N6-methyladenosine (m6A) is the most prevalent messenger RNA modification in eukaryotes and an important posttranscriptional regulator of gene expression. However, the biological roles of m6A in most insects remain largely unknown. Here, we show that m6A regulates a cytochrome P450 gene (CYP4C64) in the global whitefly pest, Bemisia tabaci, leading to insecticide resistance. Investigation of the regulation of CYP4C64, which confers resistance to the insecticide thiamethoxam, revealed a mutation in the 5′ untranslated region of this gene in resistant B. tabaci strains that introduces a predicted m6A site. We provide several lines of evidence that mRNA methylation of the adenine at this position, in combination with modified expression of m6A writers, acts to increase expression of CYP4C64 and resistance. Collectively, these results provide an example of the epitranscriptomic regulation of the xenobiotic response in insects and implicate the m6A regulatory axis in the development of insecticide resistance.
BACKGROUND: Species displacement by the outcome of interspecific competition is of particular importance to pest management. Over the past decade, spinetoram has been extensively applied in control of the two closely related thrips Megalurothrips usitatus and Frankliniella intonsa worldwide, while whether its resistance is implicated in mediating interspecific interplay of the two thrips remains elusive to date. RESULTS: Field population dynamics (from 2017 to 2019) demonstrated a trend toward displacement of F. intonsa by M. usitatus on cowpea crops, supporting an existing interspecific competition. Following exposure to spinetoram, M. usitatus became the predominate species, which suggests the use of spinetoram appears to be responsible for mediating interspecific interactions of the two thrips. Further annual and seasonal analysis (from 2016 to 2020) of field-evolved resistance dynamics revealed that M. usitatus developed remarkably higher resistance to spinetoram compared to that of F. intonsa, implying a close relationship between evolution of spinetoram resistance and their competitive interactions. After 12 generations of laboratory selection, resistance to spinetoram in M. usitatus and F. intonsa increased up to 64.50-fold and 28.33-fold, and the average realized heritability (h 2 ) of resistance was calculated as 0.2550 and 0.1602, respectively. Interestingly, two-sex life table analysis showed that the spinetoram-resistant strain of F. intonsa exhibited existing fitness costs, but not the M. usitatus. These indicate that a rapid development of spinetoram resistance and the lack of associated fitness costs may be the mechanism underlying recent dominance of M. usitatus over F. intonsa.CONCLUSION: Collectively, our results uncover the involvement of insecticide resistance in conferring displacement mechanism behind interspecific competition, providing a framework for understanding the significance of the evolutionary relationships among insects under ongoing changing environments. These findings also can be invaluable in proposing the most appropriate strategies for sustainable thrips control programs.
The bean flower thrips, Megalurothrips usitatus (Bagrall) (Thysanoptera: Thripidae), is an important pest of legume crops in South China. Yellow, blue, or white sticky traps are currently recommended for monitoring and controlling thrips, but it is not known whether one is more efficient than the other or if selectivity could be optimized by trap color. We investigated the response of thrips and beneficial insects to different-colored sticky traps on cowpea, Vigna unguiculata. More thrips were caught on blue, light blue, white, and purple traps than on yellow, green, pink, gray, red, or black traps. There was a weak correlation on the number of thrips caught on yellow traps and survey from flowers (r = 0.139), whereas a strong correlation was found for blue traps and thrips' survey on flowers (r = 0.929). On commercially available sticky traps (Jiaduo®), two and five times more thrips were caught on blue traps than on white and yellow traps, respectively. Otherwise, capture of beneficial insects was 1.7 times higher on yellow than on blue traps. The major natural enemies were the predatory ladybird beetles (63%) and pirate bugs Orius spp. (29%), followed by a number of less representative predators and parasitoids (8%). We conclude the blue sticky trap was the best to monitor thrips on cowpea in South China.
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