Differential responses between a vector species Bemisia tabaci and a nonvector species Trialeurodes vaporariorum following ingestion of tomato yellow leaf curl virus

In transmitting plant viruses, insect vectors undergo physiological and behavioral alterations. The whitefly Bemisia tabaci is a vector of tomato yellow leaf curl virus (TYLCV), causing severe damages to various horticultural crop plants. To determine whether whitefly alteration is specific to vector species, the responses to TYLCV ingestion were compared between B. tabaci and Trialeurodes vaporariorum, a nonvector for TYLCV. The two species were reared on TYLCV‐infected and noninfected tomato, a host of TYLCV, and their longevity and fecundity were determined while rearing in either tomato or eggplant, a nonhost of TYLCV. TYLCV‐ingested B. tabaci increased their developmental rates but reduced fecundity when they were reared in either tomato or eggplant compared with those of TYLCV‐free ones. In contrast, TYLCV‐ingested T. vaporariorum did not show any of the aforementioned changes when reared on both plant species. In addition, TYLCV‐ingested B. tabaci increased their levels of three heat shock protein genes ( hsp20, hsp70, and hsp90) against thermal stress, whereas TYLCV‐ingested T. vaporariorum did not. The presence of TYLCV virions was identified in two colonies of both species via polymerase chain reaction analysis. TYLCV was detected in the whole body, saliva, and eggs of B. tabaci, while TYLCV was detected only in the whole body but not in the saliva and eggs of T. vaporariorum. The present results strongly indicated that TYLCV specifically manipulate physiological processes of the vector species, B. tabaci.     

Rapid spread of tomato yellow leaf curl virus in China is aided differentially by two invasive whiteflies

Background

Tomato yellow leaf curl virus (TYLCV) was introduced into China in 2006, approximately 10 years after the introduction of an invasive whitefly, Bemisia tabaci (Genn.) B biotype. Even so the distribution and prevalence of TYLCV remained limited, and the economic damage was minimal. Following the introduction of Q biotype into China in 2003, the prevalence and spread of TYLCV started to accelerate. This has lead to the hypothesis that the two biotypes might not be equally competent vectors of TYLCV.

Methodology/Principal Findings

The infection frequency of TYLCV in the field-collected B. tabaci populations was investigated, the acquisition and transmission capability of TYLCV by B and Q biotypes were compared under the laboratory conditions. Analysis of B. tabaci populations from 55 field sites revealed the existence of 12 B and 43 Q biotypes across 18 provinces in China. The acquisition and transmission experiments showed that both B and Q biotypes can acquire and transmit the virus, however, Q biotype demonstrated superior acquisition and transmission capability than its B counterparts. Specifically, Q biotype acquired significantly more viral DNA than the B biotype, and reached the maximum viral load in a substantially shorter period of time. Although TYLCV was shown to be transmitted horizontally by both biotypes, Q biotype exhibited significantly higher viral transmission frequency than B biotype. Vertical transmission result, on the other hand, indicated that TYLCV DNA can be detected in eggs and nymphs, but not in pupae and adults of the first generation progeny.

Conclusions/Significance

These combined results suggested that the epidemiology of TYLCV was aided differentially by the two invasive whiteflies (B and Q biotypes) through horizontal but not vertical transmission of the virus. This is consistent with the concomitant eruption of TYLCV in tomato fields following the recent rapid invasion of Q biotype whitefly in China.     

Inactivation of Wolbachia Reveals Its Biological Roles in Whitefly Host

Background

The whitefly Bemisia tabaci is cryptic species complex composed of numerous species. Individual species from the complex harbor a diversity of bacterial endosymbionts including Wolbachia. However, while Wolbachia is known to have a number of different roles, its role in B. tabaci is unclear. Here, the antibiotic rifampicin is used to selectively eliminate Wolbachia from B. tabaci so as to enable its roles in whitefly development and reproduction to be explored. The indirect effects of Wolbachia elimination on the biology of Encarsia bimaculata, a dominant parasitoid of B. tabaci in South China, were also investigated.

