Cytochrome P450 metabolizing fatty acids in plants: Characterization and physiological roles

FEBS Journal

Volumn 278, Issue 2, 2011, Pages 195-205

  Pinot, Franck ^a   Beisson, Fred ^b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

catabolism; cutin; cytochrome P450; defense; epoxyacids; fatty acid; plant envelope; reproduction; sporopollenin; suberin

Indexed keywords

CYTOCHROME P450; SUBERIN;

ABIOTIC STRESS; ARABIDOPSIS; BINDING SITE; BIOSYNTHESIS; BIOTIC STRESS; CATALYSIS; DOWN REGULATION; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; ENZYME METABOLISM; FATTY ACID METABOLISM; HYDROPHOBICITY; HYDROXYLATION; LIPOGENESIS; NONHUMAN; OXIDATION; OXYGENATION; PHYLOGENY; PLANT DEFENSE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REPRODUCTION; REVIEW; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS;

CYTOCHROME P-450 ENZYME SYSTEM; FATTY ACIDS; PLANTS;

ARABIDOPSIS THALIANA;

EID: 78651088310     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07948.x     Document Type: Review

References (60)

1. Croteau R, &, Kolattukudy P, (1974) Biosynthesis of hydroxyfatty acid polymers. Enzymatic synthesis of cutin from monomer acids by cell-free preparations from the epidermis of Vicia faba leaves. Biochemistry 13, 3193-3202.
2. Soliday C, &, Kolattukudy P, (1978) Midchain hydroxylation of 16-hydroxypalmitic acid by the endoplasmic reticulum fraction from germinating Vicia faba. Arch Biochem Biophys 188, 338-347.
3. Kolattukudy P, (1981) Structure, biosynthesis and degradation of cutin and suberin. Annu Rev Plant Physiol 32, 539-567.
4. Benveniste I, Salaün J, Simon A, Reichhart D, &, Durst F, (1982) Cytochrome P450-dependent omega-hydroxylation of lauric acid by microsomes from pea seedlings. Plant Physiol 70, 122-126.
5. Salaün J, Benveniste I, Reichhart D, &, Durst F, (1981) Induction and specificity of a (cytochrome P450)-dependent laurate in-chain-hydroxylase from higher plant microsomes. Eur J Biochem 119, 651-655.
6. Salaün J, Weissbart D, Durst F, Pflieger P, &, Mioskowski C, (1989) Epoxidation of cis and trans delta-9-unsaturated lauric acids by a cytochrome P450-dependent system from higher plant microsomes. FEBS Lett 246, 120-125.
7. Schuler M, &, Werck-Reichhart D, (2003) Functional genomics of P450s. Annu Rev Plant Biol 54, 629-667.
8. Pinot F, Salaün J, Bosch H, Lesot A, Mioskowski C, &, Durst F, (1992) Omega-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.
9. Pinot F, Bosch H, Alayrac C, Mioskowski C, Vendais A, Durst F, &, Salaün J, (1993) omega-Hydroxylation of oleic acid in Vicia sativa microsomes (Inhibition by substrate analogs and inactivation by terminal acetylenes). Plant Physiol 102, 1313-1318.
10. Weissbart D, Salaün J, Durst F, Pflieger P, &, Mioskowski C, (1992) Regioselectivity of a plant lauric acid omega hydroxylase. Omega hydroxylation of cis and trans unsaturated lauric acid analogs and epoxygenation of the terminal olefin by plant cytochrome P450. Biochim Biophys Acta 1124, 135-142.
11. Kunze K, Mangold B, Wheeler C, Beilan H, &, Ortiz de Montellano P, (1983) The cytochrome P-450 active site. Regiospecificity of prosthetic heme alkylation by olefins and acetylenes. J Biol Chem 258, 4202-4207.
12. Cajacob C, &, Ortiz de Montellano P, (1986) Mechanism-based in vivo inactivation of lauric acid hydroxylases. Biochemistry 25, 4705-4711.
13. Tijet N, Helvig C, Pinot F, Le Bouquin R, Lesot A, Durst F, Salaün J, &, Benveniste I, (1998) Functional expression in yeast and characterization of a clofibrate-inducible plant cytochrome P-450 (CYP94A1) involved in cutin monomers synthesis. Biochem J 332, 583-589.
14. Benveniste I, Tijet N, Adas F, Philipps G, Salaün J, &, Durst F, (1998) CYP86A1 from Arabidopsis thaliana encodes a cytochrome P450-dependent fatty acid omega-hydroxylase. Biochem Biophys Res Commun 243, 688-693.
15. Kahn R, Le Bouquin R, Pinot F, Benveniste I, &, Durst F, (2001) A conservative amino acid substitution alters the regiospecificity of CYP94A2, a fatty acid hydroxylase from the plant Vicia sativa. Arch Biochem Biophys 391, 180-187.
16. Rupasinghe S, Duan H, &, Schuler M, (2007) Molecular definitions of fatty acid hydroxylases in Arabidopsis thaliana. Proteins 68, 279-293.
