Turnip Mosaic Virus Infection in a Perennial Arabidopsis Reduces Aphid Fecundity in the Natural Environment

In plant-virus-vector tripartite relationships, it has been recognised that viral infections alter the physiological state of host plants, enhancing vector performance and facilitating virus transmission to other host individuals. Natural tripartite systems with perennial host plants are expected to persist for a long time through clonal propagation and the spread of virus-infected hosts. Under such circumstances, viral infection may negatively affect the vector, enhancing host vigour. We used the Arabidopsis halleri-turnip mosaic virus (TuMV)-aphid system to test this hypothesis. We compared aphid performance between TuMV-infected and uninfected plants, and host transcriptomes of intact, aphid-infested, TuMV-infected, and aphid-infested TuMV-infected plants. Fewer aphids were observed on TuMV-infected plants than on uninfected plants in the natural population. Manipulative experiments revealed that aphid fecundity, but not preference or emigration, was reduced on TuMV-infected plants. The host transcriptome responses to aphids were markedly weakened in TuMV-infected plants. This attenuation occurred in the form of counter-attenuation, in which the host genes respond in opposite directions to the viruses and aphids. For example, three known host genes that promote aphid fecundity are upregulated by aphid infestation in the absence of TuMV, whereas these responses are attenuated by TuMV infection. Additionally, four genes were identified as candidate genes that may have caused the TuMV-triggered reduction in aphid fecundity. In conclusion, we showed that viral infections simultaneously suppressed aphid fecundity and host plant responses induced by aphids. These interactions may prevent the host population from collapsing and enhance the coexistence of plant-virus-vector in natural environments.