Lam, Kevin C. and Ibrahim, Ragai K. and Behdad, Bahareh and Dayanandan, Selvadurai (2007) Structure, function, and evolution of plant O-methyltransferases. Genome, 50 (11). pp. 1001-1013. ISSN 0831-2796
- Published Version
Official URL: http://dx.doi.org/10.1139/G07-077
Plant O-methyltransferases (OMTs) constitute a large family of enzymes that methylate the oxygen atom of a variety of secondary metabolites including phenylpropanoids, flavonoids, and alkaloids. O-Methylation plays a key role in lignin biosynthesis, stress tolerance, and disease resistance in plants. To gain insights into the evolution of the extraordinary diversity of plant O-methyltransferases, and to develop a framework phylogenetic tree for improved prediction of the putative function of newly identified OMT-like gene sequences, we performed a comparative and phylogenetic analysis of 61 biochemically characterized plant OMT protein sequences. The resulting phylogenetic tree revealed two major groups. One of the groups included two sister clades, one comprising the caffeoyl CoA OMTs (CCoA OMTs) that methylate phenolic hydroxyl groups of hydroxycinnamoyl CoA esters, and the other containing the carboxylic acid OMTs that methylate aliphatic carboxyl groups. The other group comprised the remaining OMTs, which act on a diverse group of metabolites including hydroxycinnamic acids, flavonoids, and alkaloids. The results suggest that some OMTs may have undergone convergent evolution, while others show divergent evolution. The high number of unique conserved regions within the CCoA OMTs and carboxylic acid OMTs provide an opportunity to design oligonucleotide primers to selectively amplify and characterize similar OMT genes from many plant species.
|Divisions:||Concordia University > Faculty of Arts and Science > Biology|
|Authors:||Lam, Kevin C. and Ibrahim, Ragai K. and Behdad, Bahareh and Dayanandan, Selvadurai|
|Journal or Publication:||Genome|
|Digital Object Identifier (DOI):||10.1139/G07-077|
|Keywords:||methylation, flavonoids, enzyme evolution, methyltransferase, caffeoyl CoA|
|Deposited By:||DANIELLE DENNIE|
|Deposited On:||08 Jun 2010 21:06|
|Last Modified:||24 Aug 2016 21:26|
Aharoni, A.M., Gaidukov, L., Khersonsky, O., Gould, S.M., Roodveldt, C., and Tawfiq, D.S. 2005. The ‘evolvability’ of promiscuous protein functions. Nat. Genet. 37: 73–76.
Akashi, T., Sawada, Y., Shimada, N., Sakurai, N., Aoki, T., and Ayabe, S. 2003. cDNA cloning and biochemical characterization of S-adenosyl-L-methionine:2,7,4′-trihydroxyisoflavone 4′-O-methyltransferase, a critical enzyme of the legume isoflavone phytoalexin pathway. Plant Cell Physiol. 44: 103–112.
Bohm, B.A. 1998. Flavonoid functions in nature. In Introduction to flavonoids. Chemistry and biochemistry of organic natural products. Vol. 2. Harwood Academic Publishers, Amsterdam. pp. 339–364.
Bugos, R., Chiang, V., and Campbell, W. 1991. cDNA cloning, sequence analysis and seasonal expression of a lignin-specific caffeic acid/5-hydroxyferulic acid O-methyltransferase of aspen. Plant Mol. Biol. 17: 1203–1215.
Busam, G., Junghanns, K., Kneusel, R., Kassemeyer, H.-H., and Matern, U. 1997. Characterization and expression of caffeoyl coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L. Plant Physiol. 115: 1039–1048.
Cacace, S., Schröder, G., Wehinger, E., Strack, D., Schmidt, J., and Schröder, J. 2003. A flavonol O-methyltransferase from Catharanthus roseus performing two sequential methylations. Phytochemistry, 62: 127–137.
