A review of the mechanisms and components that determine the transmission efficiency of Tomato yellow leaf curl virus (Geminiviridae; Begomovirus) by its whitefly vector

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Virus Research

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review of the mechanisms and components that determine theransmission efficiency of Tomato yellow leaf curl virus (Geminiviridae;egomovirus) by its whitefly vector

urad Ghanim ∗

epartment of Entomology, The Volcani Center, Bet Dagan 50250, Israel

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eywords:emisia tabaciegomovirusesirculative transmissioneceptoricroarrays

a b s t r a c t

Begomoviruses are a group of icosahedral single stranded DNA viruses exclusively transmitted by thesweet potato whitefly Bemisia tabaci in a persistent, circulative manner. In this mode of transmission,begomoviruses are acquired by their insect vector as intact virions from the plant phloem, move along thefood canal, foregut and esophagus and reach the midgut where they are absorbed into the hemolymph viathe filter chamber. The filter chamber is the site where most of the ingested food is filtered, and the firstsite where the majority of begomoviruses appear to be translocated into the hemolymph via unknownproteins or receptors. Transport from the filter chamber to the hemolymph is aided by a Heat ShockProtein 70. Virus particles not translocated across the filter chamber circulate in the midgut loop but itis not known whether absorption into the hemolymph occurs along this loop. Localization studies haveconfirmed that begomoviruses are not associated with the hindgut and absorption of virions in this organis unlikely. In the hemolymph, virions have been shown to interact with a GroEL chaperone producedby the whitefly’s endosymbiontic bacteria for ensuring their safe journey to the salivary glands. Virions
penetrate the primary salivary glands via unknown proteins or receptors and are transported and secretedoutside the whitefly to the plant with salivary secretions. Several recent studies have demonstrated theimplications of insect and endosymbiont proteins such as the heat shock protein 70 and the bacterialGroEL protein, in the transmission of begomoviruses by B. tabaci. Additional studies attempting to identifyother proteins that aid or interact with begomoviruses along their circulation pathway in the whiteflyare reviewed in this paper.
© 2014 Elsevier B.V. All rights reserved.

. Introduction

Many plant viruses rely on insect vectors for dissemination andn some cases the viruses have a negative effect on their vectors.onetheless, some vector-borne viruses including plant infect-

ng members of the Bunyaviridae, Reoviridae and Rhabdoviridaeave evolved largely unknown mechanisms allowing replication

n both plant and insect hosts (Black, 1950; de Assis Filho et al.,002; Ammar et al., 2007). Some of these viruses are delete-ious to their insect vector and are transovarially transmittedSylvester, 1973). While replication of these viruses has been shown

Please cite this article in press as: Ghanim, M., A review of tmission efficiency of Tomato yellow leaf curl virus (Geminiviridhttp://dx.doi.org/10.1016/j.virusres.2014.01.022

o occur in insects, it is not known whether the replication mech-nisms in the insect are similar to those that occur in the plant,nd whether the same viral genes are used in both hosts. Weak

∗ Tel.: +972 3 9683911; fax: +972 3 9683911.E-mail address: [email protected]

168-1702/$ – see front matter © 2014 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.virusres.2014.01.022

evidence for virus replication or accumulation was demonstratedfor other vector-borne circulative plant viruses such as luteovirusesand geminiviruses which pose a significant constraint in manyagricultural crops (Gray and Gildow, 2003; Sinisterra et al., 2005).Those viruses possibly use replication and recombination strate-gies in the host plant, but not in their insect vectors, as a strategyto broaden their host range, to invade new regions and possibly todiversify their functions (Gibbs and Cooper, 1995; Padidam et al.,1999; Lefeuvre et al., 2010).Therefore, insect vectors contribute tothe dissemination, but not diversification of these viruses. In par-ticular, begomoviruses may constitute a family of plant viruseswho are in the process of acquiring, or loosing abilities to inter-act actively with their insect vector, the whitefly Bemisia tabaci,to a point reminiscent of a host-pathogen relationship (Czosnek

he mechanisms and components that determine the trans-ae; Begomovirus) by its whitefly vector. Virus Res. (2014),

and Ghanim, 2012). This assumption is particularly pertinent whenexamining the relationship between B. tabaci and begomoviruses.Some of the investigations from the past two decades are presentedand discussed in this review.

dx.doi.org/10.1016/j.virusres.2014.01.022


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. Tomato yellow leaf curl virus as a representative ofegomoviruses

Tomato yellow leaf curl virus (TYLCV) (Geminiviridae; Bego-ovirus) is a begomovirus first reported in Israel as the causative

gent of a significant plant disease in tomato production (Cohennd Nitzany, 1966). The disease, known as tomato yellow leafurl disease (TYLCD), was associated with the whitefly vector B.abaci (Cohen and Nitzany, 1966). TYLCV is now known to occurn several regions around the world, including Asia, Middle andar East Africa, Europe, the Caribbean and North America (Czosneknd Laterrot, 1997), Japan (Kato et al., 1998), Mexico (Ascencio-banez et al., 1999), and the United States of America (Momol et al.,999). Begomoviruses, including TYLCV, are circular plant DNAiruses characterized by 22 nm × 38 nm geminate particles com-rised of two joined incomplete icosahedra encapsidating singletranded DNA genome molecules of about 2700 nucleotides (Navott al., 1991; Zhang et al., 2001). Generally, begomoviruses possesswo genomic components, DNA-A and DNA-B (bipartite), however,YLCV has only a single DNA-A-like genome component (monopar-ite ∼ 2.8 kb) (Navot et al., 1991). The genome of TYLCV possesses sixartially overlapping open reading frames (ORFs) bi-directionallyrganized in two transcriptional units that are separated by anntergenic region (IR) of approximately 300 nucleotides (Rybickit al., 2000). V1 encodes the coat protein (CP) responsible for encap-idation of the genome and involved in virus movement and vectorecognition. V2 encodes a suppressor of gene silencing to over-ome the plant defense systems (Zrachya et al., 2007). These twoRFs are encoded by the virion sense strand. The complementaryirus strand contains four ORFs: C1 which encodes a replicationssociated protein (Rep) essential for replication, C2 a transcriptionctivator protein (TrAP) involved in the activation of transcriptionrom the coat protein promoter, C3 a replication enhancer pro-ein (REn) that interacts with the C1 protein and enhances viralNA accumulation, and C4 embedded within C1. Protein productsncoded by the V2 “pre-coat” and the C4 ORFs have been implicatedn symptom expression and virus movement. The non-coding IRegion located upstream from the V2 and C1 ORFs contains key ele-ents (stem-loop structures) for the replication and transcription

f the viral genome (Jupin et al., 1994; Wartig et al., 1997; Norist al., 1998).

. The whitefly Bemisia tabaci and the species complex

B. tabaci, the whitefly vector of begomoviruses, is a siblingpecies group comprised of genetic and phenotypic variants. Morehan 35 biotypes or cryptic species and numerous haplotypes haveeen differentiated by DNA markers (Frohlich et al., 1999; De Barrot al., 2011; Liu et al., 2012; Firdaus et al., 2013). B. tabaci bio-ype differences include host range, insecticide-resistance, virusransmission efficiency, and the ability to cause plant disorders.he most predominant and damaging biotypes worldwide are the

and Q, recently termed the Middle East Asia Minor 1 (MEAM1)nd the Mediterranean (MED) species (Brown et al., 1995; Frohlicht al., 1999; Brown, 2007a,b; Dinsdale et al., 2010). The B biotypes defined by extreme fitness in arid, irrigated cropping systems,he ability to efficiently transmit both New and Old World bego-

oviruses (Gottlieb et al., 2010; Gotz et al., 2012), and the abilityo cause phytotoxic-like symptoms as a byproduct of feeding (Costand Brown, 1991; Brown et al., 1995). The Q biotype is best knownor its ability to develop resistance to certain insecticides, and to be


ell-adapted to greenhouse environments (Horowitz et al., 2005;ennehy et al., 2006, 2010). Viral disease outbreaks have beenainly associated with the exotic B biotype now widespread in

ocales where it was not endemic, suggesting it is highly fit and a

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superior, co-adapted vector for Old and New World begomoviruses.The occurrence of the B and Q biotypes in many places of the worldhas resulted from changes in environmental conditions and agri-cultural practices. For example, until 2004, only the B biotype waspresent in the US, but the Q biotype, highly resistant to variousinsecticides, rapidly spread into and became established across sev-eral states in crops sprayed with those insecticides (Dennehy et al.,2006). While the A biotype no longer poses a major threat to mostagricultural areas in the US and elsewhere, the B and Q biotypesare of great concern as pests and vectors globally. A recent sur-vey in Israel showed that the Q biotype was limited to protectedcrops in greenhouses and net houses, while the B biotype was dom-inant in open fields (Kontsedalov et al., 2012). This distribution wasattributed mainly to the ability of the Q biotype to resist insecticidesprays in protected environments and to be highly adapted to heatstress conditions (Mahadav et al., 2009), unlike the B biotype whichis known for higher susceptibility to insecticides and to heat stressconditions.

