Trans-kingdom delivery of aphid-derived small RNAs into Arabidopsis thaliana modulates plant immunity

Abstract Herbivore insects are on an evolutionary tug-of-war with plants. An important part of the plant-herbivore insect interaction is the exchange of molecules, in particular proteins (in the form of effectors) and RNA. Among RNAs, small RNAs have been identified as important molecules shaping the communication between different pests/parasites and their host, but the role of these molecules in the interaction between aphids and plants is not well understood. Here, we explored the role of aphid-derived sRNAs in the interaction between Arabidopsis thaliana and the green peach aphid, Myzus persicae . Using sRNA sequencing, we identified a significant amount of bona-fide aphid-derived sRNAs within Arabidopsis tissues. Using immunoprecipitation followed by sRNA sequencing and degradome sequencing we determined that these sRNAs are incorporated into endogenous AGO proteins, in particular AGO1, and induce the cleavage of transcripts involved in the modulation of the immune response against the aphid. Our results indicate that aphid sRNAs attenuate the immune response of Arabidopsis thaliana and can improve aphid performance. In addition, we identified that aphid-derived sRNAs are commonly injected into other aphid-host combinations. Accordingly, our work indicates that aphid-derived sRNAs are active players in aphid-host interactions.