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No Slide Title Tracing the Evolution of Benzoic acid-specific type III Polyketide Synthases (BPS and BIS) in Bonnetiaceae, Guttiferae sensu lato and Podostemaceae, Evidence from Phytochemistry S. Crockett1, L. Beerhues2 1Institute for Pharmaceutical Sciences, Department of Pharmacognosy, Karl-Franzens-University Graz, 8010 Graz, Austria 2Institute for Pharmaceutical Biology, Technische Universität Braunschweig, 38106 Braunschweig, Germany Abstract: Biphenyl synthase (BIS) and benzophenone synthase (BPS) are type III polyketide synthase (PKS) enzymes, responsible for the biosynthesis of a rich diversity of plant secondary metabolites, and share a common ancestor with chalcone synthase (CHS) enzymes, which contribute to the biosynthesis of flavonoid precursor molecules1-2. BIS is the key enzyme in biosynthesis of biphenyl and related dibenzofuran derivatives, commonly found in Rosaceae (order Rosales), while BPS catalyzes the production of benzophenone precursors, which are further modified to form xanthones and benzophenone derivatives, commonly found in Bonnetiaceae, Clusiaceae, Calophyllaceae, Pododstemaceae and Hypericaceae (order Malpighiales) (Fig. 1). These classes of compounds can serve as defence molecules, elicited in response to microbial infection2-3. Order Malpighiales (Other Families) Figure 1: Overview of biosynthetic pathways leading to compounds found in Guttiferae sensu lato, Podostemaceae and Bonnetiaceae. O OH From 1º metabolism O OH O SP/GPP O + P O HO O OH O P O OH Figure 2: A selection from the maximum likelihood majority-rule bootstrap consensus tree based on a combined 13-gene data set4. O OH phosphoenolpyruvate erythrose-4-phosphate cinnamic acid SCoA HO SCoA SCoA AP + 3X O O O O benzoyl-CoA malonyl-CoA acetyl-CoA From 1º metabolism SCoA O O O O linear tetraketide intermediate O O O C2 CoAS O CoAS BIS BPS O C1 C7 O C6 O O C2 -> C7 aldol C6 -> C1 Claisen condensation + condensation decarboxylation OH HO OH Figure 3: Overview of distribution of relevant classes of secondary metabolites. A red X through a colored bar indicates that the ability to produce this compound has been lost by that family, or that these compounds have not yet been isolated from that family. CH3 O OH HO OH As part of a project to examine the distribution of 2˚ metabolites stemming purely or in part from 3,5-dihydroxybiphenyl OH phlorbenzophenone cyclization of benzoyl-primed polyketides in Hypericum (Hypericaceae) and related taxa, the distribution Methylation Hydroxylation O O OH of xanthones, benzophenones (biosynthesized via BPS) and biphenyls (biosynthesized via BIS) as OCH3 Example: cariphenone B HO OH reported in the literature for members of a clade (see Figs. 2-3) strongly supported by molecular Hypericum carinatum (Hypericaceae)10 evidence4. Xanthones and biphenyls have been reported for all families, with the exception of biphenyls in Bonnetiaceae. This data was extracted from a database of literature reporting secondary compounds in OCH3 O OH Example: 3,5-dimethoxybiphenyl Malpighiales, constructed as part of a Dahlem Centre of Plant Sciences (DCPS) project with an ultimate Mourera fluviatilis (Podostemaceae)5 2,3„,4,6-tetrahydroxybenzophenone Stepwise prenylations & intramolecular goal of tracing compound evolution in this order ("Secondary compound evolution and the phylogeny of cyclization, oxidation, etc. yield benzophenone derivatives Malpighiales,“ S. Crockett, N. Korotkova, L. Ferrufino, M. Melzig, T. Borsch, in prep.). A comparison of Regioselective oxidative phenol data for our clade with that of other clades in Malpighiales revealed that xanthones and biphenyls are coupling reactions (CYT P450) yield xanthones found only rarely outside of the clade containing Bonnetiaceae, Clusiaceae, Calophyllaceae, para ortho OH Podostemaceae and Hypericaceae. HO O HO O OH O OH These results provoke the following questions, with reference to BIS and BPS: O OH (1) Are biphenyls present in Bonnetiaceae, but have not yet been isolated? OH O OH O 1,3,7-trihydroxyxanthone 1,3,5-trihydroxyxanthone OH O (2) Was BIS silenced in the line giving rise to Bonnetiaceae, following the split with its sister taxon? Example from: Example from: Tovomita krukovii (Clusiaceae)6 Calophyllum caledonicum (Calophyllaceae)7 garcinol (3) Has BIS been retained in other families of Malpighiales, which along with Rosaceae (where BIS also Derivatives also isolated from: Example from: Garcinia indica (Clusiaceae)9 occurs) belong to the broader Eurosid I clade, or has it evolved twice within higher plants? Bonnetia dinizii (Bonnetiaceae)8 (4) Has BPS evolved only once within Malpighiales (e.g. in this clade) or does it occur in near relatives? Figure 3: Survey of biphenyl, xanthone and benzophenone biosynthesis, with examples from Clusiaceae, Podostemaceae, Hypericaceae and Bonnetiaceae. SP , shikimate pathway; GPP, general Using a combination of analytical and bioinformatics tools, as well as currently available genomic phenylpropanoid pathway; AP, acetate pathway; BIS, biphenyl synthase; BPS, benzophenone synthase resources (e.g. the poplar genome in Malpighiales), could allow us answer to these questions. References: 1. Schröder (1999) Comprehensive Natural Products Chemistry, vol. 1. Elsevier Science, Amsterdam, pp. 749-71. 2. Beerhues and Liu Acknowledgements: ). The full literature database has been prepared as part (“Secondary Metabolite Survey of Malpighiales”) of a broader Dahlem Centre for (2009) Phytochemistry 70: 1719-27. 3. Franklin et al. (2009) Phytochemistry 70: 60-8. 4. Wurdack and Davis (2009) American J. Botany 96: 1551- Plant Sciences (DCPS) project, led by Prof. Dr. Thomas Borsch of the Botanical Garden and Botanical Museum Berlin-Dahlem, in which the first author is involved. 5. Burkhardt et al. (1992) Phytochemistry 31: 543-548. 6. Zhang et al. (2002) Planta Med. 68: 49-54. 7. Morel et al. (2000) J. Nat. Prod. 63: Funding for Sara Crockett , who sincerely thanks T. Borsch for helpful discussions, was further provided by a grant from the Austrian Science Foundation (FWF, Project 1471-1474. 8. De Oliviera et al. (1990) Phytochemistry 29: 1893-1894. 9. Krishnamurthy et al. (1981) Tetrahedron Lett. 22: 793-796. 10. Bernardi T345). et al. (2005) J. Nat. Prod. 68: 784-786..
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