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

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          Abstract

          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.

          Abstract

          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.

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          Most cited references37

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          A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree

          Background The Solanaceae is a plant family of great economic importance. Despite a wealth of phylogenetic work on individual clades and a deep knowledge of particular cultivated species such as tomato and potato, a robust evolutionary framework with a dated molecular phylogeny for the family is still lacking. Here we investigate molecular divergence times for Solanaceae using a densely-sampled species-level phylogeny. We also review the fossil record of the family to derive robust calibration points, and estimate a chronogram using an uncorrelated relaxed molecular clock. Results Our densely-sampled phylogeny shows strong support for all previously identified clades of Solanaceae and strongly supported relationships between the major clades, particularly within Solanum. The Tomato clade is shown to be sister to section Petota, and the Regmandra clade is the first branching member of the Potato clade. The minimum age estimates for major splits within the family provided here correspond well with results from previous studies, indicating splits between tomato & potato around 8 Million years ago (Ma) with a 95% highest posterior density (HPD) 7–10 Ma, Solanum & Capsicum c. 19 Ma (95% HPD 17–21), and Solanum & Nicotiana c. 24 Ma (95% HPD 23–26). Conclusions Our large time-calibrated phylogeny provides a significant step towards completing a fully sampled species-level phylogeny for Solanaceae, and provides age estimates for the whole family. The chronogram now includes 40% of known species and all but two monotypic genera, and is one of the best sampled angiosperm family phylogenies both in terms of taxon sampling and resolution published thus far. The increased resolution in the chronogram combined with the large increase in species sampling will provide much needed data for the examination of many biological questions using Solanaceae as a model system.
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            Acyltransferases in plants: a good time to be BAHD.

            Acylation is a common and biochemically significant modification of plant secondary metabolites. Plant BAHD acyltransferases constitute a large family of acyl CoA-utilizing enzymes whose products include small volatile esters, modified anthocyanins, as well as constitutive defense compounds and phytoalexins. The catalytic versatility of BAHD enzymes makes it very difficult to make functional predictions from primary sequence alone. Recent advances in genome sequencing and the availability of the first crystal structure of a BAHD member are, however, providing insights into the evolution and function of these acyltransferases within the plant kingdom.
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              Biosynthesis of plant volatiles: nature's diversity and ingenuity.

              Plant volatiles (PVs) are lipophilic molecules with high vapor pressure that serve various ecological roles. The synthesis of PVs involves the removal of hydrophilic moieties and oxidation/hydroxylation, reduction, methylation, and acylation reactions. Some PV biosynthetic enzymes produce multiple products from a single substrate or act on multiple substrates. Genes for PV biosynthesis evolve by duplication of genes that direct other aspects of plant metabolism; these duplicated genes then diverge from each other over time. Changes in the preferred substrate or resultant product of PV enzymes may occur through minimal changes of critical residues. Convergent evolution is often responsible for the ability of distally related species to synthesize the same volatile.
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                Author and article information

                Contributors
                lastr@msu.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                12 December 2017
                12 December 2017
                2017
                : 8
                : 2080
                Affiliations
                [1 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Biochemistry and Molecular Biology, , Michigan State University, ; East Lansing, MI 48824 USA
                [2 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Chemistry, , Michigan State University, ; East Lansing, MI 48824 USA
                [3 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Plant Biology, , Michigan State University, ; East Lansing, MI 48824 USA
                [4 ]ISNI 000000041936877X, GRID grid.5386.8, Present Address: Department of Molecular Biology and Genetics, , Cornell University, ; Ithaca, NY 14853 USA
                Author information
                http://orcid.org/0000-0002-4560-3783
                http://orcid.org/0000-0002-3095-9162
                http://orcid.org/0000-0002-7408-6690
                http://orcid.org/0000-0001-6974-9587
                Article
                2045
                10.1038/s41467-017-02045-7
                5727100
                29234041
                f6f821eb-ecd3-4d7c-9c59-cb1343ee21a3
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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                : 11 May 2017
                : 3 November 2017
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