RNA interference-mediated silencing of hypoxia-inducible factor 1 signaling pathway genes enhanced the hypoxia sensitivity in the brown-legged grain mite, Aleuroglyphus ovatus.

Abstract

The allergen and storage pest Aleuroglyphus ovatus (Troupeau, 1878) threatens human health and food safety. While modified atmosphere shows pest control potential, its efficacy against this species remains unverified. This study evaluates nitrogen-induced hypoxia effects on A. ovatus mortality, development, and hypoxia-response mechanisms to establish a scientific basis for targeted control strategies. A. ovatus mortality increased with prolonged hypoxia exposure and reduced oxygen concentrations. Following 1-day hypoxia treatment, hatchability declined to 60.85% of control levels under 2% O2, whereas it remained stable at 5% O2. Developmental delays of 2.51 days (5% O2) and 3.12 days (2% O2) were observed in total immature stages compared to normoxic controls. The hypoxia-inducible factor 1 (HIF1) signaling pathway-comprising HIF1α, HIF1β, and PHD-demonstrated evolutionarily conserved functionality, with synchronous expression patterns across all three genes suggesting feedback-mediated co-regulation. Crucially, RNA interference respectively targeting all three genes enhanced adult mortality, achieving 1.67-2.06-fold and 2.19-2.88-fold increases at 5% and 2% O2, compared to non-interference groups. Interference targeting HIF1α in eggs also resulted in suppressed embryonic development and hatching. Mortality acceleration, developmental delays, and pathway co-regulation under hypoxia expose vulnerabilities of A. ovatus exploitable for pest management. Data confirm that combining atmospheric controls with single-gene RNAi targeting any of these three genes enhances lethality. As a systematic dissection of the HIF1 signaling pathway's hypoxic response in arthropods-a rarely explored area-this work established an interdisciplinary strategy integrating ecological interventions and molecular silencing, providing a theoretical basis for sustainable pest control. © 2025 Society of Chemical Industry.