Herbivore insect small RNA effector suppress plant defense by cross-kingdom gene silencing

Abstract

Herbivore insects deploy salivary effectors to manipulate the defense of their host plants, however, whether insect small RNAs (sRNAs) act as effectors to regulate plant-insect interaction is currently unclear. Here, we report that a microRNA (miR29-b) from the saliva of phloem-feeding insects can transfer into the host plant phloem and fine-tune the host defense. The salivary gland’s abundant miR29-b was produced by insect Dicer 1 and insect salivary exosome is involved in its transferring and releasing into the host plant. Insect miR29-b effector hijacks plant Argonaute 1 to silence host defense geneBcl-2-associated athanogene 4(BAG4). Silencing ofBAG4suppressed the expression of phenylalanine ammonia-lyase and the accumulation of salicylic acid (SA), therefore negatively regulating host defense against herbivore insects. miR29-b is highly conserved in Hemiptera, Coleoptera, Hymenoptera, Orthoptera, and Blattaria insects and also targets theBAG4gene. Notably,BAG4orthologs exist in a wide range of plant species and may as the target of insect miR29-b. Our work provides new insight into the intriguing defense and counter-defense between herbivores and plants.TeaserPhloem-feeding insects produce and transfer small RNA into the host plants to fine-tune plant basal defense by cross-kingdom gene silencing.