Transcriptome analysis unveils the mechanisms of lipid metabolism response to grayanotoxin I stress in Spodoptera litura

PeerJ. 2023 Dec 6:11:e16238. doi: 10.7717/peerj.16238. eCollection 2023.

Abstract

Background: Spodoptera litura (tobacco caterpillar, S. litura) is a pest of great economic importance due to being a polyphagous and world-distributed agricultural pest. However, agricultural practices involving chemical pesticides have caused resistance, resurgence, and residue problems, highlighting the need for new, environmentally friendly methods to control the spread of S. litura.

Aim: This study aimed to investigate the gut poisoning of grayanotoxin I, an active compound found in Pieris japonica, on S. litura, and to explore the underlying mechanisms of these effects.

Methods: S. litura was cultivated in a laboratory setting, and their survival rate, growth and development, and pupation time were recorded after grayanotoxin I treatment. RNA-Seq was utilized to screen for differentially expressed genes (DEGs). Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses were conducted to determine the functions of these DEGs. ELISA was employed to analyze the levels of lipase, 3-hydroxyacyl-CoA dehydrogenase (HOAD), and acetyl-CoA carboxylase (ACC). Hematoxylin and Eosin (H & E) staining was used to detect the development of the fat body.

Results: Grayanotoxin I treatment significantly suppressed the survival rate, growth and development, and pupation of S. litura. RNA-Seq analysis revealed 285 DEGs after grayanotoxin I exposure, with over 16 genes related to lipid metabolism. These 285 DEGs were enriched in the categories of cuticle development, larvae longevity, fat digestion and absorption. Grayanotoxin I treatment also inhibited the levels of FFA, lipase, and HOAD in the hemolymph of S. litura.

Conclusion: The results of this study demonstrated that grayanotoxin I inhibited the growth and development of S. litura. The mechanisms might, at least partly, be related to the interference of lipid synthesis, lipolysis, and fat body development. These findings provide valuable insights into a new, environmentally-friendly plant-derived insecticide, grayanotoxin I, to control the spread of S. litura.

Keywords: Grayanotoxin I; Lipid metabolism; Spodoptera litura.

MeSH terms

  • Animals
  • Gene Expression Profiling* / methods
  • Lipase / pharmacology
  • Lipid Metabolism* / genetics
  • Spodoptera

Substances

  • grayanotoxin I
  • Lipase

Grants and funding

This work was supported by the Hunan Key Laboratory of the Research and Development of Novel Pharmaceutical Preparations; the Hunan Provincial Key Laboratory of the TCM Agricultural Biogenomics; the “14th Five-Year Plan” Application Characteristic Discipline of Hunan Province (Pharmaceutical Science); the Provincial Key R & D projects of Hunan Provincial Science and Technology Department under Grant No. 2022SK2074 and the ESI Discipline Special Project of Changsha Medical University under Grant No. 2022CYY001 and 2022CYY002. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.