The mechanism of metabolic resistance to pyrethroids and neonicotinoids fade away without selection pressure in the tarnished plant bug Lygus Lineolaris

Authors: Du, Yuzhe - Cathy; ZHU, YU-CHENG - US Department Of Agriculture (USDA); Portilla, Maribel; Zhang, Minling; Reddy, Gadi V.P.

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2023
Publication Date: 5/24/2023
Citation: Du, Y., Zhu, Y., Portilla, M., Zhang, M., Reddy, G.V. 2023. The mechanism of metabolic resistance to pyrethroids and neonicotinoids fade away without selection pressure in the tarnished plant bug Lygus Lineolaris. Pest Management Science. https://doi.org/10.1002/ps.7570.
DOI: https://doi.org/10.1002/ps.7570

Interpretive Summary: BACKGROUND: Heavy selection pressure prompted resistance development in a serious cotton pest tarnished plant bug (TPB), Lygus Lineolaris in the mid-southern USA. Conversely, a lab resistant TPB strain lost the resistance to five pyrethroids and two neonicotinoids after 36 generations without exposure to any insecticide. It is worth to examine why the resistance diminished and to determine whether the resistance reversal has practical value for insecticide resistance management in TPB populations. RESULTS: Field-collected resistant population (field-R) showed 3.9-14.4-fold resistance to five pyrethroids and two neonicotinoids. Resistance levels in the same population without insecticide exposure for 36 generations (lab-R) reduced significantly to 0.8-2.1-fold. Esterase (EST), glutathione S-transferase (GST), and cytochrome P450 monooxygenase (P450) activities significantly increased by approximately 1.92- , 1.43-, and 1.44- fold, respectively in field-R TPBs. In contrast, the three enzyme activities in the lab-R strain were not significantly elevated anymore compared to field-R. Furthermore, field-R displayed 2.50- , 1.97- and 1.48- fold elevated expression levels of EST, GST and P450 CYP6X1v genes, respectively. Similar elevation of the three gene expression levels in lab-R unexpectedly diminished to levels close to that of the lab susceptible (lab-S) TPB. CONCLUSION: Our results strongly suggested that the metabolic resistance reversal was mainly conferred by reversing the overexpression of EST, GST and cytochrome P450 CYP6X1v genes and the elevation of enzyme activities, which resulted in the recovery of the susceptibility in the resistant TPB population. The resistance reversal may be caused by the fitness cost of the resistance, rendering a disadvantage in digestion, reproduction, and eventual diminishing of resistant gene frequency in resistant populations. However, pest’s self-purging of insecticide resistance becomes strategically desirable for managing resistance in pest populations.

Technical Abstract: The tarnished plant bug (TPB) is the most economically damaging insect pest of cotton in the Mid-South USA. The use of insecticides has been the major strategy for controlling TPB, and intensive use of insecticide develops resistance. Conversely, a lab resistant (lab-R) TPB strain lost the resistance to five pyrethroids and two neonicotinoids after 36 generations without exposure to any insecticide. It is worth to examine why the resistance diminished and to determine whether the resistance reversal has practical value for insecticide resistance management in TPB populations. Field-collected resistant population (field-R) showed higher resistance to five pyrethroids and two neonicotinoids. Resistance levels in lab-R reduced significantly. Detoxification enzymes Esterase (EST), glutathione S-transferase (GST), and cytochrome P450 monooxygenase (P450) activities significantly increased respectively in field-R TPBs. In contrast, the three enzyme activities in the lab-R strain were not significantly elevated anymore compared to field-R. Furthermore, field-R displayed elevated expression levels of detoxification genes, respectively. Similar elevation of the three gene expression levels in lab-R unexpectedly diminished to levels close to that of the lab susceptible (lab-S) TPB. Our results strongly suggested that the metabolic resistance reversal was mainly conferred by reversing the overexpression of detoxification genes and the elevation of enzyme activities, which resulted in the recovery of the susceptibility in the resistant TPB population. Hence, our results strongly suggested precautions must be taken to reduce selection pressure by properly rotating insecticides with different modes of action.