Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway

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.

地球生命的多样性，源自调控形态建成与生理机能的分子网络的持续革新。植物特化代谢可产生数十万种化合物，为这类革新提供了极具代表性的例证。为阐明这类新颖化学性状的产生机制，我们结合质谱分析、RNA测序（RNA-seq）、酶活实验、RNA干扰（RNAi）以及系统发育分析等手段，对非模式物种中茄科（Solanaceae）特有的、定位于表皮毛（trichome）的酰基糖（acylsugar）生物合成通路的演化过程展开了研究。研究结果显示，整个茄科乃至单株植物均可产生数百种酰基糖，表明该性状具有极高的多样性。这条相对简短的生物合成通路在过去1亿年间经历了多轮革新循环，涵盖基因复制与分化、基因丢失、底物偏好性演化以及底物宽泛性演变等过程。本研究为解析植物化学新颖性的起源提供了机制层面的见解，同时也为探索迄今仍未得到充分研究的约30万个非模式植物物种提供了研究范式。