Detect cytochrome C oxidase- and glutathione-S-transferase-mediated detoxification in a permethrin-resistant population of lygus lineolaris

Authors: Zhu, Yu Cheng; Du, Yuzhe - Cathy; YAO, JIANXIU - Kansas State University; Liu, Xiaofen - Fanny; WANG, YANHUA - Zhejiang Academy Of Agricultural Sciences

Submitted to: Toxics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/7/2023
Publication Date: 4/4/2023
Citation: Zhu, Y., Du, Y., Yao, J., Liu, X.F., Wang, Y. 2023. Detect cytochrome C oxidase- and glutathione-S-transferase-mediated detoxification in a permethrin-resistant population of lygus lineolaris. Toxics. 11(4):342. https://doi.org/10.3390/toxics11040342.
DOI: https://doi.org/10.3390/toxics11040342

Interpretive Summary: Polyphagous tarnished plant bug (TPB) is an economically important pest on crops. To control TPB, cotton farmers sprayed up to 7 times per year during the last 10 years. Frequent spray is a driving force for target insects to develop resistance to insecticides. The TPB population in a cotton field developed at least 15-fold resistance to permethrin. To contribute the knowledge for resistance monitoring and management, resistant TPBs (Arct2175FF) were subjected to microarray and pathway functional analyses to see how many genes are up-regulated and how many genes are down-regulated by permethrin treatment on TPBs. Functional analyses will find what biological processes and molecular functions inside insect cell are altered by the insecticide. Data from novel microarray and extensive functional and pathway analyses of 6688 genes showed 3080 genes were significantly up- or down-regulated by >2-fold. Among the 1543 up-regulated genes, 255 genes code 39 different enzymes, and 15 of the 39 potentially participate in important pathways and metabolic detoxification. Oxidase is the most abundant (64) and over-expressed enzyme. Others are dehydrogenases (48), synthases (28), reductases (11), transferases (11), esterases (7), glutathione S-transferases (5 GST). P450 (1) is among the several less abundant enzymes. Pathway analysis revealed several oxidative phosphorylations (produce energy for driving other biological processes) associated with 37 oxidases and 23 reductases. One GST, coded by a gene LL_2285, participated in three pathways including drug and xenobiotics metabolisms, functionally similar to the pesticide detoxification. Therefore, oxidases and GST genes are directly and/or indirectly associated with permethrin detoxification and resistance development. Reductases, dehydrogenases, and others may also indirectly contribute to the permethrin resistance, while the two common detoxification enzymes, P450 and esterase, did not contribute significantly to the detoxification because none of them are associated with any important pathway. In addition, comparison of this study with previous study on imidacloprid resistance in the same TPB 10population showed multiple/cross resistance development in the population with a particular set of genes for different insecticide. Large numbers of protease, eggshell, and vitellogenin genes were among 1537 significantly down-regulated genes, indicating substantial fitness cost imposed on resistance development. The identification of large number of over-expressed new genes in this study establishes a foundation to explore the complicity of permethrin resistance in TPB.

Technical Abstract: Frequent sprays on cotton prompted resistance development in the tarnished plant bug (TPB). Knowledge of global gene regulation is highly desirable to better understand resistance mechanisms and develop molecular tools for monitoring and managing resistance. Novel microarray expressions of 6688 genes showed 3080 significantly up- or down-regulated genes in permethrin-treated TPBs. Among the 1543 up-regulated genes, 255 code for 39 different enzymes, and 15 of these participate in important pathways and metabolic detoxification. Oxidase is the most abundant and over-expressed enzyme. Others included dehydrogenases, synthases, reductases, and transferases. Pathway analysis revealed several oxidative phosphorylations associated with 37 oxidases and 23 reductases. One glutathione-S-transferase (GST LL_2285) participated in three pathways, including drug and xenobiotics metabolisms and pesticide detoxification. Therefore, a novel resistance mechanism of over-expressions of oxidases, along with a GST gene, was revealed in permethrin-treated TPB. Reductases, dehydrogenases, and others may also indirectly contribute to permethrin detoxification, while two common detoxification enzymes, P450 and esterase, played less role in the degradation of permethrin since none was associated with the detoxification pathway. Another potential novel finding from this study and our previous studies confirmed multiple/cross resistances in the same TPB population with a particular set of genes for different insecticide classes.