Xiaobin Shi

Differential effects of an exotic plant virus on its two closely related vectors

Concurrent spread of Tomato yellow leaf curl virus (TYLCV) with invasion of Bemisia tabaci Q rather than B in China suggests a more mutualistic relationship between TYLCV and Q than B. To assess this hypothesis, we quantified the impacts of TYLCV on the performance and competitiveness of B and Q in the laboratory. The results showed that relative to their non-infected counterparts feeding on cotton (a non-host for TYLCV), infected B exhibited significant reductions in life-history traits, whereas infected Q only showed marginal reductions. While Q performed better on TYLCV-infected tomato plants than on uninfected ones, the reverse was observed in B. Q displacement by B took one more generation on TYLCV-infected tomato plants than on healthy ones. These results demonstrate that TYLCV was indirectly mutualistic to Q but directly and indirectly parasitic to B.

Tomato yellow leaf curl virus alters the host preferences of its vector Bemisia tabaci

Bemisia tabaci, the whitefly vector of Tomato yellow leaf curl virus (TYLCV), seriously reduces tomato production and quality. Here, we report the first evidence that infection by TYLCV alters the host preferences of invasive B. tabaci B (Middle East-Minor Asia 1) and Q (Mediterranean genetic group), in which TYLCV-free B. tabaci Q preferred to settle on TYLCV-infected tomato plants over healthy ones. TYLCV-free B. tabaci B, however, preferred healthy tomato plants to TYLCV-infected plants. In contrast, TYLCV-infected B. tabaci, either B or Q, did not exhibit a preference between TYLCV-infected and TYLCV-free tomato plants. Based on gas chromatography-mass spectrometry (GCMS)analysis of plant terpene volatiles, significantly more β-myrcene, thymene, β-phellandrene, caryophyllene, (+)-4-carene, and α-humulene were released from the TYLCV-free tomato plants than from the TYLCV-infected ones. The results indicate TYLCV can alter the host preferences of its vector Bemisia tabaci B and Q.

Bemisia tabaci Q carrying tomato yellow leaf curl virus strongly suppresses host plant defenses

The concurrence of tomato yellow leaf curl virus (TYLCV) with the spread of its vector Bemisia tabaci Q rather than B in China suggests a more mutualistic relationship between TYLCV and Q. Here, we investigated the hypothesis that viruliferous B and Q have different effects on plant defenses. We found the fecundity of nonviruliferous B, nonviruliferous Q, viruliferous Q and viruliferous B was 11.080, 12.060, 10.760, and 11.220 respectively on plants previously attacked by the other biotype, however, on their respective noninfested control leaves fecundity was 12.000, 10.880, 9.760, and 8.020 respectively. Only viruliferous B had higher fecundity on viruliferous Q-infested plants than on control plants. The longevity of viruliferous B showed the same phenomenon. At 1 d infestion, the jasmonic acid content in leaves noninfested and in leaves infested with nonviruliferous B, nonviruliferous Q, viruliferous B and viruliferous Q was 407.000, 281.333, 301.333, 266.667 and 134.000 ng/g FW, respectively. The JA content was lowest in viruliferous Q-infested leaves. The proteinase inhibitor activity and expression of JA-related upstream gene LOX and downstream gene PI II showed the same trend. The substantial suppression of host defenses by Q carrying TYLCV probably enhances the spread of Q and TYLCV in China.

Transmission of Tomato Yellow Leaf Curl Virus by Bemisia tabaci as Affected by Whitefly Sex and Biotype

Bemisia tabaci is a serious pest of vegetables and other crops worldwide. The most damaging and predominant B. tabaci biotypes are B and Q, and both are vectors of tomato yellow leaf curl virus (TYLCV). Previous research has shown that Q outperforms B in many respects but comparative research is lacking on the ability of B and Q to transmit viruses. In the present study, we tested the hypothesis that B and Q differ in their ability to transmit TYLCV and that this difference helps explain TYLCV outbreaks. We compared the acquisition, retention, and transmission of TYLCV by B and Q females and males. We found that Q females are more efficient than Q males, B females, and B males at TYLCV acquisition and transmission. Although TYLCV acquisition and transmission tended to be greater for B females than B males, the differences were not statistically significant. Based on electrical penetration graphs determination of phloem sap ingestion parameters, females fed better than males, and Q females fed better than Q males, B females, or B males. These results are consistent with the occurrences of TYLCV outbreaks in China, which have been associated with the spread of Q rather than B.

