Transcriptome and metabolome comprehensive analysis reveal the molecular basis of slow-action and non-repellency of cycloxaprid against an eusocial pest, Solenopsis invicta

Chengju Du; Kaibin Jiang; Zhiping Xu; Lei Wang; Jie Chen; Cai Wang

doi:10.3389/fphys.2023.1274416

Transcriptome and metabolome comprehensive analysis reveal the molecular basis of slow-action and non-repellency of cycloxaprid against an eusocial pest, Solenopsis invicta

Front Physiol. 2023 Nov 27:14:1274416. doi: 10.3389/fphys.2023.1274416. eCollection 2023.

Authors

Chengju Du¹, Kaibin Jiang², Zhiping Xu³, Lei Wang⁴, Jie Chen⁵, Cai Wang¹

Affiliations

¹ College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, China.
² Guangdong Provincial Key Laboratory of Silviculture Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, China.
³ Shanghai Key Laboratory of Chemical Biology, School of Pharmacy, East China University of Science and Technology, Shanghai, China.
⁴ College of Plant Protection, South China Agricultural University, Guangzhou, China.
⁵ Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Institute of Plant Protection, Guangdong Academy of Agricultural Sciences, Guangzhou, China.

Abstract

The eusocial pest, red imported fire ant (Solenopsis invicta), is a highly invasive species that poses significant threats to public safety, agriculture, and the ecological environment. Cycloxaprid, a newly identified effective, slow-acting, and non-repellent insecticide against S. invicta, allows contaminated individuals to transfer the insecticide among nestmates through body contact. However, the molecular-level changes occurring in S. invicta post cycloxaprid exposure and any molecular alterations contributing to the slow demise or decreased sensitivity remain unclear. In this study, transcriptomic and metabolomic techniques were used to investigate the molecular mechanisms of S. invicta exposed to cycloxaprid. Differential analysis results revealed 275, 323, and 536 differentially expressed genes at 12, 24, and 48 h, respectively. Genes involved in lipid and energy metabolism, DNA integration, and hormone synthesis were largely upregulated at 12 h, suggesting S. invicta might actively resist cycloxaprid impacts, and predominantly downregulated at 48 h, indicating further functional impairment and impending death. Also, we observed an imbalance in olfactory perception pathways at 12 h, which may indicate a disruption in the olfactory system of S. invicta. Metabolomic results showed that the regulation of most differential metabolites (DMs) was consistent with the expression changes of their related DEGs at different time points. Our study provides insights into the mechanism underlying slow-acting and non-repellent properties of cycloxaprid against S. invicta.

Keywords: cycloxaprid; eusocial insect; formicidae; neonicotinoid insecticide; red imported fire ant.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Key R&D Program of China (No. 2021YFD1000500).