4. B. tabaci–TYLCV interactions

4.1. Parameters of acquisition, inoculation and retention by B.tabaci biotypes

The stylet of B. tabaci penetrates the plant epidermis and movesintracellularly through the parenchyma to reach the phloem (Fig. 1)which is required for both virus acquisition and inoculation. Theminimum acquisition access period (AAP) and inoculation accessperiod (IAP) of Middle Eastern TYLCV isolates varied from 15to 60 min and 15 to 30 min, respectively (Cohen and Nitzany,1966; Ioannou, 1985; Mansour and Al-Musa, 1992; Mehta et al.,1994; Czosnek et al., 2001, 2002). Similar results were reportedfor Tomato yellow leaf curl sardinia virus (TYLCSV) (Geminiviridae;Begomovirus) from Italy (Caciagli et al., 1995) and Tomato leaf curlBangalore virus (ToLCBV) (Geminiviridae; Begomovirus) from India(Muniyappa et al., 2000). Different whiteflies with access to thesame tissues for the same period of time acquire variable amountsof viral DNA (Zeidan and Czosnek, 1991). PCR detected TYLCV DNAin 20% of single insects after a 5 min AAP and in all insects aftera 10 min AAP (Navot et al., 1992; Atzmon et al., 1998; Ghanimet al., 2001a). A single whitefly was able to infect a tomato plantwith TYLCV following a 24 h AAP, and the efficiency of transmissionreached 100% when 5–15 insects were used (Czosnek et al., 2001).Similar results were obtained with the New World bipartite gemi-nivirus, Squash leaf curl virus (SLCV) (Geminiviridae; Begomovirus)(Cohen et al., 1983, 1989). Following a 48 h AAP, begomovirusesare retained in their whitefly vector for several weeks and some-times for the entire life of the insect (Czosnek and Ghanim, 2012).SLCV and TYLCV remain associated with B. tabaci during the entirelife of the vector (Cohen et al., 1989; Rubinstein and Czosnek,1997; Czosnek and Ghanim, 2012) while Tomato yellow leaf curl sar-dinia virus (TYLCSV) was undetectable after approximately 20 days(Caciagli and Bosco, 1997). Interestingly, viral DNA remains asso-ciated with whiteflies much longer than they are able to transmit.TYLCSV DNA was detectable for 20 days after a 48 h AAP whereastransmission occurred only for eight days (Caciagli et al., 1995). Fur-thermore, detection of viral DNA (by Southern blot hybridization orPCR) and CP (by Western blot immunodetection or IC-PCR) suggeststhese are not retained in B. tabaci for the same time periods. Follow-ing a 48 h AAP, TYLCV DNA was detected throughout the 5-week lifespan of the insect while the amount of TYLCV CP steadily decreased


until it was undetectable at day 12 (Rubinstein and Czosnek, 1997;Czosnek et al., 2001). The disappearance of the virus CP was asso-ciated with a rapid decrease in the ability of the whitefly to infectplants with TYLCV (Rubinstein and Czosnek, 1997) or SLCV (Cohen


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Fig. 1. The circulative transmission pathway for begomoviruses (red particles) transmitted by whiteflies and the proteins so far confirmed to interact with TYLCV. Bego-moviruses are restricted to the plant phloem (p) which facilitates dispersal by sap-sucking insects. The filter chammber (fc) in the midgut (mg) is the first site of internalizationinto the vector and occurs via endocytosis. In the filter chamber, TYLCV interacts with HSP70 (green particles), and after circulation in the insect, viruses interact with theG livary

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roEL protein (yellow particles) in the hemolymph and cross the insect primary sag: hindgut; e: esophagus; s: stylet; bacteriocytes.

t al., 1983). Similarly, a difference in the retention of viral DNA andP in B. tabaci was also observed for an Israeli isolate of the non-ransmissible bipartite begomovirus Abutilon mosaic virus (AbMV)Geminiviridae; Begomovirus) (Morin et al., 2000). Czosnek et al.2002) also reported that after a 4-day AAP, TYLCV-Is DNA persistedn B. tabaci about 15 days, while the CP was detectable only for upo seven days. Additionally they found that TYLCV was retained for

uch shorter time in the non-vector T. vaporariorum than in the. tabaci vector (Czosnek et al., 2002). The comparison of retentioneriods of TYLCV DNA and CP in the two insect species under theame conditions found that TYLCV DNA was detected in B. tabaciver the entire seven days of the experiment while the CP wasetected during the first four days only. In contrast, TYLCV DNA wasetected in T. vaporariorum only during the first six h that followedhe end of the AAP, and the CP for up to 4 h. Thus TYLCV disappearedery quickly from the non-vector T. vaporariorum once acquisitioneeding had ceased, while the DNA appears to be retained longerhan the CP even in the non-vector. In addition, gender and age ofhe whitefly also can influence transmission ability (Czosnek et al.,001). Nearly all 1–2 week-old adult females from synchronizedopulations of adult B. tabaci were able to infect tomato plants fol-

owing a 48 h AAP and 48 h IAP, however the transmission efficiencyf older insects is less (Rubinstein and Czosnek, 1997). Seventeenay-old adults acquired less than half the virus acquired by 10ay-old insects. By 3 days, this amount is only about 10%. At thege of 28 days and thereafter, the viral DNA associated with thensects is undetectable by Southern blot hybridization althoughhe transmission efficiency remains about 20%. In one study, theransmission efficiency of the Q biotype was not essentially differ-nt from that of B. Transmission of a TYLCSV isolate from Murcia,pain (TYLCSV–ES) was studied using the B, Q and S biotypes of B.


abaci (Jiang et al., 2004). Both B and Q-biotypes of B. tabaci wereble to transmit TYLCSV–ES from infected tomato plants to Solanumigrum and Datura stramonium and vice versa. No significant dif-erence was found in transmission efficiency from infected tomato

glands (psg) via endocytosis and are spit into a host plant with salivary secretions.

plants to weed plants between the B- and Q-biotypes. The S-biotypecould not survive on tomato long enough to acquire or transmitTYLCSV–ES. In these studies, the age and gender of the whiteflieswas not taken into account (Jiang et al., 2004). Another study hasshown significant differences in the transmission of TYLCV betweenB and Q biotypes from tomato to tomato, suggesting that the trans-mission efficiency of TYLCV can significantly differ between the twobiotypes (Sanchez-Campos et al., 1999). A recent study has demon-strated differential interactions between the B and Q biotypes andpossible implication in the recent spread of TYLCV in China. Among55 B and Q biotype populations collected in this study, the authorsfound that Q biotype populations demonstrated higher acquisitionand transmission capability compared with the B. The Q biotypefurther acquired more viral DNA and reached the maximum viralload in shorter time. These results suggested that the rapid spreadof TYLCV in China is aided mainly by the recent invasion of the Qbiotype in China (Pan et al., 2012). These results were supportedby another study that demonstrated significant influence by TYLCVon life history traits of the B biotype vector, while the Q biotypewas marginally influenced (Pan et al., 2013). Another recent study,which will be discussed in section 7, demonstrated the involve-ment of bacterial endosymbionts in determining the transmissionabilities of TYLCV by B and Q biotypes of B. tabaci (Gottlieb et al.,2010).