Methodology/Principal Finding

qRT-PCR and FISH were used to show that after 48 h exposure to 1.0 mg/ml rifampicin, Wolbachia was completely inactivated from B. tabaci Mediterranean (MED) without any significant impact on either the primary symbiont, Portiera aleyrodidarum or any of the other secondary endosymbionts present. For B. tabaci MED, Wolbachia was shown to be associated with decreased juvenile development time, increased likelihood that nymphs completed development, increased adult life span and increased percentage of female progeny. Inactivation was associated with a significant decrease in the body size of the 4^th instar which leads us to speculate as to whether Wolbachia may have a nutrient supplementation role. The reduction in nymph body size has consequences for its parasitoid, E. bimaculata. The elimination of Wolbachia lead to a marked increase in the proportion of parasitoid eggs that completed their development, but the reduced size of the whitefly host was also associated with a significant reduction in the size of the emerging parasitoid adult and this was in turn associated with a marked reduction in adult parasitoid longevity.

Conclusions/Significance

Wolbachia increases the fitness of the whitefly host and provides some protection against parasitization. These observations add to our understanding of the roles played by bacterial endosymbionts.     

An Invasive Whitefly Feeding on a Virus-Infected Plant Increased Its Egg Production and Realized Fecundity

Background

Plant-pathogenic begomoviruses have a complex association with their insect vectors. The interactions of begomoviruses and reproduction of their vectors are poorly understood. Bemisia tabaci is known to transmit many begomoviruses, and the spread of B. tabaci, especially the B and Q ‘biotypes’, has been accompanied by the epidemics of begomoviruses. One of these identified disease-causing agents was Tomato yellow leaf curl China virus (TYLCCNV).

Methodology/Principal Findings

In this study, we compared the egg production and realized fecundity of two ‘biotypes’ or putative species of the whitefly B. tabaci, including the alien invasive B and the indigenous ZHJ1 from Zhejiang, China, feeding on either healthy or TYLCCNV-infected tobacco plants. The ovary of the whitefly was composed of 12–22 telotrophic ovarioles. According to the morphology of the oocytes and level of yolk content, oocytes in ovarioles were divided into four developmental phases (I-IV). Significantly higher proportion of immature oocytes (phase II, III) and mature oocytes (phase IV) was observed in ovary of females that fed on TYLCCNV-infected tobacco compared to that on healthy plants. Moreover, there was significant increase of eggs laid of B whitefly that fed on TYLCCNV-infected tobacco plants during the early developmental stages. In contrast, the proportion of oocytes of different developmental phases and eggs laid had no significant differences between ZHJ1 whiteflies feeding on TYLCCNV-infected and non-infected host plants.

Conclusions/Significance

The invasive B whitefly benefits from feeding on a begomovirus-infected plant through increased egg production and realized fecundity.     

Plant Virus Differentially Alters the Plant's Defense Response to Its Closely Related Vectors

Background

The whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), is one of the most widely distributed agricultural pests. In recent years, B. tabaci Q has invaded China, and Q has displaced B in many areas now. In a number of regions of the world, invasion by B and/or Q has been followed by outbreaks of tomato yellow leaf curl virus (TYLCV). Our previous study showed TYLCV directly and indirectly modified the feeding behavior of B. tabaci in favor of Q rather than B.

Methodology/Principal Findings

In this study, we quantified the salicylic acid (SA) titers and relative gene expression of SA in tomato leaves that were infested with viruliferous or non-viruliferous B and Q. We also measured the impacts of exogenous SA on the performance of B and Q, including the effects on ovary development. SA titer was always higher in leaves that were infested with viruliferous B than with viruliferous Q, whereas the SA titer did not differ between leaves infested with non-viruliferous B and Q. The relative gene expression of SA signaling was increased by feeding of viruliferous B but was not increased by feeding of viruliferous Q. The life history traits of B and Q were adversely affected on SA-treated plants. On SA-treated plants, both B and Q had lower fecundity, shorter longevity, longer developmental time and lower survival rate than on untreated plants. Compared with whiteflies feeding on control plants, those feeding on SA-treated plants had fewer oocytes and slower ovary development. On SA-treated plants, viruliferous B had fewer oocytes than viruliferous Q.

