Resistance: DNA methylation and the evolution of pesticide-resistance genes in aphids

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Most insect species are specialist parasites that have adapted to colonize one or a few closely related plant species. Circa 10% of all insect herbivores are generalist ("polyphagous"), and these are often the most noxious pests, having evolved resistance to many pesticides. Generalist insects are prone to such "pesticide-breaking" because by being exposed to a wide range of hosts, they have already evolved resistance to many different plant chemicals. Worryingly, many of these phytochemicals have been used to derive pesticides, and this makes such generalist insects pre-adapted to pesticide-breaking. The green peach aphid (GPA) Myzus persicae can colonize over 400 different plant species, and it has evolved resistance or tolerance to 71 chemicals in 50 years. GPA has become a model to understand how "pesticide-breaking" has evolved. In a former BBSRC funded project, we discovered the molecular mechanism underpinning the insect's remarkable adaptive potential; DNA methylation by two genes (DNMT3A and 3B) enables GPA to adjust to diverse plant species and overcome pesticide toxicity without genetic modification. Genetically identical clones can adjust to a new host plant and show pesticide resistance within hours or days after exposure, and furthermore, their (genetically identical) offspring becomes increasingly well-adjusted. We have shown that the expression of detoxification genes is controlled by DNA methylation (which is an epigenetic process). We also showed that when DNMT3A/B methylation is knocked-down, that the aphids can no longer adjust. We also know that different genes are being up- or down-regulated by DNMT3A/B methylation depending on the host plant or pesticide being encountered. Building on this knowledge, our new proposal has two principal objectives: 1) Identify and describe the entire gene networks affected by de novo DNA methylation mediated by DNMT3A/B. This is important because these are the genes that enable the aphid to detect and respond to the pesticide, and hence, this will help the development of pesticides against novel insect targets. Our Project Partner Syngenta, and others, will thus be helped in their development of such pesticides. 2) Understand the evolutionary forces that generate and shape the DNA variation underpinning the genetic variation in these "resistance genes" in the DNMT3A/B pathway. This is important because the 50 years of pesticide usage will have left a decipherable signature in the genome of the aphids (and other pest insects). By studying this signature, we can optimise pest insect control strategies.The hypotheses are:1) GPA possesses genes that help the insect to detect the novel host plant / pesticides, which instigates DNMT3A/B upregulation.2) The DNMT3A/B methylated genes enable the insect to detoxify these chemicals. 3) Generalist aphids (e.g., GPA) display a larger change in DNMT3A/B expression levels upon host switch and pesticide exposure than specialist aphids (such as the cabbage aphid Brevicoryne brassicae, and the English grain aphid Sitobion avenae).4) Co-regulatory networks affected by DNMT3A/B are more extensive for generalist than specialist aphids. 5) Generalist insect pests (including herbivores, animal and human insect pests) show genome streamlining, lineage-specific gene families and gene duplication that is distinctive from specialist pest insects. 6) The historic use of pesticide treatment will have impacted the 5 evolutionary forces (mutation, recombination, gene flow, genetic drift and natural selection), which has shaped the genomic variation in GPA in populations across the world. In collaboration with our Project Partner Syngenta, we have designed three exciting experiments that test these hypotheses. We believe the knowledge generated by this research is likely to uncover new targets for insect control, and will help to optimise species-specific insect control strategies, and hence secure sustainable agriculture.