Genome sequencing and transcriptome profiling of the greenhouse whitefly, Trialeurodes vaporariorum, reveals a link between host plant adaptation and insecticide sensitivity

The glasshouse whitefly, Trialeurodes vaporariorum, is a damaging crop pest and an invasive generalist capable of feeding on a broad range of host plants. As such this species has evolved mechanisms to circumvent the wide spectrum of anti-herbivore allelochemicals produced by its host range. T. vaporariorum has also demonstrated a remarkable ability to evolve resistance to many of the synthetic insecticides used for control. To gain insight into the molecular mechanisms that underpin the polyphagy of this species and its resistance to natural and synthetic xenobiotics, we sequenced and assembled a reference genome for T. vaporariorum. Curation of genes putatively involved in the detoxification of natural and synthetic xenobiotics revealed a marked reduction in specific gene families, such as cytochrome p450s, between this species and another generalist whitefly, Bemisia tabaci. Transcriptome profiling of T. vaporariorum upon transfer to a range of different host plants revealed profound differences in the transcriptional response to more or less challenging hosts. Large scale changes in gene expression were observed during adaptation to challenging hosts with a range of genes involved in gene regulation, signalling, detoxification, and excretion differentially expressed. Remarkably, these changes in gene expression were associated with significant shifts in the tolerance of host-adapted T. vaporariorum lines to natural and synthetic insecticides. Indeed, the lines reared on nightshade host plants exhibited significant tolerance to compounds from four different insecticide classes. Functional studies provided evidence that upregulation of P450s belonging to the CYP6CM subfamily during host adaptation may contribute to the observed tolerance to natural xenobiotics. Our findings provide further insights into the ability of polyphagous insects to extensively reprogram gene expression during host adaptation and illustrate the potential implications of this on their sensitivity to synthetic insecticides.