Abstract

Virus infection frequently modifies plant phenotypes, leading to changes in behaviour and performance of their insect vectors in a way that transmission is enhanced, although this may not always be the case. Here, we investigated Bemisia tabaci response to tomato plants infected by Tomato chlorosis virus (ToCV), a non-circulative-transmitted crinivirus, and Tomato severe rugose virus (ToSRV), a circulative-transmitted begomovirus. Moreover, we examined the role of visual and olfactory cues in host plant selection by both viruliferous and non-viruliferous B. tabaci. Visual cues alone were assessed as targets for whitefly landing by placing leaves underneath a Plexiglas plate. A dual-choice arena was used to assess whitefly response to virus-infected and mock-inoculated tomato leaves under light and dark conditions. Thereafter, we tested the whitefly response to volatiles using an active air-flow Y-tube olfactometer, and chemically characterized the blends using gas chromatography coupled to mass spectrometry. Visual stimuli tests showed that whiteflies, irrespective of their infectious status, always preferred to land on virus-infected rather than on mock-inoculated leaves. Furthermore, whiteflies had no preference for either virus-infected or mock-inoculated leaves under dark conditions, but preferred virus-infected leaves in the presence of light. ToSRV-infection promoted a sharp decline in the concentration of some tomato volatiles, while an increase in the emission of some terpenes after ToCV infection was found. ToSRV-viruliferous whiteflies preferred volatiles emitted from mock-inoculated plants, a conducive behaviour to enhance virus spread, while volatiles from ToCV-infected plants were avoided by non-viruliferous whiteflies, a behaviour that is likely detrimental to the secondary spread of the virus. In conclusion, the circulative persistent begomovirus, ToSRV, seems to have evolved together with its vector B. tabaci to optimise its own spread. However, this type of virus-induced manipulation of vector behaviour was not observed for the semi persistent crinivirus, ToCV, which is not specifically transmitted by B. tabaci and has a much less intimate virus-vector relationship.

Highlights

  • An increasing number of studies demonstrate that vector-borne parasites are able to manipulate several phenotypic traits of their vertebrate or plant hosts and vectors in ways that render parasite transmission more likely

  • It is well known that plant viruses frequently induce yellowing symptoms, and such was the case of tomato plants infected with Tomato severe rugose virus (ToSRV), which showed severe symptoms including yellowing, leaf rolling, interveinal chlorosis, and mottling

  • Our results showed a significant reduction in the concentration of certain terpenes after infection of tomato plants with the begomovirus ToSRV, and some of them are known to repel non-viruliferous B. tabaci [41]

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Summary

Introduction

An increasing number of studies demonstrate that vector-borne parasites are able to manipulate several phenotypic traits of their vertebrate or plant hosts and vectors in ways that render parasite transmission more likely (reviewed by [1,2,3]). Pathogen-induced changes in plant phenotype often result in increased attraction and altered performance of vectors on infected plants, which can result in a mutualistic, antagonistic, or neutral type of interaction (reviewed by [4,5]). Most of the studied vector-borne plant viruses have been shown to modify vector behaviour primarily indirectly, by promoting physiological and morphological changes in virus-infected plants that increase plant attractiveness and preference to aphid vectors [5,6,7]

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