JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184

Different from holometabolous insects, the hemipteran species such as pea aphidAcyrthosiphon pisumexhibit reduced immune responses with the absence of the genes coding for antimicrobial peptide (AMP), immune deficiency (IMD), peptidoglycan recognition proteins (PGRPs), and other immune-related molecules. Prior studies have proved that phenoloxidase (PO)-mediated melanization, hemocyte-mediated phagocytosis, and reactive oxygen species (ROS) participate in pea aphid defense against bacterial infection. Also, the conserved signaling, Jun N-terminal kinase (JNK) pathway, has been suggested to be involved in pea aphid immune defense. However, the precise role of the JNK signaling, its interplay with other immune responses and its regulation in pea aphid are largely unknown. In this study, usingin vitrobiochemical assays andin vivobioassays, we demonstrated that the JNK pathway regulated hemolymph PO activity, hydrogen peroxide concentration and hemocyte phagocytosis in bacteria infected pea aphids, suggesting that the JNK pathway plays a central role in regulating immune responses in pea aphid. We further revealed the JNK pathway is regulated by microRNA-184 in response to bacterial infection. It is possible that in common the JNK pathway plays a key role in immune system of hemipteran insects and microRNA-184 regulates the JNK pathway in animals. Author summary As a model of hemipteran insects, pea aphid has recently been extensively studied. Interestingly, genomic analysis and biochemical assays revealed that some conserved core components, such as the immune deficiency pathway and peptidoglycan recognition proteins, are missing from the immune system of pea aphid. However, studies demonstrated that the phenoloxidase, reactive oxygen species, and phagocytosis play critical roles in the pea aphid defense against infection. Through bioinformatics analysis and biochemical assays, we found that these immune responses are under the control of the JNK pathway and that the latter is regulated by microRNA-184. Our results suggest that the JNK pathway is a key signaling pathway in the immune system of hemipteran insects, and the regulation of this pathway by microRNA-184 is conserved among animals.