AgosOBP3 knockdown disrupts host plant preference in cotton-specialized Aphis gossypii

Aphis gossypii shows strong intraspecific host specialization, making it an excellent model for olfaction-driven host adaptation. Hap1 (cotton-specialized haplotype) and Hap3 (cucurbit-specialized haplotype) are the two main haplotypes. Odorant-binding proteins (OBPs) play pivotal roles in insect host recognition and are potential RNAi targets. This study aims to elucidate the functional role of AgosOBP3 in host specialization of A. gossypii.

We used genome-wide identification, transcriptomic comparison, RNA interference, host choice assays and life table analysis to characterize AgosOBP3 function. We identified 13 OBP genes from the A. gossypii genome, among which AgosOBP3 expression in polyphagous Hap4 was significantly higher than in the cotton-specialized Hap1 (1.79-fold, P < 0.05). Life table assays confirmed that Hap1 performed well on cotton but exhibited extremely low survival and reproduction on cucumber, demonstrating typical host-specialization characteristics. RNAi-mediated silencing of AgosOBP3 (46.8% expression reduction) substantially altered host preference in Hap1: at 48 h, 70% of control aphids selected cotton, whereas 65% of treated aphids chose cucumber, representing a significant reversal in host selection. Bioassay results revealed that RNAi-treated Hap1 A. gossypii showed a 39.6% increase in fecundity on cucumber but a 39.5% decrease on cotton.

The expression level of AgosOBP3 directly governs host preference in A. gossypii toward its specialized hosts. Interference with this gene disrupts host selection preference, redirecting the cotton-specialized haplotype toward nonadapted hosts. Our results establish AgosOBP3 as a critical determinant of host specialization, offering theoretical insights and a viable molecular target for olfactory disruption-based sustainable management strategies against aphid pests. © 2026 Society of Chemical Industry.