Abstract
In plants, hydroxy-fatty acid production is mainly the result of enzymatic reactions catalyzed by cytochrome P450 dependent fatty acid hydroxylases. One can distinguish ω-hydroxylases that catalyze the hydroxylation of the terminal methyl of aliphatics acids (ω position) and sub-terminal or in-chain hydroxylases that oxidize carbons in the chain (ω-n position). Since both types of enzymes were discovered about three decades ago, the majority of investigations have focused on the CYP94 and CYP86 families, which mediate ω-hydroxylations. The activities of ω-hydroxylases in cutin synthesis have been clearly established, but the studies of LCR (LACERATA) and att1 (aberrant induction of type three genes), which are the first Arabidopsis thaliana mutants with alterations in coding sequences of CYP86A8 and CYP86A2, show that these types of ω-hydroxylases can be involved in many aspects of plant development. The existence of different ω-hydroxylases in plants with distinct regulation patterns suggests that these enzymes mediate diverse biological processes. Much less information concerning in-chain hydroxylases is available despite the fact that they were initially reported along with ω-hydroxylases. This lack of information might be explained by the very few examples of sub-terminal hydroxy-fatty acids described in plants. We present here the best characterized fatty acid hydroxylases and we discuss their possible roles in plant defense and development, fatty acid catabolism, plant reproduction and detoxification.
Similar content being viewed by others
References
Badami RC, Patil KB (1981) Structure and occurrence of unusual fatty acids in minor seed oils. Prog Lipid Res 19:119–153
Benveniste I, Salaün JP, Simon A, Reichhart D, Durst F (1982) Cytochrome P450 dependent ω-hydroxylation of lauric acid by microsomes from pea seedlings. Plant Physiol 70:122–126
Benveniste I, Saito T, Wang Y, Kandel S, Huang H, Pinot F, Kahn R, Salaün JP, Shimoji M (2006) Evolutionary relationship and substrate specificity of Arabidopsis thaliana fatty acid omega-hydroxylase. Plant Sci 170:326–338
Benveniste I, Tijet N, Adas F, Philipps G, Saläun JP, Durst F (1998) CYP86A1 from Arabidopsis thaliana encodes a cytochrome P450-dependent fatty acid omega-hydroxylase. Biochem Biophys Res Commun 243:688–693
Benveniste I, Bronner R, Wang Y, Compagnon V, Michler P, Schreiber L, Salaün J-P, Durst F, Pinot F (2005) CYP94A1, a plant cytochrome P450-catalyzing fatty acid w-hydroxylase, is selectively induced by chemical stress in Vicia sativa seedlings. Planta 221:881–890
Blée E (2002) Impact of phyto-oxylipins in plant defence. Trends Plant Sci 7:315–322
Blée E, Schuber F (1992) Efficient epoxidation of unsaturated fatty acids by a hydroperoxide-dependent oxygenase. J Biol Chem 265:12887–12894
Cahoon EB, Ripp KG, Hall SE, McGonigle B (2002) Transgenic production of epoxy fatty acids by expression of a cytochrome P450 enzyme from Euphorbia lagascae seed. Plant Physiol 128:615–624
Cabello-Hurtado F, Batard Y, Salaün JP, Durst F, Pinot F, Werck-Reichhart D (1998) Cloning, expression in yeast, and functional characterization of CYP81B1, a plant cytochrome P450 that catalyzes in-chain hydroxylation of fatty acids. J Biol Chem 273:7260–7267
Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381
Creelman RA, Tierney ML, Mullet JE (1992) Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci USA 89:4938–4941
Dickman MB, Ha YS, Yang Z, Adams B, Huang C (2003) A protein kinase from Colletotrichum trifolii is induced by plant cutin and is required for appressorium formation. Mol Plant Microb Interac 16:411–421
Duan H, Schuler MA (2005) Differential expression and evolution of the Arabidopsis CYP86A subfamily. Plant Physiol 137:1067–1081
