High frequency of ryanodine receptor and cytochrome P450 CYP9A186 mutations in insecticide-resistant field populations of Spodoptera exigua from China

Authors: TENG, HAIYUAN - Nanjing Agricultural University; ZUO, YAYUN - Nanjing Agricultural University; YUAN, JING - Nanjing Agricultural University; Fabrick, Jeffrey; WU, YIDONG - Nanjing Agricultural University; YANG, YIHUA - Nanjing Agricultural University

Submitted to: Pesticide Biochemistry and Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/18/2022
Publication Date: 8/1/2022
Citation: Teng, H., Zuo, Y., Yuan, J., Fabrick, J.A., Wu, Y., Yang, Y. 2022. High frequency of ryanodine receptor and cytochrome P450 CYP9A186 mutations in insecticide-resistant field populations of Spodoptera exigua from China. Pesticide Biochemistry and Physiology. 186. Article 105153. https://doi.org/10.1016/j.pestbp.2022.105153.
DOI: https://doi.org/10.1016/j.pestbp.2022.105153

Interpretive Summary: Insecticides are critical for the global protection of crops from insect pests. However, insecticide resistance limits efficacy and represents an increasingly intractable problem affecting crop production worldwide. The diamide, chlorantraniliprole, and the avermectin, emamectin benzoate, are two insecticides that are used extensively to target a wide number of insect pests. One such insect is the beet armyworm, Spodoptera exigua, an important global pest of many crops. Here, an ARS scientist at Maricopa, AZ and collaborators report the presence of high frequencies of mutations in two genes associated with resistance to chlorantraniliprole and emamectin benzoate among six S. exigua field populations collected in China from 2016-2019. Some S. exigua populations were found to have very high levels of resistance to both insecticides and resistance to both compounds is widespread across eastern China. A significant correlation between emamectin benzoate resistance level and the frequency of mutation in a cytochrome P450 gene (CYP9A186) was found in all six field populations, suggesting that detoxification by this enzyme is a major resistance mechanism in S. exigua. These results allow for improved monitoring of S. exigua insecticide resistance and support the need for using insecticidal compounds with different modes of action and/or other integrated pest management strategies to further delay the evolution of insecticide resistance and effectively manage S. exigua in China.

Technical Abstract: The beet armyworm, Spodoptera exigua is a global agricultural pest that is polyphagous, highly dispersive, and often difficult to control due to resistance to many insecticides. Previous studies showed that a target site mutation in the S. exigua ryanodine receptor (SeRyR) corresponding to I4743M contributes approximately 20-fold resistance to chlorantraniliprole, whereas a mutation in the cytochrome P450 enzyme CYP9A186 corresponding to F116V confers 200-fold to emamectin benzoate through enhanced metabolic detoxification. Here, high frequencies of mutations were found among six China S. exigua field populations collected from 2016-2019 resulting in SeRyR I4743M and CYP9A186 F116V substitutions, with some populations having high levels of resistance to chlorantraniliprole and emamectin benzoate, respectively. Whereas we found a significant correlation between emamectin benzoate resistance level and the allele frequency of CYP9A186 F116V, no significant correlation was found between chlorantraniliprole resistance level and SeRyR I4743M allele frequency in the six field populations. These results suggest that CYP9A186 F116V is a major resistance mechanism for emamectin benzoate in the tested field populations, whereas it is likely that resistance mechanisms other than SeRyR I4743M are responsible for resistance to chlorantraniliprole in the six China field populations. Because of the growing resistance to these two insecticides by S. exigua in China, the use of insecticidal compounds with different modes of action and/or other integrated pest management strategies are needed to further delay the evolution of insecticide resistance and effectively manage S. exigua in China.