CYP4CS5‐mediated thiamethoxam and clothianidin resistance is accompanied by fitness cost in the whitefly Bemisia tabaci

Abstract

BackgroundUnderstanding the trade‐offs between insecticide resistance and the associated fitness is of particular importance to sustainable pest control. Being as one of the most devastating pest worldwide, the whitefly Bemisia tabaci has developed resistance to various insecticides, especially neonicotinoid group. Although neonicotinoid resistance is often conferred by P450s‐mediated metabolic resistance, the relationship between such resistance and the associated fitness phenotype remains largely elusive. By gene cloning, qRT‐PCR, RNA interference (RNAi), transgenic Drosophila melanogaster, metabolism capacity in vitro and ‘two sex‐age stage’ life table study, this study aims to explore the molecular role of a P450 gene CYP4CS5 in neonicotinoid resistance and to investigate whether such resistance mechanism carries fitness costs in the whitefly.ResultsOur bioassay tests showed that a total of 13 field‐collected populations of B. tabaci MED displayed low to moderate resistance to thiamethoxam and clothianidin. Compared to the laboratory susceptible strain, we then found that an important P450 CYP4CS5 was remarkably upregulated in the field resistant populations. Such overexpression of CYP4CS5 had a good match with the resistance level among the whitefly samples. Further exposure to the two neonicotinoids resulted in an increase in CYP4CS5 expression. These results implicate that overexpression of CYP4CS5 is closely correlated with thiamethoxam and clothianidin resistance. RNAi knockdown of CYP4CS5 increased mortality of the resistant and susceptible populations after treatment with thiamethoxam and clothianidin in bioassay, while obtained an opposite result when using a transgenic line of D. melanogaster expressing CYP4CS5. Metabolic assays in vitro revealed that CYP4CS5 exhibited certain capacity of metabolizing thiamethoxam and clothianidin. These in vivo and in vitro assays indicate an essential role of CYP4CS5 in conferring thiamethoxam and clothianidin resistance in whitefly. Additionally, our life‐table analysis demonstrate that the filed‐resistant whitefly exhibited a prolonged development time, shortened longevity and reduced fecundity compared to the susceptible, suggesting an existing fitness cost as a result of the resistance.ConclusionCollectively, in addition to the important role of CYP4CS5 in conferring thiamethoxam and clothianidin resistance, we fundamentally discover such resistance mechanism is associated with fitness costs in the whitefly. These findings not only contribute to the development of neonicotinoids resistance management strategies, but also provide a new target for sustainable whitefly control.This article is protected by copyright. All rights reserved.

The Amino Acid Transporter PtCAT7 and Ammonium Nutrition Enhance the Uptake of Thiamethoxam in Citrus Rootstock Seedlings

“…Citrus trees produce multiple flushes within a year, such as in early spring, early summer, late summer, fall, and winter, coinciding with peak populations of ACP. THX, a systemic neonicotinoid insecticide, is widely applied in the fields by foliar spray, seed treatment, or root irrigation and can effectively control a variety of insects, such as S. frugiperda , Bemisia tabaci , and Megalurothrips usitatus . − Our previous study revealed that soil-applied THX was transported into citrus leaves, with higher amounts in new leaves than old leaves, and protected trees from ACP feeding for 60 to 90 days . THX was translocated to the upper part of plants via xylem mobility after being absorbed by the plant roots. , However, the molecular mechanisms of which genes or proteins are involved in xylem mobility remain unclear.…”

UDP-Glycosyltransferases UGT350C3 and UGT344L7 Confer Tolerance to Neonicotinoids in Field Populations of Aphis gossypii

“…11 Bemisia tabaci has developed 255.60-fold and 40.41fold resistance to dinotefuran and thiamethoxam, respectively. 12,13 A previous study showed that several field populations of cotton aphids in central China have developed 5.98-to 2352.96-fold and 5.98-to 2194.96-fold resistance to imidacloprid and thiamethoxam, respectively. 6 Given that the resistance of cotton aphid to neonicotinoids has continued to increase rapidly, the mechanisms of neonicotinoid detoxification in A. gossypii should be well studied.…”

“…Neonicotinoids, as broad spectrum insecticides, are widely valued because of their marked ability to control sucking and chewing insects and their lower toxicity to nontarget organisms, , as they bind to nicotinic acetylcholine receptor (nAChR), leading to nerve stimulation, paralysis, and death in insects Bemisia tabaci has developed 255.60-fold and 40.41-fold resistance to dinotefuran and thiamethoxam, respectively. , A previous study showed that several field populations of cotton aphids in central China have developed 5.98- to 2352.96-fold and 5.98- to 2194.96-fold resistance to imidacloprid and thiamethoxam, respectively . Given that the resistance of cotton aphid to neonicotinoids has continued to increase rapidly, the mechanisms of neonicotinoid detoxification in A.…”