Fauth M, Schweizer P, Buchala A, Markstädter C, Riederer M, Kato T, Kauss H (1998) Cutin monomers and surface wax constituents elicit H2O2 in conditioned cucumber hypocotyl segments and enhance the activity of other H2O2 elicitors. Plant Physiol 117:1373–1380
Francis SA, Dewey FM, Gurr SJ (1996) The role of cutinase in germling development and infection by Erysiphe graminis f. sp. hordei. Physiol Mol Plant Pathol 49:201–211
Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875
Gilbert RD, Johnson AM, Dean RA (1996) Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 48:335–346
Hamberg M, Gardner HW (1992) Oxylipin pathway to jasmonates: biochemistry and biological significance. Biochim Biophys Acta 1165:1–18
He SY, Jin Q (2003) The Hrp pilus: learning from flagella. Curr Opin Microbiol 6:15–19
Helvig C, Alayrac C, Mioskowski C, Koop D, Poullain D, Durst F, Salaün JP (1997) Suicide inactivation of cytochrome P450 by midchain and terminal acetylenes. A mechanistic study of inactivation of a plant lauric acid omega-hydroxylase. J Biol Chem 272:414–421
Imaishi H, Matsumoto Y, Ishitobi U, Ohkawa H (1999) Encoding of a cytochrome P450-dependent lauric acid monooxygenase by CYP703A1 specifically expressed in the floral buds of Petunia hybrida. Biosci Biotechnol Biochem 63:2082–2090
Imaishi H, Matsuo S, Swai E, Ohkawa H (2000) CYP78A1 preferentially expressed in developing inflorescences of Zea mays encoded a cytochrome P450-dependent lauric acid 12-monooxygenase. Biosci Biotechnol Biochem 64:1696–1701
Isseman I, Green S (1992) Activation of a member of the steroid hormone receptor superfamily by peroxisomes proliferators. Nature 347:645–650
Ito T, Meyerowitz EM (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in arabidopsis. Plant Cell 12:1541–1550
Johnson EF, Palmer CN, Griffin KJ, Hsu MH (1996) Role of the peroxisome proliferator-activated receptor in cytochrome P450 4A gene regulation. FASEB J 10:1241–1248
Kandel S, Morant M, Benveniste I, Blee E, Werck-Reichhart D, Pinot F (2005) Cloning, functional expression, and characterization of CYP709C1, the first sub-terminal hydroxylase of long chain fatty acid in plants. Induction by chemicals and methyl jasmonate. J Biol Chem 280:35881–35889
Kato T, Yamaguchi Y, Abe N, Uyehara T, Nakai T, Kodama M, Shiobara Y (1985) Structure and synthesis of unsaturated trihydroxy C18 fatty acids in rice plant suffering from rice blast disease. Tetrahedron Lett 26:2357–2360
Koiwai A, Matsuzaki T (1988) Hydroxy and normal fatty acid distribution in stigmas of Nicotiana and other plants. Phytochemistry 27:2827–2830
Kolattukudy PE (1981) Structure, biosynthesis and biodegradation of cutin and suberin. Annu Rev Plant Physiol 32:539–567
Kolattukudy PE, Rogers LM, Li D, Hwang CS, Flaishman MA (1995) Surface signaling in pathogenesis. Proc Natl Acad Sci USA 92:4080–4087
Kunze KL, Mangold BLH, Wheeler C, Beilan HS, Ortiz De Montellano PR (1983) The cytochrome P450 active site. Regiospecificity of prosthetic heme alkylation by olefins and acetylenes. J Biol Chem 258:4202–4207
Lait CG, Alborn HT, Teal PE, Tumlinson JH (2003) Rapid biosynthesis of N-linolenoyl-l-glutamine, an elicitor of plant volatiles, by membrane-associated enzyme(s) in Manduca sexta. Proc Natl Acad Sci USA 100:7027–7032
Larkin JC (1994) Isolation of a cytochrome P450 homologue preferentially expressed in developing inflorescence of Zea mays. Plant Mol Biol 25:343–353
Le Bouquin R, Skrabs M, Kahn R, Benveniste I, Salaün JP, Schreiber L, Durst F, Pinot F (2001) CYP94A5, a new cytochrome P450 from Nicotiana tabacum is able to catalyze the oxidation of fatty acids to the omega-alcohol and to the corresponding diacid. Eur J Biochem 268:3083–3090
