The Transcription of Flight Energy Metabolism Enzymes Declined with Aging While Enzyme Activity Increased in the Long-Distance Migratory Moth, Spodoptera frugiperda

SIMPLE SUMMARY: In this study, we established the overall transcriptome framework of the thorax and aging-associated expression change trajectories, and constructed the possible flight energy metabolism pathways using potential energy metabolic enzymes in Spodoptera frugiperda females. Gene expression and functional prediction indicated that most genes and pathways related to energy metabolism and other biological processes (e.g., transport, longevity and signaling) were downregulated with aging, whereas the expression of enzymes of proline oxidation and genes related to immunity and repair increased with age. The increased expression of proline oxidation enzymes with age suggests that this energy metabolic pathway also is important or linked to some aging processes. Further activity assay showed that the activities of the five tested key metabolic enzymes increased with age. The transcriptional decrease but activity increase with aging imply that these enzymes are stable. A high activity of enzymes may be crucial for a long-distance migrator. The activity ratio of GAPDH/HOAD was <1 and decreased with age, indicating that lipid is the main flight fuel for this insect, particularly in aged individuals. ABSTRACT: Of all the things that can fly, the flight mechanisms of insects are possibly the least understood. By using RNAseq, we studied the aging-associated gene expression changes in the thorax of Spodoptera frugiperda females. Three possible flight energy metabolism pathways were constructed based on 32 key metabolic enzymes found in S. frugiperda. Differential expression analysis revealed up to 2000 DEGs within old females versus young ones. Expression and GO and KEGG enrichment analyses indicated that most genes and pathways related to energy metabolism and other biological processes, such as transport, redox, longevity and signaling pathway, were downregulated with aging. However, activity assay showed that the activities of all the five tested key enzymes increased with age. The age-associated transcriptional decrease and activity increase in these enzymes suggest that these enzymes are stable. S. frugiperda is a long-distance migrator, and a high activity of enzymes may be important to guarantee a high flight capacity. The activity ratio of GAPDH/HOAD ranged from 0.594 to 0.412, suggesting that lipid is the main fuel of this species, particularly in old individuals. Moreover, the expression of enzymes in the proline oxidation pathway increased with age, suggesting that this energy metabolic pathway also is important for this species or linked to some aging-specific processes. In addition, the expression of immunity- and repair-related genes also increased with age. This study established the overall transcriptome framework of the flight muscle and aging-associated expression change trajectories in an insect for the first time.