Inter-species mRNA transfer among green peach aphids, dodder parasites, and cucumber host plants

Abstract mRNAs are transported within a plant through phloem. Aphids are phloem feeders and dodders (Cuscuta spp.) are parasites which establish phloem connections with host plants. When aphids feed on dodders, whether there is trafficking of mRNAs among aphids, dodders, and host plants and if aphid feeding affects the mRNA transfer between dodders and hosts are unclear. We constructed a green peach aphid (GPA, Myzus persicae)-dodder (Cuscuta australis)-cucumber (Cucumis sativus) tritrophic system by infesting GPAs on C. australis, which parasitized cucumber hosts. We found that GPA feeding activated defense-related phytohormonal and transcriptomic responses in both C. australis and cucumbers and large numbers of mRNAs were found to be transferred between C. australis and cucumbers and between C. australis and GPAs; importantly, GPA feeding on C. australis greatly altered inter-species mobile mRNA profiles. Furthermore, three cucumber mRNAs and three GPA mRNAs could be respectively detected in GPAs and cucumbers. Moreover, our statistical analysis indicated that mRNAs with high abundances and long transcript lengths are likely to be mobile. This study reveals the existence of inter-species and even inter-kingdom mRNA movement among insects, parasitic plants, and parasite hosts, and suggests complex regulation of mRNA trafficking.