4.2. TYLCV circulation in B. tabaci

TYLCV is vectored by B. tabaci in a persistent, circulative man-ner (Fig. 1; Ghanim et al., 2001a). Once ingested, begomovirusesare not immediately available for infection as they pass a latentperiod, in which virions pass several barriers before transmission.


The latent period is essentially the time it takes for the virus to cir-culate in the whitefly until infection. The latent period of TYLCVwas reported to be 21 h in the early 1960s (Cohen and Nitzany,1966), while later on it was measured and found to be 8 h (Ghanim


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t al., 2001a). During the latent period, begomoviruses translocaterom the insect digestive system, across the gut epithelial cells intohe hemolymph. Viral particles in the hemolymph reach the sali-ary system and finally enter the salivary duct from where theyre egested with the saliva into the plant. Translocation of bego-oviruses from the digestive tract to the hemolymph and from

he hemolymph to the salivary gland is thought to be mediated bynknown receptors and proteins (see Section 7 below). The ratef translocation of TYLCV in the whitefly has been reported byhanim et al. (2001a). By using PCR with TYLCV-specific primers,nd dissected heads, midguts, salivary glands and hemolymph asNA templates the authors were able to follow the exact trasloca-

ion times from one organ to another. TYLCV DNA was first detectedn the head after a 10-min AAP, in the midgut after 40 min and inhe hemolymph after 90 min. TYLCV was detected in the salivarylands 5.5 h after it was first detected in the hemolymph. Moreover,ncapsidated virions were immunolabeled with anti CP antibod-es, suggesting that at least part of the virus is moving as a fullyssembled virion. Virions were localized in the stylets, associatedainly with the food canal, along the lumen, as well as in the prox-

mal part of the descending midgut, the filter chamber, the distalart of the descending midgut, and in the primary salivary glandsBrown and Czosnek, 2002; Czosnek et al., 2002). TYLCSV has alsoeen observed in the midgut epithelial cells and in the cytoplasmf the primary salivary gland cells (Medina et al., 2006; Ghanimnd Medina, 2007; Caciagli et al., 2009; Ghanim et al., 2009), and inhe filter chamber, where the majority of virus is absorbed into theemolymph (Ghanim et al., 2001b, 2009). Although viral DNA wasmplified from ovaries of whiteflies that acquired TYLCV (Ghanimt al., 1998) and TYLCSV (Bosco et al., 2004), no specific labeling ofhe TYLCSV CP in ovaries was detected (Caciagli et al., 2009).

. Are begomoviruses insect pathogens?

It appears that relationships between whiteflies and bego-oviruses were established in ancient times. Fossils anatomically

imilar to recent whiteflies have been found in old amber collectedn Lebanon and this fossil was dated to ∼120 million year (MY)Schlee, 1970), however a fossil was not tested to the presence ofny viral DNA. Additionally, evidence exists to suggest that repeatsrom geminiviral DNA sequences highly homologous to regions ofhe bipartite Tomato golden mosaic virus (TGMV) (Geminiviridae;egomovirus) were integrated into the genome of some tobacconcestors during Nicotiana speciation, about 25 MY ago (Bejaranot al., 1996). Further evidence suggests that the endosymbioticacteria which aid in begomovirus transmission by B. tabaci (Morint al., 1999, 2000; Gottlieb et al., 2010), have been associated withhiteflies for the last 200 MY (Bauman et al., 1993). During this

ong-lasting virus-vector relationships, begomoviruses might havehanged CP conformation to adapt for receptors and other iner-cting proteins that mediate their recognition and circulation inhe insect host and to interact with other insect and endosymbiontroteins. These adaptations are evident when examining vector-egomovirus interactions and are reflected in the parameters ofcquisition and transmission. Transmission of a begomovirus by

whitefly from the same geographical region is much more effi-ient than when the virus and whitefly originate from differentegions, as it is the case with local B. tabaci B biotype from the USnd its interactions with SLCV (Gotz et al., 2012). Circulation ofhitefly-transmitted viruses in the different insect tissues, maybe

mechanism used by the insect to compartmentalize the virus and


void its harmful effects, however, since begomoviruses do pene-rate several cells and tissues in the whitefly, this avoidance by thehitefly is partially successful since many begomoviruses remain

ssociated with the insect vector for many days following a short


acquisition access period (AAP) (Polston et al., 1990; Caciagli et al.,1995; Rubinstein and Czosnek, 1997), and some begomovirusesare able to invade the reproductive system (Ghanim et al., 1998;Bosco et al., 2004; Wang et al., 2010) and affect many biologi-cal parameters (Rubinstein and Czosnek, 1997; Jiu et al., 2007;Matsuura and Hoshino, 2009; Sidhu et al., 2009). The long last-ing interactions between begomoviruses and whiteflies suggesta high level of adaptation of the virus to whitefly cells and tis-sues, and some level of exploitation of the whitefly by the virus.The persistence of TYLCV in B. tabaci as infectious virus for longerthan the latent period, sometimes for the entire life of the insect,(Caciagli and Bosco, 1997; Rubinstein and Czosnek, 1997), raisedthe basic question whether begomoviruses are able to replicateinside their vectors. Accumulation of viral DNA in B. tabaci rearedon a TYLCV-non host plant, after first feeding on plants infectedwith TYLCV has been interpreted as multiplication of TYLCV in itsvector (Mehta et al., 1994; Czosnek et al., 2001). Following acquisi-tion of the closely related TYLCSV, accumulation of viral DNA wasnot observed (Caciagli and Bosco, 1997). Begomovirus transcriptionin its vector was assessed by quantifying selected gene transcriptson the viral strand and the complementary strand, including theCP gene of the monopartite TYLCV and the bipartite Tomato mottlevirus (ToMoV) (Geminiviridae; Begomovirus), after the insects havefed on virus-infected tomato plants and later transferred to cot-ton plants, a non-host of the virus (Sinisterra et al., 2005). Whilethe ToMoV gene transcripts rapidly became undetectable in white-flies following transfer from tomato to cotton, TYLCV transcriptsincreased after transfer of whiteflies to cotton, and were readilydetected after 7 days suggesting that TYLCV replication occurs inthe whitefly. Transcripts of TYLCV CP gene were localized by in situhybridization using short DNA oligonucleotides complementary toCP RNA (Ghanim et al., 2009) mostly to the filter chamber and thedescending midgut.

6. Direct and indirect effects of begomoviruses on theirwhitefly host

TYLCV is associated with B. tabaci (B biotype) for its entirelife (Rubinstein and Czosnek, 1997), however, YLCSV is unde-tectable after approximately 20 days (Caciagli and Bosco, 1997).The association of TYLCV with B. tabaci B biotype females was corre-lated with a decrease in longevity compared with non-viruliferousinsects (Rubinstein and Czosnek, 1997). Following a 48-h AAP onTYLCV-infected tomato plants insects reared on eggplant, a TYLCVnon-host, the life span of the viruliferous insects decreased by 5to 7 days compared to that of non-viruliferous whiteflies. Addi-tionally, the long-term association of TYLCV with female B. tabaciwas correlated with a decrease in fertility (Rubinstein and Czosnek,1997). Following a 48-h AAP on TYLCV-infected tomato plants, themean number of eggs laid either on tomato or on eggplant signifi-cantly decreased by 25% to 50% (depending on the age of the adult).The percentage of eggs that developed into instars was similar,whether they were laid by infected or non-infected insects, sug-gesting that TYLCV influenced fecundity but not fertility. The effectof another begomovirus from China, Tomato yellow leaf curl Chinavirus (TYLCCNV) (Geminiviridae; Begomovirus) was tested on two B.tabaci biotypes from China (invasive B biotype and local ZHJ1 bio-type) (Jiu et al., 2007). Following a 48-h AAP on TYLCCNV-infectedtobacco plants longevity and fertility of viruliferous B and ZHJ1(local Chinese biotype) biotypes on cotton decreased by 40% and35%, respectively. In contrast, B biotype whiteflies fed on Tobacco


curly shoot virus (TbCSV) (Geminiviridae; Begomovirus)—infectedtobacco lived longer and were more fertile than non-viruliferouswhiteflies, while the effect of TbCSV on ZHJ1 insects was minor. In aseparate study, the infection of tomato plants by either TYLCCNV or


