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Enzyme Required for Synthesis of Antimicrobial Triterpenes in Plants

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Enzyme Required for Synthesis of Antimicrobial Triterpenes in Plants Biochemical analysis of a multifunctional cytochrome P450 (CYP51) enzyme required for synthesis of antimicrobial triterpenes in plants Katrin Geislera,b, Richard K. Hughesc, Frank Sainsburyc,1, George P. Lomonossoff c, Martin Rejzekc, Shirley Fairhurstc, Carl-Erik Olsenb, Mohammed Saddik Motawiab, Rachel E. Meltona, Andrew M. Hemmingsd,e, Søren Bakb, and Anne Osbourna,2 Departments of aMetabolic Biology and cBiological Chemistry, John Innes Centre, Norwich NR4 7UH, United Kingdom; bDepartment of Plant and Environmental Sciences, VKR Research Centre Pro-Active Plants, Faculty of Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Copenhagen, Denmark; and Schools of dChemistry and eBiological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom Edited by Joseph R. Ecker, The Salk Institute, La Jolla, CA, and approved July 18, 2013 (received for review May 15, 2013) Members of the cytochromes P450 superfamily (P450s) catalyze with sterol 14α-demethylase activity are known as obtusifoliol a huge variety of oxidation reactions in microbes and higher 14α-demethylases and constitute the CYP51G subfamily (7). organisms. Most P450 families are highly divergent, but in contrast The triterpenes are one of the largest classes of plant-derived the cytochrome P450 14α-sterol demethylase (CYP51) family is one natural products. Previously we reported the discovery of a gene of the most ancient and conserved, catalyzing sterol 14α-demethy- encoding a divergent plant CYP51 (AsCyp51H10) that is dis- lase reactions required for essential sterol synthesis across the pensable for the synthesis of essential sterols but is required for fungal, animal, and plant kingdoms. Oats (Avena spp.) produce production of specialized antimicrobial triterpene glycosides antimicrobial compounds, avenacins, that provide protection known as avenacins that confer disease resistance in oats (15). against disease. Avenacins are synthesized from the simple triter- AsCyp51H10 (also known as Saponin-deficient 2 or Sad2) was β fi pene, -amyrin. Previously we identi ed a gene encoding a mem- first identified in a screen for mutants of diploid oat that were AsCyp51H10 ber of the CYP51 family of cytochromes P450, (also unable to make avenacins (16). Subsequent analysis revealed known as Saponin-deficient 2, Sad2), that is required for avenacin fi that this gene forms part of a metabolic gene cluster for avenacin synthesis in a forward screen for avenacin-de cient oat mutants. synthesis (15). AsCYP51H10 (SAD2) belongs to a newly defined sad2 mutants accumulate β-amyrin, suggesting that they are and as yet functionally uncharacterized subfamily of CYP51 blocked early in the pathway. Here, using a transient plant expres- enzymes, the CYP51H subfamily, which also includes nine sion system, we show that AsCYP51H10 is a multifunctional P450 fi capable of modifying both the C and D rings of the pentacyclic members of unknown function from rice (7, 15, 17). The rst β β β committed step in the synthesis of avenacins is the cyclization of triterpene scaffold to give 12,13 -epoxy-3 ,16 -dihydroxy-olea- β β nane (12,13β-epoxy-16β-hydroxy-β-amyrin). Molecular modeling 2,3-oxidosqualene to -amyrin, catalyzed by the oat -amyrin and docking experiments indicate that C16 hydroxylation is likely synthase AsbAS1 (also known as SAD1) (18, 19). Biochemical β to precede C12,13 epoxidation. Our computational modeling, in analysis has shown that sad2 mutants accumulate -amyrin, β combination with analysis of a suite of sad2 mutants, provides suggesting that -amyrin may be the substrate for AsCYP51H10 insights into the unusual catalytic behavior of AsCYP51H10 and (15, 20). Partial characterization of AsCYP51H10 in yeast is its active site mutants. Fungal bioassays show that the C12,13 consistent with this observation (21). However, full character- epoxy group is an important determinant of antifungal activity. Accordingly, the oat AsCYP51H10 enzyme has been recruited from Significance primary metabolism and has acquired a different function compared — to other characterized members of the plant CYP51 family as We carried out functional analysis of the oat enzyme AsCYP51H10, fi a multifunctional stereo- and regio-speci c hydroxylase in plant which is a divergent member of the CYP51 cytochrome P450 specialized metabolism. family and showed that this enzyme is able to catalyze both hydroxylation and epoxidation of the simple triterpene β- CPMV-HT transient expression | cytochrome P450 monooxygenase CYP51 amyrin to give 12,13β-epoxy-3β,16β-dihydroxy-oleanane (12,13β- family | disease resistance | neofunctionalization | terpenes epoxy-16β-hydroxy-β-amyrin). In contrast, the canonical CYP51 enzymes are highly conserved and catalyze only sterol deme- igher plants produce a huge array of low molecular weight thylation. We further show that the C12,13 epoxy group is Hspecialized compounds (natural products) that have im- critical for antifungal activity, a discovery that has important portant functions in biotic and abiotic stress tolerance (1, 2) and implications for triterpene metabolic engineering for food, that also provide a matchless starting point for drug and agro- health, and industrial biotechnology applications. chemical discovery (3). The cytochrome P450 (P450) superfamily is the largest family of plant metabolic enzymes. The majority of Author contributions: K.G., A.M.H., S.B., and A.E.O. designed research; K.G., R.K.H., S.F., fl fi C.