Chiron, H., Drouet, A., Claudot, A.-C., Eckerskorn, C., Trost, M., Heller, W., Ernst, D., and Sandermann, H., Jr. 2000. Molecular cloning and functional expression of a stress-induced multifunctional O-methyltransferase with pinosylvin methyltransferase activity from Scots pine (Pinus sylvestris L.). Plant Mol. Biol. 44: 733–745.
Christensen, A., Gregersen, P., Olsen, C., and Collinge, D. 1998. A flavonoid 7-O-methyltransferase is expressed in barley leaves in response to pathogen attack. Plant Mol. Biol. 36: 219–227.
Collazo, P., Montoliu, L., Puigdomenech, P., and Rigau, J. 1992. Structure and expression of the lignin O-methyltransferase gene from Zea mays L. Plant Mol. Biol. 20: 857–867.
Copley, S.D. 2003. Enzymes with extra talents: moonlighting functions and catalytic promiscuity. Curr. Opin. Chem. Biol. 7: 265–272.
Croteau, R., Kutchan, T.M., and Lewis, N.G. 2000. Natural products (secondary metabolites). In Biochemistry and molecular biology of plants. Edited by B. Buchanan, W. Gruissem, and R. Jones. American Society of Plant Physiologists, Rockville, Md. pp. 1250–1318.
Dudareva, N., Murfitt, L., Mann, C., Gorenstein, N., Kolosova, N., Kish, C., Bonham, C., and Wood, K. 2000. Developmental regulation of methyl benzoate biosynthesis and emission in snapdragon flowers. Plant Cell, 12: 949–961.
Facchini, P.J. 2006. Regulation of alkaloid biosynthesis in plants. Alkaloids Chem. Biol. 63: 1–44.
Frick, S., and Kutchan, T.M. 1999. Molecular cloning and functional expression of O-methyltransferases common to isoquinoline alkaloid and phenylpropanoid biosynthesis. Plant J. 17: 329–339.
Gang, D., Lavid, N., Zubieta, C., Chen, F., Beuerle, T., Lewinsohn, E., Noel, J., and Pichersky, E. 2002. Characterization of phenylpropene O-methyltransferases from sweet basil: facile change of substrate specificity and convergent evolution within a plant O-methyltransferase family. Plant Cell, 14: 505–519.
Gauthier, A., Gulick, P., and Ibrahim, R.K. 1996. cDNA cloning and characterization of a 3′/5′-O-methyltransferase for partially methylated flavonols from Chrysosplenium americanum. Plant Mol. Biol. 32: 1163–1169.
Gauthier, A., Gulick, P., and Ibrahim, R.K. 1998. Characterization of two cDNA clones which encode O-methyltransferases for the methylation of both flavonoid and phenylpropanoid compounds. Arch. Biochem. Biophys. 351: 243–249.
Gowri, G., Bugos, R., Campbell, W., Maxwell, C., and Dixon, R.A. 1991. Stress responses in alfalfa (Medicago sativa L.). X. Molecular cloning and expression of S-adenosyl-L-methionine:caffeic acid 3-O-methyltransferase, a key enzyme of lignin biosynthesis. Plant Physiol. 97: 7–14.
He, X.-Z., Reddy, J., and Dixon, R.A. 1998. Stress responses in alfalfa (Medicago sativa L.). XXII. cDNA cloning and characterization of an elicitor-inducible isoflavone 7-O-methyltransferase. Plant Mol. Biol. 36: 43–54.
Hehmann, M., Lukacin, R., Ekiert, H., and Matern, U. 2004. Furanocoumarin biosynthesis in Ammi majus L.: cloning of bergaptol O-methyltransferase. Eur. J. Biochem. 271: 932–940.
Horowitz, N.H. 1945. On the evolution of biochemical synthesis. Proc. Natl. Acad. Sci. U.S.A. 31: 153–157.
Ibdah, M., Zhang, X.-H., Schmidt, J., and Vogt, T. 2003. A novel Mg2+-dependent O-methyltransferase in the phenylpropanoid metabolism of Mesembryanthemum crystallinum. J. Biol. Chem. 278: 43961–43972.