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YLCV had no or only marginal effects on the development, survivalnd fecundity of the B biotype. In contrast, survival and fecundityf the ZHJ1 biotype were significantly reduced on virus-infectedlants, compared to those on uninfected plants. Populations of the

biotype on uninfected and TYLCCNV-infected plants were similar;owever, population increase of the ZHJ1 biotype on TYLCCNV-

nfected plants was adversely affected (Hu et al., 2011). Similartudies testing the effect of a Japanese isolate TYLCV on the biol-gy of the Q biotype (Matsuura and Hoshino, 2009) reported thatnsects raised on infected or healthy tomato showed no differencesn survival rate or fecundity. Additionally, the proportion of 3rdnd 4th instar nymphs did not differ between infected and healthyomato plants, suggesting that infection with TYLCV is likely not tonfluence the development of nymphal instars on infected tomatolants. A similar study tested the effect of the bipartite bego-ovirus ToMoV on B. tabaci (McKenzie, 2002). B biotype females

nfected with ToMoV laid significantly more eggs on healthy tomatoompared to non-viruliferous females. The number of adults thatmerged from eggs laid by viruliferous and non-viruliferous white-ies did not significantly differ. These observations suggest thatot all begomoviruses have the same effects on their whiteflyectors and while some viruses have negative effects, other areeutral. Plants and whiteflies infected with begomoviruses haveeen also shown to influence the plant preference by whiteflies.sing the electrical penetration graph (EPG) Moreno-Delafuentet al., 2013 have shown that viruliferous whitefly adults movedlower than non-viruliferous whiteflies. EPG further showed thatYLCV-viruliferous B. tabaci fed more often from phloem sieve ele-ents and the duration of the salivation phase in phloem sieve

lements was longer in viruliferous than in non-viruliferous white-ies, suggesting the enhancement of TYLCV inoculation efficiencyMoreno-Delafuente et al., 2013). A similar study conducted inhina demonstrated additional effects induced by TYLCV on itshitefly vector (Liu et al., 2013). The results from both studies

uggested that TYLCV directly manipulates the settling, probingnd feeding behavior of its vector in a way that enhances virusransmission efficiency and spread. Those results may implicateeneficial interactions for both the virus and its vector. Anothertudy conducted in China showed that TYLCV-free Q biotype pre-erred to settle on TYLCV-infected tomato plants, while TYLCV-free. tabaci B preferred healthy tomato (Liu et al., 2013). Interestingly,YLCV-infected B. tabaci, either B or Q, did not exhibit a prefer-nce between TYLCV-infected and TYLCV-free tomato plants. Thoseesults and others further indicated that TYLCV can alter the hostreferences of its whitefly vector (Liu et al., 2009; Fang et al., 2013).everal factors could explain these contradictory results includinghe genetic background of the virus (monopartite vs. bipartite), itsrigin and its adaptation to the local whiteflies, and experimentalonditions that sometimes could drastically influence the results.dditionally, recent studies have shown that whitefly endosym-ionts influence many aspects of the whitefly biology includingirus–vector interactions, population dynamics and response tonvironmental conditions (Kontsedalov et al., 2008, 2009; Brumint al., 2011; Himler et al., 2011). Since all the studies describedbove did not take into account bacterial endosymbionts, the differ-nces obtained could partially account to these bacteria that differetween whitefly biotypes and populations worldwide.

. Discovery of proteins involved in TYLCV circulativeransmission


During begomovirus translocation in the vector, the capsid pro-ein is exposed to several whitefly tissues and organs, and it isypothesized to interact with insect receptors, chaperons and pro-eins that aid in their transmission. TYLCV is mostly acquired as an

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intact virion from the plant phloem and this is how it passes alongthe stylet, esophagus and food canal of B. tabaci. The esophagusis a chitin-lined tissue that does not allow food/virion penetrationto the hemolymph (Ghanim et al., 2001b). The first tissue throughwhich virions can cross to the hemolymph is a modification of thejunction between the esophagus, midgut and hindgut called thefilter chamber (Ghanim et al., 2001b). The filter chamber is a con-voluted structure in which membranes from the midgut, hindgutand the caeca interdigitate to form this structure that functionsas a filter for food substances such as amino acids to be absorbedinto the hemolymph, while “impure” food such as excessive sugarsare pushed into the descending midgut by the muscular caeca. Itis hypothesized that the majority of TYLCV virions are translocatedfrom the filter chamber into the hemolymph (Fig. 1), while a minor-ity of the virions circulate into the descending then the ascendingmidguts, and cross the midgut epithelial cells to the hemolymph(Ghanim and Medina, 2007; Skaljac and Ghanim, 2010). Micro-scopic studies have shown extensive location of TYLCV virionsin the filter chamber, and their concentration decreases towardthe descending and the ascending midguts (Ghanim et al., 2009;Skaljac and Ghanim, 2010 and Fig. 1). Unlike aphids and someluteoviruses, TYLCV virions cross the epithelial cells in the midgutand not the hindgut, and the specificity for virus movement acrossthe digestive system resides in this area (Czosnek et al., 2002).In the hemolymph, TYLCV virions were shown to interact with a63 kDa GroEL protein produced by the endosymbiotic bacteria ofB. tabaci, which is hypothesized to protect the virions from pro-teolysis by the insect’s immune system (Morin et al., 1999, 2000;Gottlieb et al., 2010). Extensive studies have shown that this pro-tein is produced by the B. tabaci secondary symbiont, Hamiltonelladefensa. Other GroEL proteins from other endosymbiotic bacteriaharbored in B. tabaci such as the primary symbiont Portiera andthe secondary Rickettsia, Arsenophonus and Wolbachia did not inter-act with TYLCV CP. Hamiltonella GroEL has been shown to interactwith TYLCV in the hemolymph but not in the midgut or the sali-vary glands (Gottlieb et al., 2010). TYLCV Virions cross the firstbarrier of the digestive system into the hemolymph within 1 h fol-lowing acquisition (Ghanim et al., 2001a). The second recognitionbarrier is thought to reside on the apical membrane of the pri-mary salivary gland of B. tabaci (Brown and Czosnek, 2002), unlikethe aphid-luteovirus system in which recognition resides in theaccessory salivary glands (Gildow and Rochow, 1980; Gildow andGray, 1993; Gray and Gildow, 2003). In the search for proteins thatinteract with begomoviruses while translocating in their white-fly vectors, Ohnesorge and Bejarano (2009) reported that 16 kDasmall heat shock protein belonging to HSP20—a crystalline fam-ily is able to bind TYLCSV CP. The TYLCSV CP interaction domainwith BtHSP16 was located within the conserved region of theN-terminal part of TYLCSV CP (amino acids 47–66), overlappingalmost completely with the nuclear localization signal describedfor the CP of TYLCV (Kunik et al., 1998). The region necessary fortransmission of TYLCSV by B. tabaci (amino acids 129–152) is notdirectly involved in the specific interaction between the CP andthe BtHSP16. Although this study identified a protein that interactswith TYLCSV, no specific co-localization of the protein with CP wasdemonstrated. A recent study has demonstrated that a whitefly-encoded (instead of endosymbiont-encoded) Heat Shock Protein70 (HSP70) directly interacts with TYLCV and SLCV CPs (Gotz et al.,2012). This protein was identified using a microarray screen thattested the response of viruliferous whiteflies to the acquisition andretention of TYLCV and SLCV. While the expression of a low num-ber of genes was significantly altered, the expression of HSP70


at the gene and protein levels was up-regulated in response tothe presence of these viruses in B. tabaci. Immunocapture PCR,protein coimmunoprecipitation, and virus overlay protein bindingassays confirmed an in vitro interaction between TYLCV and HSP70.


