Potential Toxic Mechanisms of Neonicotinoid Insecticides in Rice: Inhibiting Auxin-Mediated Signal Transduction

Abstract

Inappropriate application of pesticides not only causes sub-lethal effects on ecosystem service providers but also reduces crop yield and quality. As a xenobiotic signal molecule, pesticides may interact with signal transduction receptors in crops, resulting in oxidative damage and even metabolic perturbations. We discovered that three neonicotinoid insecticides (NIs), namely, imidacloprid, thiamethoxam, and clothianidin, at 0.06–0.12 kg ai/ha significantly inhibited the auxin signal pathway in rice leaves, thereby reducing the intracellular auxin (IAA) content. Molecular simulation further confirmed that NIs occupied the binding site where auxin transporter-like proteins 1 (LAX11) and 2 (LAX12), in which Thr253 and Asn66 of LAX11, as well as Thr244 and Asn57 of LAX12, were bound to the nitroguanidine of NIs via H-bonds. Meanwhile, Asn66 of LAX11 and Asn57 of LAX12 interacted with nitroguanidine via aromatic H-bonds. Moreover, phenylpropanoid biosynthesis was significantly disturbed because of the inhibited auxin signal pathway. Notably, peroxidase-coding genes were downregulated with a maximum value greater than 10-fold, resulting in decreased antioxidant metabolites flavone (37.82%) and lignin content (20.15%). Ultimately, rice biomass was reduced by up to 25.41% due to the decline in IAA content and antioxidant capacity. This study deeply explored the molecular mechanism of metabolic perturbations in crops stressed by pesticides, thus providing a scientific basis for pesticide environmental risk assessment and agricultural product safety.