A Symbiotic Virus Facilitates Aphid Adaptation to Host Plants by Suppressing Jasmonic Acid Responses

Symbiotic viruses exist in many insects; however, their functions in host insects are not well understood. In this study, we explored the role of acyrthosiphon pisum virus (APV) in the interaction of its host aphid Acyrthosiphon pisum with plants. APV is primarily located in aphid salivary glands and gut and propagated in the insect. APV is horizontally transmitted to host plants during aphid feeding, but the virus does not replicate in the host plant. When the pea host race of aphids colonized two low-fitness plants, Medicago truncatula and Vicia villosa, the virus titers in both the aphids and plants significantly increased. Furthermore, APV infection strongly promoted the survival rate of the pea host race on V. villosa. Transcriptomic analysis showed that only 0.85% of aphid genes responded to APV infection when aphids fed on V. villosa, with a fold change in transcript levels of no more than fourfold. The improved survival due to APV infection was apparently related to the inhibitory effect of the virus on levels of phytohormone jasmonic acid (JA) and JA-isoleucine. Our data suggest a benefit of the symbiotic virus to its aphid host and demonstrate a novel case of symbiotic virus-mediated three-species interaction.