Conclusions/Significance

These results indicate that TYLCV tends to induce SA-regulated plant defense against B but SA-regulated plant defense against Q was reduced. In other words, Q may have a mutualistic relationship with TYLCV that results in the reduction of the plant''s defense response.     

Feeding of Whitefly on Tobacco Decreases Aphid Performance via Increased Salicylate Signaling

Background

The feeding of Bemisia tabaci nymphs trigger the SA pathway in some plant species. A previous study showed that B. tabaci nymphs induced defense against aphids (Myzus persicae) in tobacco. However, the mechanism underlying this defense response is not well understood.

Methodology/Principal Findings

Here, the effect of activating the SA signaling pathway in tobacco plants through B. tabaci nymph infestation on subsequent M. persicae colonization is investigated. Performance assays showed that B. tabaci nymphs pre-infestation significantly reduced M. persicae survival and fecundity systemically in wild-type (WT) but not salicylate-deficient (NahG) plants compared with respective control. However, pre-infestation had no obvious local effects on subsequent M. persicae in either WT or NahG tobacco. SA quantification results indicated that the highest accumulation of SA was induced by B. tabaci nymphs in WT plants after 15 days of infestation. These levels were 8.45- and 6.14-fold higher in the local and systemic leaves, respectively, than in controls. Meanwhile, no significant changes of SA levels were detected in NahG plants. Further, biochemical analysis of defense enzymes polyphenol oxidase (PPO), peroxidase (POD), β-1,3-glucanase, and chitinase demonstrated that B. tabaci nymph infestation increased these enzymes’ activity locally and systemically in WT plants, and there was more chitinase and β-1, 3-glucanase activity systemically than locally, which was opposite to the changing trends of PPO. However, B. tabaci nymph infestation caused no obvious increase in enzyme activity in any NahG plants except POD.

Conclusions/Significance

In conclusion, these results underscore the important role that induction of the SA signaling pathway by B. tabaci nymphs plays in defeating aphids. It also indicates that the activity of β-1, 3-glucanase and chitinase may be positively correlated with resistance to aphids.     

Acylsucrose-producing tomato plants forces Bemisia tabaci to shift its preferred settling and feeding site

Background

The whitefly Bemisia tabaci (Genn.) causes dramatic damage to plants by transmitting yield-limiting virus diseases. Previous studies proved that the tomato breeding line ABL 14-8 was resistant to B. tabaci, the vector of tomato yellow leaf curl disease (TYLCD). This resistance is based on the presence of type IV glandular trichomes and acylsucrose production. These trichomes deter settling and probing of B. tabaci in ABL 14-8, which reduces primary and secondary spread of TYLCD.

Methodology/Principal Findings

Whitefly settlement preference was evaluated on the adaxial and abaxial leaf surfaces of nearly-isogenic tomato lines with and without B. tabaci-resistance traits, ‘ABL 14-8 and Moneymaker’ respectively, under non-choice and free-choice conditions. In addition, the Electrical Penetration Graph technique was used to study probing and feeding activities of B. tabaci on the adaxial and abaxial leaf surfaces of the same genotypes. B. tabaci preferred to settle on the abaxial than on the adaxial surface of ‘Moneymaker’ leaves, whereas no such preference was observed on ABL 14-8 tomato plants at the ten-leaf growth stage. Furthermore, B. tabaci preferred to feed on the abaxial than on the adaxial leaf surface of ‘Moneymarker’ susceptible tomato plants as shown by a higher number of sustained phloem feeding ingestion events and a shorter time to reach the phloem. However, B. tabaci standard probing and feeding behavior patterns were altered in ABL 14-8 plants and whiteflies were unable to feed from the phloem and spent more time in non-probing activities when exposed to the abaxial leaf surface.

