Transcriptome and behavioral effects of afidopyropen, a novel pesticide, in zebrafish embryos/larvae

Introduction: Afidopyropen is a novel Group 9D insecticide with a chordotonal organ Transient Receptor Potential Vanilloid-type (TRPV) channel modulator mode of action on crop-destroying insects like aphids and other plant-parasitic insects. There is currently little information to date regarding potential off-target effects of afidopyropen on aquatic species. Methods: To address this knowledge gap, we quantified several sub-lethal endpoints including developmental toxicity, oxidative stress, transcriptomics, and locomotor behavior in early staged zebrafish following low concentration exposure to afidopyropen. Results: Survival rates of larval fish were slightly reduced by 10% following exposure to either 10 or 100 µg/L afidopyropen over 7 days. There was no difference in reactive oxygen species (ROS) in fish among treatments; however, there was an up-regulation of both sod1 and sod2 mRNA levels at 0.1 and 1 µg/L, suggesting an oxidative stress response and mitigation of ROS. There was a significant increase in apoptosis based on acridine range staining across all treatments tested. RNA-seq revealed 380 transcripts differentially expressed in zebrafish exposed to 100 ng/L (P-value < 0.05) and 9 after FDR correction. There were 1555 transcripts differentially expressed (P-value < 0.05) and 15 after an FDR correction in zebrafish exposed to 1 µg/L. Biological processes altered by afidopyropen included proteasome, cardiac muscle contraction, oxidative phosphorylation, and ribosomes. These processes were consistently altered in zebrafish at both concentrations tested. Pathway analysis identified processes related to ion channels as up-regulated with afidopyropen exposure in larval fish, including sensory transduction, synaptic transmission, and long-term synaptic potentiation. Evidence for both hypoactivity (dark period) and hyperactivity (light period) of larval zebrafish were observed following afidopyropen exposure, potentially associated with dopamine-related gene networks and ion channels identified in transcriptomics. Discussion/Conclusion: This study improves mechanistic understanding of potential toxicity for a novel pesticide class in early fish embryogenesis.