Abstract
Together in silico and genetic mining approaches have recently designated the CYP98 family of plant cytochromes P450 as the family of enzymes that catalyzes the meta-hydroxylation step in the phenylpropanoid pathway. This meta-hydroxylation is not catalyzed on the free p-coumaric acid as anticipated, but on its conjugates with shikimic, quinic, or phenyllactic acids. While all CYP98s have in common phenol meta-hydroxylase activity, p-coumaroylshikimate remains their preferred substrate. High expression of CYP98s is detected in lignifying tissues in stems, roots, and siliques. The CYP98A3 gene disruption in Arabidopsis thaliana leads to a drastic inhibition of lignin synthesis, cell growth, and plant development. The meta-hydroxylation of phenolic precursors is thus essential for higher plant development.
Isolation of coding sequences belonging to the CYP98 family from basil, wheat, and extensive functional analysis of the recombinant enzymes, together with CYP98s from other plant taxa, helps shedding some light on mechanisms of P450s evolution. Most importantly, the occurrence of the meta-hydroxylation on esters of shikimic or quinic acids introduces a new biochemical regulation mechanism in the phenylpropanoid pathway.
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Abdulrazzak N, Pollet B, Ehlting J, Larsen K, Asnaghi C, Ronseau S, Proux C, Erhardt M, Selteer V, Renou JP, Ullmann P, Pauly M, Lapierre C, Werck-Reichhart D (2006) A coumaroyl-ester-3-hydroxylase Insertion Mutant Reveals the Existence of Nonredundant meta Hydroxylation Pathways and Essential Roles for Phenolic Precursors in Cell Expansion and Plant Growth. Plant Physiol 140:30–48
Bartlett DJ, Poulton JE, Butt VS (1972) Hydroxylation of p-coumaric acid by illuminated chloroplasts from spinach beet leaves. FEBS Lett 23:265–267
Boniwell JM, Butt VS (1986) Flavin nucleotide-dependent 3-hydroxylation of 4-hydroxyphenylpropanoid carboxylic acids by particulate preparations from potato tubers. Z Naturforsch 41c:56–60
Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C (2002a) Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J 30:47–59.
Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, Cusumano JC, Chapple C (2002b) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J 30:33–45
Gang DR, Beuerle T, Ullmann P, Werck-Reichhart D, Pichersky E (2002) Differential production of meta hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiol 130:1536–1544
Heller W, Kühnl T (1985) Elicitor induction of a microsomal 5-O-(4-coumaroyl)shikimate 3′-hydroxylase in parsley cell suspension cultures. Arch Biochem Biophys 241:453–460
Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M (2004) Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16:1446–1465
Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M (2003) Purification, cloning and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278:95–103
Kamsteeg J, Van Brederode J, Verschuren PM, Van Nigtevecht G (1981) Identification, properties and genetic control of p-coumaroyl-Coenzyme A, 3-hydroxylase isolated from petals of Silene dioica. Z Planzenphysiol 102:435–442
Kneusel RE, Matern U, Nicolay K (1989) Formation of trans-caffeoyl-CoA from trans-4-coumaroyl-CoA by Zn2+-dependent enzymes in cultured plant cells and its activation by an elicitor-induced pH shift. Arch Biochem Biophys 269:455–462
Kojima M, Takeuchi W (1989) Detection and characterization of p-coumaric acid hydroxylase in mung bean, Vigna mungo, seedlings. J Biochem 105:265–270
Kühnl T, Koch U, Heller W, Wellmann E (1987) Chlorogenic acid biosynthesis: characterization of a light-induced microsomal 5-O-(4-coumaroyl)-d-quinate/shikimate 3′-hydroxylase from carrot (Daucus carota L.) cell suspension cultures. Arch Biochem Biophys 258:226–232
Lotfy S, Fleuriet A, Macheix JJ (1994) Hydroxycinnamoyl-CoA: transferases in higher plants. II. Chracterization in Cichorium endivia and Raphanus sativus and comparison with other plants. Plant Physiol Biochem 32:355–363
Matsuno M, Nagatsu A, Ogihara Y, Ellis BE, Mizukami H (2002) CYP98A6 from Lithospermum erythrorhizon encodes 4-coumaroyl-4′-hydroxyphenyllactic acid 3-hydroxylase involved in rosmarinic acid biosynthesis. FEBS Lett 514:219–224
Morant M, Hehn A, Werck-Reichhart D (2002) Conservation and diversity of gene families explored using the CODEHOP strategy in higher plants. BMC Plant Biol 2:7
Morant M, Schoch GA, Ullmann P, Ertunç T, Little D, Olsen CA, Petersen M, Negrel J, Werck-Reichhart D (2006) Catalytic activity, duplication and evolution of the CYP98 cytochrome P450 family in wheat. Plant Mol Biol In press
Nair RB, Xia Q, Kartha CJ, Kurylo E, Hirji RN, Datla R, Selvaraj G (2002) Arabidopsis CYP98A3 mediating aromatic 3-hydroxylation. Developmental regulation of the gene, and expression in yeast. Plant Physiol 130:210–220
Negrel J, Javelle F (1997) Purification, characterization and partial amino acid sequencing of hydroxycinnamoyl-CoA:tyramine N-(hydroxycinnamoyl)transferase from tobacco cell-suspension cultures. Eur J Biochem 247:1127–1135
Niggeweg R, Michael AJ, Martin C. (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat Biotechnol 22:746–754
Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239:2370–2378
Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276:36566–36574
Stafford HA, Dresler S (1972) 4-Hydroxycinnamic acid hydroxylase and polyphenolase activities in Sorghum vulgare. Plant Physiol 49:590–595
Vaughan PF, Butt VS (1970) The action of O-dihydric phenols in the hydroxylation of p-coumaric acid by a phenolase from leaves of spinach beet (Beta vulgaris L.). Biochem J 119:89–94
Wang X, Li SM, Loscher R, Heide L (1997) 4-Coumaroyl coenzyme A 3-hydroxylase activity from cell cultures of Lithospermum erythrorhizon and its relationship to polyphenol oxidase. Arch Biochem Biophys 347:249–255
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Selected articles from the XXII International Conference on Polyphenols, Helsinki, Finland, organized by Prof. Kristiina Wähälä
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Schoch, G.A., Morant, M., Abdulrazzak, N. et al. The meta-hydroxylation step in the phenylpropanoid pathway: a new level of complexity in the pathway and its regulation. Environ Chem Lett 4, 127–136 (2006). https://doi.org/10.1007/s10311-006-0062-1
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DOI: https://doi.org/10.1007/s10311-006-0062-1