Spodoptera frugiperda transcriptional response to infestation by Steinernema carpocapsae

Abstract

Steinernema carpocapsae is an entomopathogenic nematode (EPN) used in biological control of agricultural pest insects. It enters the hemocoel of its host via the intestinal tract and releases its symbiotic bacterium Xenorhabdus nematophila, which kills the insect in less than 48 hours. Although several aspects of its interactions with insects have been extensively studied, still little is known about the immune and physiological responses of its different hosts. In order to improve this knowledge, we examined the transcriptional responses to EPN infestation of the fat body, the hemocytes and the midgut in the lepidopteran pest model Spodoptera frugiperda (Lepidoptera: Noctuidae).\n\nOur results indicate that the tissues poorly respond to the infestation at an early time post-infestation of 8 h, even though the proliferation of the bacterial symbiont within the hemocoel is detected. Only 5 genes are differentially expressed in the fat body of the caterpillars. However, strong transcriptional responses are observed at a later time point of 15 h post-infestation in all three tissues. While few genes are differentially expressed in the midgut, tissue-specific panels of induced metalloprotease inhibitors, immune receptors and antimicrobial peptides together with several uncharacterized genes are up-regulated in the fat body and the hemocytes. In addition, among the most up-regulated genes, we identified new potential immune effectors, unique to Lepidoptera, for which we present evidence of acquisition by Horizontal Gene Transfer from bacteria.\n\nAltogether, these results pave the way for further functional studies of the mobilized genes involvement in the interaction with the EPN.\n\nAuthor summaryThe Fall Armyworm, Spodoptera frugiperda, is a major agricultural pest. The caterpillars cause extensive damage to crops of importance such as corn, rice, sorghum and cotton. Originally from the Americas, it is currently becoming invasive in other parts of the world, first in Africa in 2016, then in India and now in south-east Asia. Programs of biological control against insect pests are increasingly encouraged around the world and include the use of pathogens. Entomopathogenic nematodes such as Steinernema carpocapsae are already commercialized as organic pesticides. These nematodes live in the soil and enter the body of their insect preys. Once within the insects, they release their symbiotic bacteria (Xenorhabdus nematophila in this case), which infect and kill the host in a few hours. The nematodes can then feed on the dead insects, reproduce and resume their life cycle. It is a major challenge to understand how EPN achieve their pathogenicity as well as how the insects can resist them. Here we provide the foundation for such an interaction between EPN and a Lepidoptera. We analyzed the dynamic of transcriptional response in three insect tissues (midgut, fat body and hemocytes) upon infestation by EPN. Not many studies have been performed genome-wide on such an interaction, and none on a Lepidopteran model of economical importance. Our transcriptomic approach revealed some specificities of the Lepidopteran defense mechanisms. In particular, we discovered a set of genes, acquired in Lepidoptera from bacteria by Horizontal Gene Transfer, that probably encode proteins with antibiotic activity.