A small RNA effector conserved in herbivore insects suppresses host plant defense by cross-kingdom gene silencing

Herbivore insects deploy salivary effectors to manipulate the defense of their host plants. However, it remains unclear whether small RNAs from insects can function as effectors in regulating plant-insect interactions. Here, we report that a microRNA (miR29-b) found in the saliva of the phloem-feeding whitefly (Bemisia tabaci) can transfer into the host plant phloem during feeding and fine-tune the defense response of tobacco (Nicotiana tabacum) plants. We show that the salivary gland-enriched BtmiR29-b is produced by BtDicer 1 and released into tobacco cells via salivary exosomes. Once inside the plant cells, BtmiR29-b hijacks tobacco Argonaute 1 to silence the defense gene Bcl-2-associated athanogene 4 (NtBAG4). In tobacco, NtBAG4 acts as the positive regulator of phytohormones salicylic acid (SA) and jasmonic acid (JA), enhancing plant defense against whitefly attacks. Interestingly, we also found that miR29-b acts as a salivary effector in another Hemipteran insect, the aphid Myzus persicae, which inhibits tobacco resistance by degrading NtBAG4. Moreover, miR29-b is highly conserved in Hemiptera and across other insect orders such as Coleoptera, Hymenoptera, Orthoptera, and Blattaria. Computational analysis suggests that miR29-b may also target the evolutionarily conserved BAG4 gene in other plant species. We further provide evidence showing BtmiR29-b-mediated BAG4 cleavage and defense suppression in tomato (Solanum lycopersicum). Taken together, our work reveals that a conserved miR29-b effector from insects fine-tunes plant SA- and JA-mediated defense by cross-kingdom silencing of the host plant BAG4 gene, providing new insight into the defense and counter-defense mechanisms between herbivores and their host plants.