ING ModelV

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FlvMTgttb2w(iTlbtw(mdaittermiic(becntipwCtsrTpcct2oamugliahi(ufSiR



luorescence in situ hybridization and immunolocalization also co-ocalized TYLCV and the bipartite Watermelon chlorotic stunt virusirions with HSP70 in midgut epithelial cells (Gotz et al., 2012).embrane feeding of whiteflies with anti-HSP70 antibodies and

YLCV virions resulted in an increase in TYLCV transmission sug-esting an inhibitory role for HSP70 in virus transmission; a rolehat might be related to protection against begomoviruses whileranslocating in the whitefly, and adding further evidence thategomoviruses might be harmful to their whitefly host (Gotz et al.,012). To further identify proteins that participate in begomovirus-hitefly interactions, more than 20,000 Expressed Sequence Tags

ESTs) from adult whiteflies, as well as other developmental stagesncluding nymphs, eggs, and viruliferous adults with TYLCV andoMoV, were prepared (Leshkowitz et al., 2006). This was the firstarge-scale sequencing project of ESTs from B. tabaci which led toetter understanding the genetic makeup of the whitefly relativeo other insect models. It was estimated that the genome of thehitefly is about five times the genome of Drosophila melanogaster

Brown et al., 2005). Following this sequencing, a spotted DNAicroarray containing 6000 unique ESTs from the whitefly was

eveloped and used to study several aspects of the whitefly biologynd interaction with the environment, including the resistance of tonsecticides (Ghanim and Kontsedalov, 2007), its immune responseo parasitoids (wasp Eretmocerus mundus) (Mahadav et al., 2008),o heat stress conditions in the B and the Q biotypes (Mahadavt al., 2009), and the whitefly’s response to the acquisition andetention of begomoviruses (Gotz et al., 2012). Efforts were recentlyade to sequence more ESTs from the whitefly, and recent stud-

es using next generation sequencing technologies such as thellumina platform, have generated up to 100,000 ESTs. The trans-riptional response of B. tabaci B biotype to TYLCV from ChinaTYLCCNV) (Luan et al., 2011) identified 1606 genes involved in 157iochemical pathways that were differentially expressed in virulif-rous whiteflies. This indicates that TYLCCNV can perturb the cellycle and primary metabolism in the whitefly and may explain theegative effect of this virus on the longevity and fecundity of B.abaci. The study demonstrated that TYLCCNV can activate whiteflymmune responses, such as autophagy and antimicrobial peptideroduction, which might lead to a gradual decrease of viral particlesithin the viruliferous whitefly. Further results showed that TYL-CNV can invade the ovary and fat body tissues of the whitefly andhis invasion induced autophagy in both the ovary and fat body tis-ues. Surprisingly, TYLCCNV also suppressed the whitefly immuneesponses by down-regulating the expression of genes involved inoll-like signaling and mitogen-activated protein kinase (MAPK)athways (Luan et al., 2011). A recent study sequenced the trans-riptome of the primary salivary glands (an organ with only 13–20ells) of the Q biotype of B. tabaci using an effective cDNA amplifica-ion method in combination with short read sequencing (Su et al.,012). As previously mentioned, the primary salivary gland is a keyrgan involved in the circulative transmission of begomovirusesnd likely to harbor proteins/receptor that determines the trans-ission efficiency of begomoviruses. The study obtained 13,615

nigenes including 3159 sequences and the quantity of the uni-enes obtained from the salivary glands of the whitefly was ateast four fold the salivary gland genes from other sap-suckingnsects. Functional analysis revealed genes related to metabolismnd transport. Moreover, the results showed that a number ofighly expressed genes in the salivary glands might be involved

n secretory protein processing, secretion and virus transmissionSu et al., 2012). Although many of the described studies are stillnderway, the path to considering B. tabaci as an organism with a


ully sequenced genome with rich genomic resources is still long.ome functional genomics tools that could be employed in validat-ng candidate genes involved in begomovirus transmission such asNA interference (RNAi) (Ghanim et al., 2007) are being developed,


however, many other resources such as protocols for makingtransgenic whiteflies and maintaining these transgenic strains,developing phenotypic markers and sequencing the whiteflygenome are still lacking.

8. Concluding remarks

Begomoviruses vectored by B. tabaci can cause some of the mostdevastating viral diseases in agricultural cropping systems world-wide. While new and diverse pest control strategies are adoptedfor controlling whiteflies, they continue to pose great economicimpact. Differences in plant host-preference, host range, fecun-dity, dispersal behavior, vector competency, phytotoxic feedingeffects, endosymbiont composition, invasiveness, and insecticideresistance, are all among the factors that directly influence the abil-ity of B. tabaci to become a worldwide invasive species. Researchon TYLCV–plant and TYLCV–B. tabaci interactions have resultedin hundreds of research publications describing various aspectsof the biological, molecular and cellular events underlying theseinteractions. Whitefly genomics research is expected to lead thediscovery of novel strategies for whitefly and whitefly-transmittedvirus management based on an improved understanding of molec-ular, cellular, and biological processes. The genome sequence of B.tabaci will synergize projects underway to develop and sequenceB. tabaci ESTs or cDNA libraries for functional genomics and pro-teomics analysis. The benefits are far reaching and include theirapplication to identify genes that combat abiotic and biotic stressesthat often lead to invasiveness and insecticide resistance, and tounderstand the basis for whitefly-virus specificity. Collectively,genomics, proteomics, and functional genomics efforts will initi-ate further local, regional, national and international partnershipsto expand present and future efforts aimed at determining theB. tabaci genome and proceed to undertake functional genomicsaspects that are of high interest amongst a broad user community.

References

Ammar, E.D., Khlifa, E.A., Mahmoud, A., Abol-Ela, S.E., Peterschmitt, M., 2007. Evi-dence for multiplication of the leafhopper-borne maize yellow stripe virus inits vector using ELISA and dot-blot hybridization. Archives of Virology 152,489–494.

Ascencio-Ibanez, J.T., Dıaz-Plaza, R., Mendez-Lozano, J., Monsalve-Fonnegra, Z.I.,Arguello-Astorga, G.R., Rivera-Bustamante, R.F., 1999. First report of tomato yel-low leaf curl geminivirus in Yucatan, Mexico. Plant Disease 83, 1178.

Atzmon, G., van Hoss, H., Czosnek, H., 1998. PCR-amplification of tomato yellowleaf curl virus (TYLCV) from squashes of plants and insect vectors: applicationto the study of TYLCV acquisition and transmission. European Journal of PlantPathology 104, 189–194.

Bauman, P., Munson, M.A., Lai, C.Y., Clark, M.A., Baumann, L., Moran, N.A., Camp-bell, B.C., 1993. Origin and properties of bacterial endosymbionts of aphids,whiteflies, and mealybugs. ASM News 5, 21–24.

Bejarano, E.R., Khashoggi, A., Witty, M., Lichtenstein, C.P., 1996. Integration ofmultiple repeats of geminiviral DNA into the nuclear genome of tobacco dur-ing evolution. In: Proceedings of the National Academy of Sciences USA, pp.759–764, 93.

Black, L.M., 1950. A plant virus that multiplies in its insect vector. Nature 166,852–853.

Bosco, D., Mason, G., Accotto, G.P., 2004. TYLCSV DNA, but not infectivity, can betransovarially inherited by the progeny of the whitefly vector Bemisia tabaci(Gennadius). Virology 323, 276–283.

