Abstract
Simple SummaryInsect chemosensory proteins (CSPs) are potential targets for insect pest control strategies and are proposed to function in insect chemoreception, because they play a role in crop host location by binding and transporting odorant molecules. They are also thought to have other functions, for example, in tissue regeneration and in insecticide resistance, because they also express in nonolfactory tissues and are capable of binding insecticides. However, there are few reports that provide direct evidence for this proposal. In this study, we discovered gene gain-and-loss among aphid populations, possibly associated with different insecticide resistance, and then identified and cloned a CSP gene responsive to insecticide treatments. The introduction of such gene in Drosophila fruit flies made the transgenic flies less sensitive to the treatment of different insecticides. Our study advances the research of insect CSP functions and offers valuable new information to target CSPs for pest management.It has been speculated that insect chemosensory proteins (CSPs) may have additional roles beyond olfaction. In this study, the phylogenetic and genomic analyses of the CSPs of the cotton aphid, Aphis gossypii, revealed the presence of gene gain-and-loss among different aphid field populations. Differential expressions of eight CSP genes were demonstrated after treatments with insecticides of different modes of action. The expression of AgosCSP5 was significantly upregulated by the insecticide treatments in a dose-dependent manner. The Drosophila flies overexpressing AgosCSP5 were significantly less susceptible to the insecticides, omethoate, imidacloprid and cypermethrin but not to deltamethrin and tau-fluvalinate, compared with control flies. The transgenic Drosophila flies exhibited an LC50 resistance ratio of 2.6 to omethoate, compared with control flies. Likewise, the mortality of the transgenic flies to imidacloprid and cypermethrin was significantly lower than that of the control flies (p < 0.01). Homology modelling, molecular docking and dynamic simulation supported the interactions and revealed a higher stability of AgosCSP5/insecticide complexes than AgosCSP5/semiochemical complexes. Our study demonstrates for first time the in vivo evidence for the involvement of CSP genes in insecticide resistance of crop insect pests and provides new insights of the newly discovered CSP-mediated insect resistance mechanism to insecticides.
Highlights
Control of insect pests of commercial field crops is still reliant on a considerable extent on the use of chemical insecticides, which act primarily on several targets in the central nervous system (CNS), i.e., acetylcholinesterase, sodium channels, chloride ion channels, acetylcholine receptor, ryanodine receptors, mineralocorticoid receptors and octopamine receptors [1,2]
A total of eight cotton aphid chemosensory proteins (CSPs) genes were identified from the transcriptome analysis dataset of the cotton aphid population used in this study, numbered as those of the pea aphid from the first aphid CSP genome annotation, based on their similarity with pea aphid CSPs [26]
CSP genes [12,13,27] and those annotated in the cotton aphid genome [29]
Summary
Control of insect pests of commercial field crops is still reliant on a considerable extent on the use of chemical insecticides, which act primarily on several targets in the central nervous system (CNS), i.e., acetylcholinesterase, sodium channels, chloride ion channels, acetylcholine receptor, ryanodine receptors, mineralocorticoid receptors and octopamine receptors [1,2]. The most commonly reported resistance mechanisms to insecticides involve altered target-site and metabolic resistance [2], as well as behavioural resistance and reduced cuticular penetration [3,4]. CSPs are one of the small and water-soluble proteins that are thought to be involved in insect chemosensory perception at the peripheral nerve system by binding and transporting odorant molecules to chemosensory/olfactory receptors (ORs) on olfactory neurons in insect antennae. It has been reported that CSPs have a wide binding spectrum and are broadly expressed in various nonolfactory tissues [9,11]
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