Li D, Kolattukudy PE (1995) Cloning and expression of cDNA encoding a protein that binds a palindromic promoter element essential for induction of fungal cutinase by plant cutin. J Biol Chem 270:11753–11756
Masui H, Kondo T, Kojima M (1989) An antifungal coumpound, 9,12,13,-trihydroxy-(E)-10-octadecenoic acid, from Colocasia antiquorum inoculated with Ceratocystis fimbriata. Phytochemistry 28:2613–2615
Meyer A, Gross D, Vorkefeld S, Kummer M, Schmidt J, Sembdner G, Schreiber K (1989) Metabolism of the plant-growth regulator dihydrojasmonic acid in barley shoots. Phytochemistry 28:1007–1011
Noverr MC, Erb-Downward JR, Huffnagle GB (2003) Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16:517–533
Ohta H, Shida K, Peng YL, Furusawa I, Shishiyama J, Aibara S, Morita Y (1991) A lipoxygenase pathway is activated in rice after infection with the rice blast fungus Magnaporthe grisea. Plant Physiol 97:94–98
Ortiz De Montellano PR, Reich NO (1984) Specific inactivation of fatty acid hydroxylases by acetylenic fatty acids. J Biol Chem 259:4136–4141
Petkova-Andonova M, Imaishi H, Ohkawa H (2002) CYP92B1, a cytochrome P450, expressed in Petunia flower buds, that catalyzes monooxidation of long-chain fatty acids. Biosci Biotechnol Biochem 66:1819–1828
Pinot F, Alayrac C, Mioskowski C, Durst F, Salaün JP (1994) New cytochrome P450-dependent reactions from wheat: terminal and sub-terminal hydroxylation of oleic acid by microsomes from naphthalic acid anhydride and phenobarbital induced wheat seedlings. Biochem Biophys Res Commun 198:795–803
Pinot F, Benveniste I, Salaün JP, Durst F (1998) Methyl jasmonate induces lauric acid ω-hydroxylase activity and accumulation of CYP94A1 transcripts but does not affect epoxide hydrolase activities in Vicia sativa seedling. Plant Physiol 118:1481–1486
Pinot F, Benveniste I, Salaün JP, Loreau O, Noël JP, Schreiber L, Durst F (1999) Production in vitro by the cytochrome P450 CYP94A1 of major C18 cutin monomers and potential messengers in plant–pathogen interactions. Enantioselectivity studies. Biochem J 342:27–32
Pinot F, Bosch H, Alayrac C, Mioskowski C, Vendais A, Durst F, Salaün JP (1993) ω-Hydroxylation of oleic acid in Vicia sativa microsomes. Inhibition by substrate analogs and inactivation by terminal acetylenes. Plant Physiol 102:1313–1318
Pinot F, Bosch H, Salaün JP, Durst F, Mioskowski C, Hammock BD (1997) Epoxide hydrolase activities in the microsomes and the soluble fraction from Vicia sativa seedlings. Plant Physiol Biochem 35:103–110
Pinot F, Salaün JP, Bosch H, Lesot A, Mioskowski C, Durst F (1992) ω-hydroxylation of Z9-octadecenoic, Z9,10-epoxystearic and 9,10-dihydroxystearic acids by microsomal cytochrome P450 systems from Vicia sativa. Biochem Biophys Res Commun 184:183–193
Podila GK, Dickman MB, Kolattukudy PE (1988) Transcriptional activation of a cutinase gene in isolated fungal nuclei by plant monomers. Science 242:922–925
Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plants P450s in optimized redox environment. Meth Enzymol 272:51–64
Salaün JP, Benveniste I, Reichhart D, Durst F (1978) A microsomal (cytochrome P-450) linked lauric-acid-monooxygenase from aged Jerusalem-artichoke-tuber tissues. Eur J Biochem 90:155–159
Salaün J-P, Benveniste I, Reichhart D, Durst F (1981) Induction and specificity of a cytochrome P450 dependent lauric acid in-chain hydroxylase from higher plant microsomes. Eur J Biochem 119:651–655
Salaün JP, Benveniste I, Fonne R, Gabriac B, Reichhart D, Simon A, Durst F (1982) Hydroxylations microsomales de l’acide laurique catalysées par le cytochrome P450 chez les plantes supérieures. Physiologie Végétale 20:613–621