Brown, J.K., 2007a. The Bemisia tabaci species complex: genetic and phenotypic vari-ation and relevance to TYLCV-vector interactions. In: Czosnek, H. (Ed.), ToamtoYellow Leaf Curl Virus Disease: Management, Molecular Biology, Breeding forresistance. Springer, Dordrech, pp. 25–56.

Brown, J.K., 2007b. The Bemisia tabaci species complex: genetic and phenotypic vari-ation and relevance to TYLCV–vector interactions. In: Tomato Yellow Leaf CurlVirus Disease. Springer, New York and Tokyo, pp. 25–55, 447 pp.

Brown, J.K., Lambert, G.M., Ghanim, M., Czosnek, H., Galbraith, D.W., 2005.Nuclear DNA content of the whitefly Bemisia tabaci (Genn.) (Aleyrodidae:


Homoptera/Hemiptera) estimated by flow cytometry. Bulletin of EntomologicalResearch 95, 309–312.

Brown, J.K., Czosnek, H., 2002. Whitefly transmission of plant viruses. In: Plumb,R.T. (Ed.), Advances in Botanical Research. Academic press, New York, NY, pp.65–100.


http://refhub.elsevier.com/S0168-1702(14)00036-7/sbref0005





















































































































































































































































































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rown, J.K., Frohlich, D.R., Rosell, R.C., 1995. The sweetpotato or silverleafwhiteflies—biotypes of Bemisia tabaci or a species complex. Annual Review ofEntomology 40, 511–534.

rumin, M., Kontsedalov, S., Ghanim, M., 2011. Rickettsia influences thermotolerancein the whitefly Bemisia tabaci B biotype. Insect Science 18, 57–66.

aciagli, P., Medina, V., Marian, D., Vecchiati, M., Masenga, V., Mason, G., Falcioni,T., Noris, E., 2009. Virion stability is important for the circulative transmis-sion of Tomato yellow leaf curl sardinia virus by Bemisia tabaci, but virion accessto salivary glands does not guarantee transmissibility. Journal of Virology 83,5784–5795.

aciagli, P., Bosco, D., 1997. Quantitation over time of tomato yellow leaf curl gemi-nivirus DNA in its whitefly vector. Phytopathology 87, 610–613.

aciagli, P., Bosco, D., Al-Bitar, L., 1995. Relationships of the Sardinian isolate oftomato yellow leaf curl geminivirus with its whitefly vector Bemisia tabaci Gen.European Journal of Plant Pathology 101, 163–170.

ohen, S., Duffus, J.E., Liu, H.Y., 1989. Acquisition, interference, and retention ofcucurbit leaf curl viruses in whiteflies. Phytopathology 79, 109–113.

ohen, S., Duffus, J.E., Larsen, R.C., Liu, H.Y., Flock, R.A., 1983. Purification, sero-logy, and vector relationships of Squash leaf curl virus, a whitefly-transmittedgeminivirus. Phytopathology 73, 1669–1673.

ohen, S., Nitzany, F.E., 1966. Transmission and host range of the tomato yellow leafcurl virus. Phytopathology 56, 1127–1131.

osta, H.S., Brown, J.K., 1991. Variation in biological characteristics and in esterasepatterns among populations of Bemisia tabaci (Genn.) and the association of onepopulation with silverleaf symptom development. Entomologia experimentaliset Applicata 61, 211–219.

zosnek, H., Ghanim, M., 2012. Back to basics: are begomoviruses whiteflypathogens? Journal of Integrative Agriculture 11, 225–234.

zosnek, H., Ghanim, M., Ghanim, M., 2002. Circulative pathway of begomovirusesin the whitefly vector Bemisia tabaci—insights from studies with Tomato yellowleaf curl virus. Annals of Applied Biology 140, 215–231.

zosnek, H.G., Ghanim, M., Rubinstein, G., Morin, S., Fridman, V., Zeidan, M., 2001.Whiteflies: Vectors, and victims (?), of geminiviruses. In: Maramorosch, K. (Ed.),Advances in Virus Research, 57. Academic Press, New York, NY, pp. 291–322.

zosnek, H., Laterrot, H., 1997. A world-wide survey of tomato yellow leaf curl viruses.Archives of Virology 142, 1391–1406.

e Barro, P.J., Liu, S.S., Boykin, L.M., Dinsdale, A.B., 2011. Bemisia tabaci: a statementof species status. Annual Review of Entomology 56, 1–19.

ennehy, T.J., Degain, B.A., Harpold, V.S., Zaborac, M., Morin, S., Fabrick, J.A., Nichols,R.L., Brown, J.K., Byrne, F.J., Li, X., 2010. Extraordinary resistance to insecticidesreveals exotic Q biotype of Bemisia tabaci (Gennadius) in the New World. Journalof Economic Entomology 103, 2174–2186.

ennehy, T.J., DeGain, B., Harpold, G., Brown, J.K., Byrne, F., Morin, S., Nichols, R.L.,2006. First new world report of Q biotype of Bemisia tabaci (Gennadius) revealshigh levels of resistance to insecticides. RPM Newsletter 5, 18–19.

insdale, A.B., Cook, L., Riginos, C., Buckley, Y.M., De Barro, P., 2010. Refined globalanalysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyro-didae) mitochondrial cytochrome oxidase I to identify species level geneticboundaries. Annals of the Entomological Society of America 103, 196–208.

ang, Y., Jiao, X., Xie, W., Wang, S., Wu, Q., Shi, X., Chen, G., Su, Q., Yang, X., Pan, H.,Zhang, Y., 2013. Tomato yellow leaf curl virus alters the host preferences of itsvector Bemisia tabaci. Scientific Reports 3, 2876.

e Assis Filho, F.M., Naidu, R.A., Deom, C.M., Sherwood, J.L., 2002. Dynamics of Tomatospotted wilt virus replication in the alimentary canal of two thrips species. Phy-topathology 92, 729–733.

irdaus, S., Vosman, B., Hidayati, N., Supena, E.D.J., Visser, R.G.F., van Heusden, A.W.,2013. The Bemisia tabaci species complex: additions from different parts of theworld. Insect Science, http://dx.doi.org/10.1111/1744-7917.12001.

rohlich, D., Torres-Jerez, I., Bedford, I.D., Markham, P.G., Brown, J.K., 1999. Aphylogeographic analysis of the Bemisia tabaci species complex based on mito-chondrial DNA markers. Molecular Ecology 8, 1593–1602.

hanim, M., Brumin, M., Popovski, S., 2009. A simple, rapid and inexpensive methodfor localization of Tomato yellow leaf curl virus and Potato leafroll virus in plantand insect vectors. Journal of Virological Methods 159, 311–314.

hanim, M., Kontsedalov, S., Czosnek, H., 2007. Tissue-specific gene silencing by RNAinterference in the whitefly Bemisia tabaci (Gennadius). Insect Biochemistry andMolecular Biology 37, 732–738.

hanim, M., Medina, V., 2007. Localization of tomato yellow leaf curl virus in its white-fly vector Bemisia tabaci. In: Czosnek, H. (Ed.), Tomato Yellow Leaf Curl VirusDisease: Management, Molecular Biology, Breeding for Resistance. Springer,Dordrecht, pp. 171–183.

hanim, M., Kontsedalov, S., 2007. Gene expression in pyriproxyfen-resistantBemisia tabaci Q biotype. Pest Management Science 63, 776–783.

hanim, M., Morin, S., Czosnek, H., 2001a. Rate of tomato yellow leaf curl virus (TYLCV)translocation in the circulative transmission pathway of its vector, the whiteflyBemisia tabaci. Phytopathology 91, 188–196.

hanim, M., Rosell, R.C., Campbell, L.R., Czosnek, H., Brown, J.K., Ullman, D.E., 2001b.Microscopic analysis of the digestive, salivary and reproductive organs of Bemisiatabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B. Journal of Morphology248, 22–40.

hanim, M., Morin, S., Zeidan, M., Czosnek, H.G., 1998. Evidence for transovarial


transmission of tomato yellow leaf curl virus by its vector, the whitefly Bemisiatabaci. Virology 240, 295–303.

ibbs, M.J., Cooper, J.I., 1995. A recombinational event in the history of luteovirusesprobably induced by basepairing between the genomes of two distinct viruses.Virology 206, 1129–1132.

