An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

ABSTRACT Aphids are sap-feeding insects that colonize a broad range of plant species and often cause feeding damage and transmit plant pathogens, including bacteria, viruses and viroids. These insects feed from the plant vascular tissue, predominantly the phloem. However, it remains largely unknown how aphids, and other sap-feeding insects, establish intimate long-term interactions with plants. To identify aphid virulence factors, we took advantage of the ability of the green peach aphid Myzus persicae to colonize divergent plant species. We found that a M. persicae clone of near-identical females establishes stable colonies on nine plant species of five representative plant eudicot and monocot families that span the angiosperm phylogeny. Members of the novel aphid Ya family are differentially expressed in aphids on the nine plant species, are co-regulated and organized as tandem repeats in aphid genomes. Interestingly, aphids translocate Ya transcripts into plants and some transcripts migrate systemically within several plant species. RNAi-mediated knock down of Ya genes reduces M. persicae fecundity and M. persicae produces more progeny on transgenic plants that heterologously produce one of the systemically migrating Ya transcripts as a long non-coding (lnc)RNA. Taken together, our work led to the discovery of a new host-responsive aphid gene family that operate as virulence factors. Transcripts of this family translocate into plants, including a lncRNA that migrates systemically and promotes aphid reproduction. Significance Statement The green peach aphid Myzus persicae causes yield losses of a diverse range of economically important crops primarily as a vector of more than 100 different plant pathogens. We found that a single genotype of M. persicae is able to colonize nine plant species, including diverse dicots and maize, indicating that this aphid is truly polyphagous. Members of a new aphid Ya family undergoes coordinated expression changes in M. persicae depending on the plant species. The aphids translocate Ya transcripts into plants during feeding and these RNAs migrate to systemic leaves. Moreover, heterologous in planta expression of M. persicae Ya1 as a long non-coding RNA promotes aphid reproduction. Our findings indicate that cross kingdom deployment of RNA is more common than thought.