Multi-omics analyses provide molecular insights into host immune responses and metabolic disruption in Spodoptera frugiperda parasitized by Pyemotes zhonghuajia.

BACKGROUND Host-parasitoid interactions are intricate biological processes in which the host's immune system mounts diverse physiological responses to counter parasitic infection. This study presents a comprehensive investigation into the molecular responses underlying the parasitism of the fall armyworm (Spodoptera frugiperda) by Pyemotes zhonghuajia, a parasitic mite with promising potential as a biocontrol agent. RESULTS Using an integrated multi-omics approach-combining lipidomics, transcriptomics, and proteomics-we examined the effects of P. zhonghuajia parasitism on S. frugiperda at sublethal (10 mites) and lethal (40 mites) densities. Lipidomic analysis revealed significant alterations across 32 lipid classes, including a marked reduction in triglycerides and membrane-associated lipids, indicating impaired energy metabolism and disrupted cellular integrity. Transcriptomic analysis identified 1287 differentially expressed genes (DEGs) under sublethal parasitism and 1774 DEGs under lethal parasitism, with key pathways involved in immune response, detoxification, and lipid metabolism. Proteomic analysis quantified over 4000 proteins, identifying 74 and 247 differentially expressed proteins (DEPs) under sublethal and lethal parasitism, respectively. Integrated analysis highlighted key immune-related proteins, such as small heat shock proteins and C-type lectins, as central to the host immune response. CONCLUSION These findings shed light on how P. zhonghuajia manipulates host immunity and metabolism, identifying potential biomarkers for pest management and contributing to the development of sustainable, RNAi-compatible biocontrol strategies. © 2025 Society of Chemical Industry.