-E.O., M.S.M., R.E.M., and A.M.H. performed research; K.G., F.S., G.P.L., and R.E.M. plant P450 families are highly divergent, re ecting diversi cation contributed new reagents/analytic tools; K.G., M.R., S.F., C.-E.O., M.S.M., R.E.M., A.M.H., and neofunctionalization as new metabolic pathways evolve (4– S.B., and A.E.O. analyzed data; and K.G., G.P.L., M.R., A.M.H., S.B., and A.E.O. wrote 6). In contrast, the cytochrome P450 14α-sterol demethylase the paper. (CYP51) family is one of the most ancient of the P450 families, Conflict of interest statement: A.E.O. is a co-inventor on a patent filing on AsCYP51H10. and the function of CYP51 enzymes is highly conserved across This article is a PNAS Direct Submission. fungi, plants, and animals (7, 8). These enzymes are sterol Freely available online through the PNAS open access option. – demethylases required for the synthesis of essential sterols (9 1Present address: Australian Institute for Bioengineering and Nanotechnology, University 14). Although different sterol substrates are used (e.g., lanosterol of Queensland, St Lucia QLD 4072, Australia. in mammals and yeast and obtusifoliol in plants), the reaction 2To whom correspondence should be addressed. E-mail: [email protected]. — α mechanism 14 -demethylation and subsequent formation of This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. a Δ14–15 double bond—is preserved. In plants, CYP51 enzymes 1073/pnas.1309157110/-/DCSupplemental. E3360–E3367 | PNAS | Published online August 12, 2013 www.pnas.org/cgi/doi/10.1073/pnas.1309157110 Downloaded by guest on September 29, 2021 ization of the biochemical function of AsCYP51H10 has not yet the AsbAS1 and AsCYP51H10 constructs. Leaf tissue was har- PNAS PLUS been carried out. vested after 6 d, and protein extracts were analyzed by immu- Triterpenes have a wide range of commercial applications as noblot analysis using polyclonal antisera raised against AsbAS1 agrochemicals, food additives, and pharmaceuticals and as (attempts to raise antisera specific for AsCYP51H10 were un- foaming agents in the beverage, food, and cosmetics industries successful). AsbAS1 protein was readily detectable in protein (22). Commercial exploitation of triterpenes has been limited extracts from leaves infiltrated with the AsbAS1 construct alone thus far by their recalcitrance to synthetic chemistry and their or the AsbAS1 and AsCYP51H10 constructs together, as expec- occurrence in low abundance in complex mixtures in plants (23). ted (Fig. 1C). The triterpene content of infiltrated leaf material The availability of enzymes that can stereo- and regio-specifically then was analyzed using GC-MS. The total ion chromatogram functionalize triterpene scaffolds will open opportunities for the (TIC) from AsbAS1-infiltrated leaf extracts revealed a peak with production of novel triterpenes using synthetic biology ap- a retention time of 17.8 min that was not observed in the empty proaches. Several triterpene-modifying P450s from eudicots have vector control (Fig. 1D). The fragmentation pattern of this peak been characterized recently by heterologous expression in yeast. was identical to that of β-amyrin (Fig. S1A). β-Amyrin was not These include CYP93E1 from soybean, which hydroxylates detected in the empty vector-treated control leaves or leaves that β-amyrin and sophoradiol at position C24 (24); two P450s from had been infiltrated with the AsCYP51H10 construct alone (Fig. liquorice, one (CYP88D6) that converts β-amyrin to 11-oxo- 1D). Coexpression of AsbAS1 and AsCYP51H10 resulted in β-amyrin and a second (CYP72A154) that converts 11-oxo- a substantial reduction in β-amyrin and the appearance of a new β-amyrin to glycyrrhizin acid (25, 26); and CYP716A12 from peak with a retention time of 19.1 min (Fig. 1D), indicating that Medicago truncatula,aβ-amyrin 28-oxidase that converts β-amyrin AsCYP51H10 is able to modify β-amyrin. to oleanolic acid (27, 28). These enzymes belong to different P450 families, indicating that the ability to oxygenate β-amyrin Identification of the AsCYP51H10 Product. The extracted ionization has arisen multiple times during evolution. spectrum for the new peak revealed a molecular ion at m/z 602 Here we show that AsCYP51H10 is a multifunctional CYP51 (retention time = 19.08 min; Fig. 2A). Given that we analyzed that is able to convert β-amyrin to a product that we determined trimethylsilyl (TMS)-derivatized extracts and the AsCYP51H10 by NMR spectrometry (NMR) to be 12,13β-epoxy-3β,16β-dihy- product is derived from β-amyrin, a mass of 602 is consistent with droxy-oleanane (12,13β-epoxy-16β-hydroxy-β-amyrin).
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