Immune gene regulation in the gut during metamorphosis in a holo- versus a hemimetabolous insect

Philos Trans R Soc Lond B Biol Sci. 2019 Oct 14;374(1783):20190073. doi: 10.1098/rstb.2019.0073. Epub 2019 Aug 26.

Abstract

During metamorphosis, holometabolous insects completely replace the larval gut and must control the microbiota to avoid septicaemia. Rapid induction of bactericidal activity in the insect gut at the onset of pupation has been described in numerous orders of the Holometabola and is best-studied in the Lepidoptera where it is under control of the 20-hydroxyecdysone (20E) moulting pathway. Here, using RNAseq, we compare the expression of immune effector genes in the gut during metamorphosis in a holometabolous (Galleria mellonella) and a hemimetabolous insect (Gryllus bimaculatus). We find that in G. mellonella, the expression of numerous immune effectors and the transcription factor GmEts are upregulated, with peak expression of three antimicrobial peptides (AMPs) and a lysozyme coinciding with delamination of the larval gut. By contrast, no such upregulation was detectable in the hemimetabolous Gr. bimaculatus. These findings support the idea that the upregulation of immune effectors at the onset of complete metamorphosis is an adaptive response, which controls the microbiota during gut replacement. This article is part of the theme issue 'The evolution of complete metamorphosis'.

Keywords: Galleria mellonella; Gryllus bimaculatus; RNAseq; antimicrobial peptides; gut metamorphosis; lysozyme.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Gastrointestinal Tract / growth & development
  • Gastrointestinal Tract / immunology
  • Gene Expression Regulation, Developmental / immunology*
  • Gryllidae / genetics
  • Gryllidae / growth & development*
  • Gryllidae / immunology
  • Larva / genetics
  • Larva / growth & development
  • Larva / immunology
  • Metamorphosis, Biological / genetics*
  • Metamorphosis, Biological / immunology
  • Moths / genetics
  • Moths / growth & development*
  • Moths / immunology
  • Nymph / genetics
  • Nymph / growth & development
  • Nymph / immunology