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 function as effectors in regulating plant-insect interactions. Here, we report that a microRNA (miR29-b) found in the saliva of phloem-feeding whitefly (Bemisa tabaci) can transfer into the host plant phloem during feeding and fine-tune the defense response of tobacco (Nicotiana tabacum). The salivary gland-enriched BtmiR29-b was produced by BtDicer 1 and released into tobacco via salivary exosomes. Once inside the plant, 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, where it also inhibits tobacco resistance by degrading NtBAG4. Moreover, miR29-b is highly conserved not only in Hemiptera, but also across other insect orders such as Coleoptera, Hymenoptera, Orthoptera, and Blattaria. Computational analysis suggests that miR29-b may target the evolutionarily conserved BAG4 gene in other plant species as well. We further provide evidence on BtmiR29-b mediated BAG4 cleavage and defense suppress in tomato (Solanum lycopersicum). Taken together, our work demonstrated an insect-conserved miR29-b effector fine-tuning plant SA/JA-mediated defense by cross-kingdom silencing of the host BAG4 gene. These findings provide new insight into the defense and counter-defense mechanisms between herbivores and their host plants.