PRESS xxx (2014) xxx–xxx 7

Gildow, F.E., Gray, S.M., 1993. The aphid salivary gland basal lamina as a selec-tive barrier associated with vector-specific transmission of barley yellow dwarfluteovirus. Phytopathology 83, 1293–1302.

Gildow, F.E., Rochow, W.F., 1980. Role of accessory salivary glands in aphid trans-mission of barely yellow dwarf virus. Virology 104, 97–108.

Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Kontsedalov, S., Skaljac, M., Brumin,N., Sobol, I., Czosnek, H., Vavre, F., Fleury, F., Ghanim, M., 2010. The transmissionefficiency of tomato yellow leaf curl virus is correlated with the presence of a specificsymbiotic bacterium species. Journal of Virology 84, 9310–9317.

Gotz, M., Popovski, S., Kollenberg, M., Gorovits, R., Brown, J.K., Cicero, J., Czos-nek, H., Winter, S., Ghanim, M., 2012. Implication of Bemisia tabaci heatshock protein 70 in begomovirus–whitefly interactions. Journal of Virology 86,13241–13252.

Gray, S., Gildow, F.E., 2003. Luteovirus–aphid interactions. Annual Reviews of Phy-topathology 41, 539–566.

Himler, A.G., Adachi-Hagimori, T., Bergen, J.E., Kozuch, A., Kelly, S.E., Tabashnik, B.E.,Chiel, E., Duckworth, V.E., Dennehy, T.J., Zchori-Fein, E., Hunter, M.S., 2011. Rapidspread of a bacterial symbiont in an invasive whitefly is driven by fitness benefitsand female bias. Science 332 (6026), 254–256.

Horowitz, A.R., Kontsedalov, S., Khasdan, V., Ishaaya, I., 2005. Biotypes B and Q ofBemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance.Archives of Insect Biochemistry and Physiology 58, 216–225.

Hu, J., De Barro, P., Zhao, H., Wang, J., Nardi, F., Liu, S.-H., 2011. An extensive fieldsurvey combined with a phylogenetic analysis reveals rapid and widespreadinvasion of two alien whiteflies in China. PLoS One 6, e16061.

Ioannou, N., 1985. Yellow leaf curl and other diseases of tomato in Cyprus. PlantPathology 345, 428–434.

Jiang, Y.X., Dde Blas, C., Bedford, I.D., Nombela, G., Muniz, M., 2004. Effect of Bemisiatabaci biotype in the transmission of tomato yellow leaf curl sardinia virus(TYLCSV–ES) between tomato and common weeds. Spanish Journal of Agricul-tural Research 2, 115–119.

Jiu, M., Zhou, X.P., Tong, L., Xu, J., Yang, X., Wan, F.H., Liu, S.S., 2007. Vector-virusmutualism accelerates population increase of an invasive whitefly. PLoS One 2,e182.

Jupin, I., De Kouchkovsky, F., Jouanneau, F., Gronenborn, B., 1994. Movement oftomato yellow leaf curl geminivirus (TYLCV): involvement of the protein encodedby ORF C4. Virology 204, 82–90.

Kato, K., Onuki, M., Fuji, S., Hanada, K., 1998. The first occurrence of tomato yellowleaf curl virus in tomato (Lycopersicon esculentum Mill.) in Japan. Annals of thePhytopathological Society of Japan 64, 552–559.

Kontsedalov, S., Abu-Moch, F., Lebedev, G., Czosnek, H., Horowitz, A.Rami, Ghanim,M., 2012. Bemisia tabaci biotype dynamics and resistance to insecticides in Israelduring the years 2008–2010. Journal of Integrative Agriculture 11 (2), 312–320.

Kontsedalov, S., Gottlieb, Y., Ishaaya, I., Nauen, R., Horowitz, A.R., Ghanim, M., 2009.Toxicity of spiromesifen on the developmental stages of Bemisia tabacibiotypeB. Pest Management Science 65, 5–13.

Kontsedalov, S., Zchori-Fein, E., Chiel, E., Gottlieb, Y., Inbar, M., Ghanim, M., 2008.The presence of Rickettsia is associated with increased susceptibility of Bemisiatabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science 64,789–792.

Kunik, T., Palanichelvam, K., Czosnek, H., Citovsky, V., Gafni, Y., 1998. Nuclear Importof a geminivirus capsid protein in plant and insect cells: implications for the ViralNuclear Entry. The Plant Journal 13, 121–129.

Lefeuvre, P., Martin, D.P., Harkins, G., Lemey, P., Gray, A.J.A., Meredith, S., Lakay, F.,Monjane, A., Lett, J.M., Varsani, A., Heydarnejad, J., 2010. The spread of tomato yel-low leaf curl virus from the middle east to the world. PLoS Pathogens 6, e1001164.

Leshkowitz, D., Gazit, S., Reuveni, E., Ghanim, M., Czosnek, H., McKenzie, C., ShattersJr., R.G., Brown, J.K., 2006. Whitefly (Bemisia tabaci) genome project: analysis ofsequenced clones from egg, instar, and adult (viruliferous and non-viruliferous)cDNA libraries. BMC Genomics 7, 79.

Liu, S.S., Colvin, J., De Barro, P.J., 2012. Species concepts as applied to the whiteflyBemisia tabaci systematics: how many species are there? Journal of IntegrativeAgriculture 11, 176–186.

Liu, J., Zhao, H., Jiang, K., Zhou, X.P., Liu, S.S., 2009. Differential indirect effects of twoplant viruses on an invasive and an indigenous whitefly vector: implications forcompetitive displacement. Annals of Applied Biology 155, 39–448.

Liu, B.M., Preisser, E.L., Chu, D., Pan, H.P., Xie, W., Wang, S.L., Wu, Q.J., Zhou, X.G.,Zhang, Y.J., 2013. Multiple forms of vector manipulation by a plant-infectingvirus: Bemisia tabaci and tomato yellow leaf curl virus. Journal of Virology 87,4929–4937.

Luan, J.B., Li, J.M., Varela, N., Wang, Y.L., Li, F.F., Bao, Y.Y., Zhang, C.X., Liu, S.S., Wang,X.W., 2011. Global analysis of the transcriptional response of whitefly to tomatoyellow leaf curl china virus reveals their relationship of coevolved adaptations.Journal of Virology 85, 3330–3340.

Mahadav, A., Kontsedalov, S., Czosnek, H., Ghanim, M., 2009. Thermotolerance andgene expression following heat stress in the whitefly Bemisia tabaci B and Qbiotypes. Insect Biochemistry and Molecular Biology 39, 668–676.

Mahadav, A., Gerling, D., Gottlieb, Y., Czosnek, H., Ghanim, M., 2008. Parasitization bythe wasp Eretmocerus mundus induces transcription of genes related to immuneresponse and symbiotic bacteria proliferation in the whitefly Bemisia tabaci. BMCGenomics 9, 342.


Mansour, A., Al-Musa, A., 1992. Tomato yellow leaf curl virus: host range and virus-vector relationships. Plant Pathology 41, 122–125.