Conclusions/Significance

The distorted behavior of B. tabaci on ABL 14-8 protects tomato plants from the transmission of phloem-restricted viruses such as Tomato yellow leaf curl virus (TYLCV), and forces whiteflies to feed on the adaxial side of leaves where they feed less efficiently and become more vulnerable to natural enemies.     

Tomato Yellow Leaf Curl Virus Benefits Population Growth of the Q Biotype of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae)

Plant viruses can directly influence their insect vectors, and indirectly through their shared host plant, altering their behavior and performance in a mutualistic or rather antagonistic manner. One of the most studied begomovirus, Tomato yellow leaf curl virus (TYLCV), may also facilitate the expansion of its vector, the whitefly Bemisia tabaci (Gennadius). Considering the likely expansion of the disease and its major vector, we studied the direct and the indirect effects of a Mediterranean isolate of this virus (TYLCV-IL) on the biological performance of the Q biotype of B. tabaci. The following parameters were examined: development time and viability of nymphs, sex ratio, fecundity, and fertility and longevity. The results varied from positive to neutral depending on the parameter and the effect studied. TYLCV accelerated nymphal developmental and increased male longevity of B. tabaci when viruliferous insects developed on TYLCV-immune eggplants (direct effects). An indirect, positive effect of TYLCV-infected plants was observed on fecundity of B. tabaci, which laid more eggs on virus-infected than on noninfected tomato plants. Our results show that TYLCV enhances the population increase of its whitefly vector and that there is a high risk of rapid expansion of both the virus and its vector—the MED species of B. tabaci—into new areas when both agents interact together.     

The Immune Strategy and Stress Response of the Mediterranean Species of the Bemisia tabaci Complex to an Orally Delivered Bacterial Pathogen

Background

The whitefly, Bemisia tabaci, a notorious agricultural pest, has complex relationships with diverse microbes. The interactions of the whitefly with entomopathogens as well as its endosymbionts have received great attention, because of their potential importance in developing novel whitefly control technologies. To this end, a comprehensive understanding on the whitefly defense system is needed to further decipher those interactions.

Methodology/Principal Findings

We conducted a comprehensive investigation of the whitefly''s defense responses to infection, via oral ingestion, of the pathogen, Pseudomonas aeruginosa, using RNA-seq technology. Compared to uninfected whiteflies, 6 and 24 hours post-infected whiteflies showed 1,348 and 1,888 differentially expressed genes, respectively. Functional analysis of the differentially expressed genes revealed that the mitogen associated protein kinase (MAPK) pathway was activated after P. aeruginosa infection. Three knottin-like antimicrobial peptide genes and several components of the humoral and cellular immune responses were also activated, indicating that key immune elements recognized in other insect species are also important for the response of B. tabaci to pathogens. Our data also suggest that intestinal stem cell mediated epithelium renewal might be an important component of the whitefly''s defense against oral bacterial infection. In addition, we show stress responses to be an essential component of the defense system.

Conclusions/Significance

We identified for the first time the key immune-response elements utilized by B. tabaci against bacterial infection. This study provides a framework for future research into the complex interactions between whiteflies and microbes.     

Infection of Bacterial Endosymbionts in Insects: A Comparative Study of Two Techniques viz PCR and FISH for Detection and Localization of Symbionts in Whitefly,Bemisia tabaci

