Aphid-derived cross-kingdom RNA dynamics underpin maize resistance

Abstract

Aphids are major pests of maize (Zea mays), yet the molecular mechanisms underlying their interactions with host plants remain poorly understood. Here, we identified and functionally characterized long non-coding RNAs (lncRNAs) from the aphid-specific Ya gene family in the cereal-specialist aphids Rhopalosiphum maidis and R. padi. We showed that Ya genes formed lineage-specific clusters and were transcriptionally active across both species. Multiple Ya transcripts secreted into maize tissues exhibited remarkable stability compared with rapidly degraded aphid mRNAs and migrated systemically, as visualized in planta using an RNA switch-controlled RNA-triggered fluorescence system. RNA interference of Ya genes significantly reduced aphid fecundity, while ectopic expression of Ya lncRNAs in maize enhanced aphid colonization. Importantly, maize genotypes differing in aphid resistance selectively influenced the persistence of aphid mRNAs but not Ya lncRNAs, indicating a decoupled fate of distinct aphid RNA classes in planta. These findings establish Ya lncRNAs as cross-kingdom effectors critical for aphid virulence, and suggest new molecular markers for breeding aphid-resistant maize.