Salaün JP, Simon A, Durst F (1986) Specific induction of lauric acid ω-hydroxylase by clofibrate, diethylhexyl-phtalate and 2,4-dichlorophenoxyacetic acid in higher plants. Lipids 21:776–779
Scheller U, Zimmer T, Kärgel E, Schunck WH (1996) Characterization of the n-alkane and fatty acid hydroxylating cytochrome P450 forms 52A3 and 52A4. Arch Biochem Biophys 328:245–254
Scheller U, Zimmer T, Becher D, Schauer F, Schunck WH (1998) Oxygenation cascade in conversion of n-alkanes to α,ω-dioic acids catalyzed by cytochrome P450 52A3. J Biol Chem 273:32528–32534
Schweizer P, Felix G, Buchala A, Müller C, Métraux JP (1996a) Perception of free cutin monomers by plant cells. Plant J 10:331–341
Schweizer P, Jeanguenat A, Whitacre D, Métraux JP, Mösinger E (1996b) Induction of resistance in barley against Erysiphe graminis f. sp. Hordei by free cutin monomers. Physiol Mol Plant Pathol 49:103–120
Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, Metraux JP, Nawrath C (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12:721–738
Simpson AECM (1997) The cytochrome P450 4 (CYP4) family. Gen Pharmacol 28:351–359
Soliday CL, Kolattukudy PE (1977) Biosynthesis of cutin. W-hydroxylation of fatty acids by a microsomal preparation from germinating Vicia faba. Plant Physiol 59:1116–1121
Soliday CL, Kolattukudy PE (1978) Midchain hydroxylation of 16-hydroxypalmitic acid by the endoplasmic reticulum fraction from germinating Vicia faba. Arch Biochem Biophys 188:338–347
Spector AA, Fang X, Snyder GD, Weintraub NL (2004) Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog Lipid Res 43:55–90
Summerer S, Hanano A, Utsumi S, Arand M, Schuber F, Blée E (2002) Stereochemical features of the hydrolysis of 9,10-epoxystearic acid catalysed by plant and mammalian epoxide hydrolases. Biochem J 366:471–480
Theodoulou FL, Clark IL, Pallett KE, Hallahan DL (1999) Nucleotide sequence of Cla 30 (Accession No. Y17386), a xenobiotic-inducible member of the GST superfamily from Triticum aestivum L. Plant Physiol 119:1567
Tijet N, Helvig C, Pinot F, Le Bouquin R, Lesot A, Durst F, Salaün JP, Benveniste I (1998) Functional expression in yeast and characterization of a clofibrate-inducible plant cytochrome P450 (CYP94A1) involved in cutin monomers synthesis. Biochem J 332:583–589
Watson CJ, Froehlich JE, Josefsson CA, Chapple C, Durst F, Benveniste I, Coolbaugh RC (2001) Localization of CYP86B1 in the outer envelope of chloroplasts. Plant Cell Physiol 42:873–878
Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, Wisman E, Steiner-Lange S, Saedler H, Yephremov A (2001) Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid w-hydroxylation in development. Proc Natl Acad Sci USA 98:9694–9699
Wolf G (1996) Adipocyte differentiation is regulated by a prostaglandin liganted to the nuclear peroxisome proliferator-activated receptor. Nutr Rev 54:290–292
Woloshuk CP, Kolattukudy PE (1986) Mechanism by which contact with plant cuticle triggers cutinase gene expression in the spores of Fusarium solani f. sp. pisi. Proc Natl Acad Sci USA 83:1704–1708
Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J 23:2903–2913
Zimmerlin A, Durst F (1992) Aryl hydroxylation of the herbicide diclofop by a wheat cytochrome P-450 monooxygenase: substrate specificity and physiological activity. Plant Physiol 100:847–881
Acknowledgments
Kandel S. is grateful to the French Ministry of Research for supporting her PhD thesis.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kandel, S., Sauveplane, V., Olry, A. et al. Cytochrome P450-dependent fatty acid hydroxylases in plants. Phytochem Rev 5, 359–372 (2006). https://doi.org/10.1007/s11101-006-9041-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-006-9041-1