Insect symbiont facilitates vector acquisition, retention and transmission of plant virus

Su, Qi; Pan, Huipeng; Liu, Baiming; Chu, Dong; Xie, Wen; Wu, Qingjun; Wang, Shaoli; Xu, Baoyun; Zhang, Youjun

doi:10.1038/srep01367

Cited by 83 publications

(88 citation statements)

References 55 publications

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“…We cultivated healthy tomato and cotton in a potting mix in 1.5-L pots (one plant/pot) under natural light and controlled temperature (26 ± 2°C) in a glasshouse. When these plants grew to the 6–7 true-leaf stage, they were used in the experiments42.…”

Section: Methodsmentioning

confidence: 99%

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

Pan

Chu

Liu

et al. 2013

Sci Rep

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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.

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Section: Methodsmentioning

confidence: 99%

“…Tomato plants were inoculated at the 3 rd true-leaf stage. Tomato plants were assumed to be infected with TYLCV when they developed characteristic leaf-curl symptoms42.…”

Section: Methodsmentioning

confidence: 99%

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

Pan

Chu

Liu

et al. 2013

Sci Rep

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“…In some cases the viruses and vectors have a mutualistic relationship, resulting in increased longevity and fecundity of the insects, while in other cases the viruses are antagonistic to the vectors; differences have led to increased invasiveness of some whiteflies (Jiu et al, 2007;Mann et al, 2008;Pan et al, 2013). Recently some of these differences have been attributed to yet another player, a bacterial endosymbiont of the insect vector (Su et al, 2013). These interactions also involve plant volatile compounds, and may include the subviral satellites of geminiviruses .…”

Section: Transmission By Whitefliesmentioning

confidence: 97%

Plants, viruses and the environment: Ecology and mutualism

2015

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Since the discovery of Tobacco mosaic virus nearly 120 years ago, most studies on viruses have focused on their roles as pathogens. Virus ecology takes a different look at viruses, from the standpoint of how they affect their hosts׳ interactions with the environment. Using the framework of symbiotic relationships helps put the true nature of viruses into perspective. Plants clearly have a long history of relationships with viruses that have shaped their evolution. In wild plants viruses are common but usually asymptomatic. In experimental studies plant viruses are sometimes mutualists rather than pathogens. Virus ecology is closely tied to the ecology of their vectors, and the behavior of insects, critical for transmission of many plant viruses, is impacted by virus-plant interactions. Virulence is probable not beneficial for most host-virus interactions, hence commensal and mutualistic relationships are almost certainly common, in spite of the paucity of literature on beneficial viruses.

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“…In those experiments, the amounts of virus were appraised during whitefly rearing on a nonvirus-host plant after a short virus acquisition period on infected plants, under standard laboratory conditions (1,29,38,39). None of those studies was conclusive.…”

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confidence: 99%

Replication of Tomato Yellow Leaf Curl Virus in Its Whitefly Vector, Bemisia tabaci

Pakkianathan

Kontsedalov

Lebedev

et al. 2015

J Virol

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Tomato yellow leaf curl virus (TYLCV) is a begomovirus transmitted exclusively by the whitefly Bemisia tabaci in a persistent, circulative manner. Replication of TYLCV in its vector remains controversial, and thus far, the virus has been considered to be nonpropagative. Following 8 h of acquisition on TYLCV-infected tomato plants or purified virions and then transfer to non-TYLCV-host cotton plants, the amounts of virus inside whitefly adults significantly increased (>2-fold) during the first few days and then continuously decreased, as measured by the amounts of genes on both virus DNA strands. Reported alterations in insect immune and defense responses upon virus retention led us to hypothesize a role for the immune response in suppressing virus replication. After virus acquisition, stress conditions were imposed on whiteflies, and the levels of three viral gene sequences were measured over time. When whiteflies were exposed to TYLCV and treatment with two different pesticides, the virus levels continuously increased. Upon exposure to heat stress, the virus levels gradually decreased, without any initial accumulation. Switching of whiteflies between pesticide, heat stress, and control treatments caused fluctuating increases and decreases in virus levels. Fluorescence in situ hybridization analysis confirmed these results and showed virus signals inside midgut epithelial cell nuclei. Combining the pesticide and heat treatments with virus acquisition had significant effects on fecundity. Altogether, our results demonstrate for the first time that a single-stranded DNA plant virus can replicate in its hemipteran vector. IMPORTANCEPlant viruses in agricultural crops are of great concern worldwide. Many of them are transmitted from infected to healthy plants by insects. Persistently transmitted viruses often have a complex association with their vectors; however, most are believed not to replicate within these vectors. Such replication is important, as it contributes to the virus's spread and can impact vector biology. Tomato yellow leaf curl virus (TYLCV) is a devastating begomovirus that infects tomatoes. It is persistently transmitted by the whitefly Bemisia tabaci but is believed not to replicate in the insect. To demonstrate that TYLCV is, in fact, propagative (i.e., it replicates in its insect host), we hypothesized that insect defenses play a role in suppressing virus replication. We thus exposed whitefly to pesticide and heat stress conditions to manipulate its physiology, and we showed that under such conditions, the virus is able to replicate and significantly influence the insect's fecundity. (Begomovirus, Geminiviridae) is the name given to a complex of single-stranded DNA (ssDNA) plant viruses that cause tremendous losses of tomato crops worldwide (1). Begomoviruses are transmitted by several biotypes of the whitefly Bemisia tabaci (2, 3). Begomoviruses have either a single (monopartite) or two (bipartite) circular ssDNA genomes of ϳ2,700 nucleotides each. Each genome is encapsidated in an ϳ25...

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Insect symbiont facilitates vector acquisition, retention and transmission of plant virus

Cited by 83 publications

References 55 publications

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

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

Plants, viruses and the environment: Ecology and mutualism

Replication of Tomato Yellow Leaf Curl Virus in Its Whitefly Vector, Bemisia tabaci

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