Biochemical and molecular characterization of neonicotinoid resistance in the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois)

Authors: Du, Yuzhe - Cathy; Scheibener, Shane; Zhu, Yu Cheng; Portilla, Maribel; Reddy, Gadi V.P.

Submitted to: Comparative Biochemistry and Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/30/2023
Publication Date: 10/14/2023
Citation: Du, Y., Scheibener, S.A., Zhu, Y., Portilla, M., Reddy, G.V. 2023. Biochemical and molecular characterization of neonicotinoid resistance in the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois). Comparative Biochemistry and Physiology. https://doi.org/10.1016/j.cbpc.2023.109765.
DOI: https://doi.org/10.1016/j.cbpc.2023.109765

Interpretive Summary: In the southern United States, neonicotinoids are commonly applied as foliar insecticides to control the tarnished plant bug (TPB). In this study, we conducted laboratory spraying bioassays to determine the toxicity of five neonicotinoids and sulfoxaflor to susceptible and late fall field-collected adult TPBs from Coahoma County of Mississippi. Compared to a susceptible population, the field-collected TPBs exhibited the highest resistance to imidacloprid up to 19.5-fold, moderate resistance to acetamiprid, clothianidin , thiamethoxam and the lowest resistance to thiacloprid and sulfoxaflor , respectively. In the field-collected TPBs, activities of three detoxification enzymes, general esterase, glutathione S-transferase (GST) and CYP450 monooxygenase (P450) were significantly increased by 3.43-, 1.48- and 2.7-fold, respectively, when compared to the susceptible TPB. Additionally, the expression of one esterase, one GST and three P450 detoxification genes were significantly elevated compared with susceptible TPB population. Our findings provide valuable information for selection and adoption of neonicotinoid insecticides for resistance management of TPBs and minimizing toxic risk to foraging bees.

Technical Abstract: In the southern United States, neonicotinoids are commonly applied as foliar insecticides to control sucking insect pests, such as the tarnished plant bug (TPB, Lygus lineolaris). In this study, we conducted laboratory spraying bioassays to determine the toxicity of five neonicotinoids and one sulfoximines class (sulfoxaflor) to susceptible and late fall field-collected adult TPBs from Coahoma County of Mississippi. Compared to a susceptible population, the field-collected TPBs exhibited the highest resistance to imidacloprid (up to 19.5-fold), moderate resistance to acetamiprid (9.43-fold), clothianidin (13.68-fold), thiamethoxam (7.88-fold) and the lowest resistance to thiacloprid (4.61-fold) and sulfoxaflor (1.82-fold), respectively. A synergist study demonstrated that piperonyl butoxide (PBO) significantly increased the toxicity of imidacloprid by 22.2-fold (synergistic ratio of LC50s), and thiamethoxam by 15.3-fold against resistant TPBs, while triphenyl phosphate (TPP) and diethyl maleate (DEM) only showed 2-3-fold synergism to both neonicotinoids. In the field-collected TPBs, activities of three detoxification enzymes, general esterase, glutathione S-transferase (GST) and CYP450 monooxygenase (P450) were significantly increased by 3.43-, 1.48- and 2.7-fold, respectively, when compared to the susceptible TPB. Additionally, after 48 h exposure to imidacloprid or thiamethoxam, resistant TPBs exhibited elevated esterase activities, decreased GST activities, and no significant changes on P450 activities. Further examinations revealed that the expression of one esterase, one GST and three P450 detoxification genes were significantly elevated compared with susceptible TPB population. Overall, these results suggest that elevated P450s expression level and enzyme activity are an important mechanism for metabolic resistant in TPBs to neonicotinoids. Our findings also provide valuable information for selection and adoption of neonicotinoid insecticides for resistance management of TPBs and minimizing toxic risk to foraging bees.