Spodoptera frugiperda transcriptional response to infestation by Steinernema carpocapsae

Louise Huot,Simon George,Bernard Duvic,Pierre-Alain Girard,Nicolas Nègre,Dany Severac

doi:10.1038/s41598-019-49410-8

Louise Huot, Simon George + Show 4 more

Open Access

https://doi.org/10.1038/s41598-019-49410-8

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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. In order to improve our knowledge about the physiological responses of its different hosts, we examined the transcriptional responses to EPN infestation of the fat body, the hemocytes and the midgut in the lepidopteran pest Spodoptera frugiperda. The tissues poorly respond to the infestation at an early time post-infestation of 8 h with only 5 genes differentially expressed in the fat body of the caterpillars. Strong transcriptional responses are observed at a later time point of 15 h post-infestation in all three tissues. Few genes are differentially expressed in the midgut but 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. Among the most up-regulated genes, we identified new potential immune effectors, unique to Lepidoptera, which show homology with bacterial genes of unknown function. Altogether, these results pave the way for further functional studies of the responsive genes’ involvement in the interaction with the EPN.

Highlights

There is a growing desire in Europe to reduce the use of chemical pesticides on agricultural land, because of their toxicity for the environment and human health (European Directive EC91/414)
Eight hours post infestation, nematodes are supposed to have travelled in the intestinal tract of S. frugiperda larvae, crossed the intestinal barrier and started releasing their symbiotic bacteria, Xenorhabdus nematophila, within the hemocoel of the caterpillar[16]
While we found no evidence of a direct response to entomopathogenic nematode (EPN) by the midgut, we investigated whether this tissue may share a common immune response with the fat body or the hemocytes

Summary

Introduction

There is a growing desire in Europe to reduce the use of chemical pesticides on agricultural land, because of their toxicity for the environment and human health (European Directive EC91/414). The development of alternative methods for the control of crop pests is encouraged These methods include the use of predators and pathogens of insect pests such as viruses, bacteria, fungi, parasitoid wasps and entomopathogenic nematodes (EPNs). EPNs of the genus Steinernema associated with the symbiotic bacterium Xenorhabdus are among the most widely used and studied biological control agents[1] They pose little threat to human health and non-target species[2], but are capable of killing a broad spectrum of insect pests including the moth Spodoptera frugiperda (Lepidoptera: Noctuidae)[3,4]. By the use of transcriptomic approaches on whole larvae or adult flies, the authors showed the overexpression of a large number of immune-related genes involved in defense responses such as coagulation, melanisation and the production of antimicrobial peptides, and in several immune and stress-reponse pathways (Toll, Imd, Jak/Stat or JNK)

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