Paternal knockdown of tRNA(cytosine-5-)-methyltransferase (Dnmt2) increases offspring susceptibility to infection in red flour beetles

Insect Mol Biol. 2022 Dec;31(6):711-721. doi: 10.1111/imb.12798. Epub 2022 Jul 18.

Abstract

Intergenerational effects from fathers to offspring are increasingly reported from diverse organisms, but the underlying mechanisms remain speculative. Paternal trans-generational immune priming (TGIP) was demonstrated in the red flour beetle Tribolium castaneum: non-infectious bacterial exposure of fathers protects their offspring against an infectious challenge for at least two generations. Epigenetic processes, such as cytosine methylation of nucleic acids, have been proposed to enable transfer of information from fathers to offspring. Here we studied a potential role in TGIP of the Dnmt2 gene (renamed as Trdmt1 in humans), which encodes a highly conserved enzyme that methylates different RNAs, including specific cytosines of a set of tRNAs. Dnmt2 has previously been reported to be involved in intergenerational epigenetic inheritance in mice and protection against viruses in fruit flies. We first studied gene expression and found that Dnmt2 is expressed in various life history stages and tissues of T. castaneum, with high expression in the reproductive organs. RNAi-mediated knockdown of Dnmt2 in fathers was systemic, slowed down offspring larval development and increased mortality of the adult offspring upon bacterial infection. However, these effects were independent of bacterial exposure of the fathers. In conclusion, our results point towards a role of Dnmt2 for paternal effects, while elucidation of the mechanisms behind paternal TGIP needs further studies.

Keywords: Tribolium castaneum; parental knockdown; paternal effects; tRNA methylation; tRNA methyltransferase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Coleoptera* / genetics
  • Cytosine
  • DNA (Cytosine-5-)-Methyltransferases* / genetics
  • Disease Susceptibility
  • Gene Knockdown Techniques
  • Insect Proteins* / genetics
  • Male
  • RNA, Transfer

Substances

  • Cytosine
  • DNA (Cytosine-5-)-Methyltransferases
  • RNA, Transfer
  • Insect Proteins