Generalist (polyphagous) herbivores can feed and reproduce on many different plant species and include some of the most pesticide resistant and notorious pests in agriculture. An evolutionary link between host plant range and the development of pesticide resistance has been suggested. Although crucial for devising efficient crop protection strategies, the mechanisms underlying rapid adaptation are not well understood, especially in generalists. The spider mite Tetranychus urticae is a global pest known to feed on 1,100 different hosts from 140 plant families, including most major crops. With experimental advances and new tools developed for T. urticae, we are now poised for fundamental advances in understanding the molecular genetic make-up of adaption in generalist pests.
In POLYADAPT, we first generated a large collection of fully inbred and resistant mite strains and described the sampled genomic variation in the context of selection and adaptation, with a focus on gene copy number variation. We studied gene regulation mechanisms and quantified cis versus trans regulation of gene expression on a genome wide scale. Abundant trans-effects were identified related to detoxification gene families in multiple resistant strains. We then created a unique population resource via crossing schemes that allowed us to map master regulators of gene expression (an eQTL analysis). We found that a single trans eQTL hotspot controlled large differences in the expression of a subset of genes in different detoxification gene families, as well as other genes associated with host plant use. As validated by additional approaches, genetic variation in a nuclear hormone receptor related to HR96 was identified as the causal factor for gene expression variation.
Next, in several highly replicated experimental evolution studies, combined with Bulk Segregant Analysis (BSA), we uncovered without a prior hypothesis the genomic loci that underlie complex cases of resistance and plant adaptation. A core set of adaptation genes was validated by functional expression, electrophysiology and gene editing. For the latter, a revolutionary gene editing method was developed in POLYADPAT.
In summary, POLYADAPT has exploited and created new genomic tools that allowed to elucidate the molecular genetic mechanisms of extreme adaptation in polyphagous pests. This will in the long term lead to innovative methods of pest management.