Bacterial endosymbionts have been associated with arthropods and large number of the insect species show interaction with such bacteria. Different approaches have been used to understand such symbiont- host interactions. The whitefly, Bemisia tabaci, a highly invasive agricultural pest, harbors as many as seven different bacterial endosymbionts. These bacterial endosymbionts are known to provide various nutritional, physiological, environmental and evolutionary benefits to its insect host. In this study, we have tried to compare two techniques, Polymerase chain reaction (PCR) and Flourescence in situ Hybridisation (FISH) commonly used for identification and localization of bacterial endosymbionts in B. tabaci as it harbors one of the highest numbers of endosymbionts which have helped it in becoming a successful global invasive agricultural pest. The amplified PCR products were observed as bands on agarose gel by electrophoresis while the FISH samples were mounted on slides and observed under confocal microscope. Analysis of results obtained by these two techniques revealed the advantages of FISH over PCR. On a short note, performing FISH, using LNA probes proved to be more sensitive and informative for identification as well as localization of bacterial endosymbionts in B. tabaci than relying on PCR. This study would help in designing more efficient experiments based on much reliable detection procedure and studying the role of endosymbionts in insects.     

Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non‐vector herbivore

Plants frequently engage in simultaneous interactions with diverse classes of biotic antagonists. Differential induction of plant defence pathways by these antagonists, and interactions between pathways, can have important ecological implications; however, these effects are currently not well understood. We explored how Tomato yellow leaf curl virus (TYLCV) influenced the performance of its vector (Bemisia tabaci) and a non‐vector herbivore (Tetranychus urticae) occurring separately or together on tomato plants (Solanum lycopersicum). TYLCV enhanced the performance of B. tabaci, although this effect was statistically significant only in the absence of T. urticae, which adversely affected B. tabaci performance regardless of infection status. In contrast, the performance of T. urticae was enhanced (only) by the combined presence of TYLCV and B. tabaci. Analyses of phytohormone levels and defence gene expression in wild‐type tomatoes and various plant‐defence mutants indicate that the enhancement of herbivore performance (for each species) entails the disruption of downstream defences in the jasmonic acid (JA) pathway. For T. urticae, this disruption appears to involve antagonistic effects of salicylic acid (SA), which is cumulatively induced to high levels by B. tabaci and TYLCV. In contrast, TYLCV was found to suppress JA‐mediated responses to B. tabaci via mechanisms independent of SA.     

Bacterial Composition of the Human Upper Gastrointestinal Tract Microbiome Is Dynamic and Associated with Genomic Instability in a Barrett’s Esophagus Cohort

Background

The incidence of esophageal adenocarcinoma (EAC) has increased nearly five-fold over the last four decades in the United States. Barrett’s esophagus, the replacement of the normal squamous epithelial lining with a mucus-secreting columnar epithelium, is the only known precursor to EAC. Like other parts of the gastrointestinal (GI) tract, the esophagus hosts a variety of bacteria and comparisons among published studies suggest bacterial communities in the stomach and esophagus differ. Chronic infection with Helicobacter pylori in the stomach has been inversely associated with development of EAC, but the mechanisms underlying this association remain unclear.

Methodology

The bacterial composition in the upper GI tract was characterized in a subset of participants (n=12) of the Seattle Barrett’s Esophagus Research cohort using broad-range 16S PCR and pyrosequencing of biopsy and brush samples collected from squamous esophagus, Barrett’s esophagus, stomach corpus and stomach antrum. Three of the individuals were sampled at two separate time points. Prevalence of H. pylori infection and subsequent development of aneuploidy (n=339) and EAC (n=433) was examined in a larger subset of this cohort.

Results/Significance

Within individuals, bacterial communities of the stomach and esophagus showed overlapping community membership. Despite closer proximity, the stomach antrum and corpus communities were less similar than the antrum and esophageal samples. Re-sampling of study participants revealed similar upper GI community membership in two of three cases. In this Barrett’s esophagus cohort, Streptococcus and Prevotella species dominate the upper GI and the ratio of these two species is associated with waist-to-hip ratio and hiatal hernia length, two known EAC risk factors in Barrett’s esophagus. H. pylori-positive individuals had a significantly decreased incidence of aneuploidy and a non-significant trend toward lower incidence of EAC.     

