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Tobacco NtOMT2 was previously reported as an inducible, o-diphenol O-methyltransferase (OMT) that exhibits similar preferences towards quercetin and caffeic acid as substrates. In this report, we further examine the substrate specificity of NtOMT2 based on enzyme assays, kinetic data and phylogenetic analysis. We demonstrate that NtOMT2 is a flavonol OMT that catalyzes multiple O-methylation of the flavonol quercetin giving rise to its mono-, di- and trimethyl ether derivatives. Mono-methylation of quercetin on the 3-, 3′-/4′- and 7-hydroxyl groups occurs in a random fashion according to the physio-chemical properties of their hydroxyl groups, together with their similar binding energies in the NtOMT2 binding pocket. Homology modeling of NtOMT2 with the Medicago sativa COMT as a template indicates that the H-bonding network between the functional hydroxyl groups and the neighboring residues allowed NtOMT2 to establish a number of energetically similar binding arrangements with slightly different binding modes; thus resulting in a random multiple methylation. NtOMT2 functions as a proximity and orientation agent in using the general base catalysis for multiple methylation of quercetin. This is the first report to indicate that quercetin multiple methylation is catalyzed by a single gene product.
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