Location of Geminiviruses in the Whitefly Bemisia tabaci (Homoptera: Aleyrodidae)

Tomato yellow leaf curl virus (TYLCV) is the name given to a complex of geminiviruses infecting tomato cultures worldwide. TYLCV is transmitted by a single insect species, the whitefly Bemisia tabaci. Herein we show that a TYLCV isolate from Israel (TYLCV-Is) can be transmitted among whiteflies in a sex-dependent manner, in the absence of any other source of virus. TYLCV was transmitted from viruliferous males to females and from viruliferous females to males but not among insects of the same sex. Transmission took place when insects were caged in groups or in couples, in a feeding chamber or on cotton plants, a TYLCV nonhost. The recipient insects were able to efficiently inoculate tomato test plants. Insect-to-insect virus transmission was instrumental in increasing the number of whiteflies capable of infecting tomato test plants in a whitefly population. TYLCV was present in the hemolymph of whiteflies caged with viruliferous insects of the other sex; therefore, the virus follows, at least in part, the circulative pathway associated with acquisition from infected plants. Taken as a whole, these results imply that a plant virus can be sexually transmitted from insect to insect.Tomato yellow leaf curl virus (TYLCV) is the name given to a complex of genetically different geminiviruses (family Geminiviridae, genus Begomovirus) affecting tomato cultures worldwide (11). TYLCV is transmitted exclusively by the whitefly Bemisia tabaci in a circulative manner (7,28). Although acquisition and transmission parameters of TYLCV (as well as other begomoviruses) have been studied extensively (1,5,22,25,31), the association between TYLCV and B. tabaci is still poorly understood. Using a local virus isolate and an insect colony maintained in the laboratory, we have found that the association of TYLCV with its insect vector is suggestive of a pathogen-host interaction. Once acquired, the genome of the virus remains associated with the insect for its entire adult life. This long-term relationship was associated with a decrease in virus transmission efficiency, longevity, and fecundity of the insect (28). The virus was transmitted to the progenies of viruliferous whiteflies for at least two generations (13). In this study we have investigated the question of whether TYLCV can be transmitted from insect to insect in a sex-dependent manner.Transmission of viruses through the gametes of insects has been documented, especially for Drosophila spp. (3). One of the best-studied virus of this kind is the Drosophila S virus (DSV), a reolike virus (20) which causes developmental malformation (the S phenotype) in the SimES strain of Drosophila simulans (10). Microscopic observations revealed invasion of early differentiating male and female germ cells by DSV particles (21). DSV was transovarially transmitted to some of the progenies. The rate of virus transmission by males was lower than that by females, probably because the proportion of infected spermatozoa was relatively smaller (21). Another wellstudied virus is the baculovirus-like go...

Section: Discussionmentioning

confidence: 99%

Tomato Yellow Leaf Curl Geminivirus (TYLCV-Is) Is Transmitted among Whiteflies ( Bemisia tabaci ) in a Sex-Related Manner

Ghanim

Czosnek

2000

“…Once acquired, virions are transmissible for the life of the whitefly (4, 7). The current model for the transmission pathway is based on the aphid-transmitted polero-and luteoviruses (luteovirids), in vivo transmission parameters, anatomical studies, and transmission electron microscopy localization (4)(5)(6)(8)(9)(10). In aphids and whiteflies, the gut membrane is thought to regulate transmission competency (8,11), whereas the salivary tissues regulate the specificity of vector-virus interactions.…”

mentioning

confidence: 99%

Implication of the Bacterial Endosymbiont Rickettsia spp. in Interactions of the Whitefly Bemisia tabaci with Tomato yellow leaf curl virus