Bacterial Diversity Associated with Wild Caught Anopheles Mosquitoes from Dak Nong Province,Vietnam Using Culture and DNA Fingerprint

Background

Microbiota of Anopheles midgut can modulate vector immunity and block Plasmodium development. Investigation on the bacterial biodiversity in Anopheles, and specifically on the identification of bacteria that might be used in malaria transmission blocking approaches, has been mainly conducted on malaria vectors of Africa. Vietnam is an endemic country for both malaria and Bancroftian filariasis whose parasitic agents can be transmitted by the same Anopheles species. No information on the microbiota of Anopheles mosquitoes in Vietnam was available previous to this study.

Method

The culture dependent approach, using different mediums, and culture independent (16S rRNA PCR – TTGE) method were used to investigate the bacterial biodiversity in the abdomen of 5 Anopheles species collected from Dak Nong Province, central-south Vietnam. Molecular methods, sequencing and phylogenetic analysis were used to characterize the microbiota.

Results and Discussion

The microbiota in wild-caught Anopheles was diverse with the presence of 47 bacterial OTUs belonging to 30 genera, including bacterial genera impacting Plasmodium development. The bacteria were affiliated with 4 phyla, Actinobacteria, Bacteroidetes, Firmicutes and Proteobacteria, the latter being the dominant phylum. Four bacterial genera are newly described in Anopheles mosquitoes including Coxiella, Yersinia, Xanthomonas, and Knoellia. The bacterial diversity per specimen was low ranging from 1 to 4. The results show the importance of pairing culture and fingerprint methods to better screen the bacterial community in Anopheles mosquitoes.

Conclusion

Sampled Anopheles species from central-south Vietnam contained a diverse bacterial microbiota that needs to be investigated further in order to develop new malaria control approaches. The combination of both culture and DNA fingerprint methods allowed a thorough and complementary screening of the bacterial community in Anopheles mosquitoes.     

Effect of Saccharomyces boulardii and Mode of Delivery on the Early Development of the Gut Microbial Community in Preterm Infants

Background

Recent advances in culture-independent approaches have enabled insights into the diversity, complexity, and individual variability of gut microbial communities.

Objectives

To examine the effect of oral administration of Saccharomyces (S.) boulardii and mode of delivery on the intestinal microbial community in preterm infants.

Study Design

Stool samples were collected from preterm newborns randomly divided into two groups: a probiotic-receiving group (n = 18) or a placebo group (n = 21). Samples were collected before probiotic intake (day 0), and after 2 and 6 weeks of supplementation. The composition of colonizing bacteria was assessed by 16S ribosomal RNA (rRNA) gene sequencing of fecal samples using the Ion 16S Metagenomics Kit and the Ion Torrent Personal Genome Machine platform.

Results

A total of 11932257 reads were generated, and were clustered into 459, 187, and 176 operational taxonomic units at 0 days, 2 weeks, and 6 weeks, respectively. Of the 17 identified phyla, Firmicutes Actinobacteria, Proteobacteria, and Bacteroidetes were universal. The microbial community differed at day 0 compared with at 2 weeks and 6 weeks. There was a tendency for increased bacterial diversity at 2 weeks and 6 weeks compared with day 0, and infants with a gestational age of 31 weeks or higher presented increased bacterial diversity prior to S. boulardii administration. Firmicutes and Proteobacteria remained stable during the observation period, whereas Actinobacteria and Bacteroidetes increased in abundance, the latter particularly more sharply in vaginally delivered infants.

Conclusion

While the mode of delivery may influence the development of a microbial community, this study had not enough power to detect statistical differences between cohorts supplemented with probiotics, and in a consequence, to speculate on S. boulardii effect on gut microbiome composition in preterm newborns.     