Matsuura, S., Hoshino, S., 2009. Effect of tomato yellow leaf curl disease on repro-duction of Bemisia tabaci Q biotype (Hemiptera: Aleyrodidae) on tomato plants.Applied Entomology and Zoology 44, 143–148.















































































































































































































































































































































































































































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cKenzie, C.L., 2002. Effect of tomato mottle virus (ToMoV) on Bemisia tabaci bio-type B (Homoptera: Aleyrodidae) oviposition and adult survivorship on healthytomato. Florida Entomologist 85, 367–368.

edina, V., Pinner, M.S., Bedford, I.D., Achon, M.A., Gemeno, C., Markham, P.G., 2006.Immunolocalization of tomato yellow leaf curl Sardinia virus in natural host plantsand its vector Bemisia tabaci. Journal of Plant Pathology 88, 299–308.

ehta, P., Wyman, J.A., Nakhla, M.K., Maxwell, D.P., 1994. Transmission of tomatoyellow leaf curl geminivirus by Bemisia tabaci. Journal of Economic Entomology87, 1291–1297.

omol, M.T., Simone, G.W., Dankers, W., Sprenkel, R.K., Olson, S.M., Mimol, E.A.,Polston, J.E., Hiebert, E., 1999. First report of tomato yellow leaf curl virus in tomatoin south Georgia. Plant Disease 83, 487.

orin, S., Ghanim, M., Sobol, I., Czosnek, H., 2000. The GroEL protein of thewhitefly Bemisia tabaci interacts with the coat protein of transmissible andnon-transmissible begomoviruses in the yeast two-hybrid system. Virology 276,404–416.

orin, S., Ghanim, M., Zeidan, M., Czosnek, H., Verbeek, M., van den Heuvel, J.F.J.M.,1999. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisiatabaci is implicated in the circulative transmission of Tomato yellow leaf curlvirus. Virology 30, 75–84.

oreno-Delafuente, A., Garzo, E., Moreno, A., Fereres, A., 2013. A plant virus manip-ulates the behavior of its whitefly vector to enhance its transmission efficiencyand spread. PLoS One 8, e61543.

uniyappa, V., Venkatesh, H.M., Ramappa, H.K., Kulkarni, R.S., Zeidan, M., Tarba, C.-Y., Ghanim, M., Czosnek, H., 2000. Tomato leaf curl virus from Bangalore (ToLCV-Ban4): sequence comparison with Indian ToLCV isolates, detection in plants andinsects, and vector relationships. Archives of Virology 145, 1583–1598.

avot, N., Zeidan, M., Pichersky, E., Zamir, D., Czosnek, H., 1992. Use of polymerasechain reaction to amplify tomato yellow leaf curl virus DNA from infected plantsand viruliferous whiteflies. Phytopathology 82, 1199–1202.

avot, N., Pichersky, E., Zeidan, M., Zamir, D., Czosnek, H., 1991. Tomato yellow leafcurl virus: a whitefly-transmitted geminivirus with a single genomic component.Virology 185, 151–161.

oris, E., Vaira, A.M., Caciagli, P., Masenga, V., Gronemborn, B., Accotto, G.P., 1998.Amino acids in the capsid protein of tomato yellow leaf curl virus that are crucialfor systemic infection, particle formation, and insect transmission. Journal ofVirology 72, 10050–10057.

hnesorge, S., Bejarano, E.R., 2009. Begomovirus coat protein interacts with a smallheatshock protein of its transmission vector (Bemisia tabaci). Insect MolecularBiology 18, 693–703.

adidam, M., Sawyer, S., Fauquet, C.M., 1999. Possible emergence of new gemi-niviruses by frequent recombination. Virology 265, 218–225.

an, H.P., Chu, D., Liu, B.M., Shi, X.B., Guo, L.T., Xie, W., Carrière, Y., Li, X.C., Zhang,Y.J., 2013. Differential effects of an exotic plant virus on its two closely related


vectors. Scientific Reports 3, 2230.an, H., Chu, D., Yan, W., Su, Q., Liu, B., Wang, S., Wu, Q., Xie, W., Jiao, X., Li, R., Yang,

N., Yang, X., Xu, B., Brown, J.K., Zhou, X., Zhang, Y., 2012. Rapid spread of tomatoyellow leaf curl virus in China is aided differentially by two invasive whiteflies.PLoS One 7 (4), e34817.


Polston, J.E., Al-Musa, A., Perring, T.M., Dodds, J.A., 1990. Association of the nucleicacid of squash leaf curl geminivirus with the whitefly Bemisia tabaci. Phytopatho-logy 80, 850–856.

Rubinstein, G., Czosnek, H.G., 1997. Long-term association of tomato yellow leafcurl virus (TYLCV) with its whitefly vector Bemisia tabaci: effect on the insecttransmission capacity, longevity and fecundity. Journal of General Virology 78,2683–2689.

Rybicki, E.P., Briddon, R.W., Brown, J.K., Fauquet, C.M., Maxwell, D.P., Stanley,J., Harrison, B.D., Markham, P.G., Bisaro, D.M., Robinson, D., 2000. FamilyGeminiviridae. In: Van Regenmortel, M.H.V., Fauquet, C.M., Bishop, D.H.L.,Carstens, E., Estes, M., Lemon, S., Maniloff, J., Mayo, M.A., McGeoch, D., Pringle,C., Wickner, R. (Eds.), Virus Taxonomy, Seventh Report of the InternationalCommittee on Taxonomy of Viruses. Academic Press, New York, NY, pp.285–297.

Sanchez-Campos, S., Navas-Castillo, J., Camero, R., Soria, C., Diaz, J.A., Moriones, E.,1999. Displacement of tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is intomato epidemics in Spain. Phytopathology 89, 1038–1043.

Schlee, D., 1970. Verwandtschaftsforschung an fossilen und rezenten Aleyrodina(Insectas, Hemiptera). Stuttgarter Beiträge zur Naturkunde 213, 1–74.

Sidhu, J.S., Mann, R.S., Butter, N.S., 2009. Deleterious effects of cotton leaf curl viruson longevity and fecundity of whitefly, Bemisia tabaci (Gennadius). Journal ofEntomology 6, 62–66.

Sinisterra, X.H., McKenzie, C.L., Hunter, W.B., Powell, C.A., Shatters Jr., R.G., 2005.Differential transcriptional activity of plant-pathogenic begomoviruses in theirwhitefly vector (Bemisia tabaci, Gennadius: Hemiptera Aleyrodidae). Journal ofGeneral Virology 86, 1525–1532.

Skaljac, M., Ghanim, M., 2010. Tomato yellow leaf curl virus and theplant–virus–vector interactions. Israel Journal of Plant Sciences 58,103–111.

Su, Y.L., Li, J.M., Li, M., Luan, J.B., Ye, X.D., Wang, X.W., Liu, S.S., 2012. Transcriptomicanalysis of the salivary glands of an invasive whitefly. PLoS One 7 (6), e39303.

Sylvester, E.S., 1973. Reduction of excretion, reproduction, and survival in Hyper-omyzus lactucae fed on plants infected with isolates of sowthistle yellow veinvirus. Virology 56, 632–635.

Wang, X.W., Luan, J.B., Li, J.M., Bao, Y.Y., Zhang, C.X., Liu, S.S., 2010. De novo charac-terization of a whitefly transcriptome and analysis of its gene expression duringdevelopment. BMC Genomics 11, 400.

Wartig, L., Kheyr-Pour, A., Noris, E., De Kouchkovsky, F., Jouanneau, F., Gronemborn,B., Jupin, I., 1997. Genetic analysis of the monopartite tomato yellow leaf curlgeminivirus: roles of V1, V2, and C2 ORFs in viral pathogenesis. Virology 228,132–140.

Zeidan, M., Czosnek, H.G., 1991. Acquisition of tomato yellow leaf curl virus by thewhitefly Bemisia tabaci. Journal of General Virology 72, 2607–2614.

Zhang, W., Olson, N.H., Baker, T.S., Faulkner, L., Agbandje-McKenna, M., Boulton, M.I.,


Davies, J.W., McKenna, R., 2001. Structure of the Maize streak virus geminateparticle. Virology 279, 471–477.

Zrachya, A., Glick, E., Levy, Y., Arazi, T., Citovsky, V., Gafni, Y., 2007. Suppressorof RNA silencing encoded by tomato yellow leaf curl virus-Israel. Virology 358,159–165.

























































































































































































































































































































































































































































































































































































































































































































Documents

A review of the mechanisms and components that determine the transmission efficiency of Tomato yellow leaf curl virus (Geminiviridae; Begomovirus) by its whitefly vector