Fruity, sticky, stinky, spicy, bitter, addictive, and deadly: evolutionary signatures of metabolic complexity in the Solanaceae

Covering: 2000-2022Plants collectively synthesize a huge repertoire of metabolites. General metabolites, also referred to as primary metabolites, are conserved across the plant kingdom and are required for processes essential to growth and development. These include amino acids, sugars, lipids, and organic acids. In contrast, specialized metabolites, historically termed secondary metabolites, are structurally diverse, exhibit lineage-specific distribution and provide selective advantage to host species to facilitate reproduction and environmental adaptation. Due to their potent bioactivities, plant specialized metabolites attract considerable attention for use as flavorings, fragrances, pharmaceuticals, and bio-pesticides. The Solanaceae (Nightshade family) consists of approximately 2700 species and includes crops of significant economic, cultural, and scientific importance: these include potato, tomato, pepper, eggplant, tobacco, and petunia. The Solanaceae has emerged as a model family for studying the biochemical evolution of plant specialized metabolism and multiple examples exist of lineage-specific metabolites that influence the senses and physiology of commensal and harmful organisms, including humans. These include, alcohols, phenylpropanoids, and carotenoids that contribute to fruit aroma and color in tomato (fruity), glandular trichome-derived terpenoids and acylsugars that contribute to plant defense (stinky & sticky, respectively), capsaicinoids in chilli-peppers that influence seed dispersal (spicy), and steroidal glycoalkaloids (bitter) from Solanum, nicotine (addictive) from tobacco, as well as tropane alkaloids (deadly) from Deadly Nightshade that deter herbivory. Advances in genomics and metabolomics, coupled with the adoption of comparative phylogenetic approaches, resulted in deeper knowledge of the biosynthesis and evolution of these metabolites. This review highlights recent progress in this area and outlines opportunities for - and challenges of-developing a more comprehensive understanding of Solanaceae metabolism.