Multi-omic analysis of a hyper-diverse plant metabolic pathway reveals evolutionary routes to biological innovation

The diversity of life on Earth is a result of continual innovations in molecular networks influencing morphology and physiology. Plant specialized metabolism produces hundreds of thousands of compounds, offering striking examples of these innovations. To understand how this novelty is generated, we investigated the evolution of the Solanaceae family-specific, trichome-localized acylsugar biosynthetic pathway using a combination of mass spectrometry, RNA-seq, enzyme assays, RNAi and phylogenetics in non-model species. Our results reveal that hundreds of acylsugars are produced across the Solanaceae family and even within a single plant, revealing this phenotype to be hyper-diverse. The relatively short biosynthetic pathway experienced repeated cycles of innovation over the last 100 million years that include gene duplication and divergence, gene loss, evolution of substrate preference and promiscuity. This study provides mechanistic insights into the emergence of plant chemical novelty, and offers a template for investigating the ∼300,000 non-model plant species that remain underexplored.