13Steinernema carpocapsae is an entomopathogenic nematode (EPN) used in biological control 14 of agricultural pest insects. It enters the hemocoel of its host via the intestinal tract and releases 15 its symbiotic bacterium Xenorhabdus nematophila, which kills the insect in less than 48 hours. 16 Although several aspects of its interactions with insects have been extensively studied, still 17 little is known about the immune and physiological responses of its different hosts. In order to 18 improve this knowledge, we examined the transcriptional responses to EPN infestation of the 19 fat body, the hemocytes and the midgut in the lepidopteran pest model Spodoptera frugiperda 20 (Lepidoptera: Noctuidae). 21 Our results indicate that the tissues poorly respond to the infestation at an early time post-22 infestation of 8 h, even though the proliferation of the bacterial symbiont within the hemocoel 23 is detected. Only 5 genes are differentially expressed in the fat body of the caterpillars.
24However, strong transcriptional responses are observed at a later time point of 15 h post-25 infestation in all three tissues. While few genes are differentially expressed in the midgut, 26 tissue-specific panels of induced metalloprotease inhibitors, immune receptors and 27 antimicrobial peptides together with several uncharacterized genes are up-regulated in the fat 28 body and the hemocytes. In addition, among the most up-regulated genes, we identified new 29 potential immune effectors, unique to Lepidoptera, for which we present evidence of 30 acquisition by Horizontal Gene Transfer from bacteria.
31Altogether, these results pave the way for further functional studies of the mobilized genes' 32 involvement in the interaction with the EPN. 33 3 34Author summary 35 The Fall Armyworm, Spodoptera frugiperda, is a major agricultural pest. The caterpillars cause 36 extensive damage to crops of importance such as corn, rice, sorghum and cotton. Originally 37 from the Americas, it is currently becoming invasive in other parts of the world, first in Africa 38 in 2016, then in India and now in south-east Asia. Programs of biological control against insect 39 pests are increasingly encouraged around the world and include the use of pathogens. 40 Entomopathogenic nematodes such as Steinernema carpocapsae are already commercialized 41 as organic pesticides. These nematodes live in the soil and enter the body of their insect preys. 42 Once within the insects, they release their symbiotic bacteria (Xenorhabdus nematophila in this 43 case), which infect and kill the host in a few hours. The nematodes can then feed on the dead 44 insects, reproduce and resume their life cycle. It is a major challenge to understand how EPN 45 achieve their pathogenicity as well as how the insects can resist them. Here we provide the 46 foundation for such an interaction between EPN and a Lepidoptera. We analyzed the dynamic 47 of transcriptional response in three insect tissues (midgut, fat body and hemocytes) upon 48 infestation by EPN. Not many...