Virus infection of a weed increases vector attraction to and vector fitness on the weed

Weeds are important in the ecology of field crops, and when crops are harvested, weeds often become the main hosts for plant viruses and their insect vectors. Few studies, however, have examined the relationships between plant viruses, vectors, and weeds. Here, we investigated how infection of the weed Datura stramonium L. by tomato yellow leaf curl virus (TYLCV) affects the host preference and performance of the TYLCV vector, Bemisia tabaci (Gennadius) Q. The results of a choice experiment indicated that B. tabaci Q preferentially settled and oviposited on TYLCV-infected plants rather than on healthy plants. In addition, B. tabaci Q performed better on TYLCV-infected plants than on healthy plants. These results demonstrate that TYLCV is indirectly mutualistic to B. tabaci Q. The mutually beneficial interaction between TYLCV and B. tabaci Q may help explain the concurrent outbreaks of TYLCV and B. tabaci Q in China.

Three-Way Interactions Between the Tomato Plant, Tomato Yellow Leaf Curl Virus, and Bemisia tabaci (Hemiptera: Aleyrodidae) Facilitate Virus Spread

ABSTRACT Plant defense responses can greatly affect plant viruses and their herbivore vectors. The current article reports on plant defense responses involving jasmonic acid (JA), salicylic acid (SA), and proteinase inhibitor (PI) in the three-way interaction between tomato plants, tomato yellow leaf curl virus, and the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). The results showed that feeding by viruliferous B. tabaci increases the longevity and fecundity of nonviruliferous B. tabaci that subsequently feed on the same plant. Feeding by nonviruliferous B. tabaci alone suppressed plant defense responses involving JA and PI but induced responses involving SA. Feeding by viruliferous B. tabaci increased the suppression of plant defenses involving JA and PI but did not increase responses involving SA. These results indicate that the interactive effects of tomato yellow leaf curl virus and B. tabaci on plants increase vector fitness and virus transmission by reducing plant defense.

The Salicylic Acid-Mediated Release of Plant Volatiles Affects the Host Choice of Bemisia tabaci

The whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) causes serious crop losses worldwide by transmitting viruses. We have previously shown that salicylic acid (SA)-related plant defenses directly affect whiteflies. In this study, we applied exogenous SA to tomato plants in order to investigate the interaction between SA-induced plant volatiles and nonviruliferous B. tabaci B and Q or B- and Q-carrying tomato yellow leaf curl virus (TYLCV). The results showed that exogenous SA caused plants to repel nonviruliferous whiteflies, but the effect was reduced when the SA concentration was low and when the whiteflies were viruliferous. Exogenous SA increased the number and quantity of plant volatiles—especially the quantity of methyl salicylate and δ-limonene. In Y-tube olfactometer assays, methyl salicylate and δ-limonene repelled the whiteflies, but the repellency was reduced for viruliferous Q. We suggest that the release of plant volatiles as mediated by SA affects the interaction between whiteflies, plants, and viruses. Further studies are needed to determine why viruliferous Q is less sensitive than nonviruliferous Q to repellent plant volatiles.

Odor, Not Performance, Dictates Bemisia tabaci's Selection between Healthy and Virus Infected Plants

