Vector fitness mosaic enationPea virus Bean leaf roll mosaic virus enationPea virus spotted wilt Tomato This articleis protected by copyright. All rightsreserved. C) Direct effects of circulative viruses

yellow virus

Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

- Poleroviridae Bunyaviridae Poleroviridae Poleroviridae Poleroviridae Poleroviridae Poleroviridae Begomovirus Poleroviridae Bunyaviridae Poleroviridae Poleroviridae Poleroviridae Poleroviridae Poleroviridae Poleroviridae

Comment citer cedocument:

A. persicaeM. graminumS. avenaeS. B. A. pisum occidentalis F. R. padi graminumS. avenaeS. persicaeM. A. pisum A. pisum A. pisum occidentalis F. R. padi

tabaci gossypii

C. annuum T. aestivum A. sativa T. aestivum tuberosumS. sativumP. sativumP. V. faba C. annuum A. sativa C. sativus tuberosumS. A. sativa T. aestivum lycopersicum S. sativumP.

+ + + + + + + + + 0 + + + – + +

Maris 2004a Jiménez Montllor Fereres Castle Wu Wu Hodge Maris Montllor Carmo Alvarez Montllor Fiebig Maluta Wu et alet al.et et alet

etal. etal et alet & - & Sousa etal etal - alet

., 2014 ., 2014

Martínez Berger, 1993 , 2014 Powell, 2008 & & & ., 2004 ., 2004

Gildow, 1986 , Gildow, 1986 Gildow, 1986

., 2014 ., 2007 2004 ., 1989 et alet

., 2016 etal

Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect leaf curlvirus Tomato yellow virus spotted wilt Tomato Vector feeding behavior virusnecrosis Soybean vein leaf curlvirus Tomato yellow Vector fitness leaf curlvirus Tomato yellow Vector arrestment dwarf virus black Southern rice virusnecrosis Soybean vein virus borne yellows Cucurbit aphid virus leafPotato roll dwarf virus Barley yellow This articleis protected by copyright. All rightsreserved. positive negativor healthy ones. This isdue to plantcolor, odor, metabolism alteredetc. by viruses, which provide Fig Legend to figure positive,+: .

streaked The transmission cycle. Virus

– Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 : negative,: 0:

- Poleroviridae Poleroviridae Geminiviridae Bunyaviridae Bunyaviridae Geminiviridae Geminiviridae Reoviridae Poleroviridae

e cues for subsequent virus acquisition during insect

Comment citer cedocument: neutral effect.

B. tabaci occidentalis F. N. B. B. furcifera Sogatella N. A. gossypii persicaeM. R. padi

tabaci tabaci variabilis variabilis - free insect vectors are more

G. max lycopersicum S. lycopersicum S. Oryza sativa G. max C. sativus tub S. T. aestivum lycopersicum S. stramonium D.

erosum

attracted + + + + + + + + +

feeding Keough Maluta 2013 Moreno Lu Keough Carmo Rajabaskar Rajabaskar Ingwell Medina 2013 Moreno Stafford

to infected plants than to et alet

- ., 2016 Sousa . Again, a - etal et alet - - etal etal. Ortega etal Delafuente Delafuente etal etal ., 2014 ., 2012; ., 2016 ., 2011 , 2016 et

., 2014 ., 2014 et al. al cquisition ., 2016

etal etal , 2009;

., .,

is Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. assisted by vector factors, thecycle rest allowto for longer e.g. viruses) periods. During are retained in the insects acquisitionafter for short (non virus (CaMV) responds instantly to perception viruses, working alteringon plantdefense responses and other pathways, may interfere with the behavior, facilitatedoften by viral modifications theof plantspromoting ‘acquisition

encouraging viruliferous vectors to preferhealthy over infected plants or enhancing theirfitness e.g.

of insectsby plants,with plantdefense responses and with other pathways. At least one Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470

longerfeeding circulative for and - lasting transmissibility. After virus inoculation inanewhost, which could be retention Comment citer cedocument: , insectsbe may manipulated by viruses to promote tran the vector’s presenceby forming transmission morphs. Viruses

arts.

deterrence

- circulative viruses) or longer(circulative

for non - circul ative viruses. For this, - friendly’feeding smission, Version postprint Dader , B.,Then,C.,Berthelot, E.,Ducousso, M.,Ng, J.C.K.,Drucker, C.M.(2017). Insect transmission ofplantviruses: multilayered interactions optimizeviral propagation. Insect This articleis protected by copyright. All rightsreserved. Science, 24 (6),929-946 . ,DOI: 10.1111/1744-7917.12470 Comment citer cedocument: