Fitness Costs of Chlorantraniliprole Resistance Related to the SeNPF Overexpression in the Spodoptera exigua (Lepidoptera: Noctuidae)

Int J Mol Sci. 2021 May 10;22(9):5027. doi: 10.3390/ijms22095027.

Abstract

Spodopteraexigua, a multifeeding insect pest, has developed a high level of resistance to chlorantraniliprole, which is a benzoylurea insecticide that targets the ryanodine receptors (RyRs). Herein, the resistant strain (SE-Sel) and sensitive strain (SE-Sus) were obtained by bidirectional screening for six generations. The potential oviposited eggs and oviposition rate of the SE-Sel strain were dramatically lower than those of the SE-Sus strain; on the contrary, the weights of prepupae and preadult were significantly increased. As a post-mating response, the higher number of non-oviposited eggs in the SE-Sel strain was caused by a lower mating rate. In addition, the expression levels of vitellogenin (SeVg) and its receptor (SeVgR) in the SE-Sel strain were consistently lower than those in the SE-Sus strain. An RyRI4743M mutation, contributing to the resistance to chlorantraniliprole, was located in the S3 transmembrane segments and might have affected the release of calcium ions; it led to the upregulated expression of the neuropeptide SeNPF and its receptor SeNPFR, and the mating and oviposition rate were significantly recovered when the SeNPF was knocked down though RNA interference (RNAi) in the male adult of the SE-Sel strain. Moreover, the expression of the juvenile hormone-binding proteins SeJHBWDS3 and SeJHBAN in the male adult of the SE-Sel strain was significantly decreased, which proved the existence of a fitness cost from another angle. Therefore, these results indicate that the fitness cost accompanied by chlorantraniliprole resistance in S. exigua may be related to the decrease in mating desire due to SeNPF overexpression.

Keywords: mating rate; oviposition; post-mating response; ryanodine receptors; vitellogenin.

MeSH terms

  • Animals
  • Carrier Proteins / genetics
  • Disease Resistance / drug effects
  • Disease Resistance / genetics
  • Egg Proteins / genetics
  • Genetic Fitness / genetics
  • Insect Proteins / genetics*
  • Insecticide Resistance / genetics*
  • Insecticides / pharmacology
  • Mutation / genetics
  • Neuropeptides / genetics
  • RNA Interference
  • Receptors, Cell Surface / genetics
  • Receptors, Neuropeptide / genetics
  • Spodoptera / drug effects
  • Spodoptera / genetics*
  • Vitellogenins / genetics
  • ortho-Aminobenzoates / adverse effects
  • ortho-Aminobenzoates / pharmacology*

Substances

  • Carrier Proteins
  • Egg Proteins
  • Insect Proteins
  • Insecticides
  • Neuropeptides
  • Receptors, Cell Surface
  • Receptors, Neuropeptide
  • Vitellogenins
  • juvenile hormone-binding protein, insect
  • ortho-Aminobenzoates
  • vitellogenin receptor
  • neuropeptide F
  • chlorantranilipole