Ibrahim, R.K. 1997. Plant O-methyltransferase signatures. Trends Plant Sci. 2: 249–250.
Ibrahim, R.K., and Anzellotti, D. 2003. The enzymatic basis of flavonoid biodiversity. In Integrative phytochemistry: from ethnobotany to molecular ecology. Edited by J.T. Romeo. Pergamon, New York. pp. 1–36.
Ibrahim, R.K., and Muzac, I. 2000. The methyltransferase gene superfamily: a tree with multiple branches. In Evolution of metabolic pathways. Edited by J.T. Romeo, R.K. Ibrahim, L. Varin, and V. De Luca. Pergamon, New York. pp. 349–384.
Ibrahim, R.K., De Luca, V., Khouri, H., Latchinian, L., Brisson, L., and Charest, J.-P. 1987. Enzymology and compartmentation of polymethylated flavonol glucosides in Chrysosplenium americanum. Phytochemistry, 26: 1237–1245.
Ibrahim, R.K., Bruneau, A., and Bantignies, B. 1998. Plant O-methyltransferases: molecular analysis, common signature and classification. Plant Mol. Biol. 36: 1–10.
Inoue, K., Sewalt, V., Balance, G., Ni, W., Stürzer, C., and Dixon, R.A. 1998. Developmental expression and substrate specificities of alfalfa caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase in relation to lignification. Plant Physiol. 117: 761–770.
Joshi, C.P., and Chiang, V.L. 1998. Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol. Biol. 37: 663–674.
Larsson, K.A.E., Zetterlund, I., Delp, G., and Jonsson, L.M.V. 2006. N-Methyltransferase involved in gramine biosynthesis in barley: cloning and characterization. Phytochemistry, 67: 2002–2008.
Lavid, N., Wang, J., Shalit, M., Guterman, I., Bar, E., Bruerle, T., et al. 2002. O-Methyltransferases involved in the biosynthesis of volatile phenolic derivatives in rose petals. Plant Physiol. 129: 1899–1907.
Lee, J., Vogt, T., Hause, B., and Löbler, M. 1997. Methyl jasmonate induces an O-methyltransferase in barley. Plant Cell Physiol. 38: 851–862.
Lewis, N.G., and Yamamoto, E. 1990. Lignin: occurrence, biogenesis and biodegradation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41: 455–496.
Li, L., Popko, J., Zhang, X.-H., Osakabe, K., Tsai, C.-J., Joshi, C., and Chiang, V. 1997. A novel multifunctional O-methyltransferase implicated in a dual methylation pathway associated with lignin biosynthesis in loblolly pine. Proc. Natl. Acad. Sci. U.S.A. 94: 5461–5466.
Li, L., Osakabe, Y., Joshi, C., and Chiang, V.L. 1999. Secondary xylem-specific expression of caffeoyl coenzyme A 3-O-methyltransferase plays an important role in the methylation pathway associated with lignin biosynthesis in loblolly pine. Plant Mol. Biol. 40: 555–565.
Maddison, D.R., and Maddison, W.P. 2000. MacClade. Version 4.02 [computer program]. Sinauer Associates, Sunderland, Mass.
Martin, J.L., and McMillan, F.M. 2002. S-Adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol. 12: 783–793.
Martz, F., Maury, S., Pincon, G., and Legrand, M. 1998. cDNA cloning, substrate specificity and expression study of tobacco caffeoyl CoA 3-O-methyltransferase, a lignin biosynthetic enzyme. Plant Mol. Biol. 36: 427–437.
Maxwell, C., Harrison, M., and Dixon, R.A. 1993. Molecular characterization and expression of alfalfa isoliquiritigenin 2′-O-methyltransferase, an enzyme specifically involved in the biosynthesis of an inducer of Rhizobium meliloti nodulation genes. Plant J. 4: 971–981.
McAlister, F., Jenkins, C., and Watson, J. 1998. Sequence and expression of a stem-abundant caffeic acid O-methyltransferase cDNA from perennial ryegrass (Lolium perenne). Aust. J. Plant Physiol. 25: 225–235.
