Evolution of a flipped pathway creates metabolic innovation in tomato trichomes through BAHD enzyme promiscuity

• Published in: Nature communications Vol. 8; no. 1; pp. 2080 - 13
• Main Authors: Fan, Pengxiang, Miller, Abigail M., Liu, Xiaoxiao, Jones, A. Daniel, Last, Robert L.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12.12.2017; Nature Publishing Group; Nature Portfolio
• Subjects: 631/181/735; 631/449/2667; 631/45/320; Acylation - physiology; Acyltransferases - chemistry; Acyltransferases - genetics; Acyltransferases - metabolism; Amino acid sequence; Amino Acids - chemistry; Biodiversity; Biological evolution; Evolution; Evolution, Molecular; Genomics; Humanities and Social Sciences; Innovations; Leaves; Lycopersicon esculentum - physiology; Mass Spectrometry; Metabolic Networks and Pathways - genetics; Metabolism; Metabolites; multidisciplinary; Mutagenesis; Plant protection; Plant Proteins - genetics; Plant Proteins - metabolism; Plants (botany); Science; Science (multidisciplinary); Species diversity; Substrate Specificity - genetics; Sucrose - chemistry; Sucrose - metabolism; Sugar; Tomatoes; Trichomes; Trichomes - enzymology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-017-02045-7

Plants produce hundreds of thousands of structurally diverse specialized metabolites via multistep biosynthetic networks, including compounds of ecological and therapeutic importance. These pathways are restricted to specific plant groups, and are excellent systems for understanding metabolic evolution. Tomato and other plants in the nightshade family synthesize protective acylated sugars in the tip cells of glandular trichomes on stems and leaves. We describe a metabolic innovation in wild tomato species that contributes to acylsucrose structural diversity. A small number of amino acid changes in two acylsucrose acyltransferases alter their acyl acceptor preferences, resulting in reversal of their order of reaction and increased product diversity. This study demonstrates how small numbers of amino acid changes in multiple pathway enzymes can lead to diversification of specialized metabolites in plants. It also highlights the power of a combined genetic, genomic and in vitro biochemical approach to identify the evolutionary mechanisms leading to metabolic novelty. Plants produce large numbers of structurally diverse metabolites through multistep pathways that often use the same precursors. Here the authors utilize the pathway leading to the production of acylated sucroses in the tomato plant to illustrate how metabolite diversity can arise through biochemical pathway evolution.