Rhus and aphids (PRJCA043172)
Coevolutionary arms races are a powerful driver of reciprocal adaptation, yet the mechanisms linking plant-insect interactions to metabolic diversification remain poorly understood. Here, we dissect the 48-million-year mutualism between Rhus trees and gall-inducing aphids, revealing how ethylene signaling mediates the delicate balance between host defense and parasite manipulation. Phylogenomic analyses uncover X chromosome fission in aphids and parallel selection in Rhus defense genes. Through integrated multi-omics and functional assays, we demonstrate that aphid effector proteins, particularly ScCathB3, selectively degrade ethylene-induced chitinases to suppress plant immunity. Concurrently, Rhus plants reorganize ethylene-activated metabolic pathways to hyperaccumulate hydrolyzable tannins, which constitute up to 70% of gall dry weight, a striking example of chemical defense escalation. Crucially, we identify that galloylation, the key step in tannin biosynthesis, requires obligate heterotetrameric serine carboxypeptidase-like acyltransferase (SCPL-AT) complexes. These enzyme assemblies represent an evolutionary innovation ensuring metabolic precision in high-tannin production. Our findings redefine the Rhus-aphid system as a dual-force coevolutionary model, where pathogen-like effector-mediated manipulation converges with host metabolic pathway innovation. This study not only advances our understanding of plant-insect coevolution but also provides a framework for engineering sustainable tannin bioproduction, with potential applications in biomaterials, pharmaceuticals, and agrochemicals.