Influences of tetracycline on the reproduction of the B biotype of Bemisia tabaci (Homoptera: Aleyrodidae)

Wolbachia are extensively harbored by Bemisia tabaci (Gennadius) populations, which could induce reproductive alteration in the whitefly. Previous studies have indicated that Wolbachia in B. tabaci could be effectively eliminated by antibiotics. In the present study, the antibiotic tetracycline was used to remove Wolbachia from the B-biotype of B. tabaci, and its influences on the reproduction and development of the whitefly were investigated by biological crossing experiments. The results indicated that antibiotic treatment could induce almost complete unidirectional cytoplasmic incompatibility in B. tabaci populations. Specifically, the offspring sex ratio from the antibiotic-treated female × untreated male crossings was significantly male-biased. Moreover, the antibiotic cure also induced a developmental delay in the offspring of the whiteflies. However, molecular detection revealed that Wolbachia was not completely eliminated from the host whiteflies by tetracycline. Our data suggested that the reduction but not elimination of Wolbachia by antibiotic treatment could definitely alter the reproductive consequences and developmental process of the whitefly B. tabaci. This is the first report of unidirectional cytoplasmic incompatibility caused by Wolbachia in B. tabaci.     

Infection of tomato by Tomato Yellow Leaf Curl Virus alters the foraging behavior and parasitism of the parasitoid Encarsia formosa on Bemisia tabaci

Encarsia formosa Gahan is a solitary endoparasitoid that is commercially reared and released for augmentative biological control of whiteflies including Bemisia tabaci (Gennadius). Bemisia tabaci biotypes B and Q are two most invasive species that greatly reduce crop yields in China by feeding on plant sap and by transmitting Tomato Yellow Leaf Curl Virus (TYLCV). The effects of TYLCV infection of tomato on E. formosa foraging on B. tabaci B and Q are unknown. In Y-tube olfactometer assays in the present study, E. formosa significantly preferred TYLCV-infected tomato plants over TYLCV-free plants. The wasp females also significantly preferred TYLCV-infected tomato plants infested with 3rd-instar nymphs of B. tabaci biotype Q over TYLCV-free plants with biotype Q nymphs. However, no significant differences were observed when B. tabaci biotype B was infested on tomato plants. The oviposition bioassays confirmed that TYLCV infection on tomato plants resulted in the recruitment of parasitoids. These results indicate that TYLCV-infection of tomato increase the foraging of E. formosa on B. tabaci, as differs on the B and Q biotypes.     

A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread

Plant viruses can produce direct and plant-mediated indirect effects on their insect vectors, modifying their life cycle, fitness and behavior. Viruses may benefit from such changes leading to enhanced transmission efficiency and spread. In our study, female adults of Bemisia tabaci were subjected to an acquisition access period of 72 h in Tomato yellow leaf curl virus (TYLCV)-infected and non-infected tomato plants to obtain viruliferous and non-viruliferous whiteflies, respectively. Insects that were exposed to virus-infected plants were checked by PCR to verify their viruliferous status. Results of the Ethovision video tracking bioassays indicated that TYLCV induced an arrestant behavior of B. tabaci, as viruliferous whitefly adults remained motionless for more time and moved slower than non-viruliferous whiteflies after their first contact with eggplant leaf discs. In fact, Electrical Penetration Graphs showed that TYLCV-viruliferous B. tabaci fed more often from phloem sieve elements and made a larger number of phloem contacts (increased number of E1, E2 and sustained E2 per insect, p<0.05) in eggplants than non-viruliferous whiteflies. Furthermore, the duration of the salivation phase in phloem sieve elements (E1) preceding sustained sap ingestion was longer in viruliferous than in non-viruliferous whiteflies (p<0.05). This particular probing behavior is known to significantly enhance the inoculation efficiency of TYLCV by B. tabaci. Our results show evidence that TYLCV directly manipulates the settling, probing and feeding behavior of its vector B. tabaci in a way that enhances virus transmission efficiency and spread. Furthermore, TYLCV-B. tabaci interactions are mutually beneficial to both the virus and its vector because B. tabaci feeds more efficiently after acquisition of TYLCV. This outcome has clear implications in the epidemiology and management of the TYLCV-B. tabaci complex.