Viral manipulation of vector behaviour: cucumber mosaic virus has differential effects on specialist versus generalist aphids infesting Arabidopsis thaliana.

Abstract

BACKGROUND: Cucumber mosaic virus (CMV) is vectored by aphids. Infection of Arabidopsis thaliana plants with CMV affects their attractiveness to aphids (Myzus persicae) and the performance of aphids confined on these plants. CMV-induced changes in plant-aphid interactions ('viral manipulation') may promote transmission. M. persicae, an efficient CMV vector is a 'generalist', i.e., it has many plant hosts. A. thaliana is also exploited by crucifer-specialist aphids including Lipaphis erysimi (an efficient CMV vector) and Brevicoryne brassicae (a poor CMV vector). We explored the hypothesis that CMV-induced viral manipulation of aphid behaviour would exert stronger effects on M. persicae than on crucifer-specialists. RESULTS: M. persicae, B. brassicae and L. erysimi were released in microcosms and allowed to choose to settle on either CMV-infected or mock-inoculated plants. Initial experiments showed that as systemic CMV infection developed in A. thaliana, aphids of M. persicae were decreasingly likely to settle on infected plants. In subsequent experiments, using plants at 14 days post-infection, it was found that aphids of M. persicae were faster to choose between infected and uninfected plants than specialist aphids, but that both the generalist and specialists were less likely to settle on CMV-infected plants. Olfactometry showed that volatiles emitted by CMV-infected plants attracted M. persicae, and although the specialists showed no significant preferences, greater numbers of aphids of all three species responded when CMV-infected plant volatiles were presented to them. CONCLUSIONS: As CMV infection develops, A. thaliana becomes less susceptible to aphid colonisation, however, plants continue to emit attractive olfactory cues. This is consistent with a model in which aphids are attracted to infected plants but discouraged from settling (e.g., by gustatory cues), which encourages aphids to carry CMV to non-infected plants. CMV appears to be more successful in manipulating the interactions of A. thaliana with the generalist aphid M. persicae, than with the crucifer specialists B. brassicae or L. erysimi.