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

There are about 300,000 species of plant on Earth, which together produce over a million different small molecules called metabolites. Plants use many of these molecules to grow, to communicate with each other or to defend themselves against pests and disease. Humans have co-opted many of the same molecules as well; for example, some are important nutrients while others are active ingredients in medicines. Many plant metabolites are found in almost all plants, but hundreds of thousands of them are more specialized and only found in small groups of related plant species. These specialized metabolites have a wide variety of structures, and are made by different enzymes working together to carry out a series of biochemical reactions. Acylsugars are an example of a group of specialized metabolites with particularly diverse structures. These small molecules are restricted to plants in the Solanaceae family, which includes tomato and tobacco plants. Moghe et al. have now focused on acylsugars to better understand how plants produce the large diversity of chemical structures found in specialized metabolites, and how these processes have evolved over time. An analysis of over 35 plant species from across the Solanaceae family revealed hundreds of acylsugars, with some plants accumulating 300 or more different types of these specialized metabolites. Moghe et al. then looked at the enzymes that make acylsugars from a poorly studied flowering plant called Salpiglossis sinuata, partly because it produces a large diversity of these small molecules and partly because it sits in a unique position in the Solanaceae family tree. The activities of the enzymes were confirmed both in test tubes and in plants. This suggested that many of the enzymes were “promiscuous”, meaning that they could likely use a variety of molecules as starting points for their chemical reactions. This finding could help to explain how this plant species can make such a wide variety of acylsugars. Moghe et al. also discovered that many of the enzymes that make acylsugars are encoded by genes that were originally copies of other genes and that have subsequently evolved new activities. Plant scientists and plant breeders value tomato plants that produce acylsugars because these natural chemicals protect against pests like whiteflies and spider mites. A clearer understanding of the diversity of acylsugars in the Solanaceae family, as well as the enzymes that make these specialized metabolites, could help efforts to breed crops that are more resistant to pests. Some of the enzymes related to those involved in acylsugar production could also help to make chemicals with pharmaceutical value. These new findings might also eventually lead to innovative ways to produce these chemicals on a large scale.