Meyermans, H., Morreel, K., Lapierre, C., Pollet, B., De Bruyn, A., Busson, R., et al. 2000. Modifications in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J. Biol. Chem. 275: 36899–36909.
Morishige, T., Tsujita, T., Yamada, Y., and Sato, F. 2000. Molecular characterization of S-adenosyl-L-methionine: 3′-hydroxy-N-methylcoclaurine 4′-O-methyltransferase involved in isoquinoline alkaloid biosynthesis in Coptis japonica. J. Biol. Chem. 275: 23398–23405.
Morishige, T., Dubouzet, E., Choi, K.-B., Yazaki, K., and Sato, F. 2002. Molecular cloning of columbamine O-methyltransferase from cultured Coptis japonica cells. Eur. J. Biochem. 269: 5659–5667.
Muzac, I., Wang, J., Anzellotti, D., Zhang, H., and Ibrahim, R.K. 2000. Functional expression of an Arabidopsis cDNA clone encoding a flavonol 3′-O-methyltransferase and characterization of the gene product. Arch. Biochem. Biophys. 375: 385–388.
NDong, C., Anzellotti, D., Ibrahim, R.K., Huner, N., and Sarhan, F. 2003. Daphnetin methylation by a novel O-methyltransferase is associated with cold acclimation and photosystem II excitation pressure in rye. J. Biol. Chem. 278: 6854–6861.
Nicholas, K.B., and Nicholas, H.B. 1997. GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors. Available from http://www.nrbsc.org/downloads/.
Ohno, S. 1970. Evolution by gene duplication. Springer-Verlag, New York.
Osakabe, K., Tsao, C., Li, L., Popko, J., Umezawa, T., Carraway, D., et al. 1999. Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc. Natl. Acad. Sci. U.S.A. 96: 8955–8960.
Ounaroon, A., Decker, G., Schmidt, J., Lottspiech, F., and Kutchan, T.M. 2003. (R,S)-Reticuline 7-O-methyltransferase and (R,S)-norcoclaurine 6-O-methyltransferase of Papaver somniferum: cDNA cloning and characterization of methyl transfer enzymes of alkaloid biosynthesis in opium poppy. Plant J. 36: 808–819.
Parvathi, K., Chen, F., Guo, D., Blount, J.W., and Dixon, R.A. 2001. Substrate preferences of O-methyltransferases in alfalfa suggest new pathways for 3-O-methylation of monolignols. Plant J. 25: 193–202.
Pellegrini, L., Geoffroy, P., Fritig, B., and Legrand, M. 1993. Molecular cloning and expression of a new class of o-diphenol O-methyltransferases induced in tobacco (Nicotiana tabacum L.) leaves by infection or elicitor treatment. Plant Physiol. 103: 509–517.
Pichersky, E., and Gang, D.R. 2000. Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci. 5: 439–445.
Ross, J., Nam, K., D’Auria, J., and Pichersky, E. 1999. S-Adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch. Biochem. Biophys. 367: 9–16.
Schmitt, D., Pakusch, A.-E., and Matern, U. 1991. Molecular cloning, induction and taxonomic distribution of caffeoyl CoA 3-O-methyltransferase, an enzyme involved in disease resistance. J. Biol. Chem. 266: 17416–17423.
Schröder, G., Wehinger, E., Lukačin, R., Wellmann, F., Seefelder, W., Schwab, W., and Schröder, J. 2004. Flavonoid methylation: a novel 4′-O-methyltransferase from Catharanthus roseus, and evidence that partially methylated flavanones are substrates of four different flavonoid dioxygenases. Phytochemistry, 65: 1085–1094.
Schubert, H.L., Blumethal, R.M., and Cheng, X. 2003. Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci. 28: 329–335.
Seo, H., Song, J., Cheong, J.-J., Lee, Y.-H., Lee, Y.-W., Hwang, I., Lee, J., and Choi, Y. 2001. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc. Natl. Acad. Sci. U.S.A. 98: 4788–4793.
