Partner-specific induction of Spodoptera frugiperda immune genes in response to the entomopathogenic nematobacterial complex Steinernema carpocapsae-Xenorhabdus nematophila

The Steinernema carpocapsae-Xenorhabdus nematophila association is a nematobacterial complex (NBC) used in biological control of insect crop pests. The ability of this dual pathogen to infest and kill an insect strongly depends on the dialogue between the host’s immune system and each partner of the complex. Even though this dialogue has been extensively studied from the two partners’ points of view in several insect models, still little is known about the structure and the molecular aspects of the insects9 immune response to the dual infection. Here, we used the lepidopteran pest Spodoptera frugiperda as a model to analyze the respective impact of each NBC partner in the spatiotemporal immune responses that are induced after infestation. To this aim, we first analyzed the expression variations of the insect’s immune genes in the fat bodies and hemocytes of infested larvae by using previously obtained RNAseq data. We then selected representative immune genes for RT-qPCR investigations of the temporal variations of their expressions after infestation and of their induction levels after independent injections of each partner. We found that the fat body and the hemocytes both produce potent and stable immune responses to the infestation by the NBC, which correspond to combinations of bacterium- and nematode-induced ones. Consistent with the nature of each pathogen, we showed that X. nematophila mainly induces genes classically involved in antibacterial responses, whereas S. carpocapsae is responsible for the induction of lectins and of genes expected to be involved in melanization and cellular encapsulation. In addition, we found that two clusters of unknown genes dramatically induced by the NBC also present partner-specific induction profiles, which paves the way for their functional characterization. Finally, we discuss putative relationships between the variations of the expression of some immune genes and the NBC’s immunosuppressive strategies.