The effects of Cucumber Mosaic Virus infection on interactions of Arabidopsis thaliana with specialist and non-specialist aphids

Abstract: Cucumber mosaic virus (CMV) is an agriculturally important plant virus, and it also
infects the model plant, Arabidopsis thaliana. CMV is transmitted by aphids, which are major agricultural pests that not only cause direct damage but also vector over 400 plant viruses to a vast range of plant species worldwide. CMV infection can modify its host plant phenotypes to induce changes in aphid behaviour that in some cases may optimise viral transmission. Thus, understanding CMV-aphid-plant interactions could be very useful for the improvement of sustainable management of CMV and other aphid-transmitted viruses. I hypothesised that whereas CMV-induced plant phenotypes modify the settling behaviours and the plant volatile blend preferences of the generalist (i. e., feeds on a broad range of plants) aphid Myzus persicae, it would not affect in the same ways the crucifer specialists (i.e., feeds on specific plant species) aphids Lipaphis erysimi and Brevicoryne brassicae. In free choice settling assays, observations at 1 h post-release showed that the aphids of M. persicae were faster to settle on plants than the specialist aphids. Nonetheless, it was found that by 24 h post-release aphids of all three species preferred to settle on uninfected A. thaliana plants. This indicates that generalist and specialist aphids were deterred from settling on CMV-infected plants. By contrast, in olfactometry assays where aphids were allowed to choose between plant volatile blends emitted by uninfected (mock-inoculated) or CMV-infected plants, the generalist aphids showed a strong preference for the CMV-induced plant volatile blend whilst the crucifer specialists showed no significant preferences. Aphids of all three species made fewer choices when presented only with volatile blends emitted by uninfected plants, compared with volatile combinations of CMV and noninfected plants. Overall, my findings suggest that for A. thaliana, CMV-induced plant phenotypes affect the settling behaviour of both the generalist and the specialist aphids, but only the generalist, Myzus persicae was significantly influenced by olfactory cues. Therefore, CMV can modify interactions between A. thaliana plants and generalist and crucifer-specialist aphids but to different degrees. CMV most effectively modifies the behaviour of the generalist M. persicae in ways that might optimise its onward transmission by causing plants to emit attractive volatile blends while making the plants resistant to settling.