Swofford, D.L. 2001. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4 [computer program]. Sinauer Associates, Sunderland, Mass.
Takeshita, N., Fujiwara, H., Mimura, H., Fitchen, J., Yamada, Y., and Sato, F. 1995. Molecular cloning and characterization of S-adenosyl-L-methionine:scoulerine 9-O-methyltransferase from cultured cells of Coptis japonica. Plant Cell Physiol. 36: 29–36.
Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W — improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.
Vernon, D., and Bohnert, H. 1992. A novel methyltransferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. EMBO J. 11: 2077–2085.
Vidgren, J., Svensson, L.A., and Liljas, A. 1994. Crystal structure of catechol O-methyltransferase. Nature (London), 368: 354–358.
Wang, J., Dudareva, N., Bhakta, S., Raguso, R., and Pichersky, E. 1997. Floral scent production in Clarkia breweri (Onagraceae). II. Localization and developmental modulation of the enzyme S-adenosyl-L-methionine:(iso)eugenol O-methyltransferase and phenylpropanoid emission. Plant Physiol. 114: 213–221.
Wein, M., Lavid, N., Lunkenbein, S., Lewinsohn, E., Schwab, W., and Kaldenhoff, R. 2002. Isolation, cloning and expression of a multifunctional O-methyltransferase capable of forming 2,5-dimethyl-4-methoxy-4(2H)-furanone, one of the key aroma compounds in strawberry fruits. Plant J. 31: 755–765.
Willits, M.G., Giovanni, M., Prata, R., Kramer, C., De Luca, V., Steffens, J., and Graser, G. 2004. Biotransformation of modified flavonoids: an example of in vivo diversification of secondary metabolites. Phytochemistry, 65: 31–41.
Wink, M. 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry, 64: 3–19.
Wu, Q., Preisig, C., and VanEtten, H. 1997. Isolation of the cDNA encoding (+)6a-hydroxymaackiain 3-O-methyltransferase, the terminal step for the synthesis of the phytoalexin pisatin in Pisum sativum. Plant Mol. Biol. 35: 551–560.
Wu, S., Watanabe, N., Mita, S., Dohra, H., Ueda, Y., Shibuya, M., and Ebizuka, Y. 2004. The key role of phloroglucinol O-methyltransferase in the biosynthesis of Rosa chinensis volatile 1,3,5-trimethoxybenzene. Plant Physiol. 135: 95–102.
Yang, H., Ahn, J.-H., Ibrahim, R.K., Lee, S., and Lim, Y. 2004. The three-dimensional structure of Arabidopsis thaliana O-methyltransferase by homology-based modelling. J. Mol. Graph. Model. 23: 77–87.
Ye, Z.-H., and Varner, J. 1995. Differential expression of two O-methyltransferases in lignin biosynthesis in Zinnia elegans. Plant Physiol. 108: 459–467.
Ye, Z.-H., Kneusel, R., Matern, U., and Varner, J.E. 1994. An alternative methylation pathway in lignin biosynthesis in Zinnia. Plant Cell, 6: 1427–1439.
Yoshikuni, Y., Ferrin, T.E., and Keasling, J.D. 2006. Designed divergent evolution of enzyme function. Nature (London), 440: 1078–1082.
Zhang, X.-H., and Chinnappa, C. 1997. Molecular characterization of a cDNA encoding caffeoyl coenzyme A 3-O-methyltransferase of Stellaria longipes. J. Biosci. 22: 161–175.
Zhou, J.-M., Gold, N.D., Martin, V.J.J., Wollenweber, E., and Ibrahim, R.K. 2006. Sequential O-methylation of tricetin by a single gene product in wheat. Biochim. Biophys. Acta, 1760: 1115–1124.
Zhu, B.T., Enzell, E.L., and Liehr, J.G. 1994. Catechol O-methyltransferase-catalyzed rapid O-methylation of mutagenic flavonoids. J. Biol. Chem. 269: 292–299.
Zubieta, C., He, X.-Z., Dixon,
Repository Staff Only: item control page