Although, insect herbivores are generally thought to select hosts that favor the fitness of their progeny, this “mother-knows-best” hypothesis may be challenged by the presence of a plant virus. Our previous study showed that the whitefly, Bemisia tabaci, the obligate vector for transmitting Tomato yellow leaf curl virus (TYLCV), preferred to settle and oviposit on TYLCV-infected rather than healthy host plant, Datura stramonium. The performances of B. tabaci larvae and adults were indeed improved on virus-infected D. stramonium, which is consistent with “mother-knows-best” hypothesis. In this study, B. tabaci Q displayed the same preference to settle and oviposit on Tomato spotted wilt virus (TSWV)-infected host plants, D. stramonium and Capsicum annuum, respectively. As a non-vector of TSWV, however, insect performance was impaired since adult body size, longevity, survival, and fecundity were reduced in TSWV infected D. stramonium. This appears to be an odor-mediated behavior, as plant volatile profiles are modified by viral infection. Infected plants have reduced quantities of o-xylene and α-pinene, and increased levels of phenol and 2-ethyl-1-hexanol in their headspace. Subsequent behavior experiments showed that o-xylene and α-pinene are repellant, while phenol and 2-ethyl-1-hexanol are attractive. This indicates that the preference of B. tabaci for virus-infected plants is modulated by the dynamic changes in the volatile profiles rather than the subsequent performances on virus-infected plants.

Plants Pre-Infested With Viruliferous MED/Q Cryptic Species Promotes Subsequent Bemisia tabaci Infestation

The sweet potato whitefly, Bemisia tabaci, is one of the most invasive insect pests worldwide. The two most destructive whitefly cryptic species are MEAM1/B and MED/Q. Given that MED/Q has replaced MEAM1/B in China and the invasion of MED/Q has coincided with the outbreak of tomato yellow leaf curl virus (TYLCV), we hypothesize that pre-infestation with viruliferous B. tabaci will affect the subsequent host preferences. To test this hypothesis, we (1) conducted bioassays to compare the host preference of viruliferous and non-viruliferous MEAM1/B and MED/Q, respectively, on plants pre-infested with viruliferous and non-viruliferous MEAM1/B and MED/Q; (2) profiled plant volatiles using GC-MS; and (3) functionally characterized chemical cues could potentially modulate B. tabaci-TYLCV-tomato interactions, including ρ-cymene, thujene and neophytadiene, using a Y-tube olfactometer. As a result, plants pre-infested with MEAM1/B whiteflies carrying TYLCV or not, did not attract more or less B or Q whiteflies. Plants pre-infested with non-viruliferous MED/Q resisted MEAM1/B but did not affect MED/Q. However, plants pre-infested with viruliferous MED/Q attracted more whiteflies. Feeding of viruliferous MED/Q reduced the production of ρ-cymene, and induced thujene and neophytadiene. Functionally analyses of these plant volatiles show that ρ-cymene deters while neophytadiene recruits whiteflies. These combined results suggest that pre-infestation with viruliferous MED/Q promotes the subsequent whitefly infestation and induces plant volatile neophytadiene which recruits whiteflies.

Different effects of exogenous jasmonic acid on preference and performance of viruliferous Bemisia tabaci B and Q

The sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), B and Q biotypes have caused severe losses to crops and vegetables through virus transmission. Our previous studies showed that Q is more efficient than B in acquisition and transmission of tomato yellow leaf curl virus (TYLCV) and viruliferous Q is better equipped than B in counterattacking jasmonic acid (JA)‐related plant defense. To understand how plant‐mediated defensive responses involving JA affect insect vectors within a tritrophic framework of plants, insects, and viruses, we examined the effects of exogenous JA on preference and performance of non‐viruliferous and viruliferous B and Q on tomato plants (Solanum lycopersicum L., Solanaceae). Our results demonstrated a significantly lower fecundity, shorter longevity, shorter developmental time, and lower survival rate of whiteflies on JA‐treated than on control plants. In addition, viruliferous Q performed significantly better than B in fecundity, longevity, developmental time, and survival rate. When given a choice between JA‐treated and control tomato plants, viruliferous Q was not repelled to JA‐treated plants when the JA concentration was 0.01 and 0.1 mm, whereas others all preferred the untreated control plants. Exogenous JA increased the concentration and the composition of plant volatiles, such as α‐terpinene and β‐ocimene, which deterred whiteflies in a Y‐tube bioassay. It is worth noting that Q has a mutualistic relationship with TYLCV to counteract the host defenses. A better understanding of tritrophic interactions between plants, insects, and viruses will facilitate the development of sustainable management of this invasive global pest.