Integration of transcriptome and proteome reveals molecular mechanisms underlying stress responses of the cutworm, Spodoptera litura, exposed to different levels of lead (Pb)

Abstract

Heavy metals are major environmental pollutants that affect organisms across different trophic levels. Herbivorous insects play an important role in the bioaccumulation, and eventually, biomagnification of these metals. Although effects of heavy metal stress on insects have been well-studied, the molecular mechanisms underlying their effects remain poorly understood. Here, we used the RNA-Seq profiling and isobaric tags for relative and absolute quantitation (iTRAQ) approaches to unravel these mechanisms in the polyphagous pest Spodoptera litura exposed to lead (Pb) at two different concentrations (12.5 and 100 mg Pb/kg; PbL and PbH, respectively). Altogether, 1392 and 1630 differentially expressed genes (DEGs) and 58, 114 differentially expressed proteins (DEPs) were identified in larvae exposed to PbL and PbH, respectively. After exposed to PbL, the main up-regulated genes clusters and proteins in S. litura larvae were associated with their metabolic processes, including carbohydrate, protein, and lipid metabolism, but the levels of cytochrome P450 associated with the pathway of xenobiotic biodegradation and metabolism were found to be decreased. In contrast, the main up-regulated genes clusters and proteins in larvae exposed to PbH were enriched in the metabolism of xenobiotic by cytochrome P450, drug metabolism-cytochrome P450, and other drug metabolism enzymes, while the down-regulated genes and proteins were found to be closely related to the lipid (lipase) and protein (serine protease, trypsin) metabolism and growth processes (cuticular protein). These findings indicate that S. litura larvae exposed to PbL could enhance food digestion and absorption to prioritize for growth rather than detoxification, whereas S. litura larvae exposed to PbH reduced food digestion and absorption and channelized the limited energy for detoxification rather than growth. These contrasting results explain the dose-dependent effects of heavy metal stress on insect life-history traits, wherein low levels of heavy metal stress induce stimulation, while high levels of heavy metal stress cause inhibition at the transcriptome and proteome levels.

Keywords: Lead (Pb) stress response; Molecular mechanisms; Proteomics; Spodoptera litura; Transcriptomics.