Kliot

Cilia

Czosnek

et al. 2014

100

Numerous animal and plant viruses are transmitted by arthropod vectors in a persistent, circulative manner. Tomato yellow leaf curl virus (TYLCV) is transmitted by the sweet potato whitefly Bemisia tabaci. We report here that infection with Rickettsia spp., a facultative endosymbiont of whiteflies, altered TYLCV-B. tabaci interactions. A B. tabaci strain infected with Rickettsia acquired more TYLCV from infected plants, retained the virus longer, and exhibited nearly double the transmission efficiency compared to an uninfected B. tabaci strain with the same genetic background. Temporal and spatial antagonistic relationships were discovered between Rickettsia and TYLCV within the whitefly. In different time course experiments, the levels of virus and Rickettsia within the insect were inversely correlated. Fluorescence in situ hybridization analysis of Rickettsia-infected midguts provided evidence for niche exclusion between Rickettsia and TYLCV. In particular, high levels of the bacterium in the midgut resulted in higher virus concentrations in the filter chamber, a favored site for virus translocation along the transmission pathway, whereas low levels of Rickettsia in the midgut resulted in an even distribution of the virus. Taken together, these results indicate that Rickettsia, by infecting the midgut, increases TYLCV transmission efficacy, adding further insights into the complex association between persistent plant viruses, their insect vectors, and microorganism tenants that reside within these insects. IMPORTANCEInterest in bacterial endosymbionts in arthropods and many aspects of their host biology in agricultural and human health systems has been increasing. A recent and relevant studied example is the influence of Wolbachia on dengue virus transmission by mosquitoes. In parallel with our recently studied whitefly-Rickettsia-TYLCV system, other studies have shown that dengue virus levels in the mosquito vector are inversely correlated with bacterial load. Our work here presents evidence of unifying principles between vectors of plant and animal viruses in a role for endosymbionts in manipulating vector biology and pathogen transmission. Our results demonstrate the influence of an interesting and prominent bacterial endosymbiont in Bemisia tabaci in TYLCV transmission, a worldwide disease infecting tomatoes. Besides its agricultural importance, this system provides interesting insights into Bemisia interaction with these newly discovered endosymbionts.

“…Similar to other whiteflyborne geminiviruses, B. tabaci transmits TYLCV in a persistent-circulative nonpropagative manner (15), while some evidence points to viral transcriptional activity in the vector (38). During feeding, TYLCV virions are ingested through the stylet, taken up by midgut epithelial cells, and mobilized to the hemolymph, where they circulate until they enter the salivary glands, from which they are discharged into the plant (9,11,17,24). TYLCV coat protein (CP) is the only virus-encoded protein required for vector-mediated transmission (1,5,19,34).…”

mentioning

confidence: 99%

The Transmission Efficiency of Tomato Yellow Leaf Curl Virus by the Whitefly Bemisia tabaci Is Correlated with the Presence of a Specific Symbiotic Bacterium Species

Gottlieb

Zchori-Fein

Mozes-Daube

et al. 2010

278

232

Tomato yellow leaf curl virus (TYLCV) (Geminiviridae: Begomovirus) is exclusively vectored by the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). TYLCV transmission depends upon a 63-kDa GroEL protein produced by the vector's endosymbiotic bacteria. B. tabaci is a species complex comprising several genetically distinct biotypes that show different secondary-symbiont fauna. In Israel, the B biotype harbors Hamiltonella, and the Q biotype harbors Wolbachia and Arsenophonus. Both biotypes harbor Rickettsia and Portiera (the obligatory primary symbionts). The aim of this study was to determine which B. tabaci symbionts are involved in TYLCV transmission using B. tabaci populations collected in Israel. Virus transmission assays by B. tabaci showed that the B biotype efficiently transmits the virus, while the Q biotype scarcely transmits it. Yeast two-hybrid and protein pulldown assays showed that while the GroEL protein produced by Hamiltonella interacts with TYLCV coat protein, GroEL produced by Rickettsia and Portiera does not. To assess the role of Wolbachia and Arsenophonus GroEL proteins (GroELs), we used an immune capture PCR (IC-PCR) assay, employing in vivo-and in vitro-synthesized GroEL proteins from all symbionts and whitefly artificial feeding through membranes. Interaction between GroEL and TYLCV was found to occur in the B biotype, but not in the Q biotype. This assay further showed that release of virions protected by GroEL occurs adjacent to the primary salivary glands. Taken together, the GroEL protein produced by Hamiltonella (present in the B biotype, but absent in the Q biotype) facilitates TYLCV transmission. The other symbionts from both biotypes do not seem to be involved in transmission of this virus.