Adaptation of insect herbivores to plant defense: Genome-wide transcriptional responses of the lepidopteran midgut to changes in plant defense chemistry
Final Report Abstract
Higher plants produce an extraordinary range of defensive compounds that repel attack by most insect herbivores. Determining how polyphagous insects adapt metabolically to changes in host-plant chemistry is key to understanding patterns of host utilization by insects and, more generally, evolutionary diversification of plant-insect interactions. Here, we used RNA-seq to comprehensively characterize the midgut transcriptional response of the generalist insect herbivore Trichoplusia ni reared on two chemically distinct host plants, thale cress (Arabidopsis thaliana) and cultivated tomato (Solanum lycopersicum). In comparison to tomato-reared larvae, insects grown on Arabidopsis exhibited high expression of genes encoding detoxification enzymes, including cytochromes P450, esterases, glutathione-S-transferases, and UDP-glycosyltransferases. Induced expression of many genes was triggered by dietary glucosinolates and dependent on the plant defense hormone jasmonate. T. ni's response to jasmonate-regulated defense in tomato, which is dominated by proteinase inhibitors and other anti-nutritive compounds, was characterized by massive induction of genes encoding digestive serine proteases. Moreover, glucosinolate-responsive T. ni genes were either not regulated or were repressed in tomato-reared larvae. These findings provide compelling evidence for host plant-specific reprogramming of insect digestive physiology, and further indicate that insect responses to host-plant chemistry are more complex that previously realized. Our results also demonstrate the power of high-throughput transcriptome sequencing in delineating mechanisms of metabolic adaptation and chemical coevolution in any plant-insect interaction.