A non-persistently transmitted-virus induces a pull–push strategy in its aphid vector to optimize transmission and spread

Carmo-Sousa, Michele; Moreno, Aránzazu; Garzo, Elisa; Fereres, Alberto

doi:10.1016/j.virusres.2013.12.012

Cited by 110 publications

(117 citation statements)

References 51 publications

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“…In melon ( Cucumis melo ), CMV infection elevates phloem sugar levels [40], which might benefit aphids. However, if similar phloem sugar increases occur in Cucurbita pepo or Cucumis sativus , any beneficial effect on the aphids must be negated by other biochemical changes since CMV infection renders these plants unpalatable to M. persicae and A. gossypii [19, 20]. Another possibility is that amino acid levels increase in CMV-infected tobacco; this might explain enhanced aphid performance on TuMV-infected Arabidopsis [14].…”

Section: Discussionmentioning

confidence: 99%

“…CMV-infected cucurbits attract aphids through changes in VOC emission but the decreased palatability of these plants subsequently repels them [19, 20]. In Arabidopsis, CMV also induces unpalatability, which encourages aphid dispersion [18].…”

Section: Discussionmentioning

confidence: 99%

“…However, a virus can induce opposite effects on host-vector interactions in different hosts. For example, rather than enhancing survival and reproduction, CMV induces feeding deterrence against M. persicae in Arabidopsis [18] and against M. persicae as well as Aphis gossypii in the ‘Dixie’ variety of squash and in cucumber ( Cucumis sativus ) [19, 20]. Similar contrasts have been noted for potyviruses.…”

Section: Introductionmentioning

confidence: 88%

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Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco

Tungadi

Groen

Murphy

et al. 2017

Virol J

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BackgroundAphids, including the generalist herbivore Myzus persicae, transmit cucumber mosaic virus (CMV). CMV (strain Fny) infection affects M. persicae feeding behavior and performance on tobacco (Nicotiana tabacum), Arabidopsis thaliana and cucurbits in varying ways. In Arabidopsis and cucurbits, CMV decreases host quality and inhibits prolonged feeding by aphids, which may enhance virus transmission rates. CMV-infected cucurbits also emit deceptive, aphid-attracting volatiles, which may favor virus acquisition. In contrast, aphids on CMV-infected tobacco (cv. Xanthi) exhibit increased survival and reproduction. This may not increase transmission but might increase virus and vector persistence within plant communities. The CMV 2b counter-defense protein diminishes resistance to aphid infestation in CMV-infected tobacco plants. We hypothesised that in tobacco CMV and its 2b protein might also alter the emission of volatile organic compounds that would influence aphid behavior.ResultsAnalysis of headspace volatiles emitted from tobacco plants showed that CMV infection both increased the total quantity and altered the blend produced. Furthermore, experiments with a CMV 2b gene deletion mutant (CMV∆2b) showed that the 2b counter-defense protein influences volatile emission. Free choice bioassays were conducted where wingless M. persicae could choose to settle on infected or mock-inoculated plants under a normal day/night regime or in continual darkness. Settling was recorded at 15 min, 1 h and 24 h post-release. Statistical analysis indicated that aphids showed no marked preference to settle on mock-inoculated versus infected plants, except for a marginally greater settlement of aphids on mock-inoculated over CMV-infected plants under normal illumination.ConclusionsCMV infection of tobacco plants induced quantitative and qualitative changes in host volatile emission and these changes depended in part on the activity of the 2b counter-defense protein. However, CMV-induced alterations in tobacco plant volatile emission did not have marked effects on the settling of aphids on infected versus mock-inoculated plants even though CMV-infected plants are higher quality hosts for M. persicae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12985-017-0754-0) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 88%

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Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco

Tungadi

Groen

Murphy

et al. 2017

Virol J

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“…This moves the insects rapidly away from the plant to new hosts, a strategy that enhances the transmission of CMV, which only requires very brief feeding periods both for acquisition and transmission (Carmo-Sousa et al, 2014;Mauck et al, 2010). This work led to the hypothesis that viruses can induce volatiles that attract insect vectors, but the persistently-transmitted viruses induce profeeding behavior as well, while the nonpersistently-transmitted viruses induce antifeeding behavior to rapidly move vectors off once the virus is acquired (Mauck et al, 2012).…”

Section: Transmission By Aphidsmentioning

confidence: 99%

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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“…Directly modified feeding behaviors that increase virus transmission have been reported for persistently TSWV-infected Frankliniella occidentalis thrips [94]. The non-persistently aphid-transmitted CMV was similarly found to induce specific changes in the host plant such as suppression of the jasmonic acid signaling pathway that affected aphid behavior leading to enhanced performance, which appear to be indirectly linked to the viral 2b protein [24,95]. The geminivirus tomato yellow leaf curl virus (TYLCV) was shown to manipulate feeding behaviors of whiteflies to increase virus transmission [96].…”

Section: Critical Steps In Virus–insect Interactions As Potential mentioning

confidence: 99%

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

Dietzgen

Mann

Johnson

2016

Viruses

178

142

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Acquisition and transmission by an insect vector is central to the infection cycle of the majority of plant pathogenic viruses. Plant viruses can interact with their insect host in a variety of ways including both non-persistent and circulative transmission; in some cases, the latter involves virus replication in cells of the insect host. Replicating viruses can also elicit both innate and specific defense responses in the insect host. A consistent feature is that the interaction of the virus with its insect host/vector requires specific molecular interactions between virus and host, commonly via proteins. Understanding the interactions between plant viruses and their insect host can underpin approaches to protect plants from infection by interfering with virus uptake and transmission. Here, we provide a perspective focused on identifying novel approaches and research directions to facilitate control of plant viruses by better understanding and targeting virus–insect molecular interactions. We also draw parallels with molecular interactions in insect vectors of animal viruses, and consider technical advances for their control that may be more broadly applicable to plant virus vectors.

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A non-persistently transmitted-virus induces a pull–push strategy in its aphid vector to optimize transmission and spread

Cited by 110 publications

References 51 publications

Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco

Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco

Plants, viruses and the environment: Ecology and mutualism

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

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