Deciphering genomic arms race between the chemical defense of a tree and counter-defense of insect herbivores

Abstract

Background Plant secondary metabolites play important roles in defense against herbivorous insects. However, many insects can overcome plant defenses even when they produce a rich toxin load, and there is an expected arms race between plants evolving new toxins and insects evolving to overcome them. Results Here we deciphered genomic features linked to arms race in the tree of heaven that can produce a high richness of secondary metabolites with about 745 compounds and two monophagous weevils that only feed on this tree species. We first assembled chromosome-level genomes for the tree of heaven and two weevils. Comparative genomics showed an expansion of genes related to synthesizing secondary metabolites in the tree, while in the weevils, genes related to detoxification and chemosensing expanded. The expansion of core genes involved in quassinoid biosynthesis in the tree was linked to tandem duplication and whole genome duplication, while the expansion of detoxifying GST and chemosensing SNMP genes in the two weevils was linked to tandem duplication and novel genes, respectively. Conclusions The results indicate that plants and insect herbivores reshaped their genomes each other in common and unique ways underlying their arms race of defense and countering defense, improving our understanding of genome evolution driven by tropical interactions.