17. Pinot F, Benveniste I, Salaün J, Loreau O, NoÃl J, 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.
18. Kandel S, Sauveplane V, Compagnon V, Franke R, Millet Y, Schreiber L, Werck-Reichhart D, &, Pinot F, (2007) Characterization of a methyl jasmonate and wounding-responsive cytochrome P450 of Arabidopsis thaliana catalyzing dicarboxylic fatty acid formation in vitro. FEBS J 274, 5116-5127.
19. Kandel S, Morant M, Benveniste I, Blée 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.
20. Cabello-Hurtado F, Batard Y, Salaün J, 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.
21. Sauveplane V, Kandel S, Kastner P, Ehlting J, Compagnon V, Werck-Reichhart D, &, Pinot F, (2009) Arabidopsis thaliana CYP77A4 is the first cytochrome P450 able to catalyze the epoxidation of free fatty acids in plants. FEBS J 276, 719-735.
22. Le Bouquin R, Skrabs M, Kahn R, Benveniste I, Salaün J, 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.
23. 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 omega-hydroxylation in development. Proc Natl Acad Sci USA 98, 9694-9699.
24. Xiao F, Goodwin S, Xiao Y, Sun Z, Baker D, Tang X, Jenks M, &, Zhou J, (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J 23, 2903-2913.
25. Höfer R, Briesen I, Beck M, Pinot F, Schreiber L, &, Franke R, (2008) The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid omega-hydroxylase involved in suberin monomer biosynthesis. J Exp Bot 59, 2347-2360.
26. Compagnon V, Diehl P, Benveniste I, Meyer D, Schaller H, Schreiber L, Franke R, &, Pinot F, (2009) CYP86B1 is required for very long chain omega-hydroxyacid and alpha, omega-dicarboxylic acid synthesis in root and seed suberin polyester. Plant Physiol 150, 1831-1843.
27. Li Y, Beisson F, Koo A, Molina I, Pollard M, &, Ohlrogge J, (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104, 18339-18344.
28. Molina I, Li-Beisson Y, Beisson F, Ohlrogge J, &, Pollard M, (2009) Identification of an Arabidopsis feruloyl-coenzyme A transferase required for suberin synthesis. Plant Physiol 151, 1317-1328.
29. Serra O, Soler M, Hohn C, Sauveplane V, Pinot F, Franke R, Schreiber L, Prat S, Molinas M, &, Figueras M, (2009) CYP86A33-targeted gene silencing in potato tuber alters suberin composition, distorts suberin lamellae, and impairs the periderm's water barrier function. Plant Physiol 149, 1050-1060.
30. Han J, Clement J, Li J, King A, Ng S, &, Jaworski J, (2010) The cytochrome P450 CYP86A22 is a fatty acyl-CoA omega-hydroxylase essential for Estolide synthesis in the stigma of Petunia hybrida. J Biol Chem 285, 3986-3996.
31. Cahoon E, Ripp K, Hall S, &, 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.
32. Kandel S, Sauveplane V, Olry A, Diss L, Benveniste I, &, Pinot F, (2006) Cytochrome P450-dependent fatty acids hydroxylases in plants. Phytochem Rev 5, 359-372.
33. Soliday C, &, Kolattukudy P, (1977) Biosynthesis of cutin omega-hydroxylation of fatty acids by a microsomal preparation from germinating Vicia faba. Plant Physiol 59, 1116-1121.
34. Li-Beisson Y, Pollard M, Sauveplane V, Pinot F, Ohlrogge J, &, Beisson F, (2009) Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc Natl Acad Sci USA 106, 22008-22013.
35. Li Y, &, Beisson F, (2009) The biosynthesis of cutin and suberin as an alternative source of enzymes for the production of bio-based chemicals and materials. Biochimie 91, 685-691.
36. Blackmore S, Wortley A, Skvarla J, &, Rowley J, (2007) Pollen wall development in flowering plants. New Phytol 174, 483-498.
37. Morant M, JÃrgensen K, Schaller H, Pinot F, MÃller B, Werck-Reichhart D, &, Bak S, (2007) CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19, 1473-1487.
38. Dobritsa A, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, MÃller B, &, Preuss D, (2009) CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151, 574-589.
39. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, et al. (2010) Cytochrome P450 family member CYP704B2 catalyzes the omega-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22, 173-190.
40. Parker D, &, Köller W, (1998) Cutinase and other lipolytic esterases protect bean leaves from infection by Rhizoctonia solani. Mol Plant Microbe Interact 11, 514-522.
41. Schweizer P, Jeanguenat A, Whitacre D, Métraux JP, &, Mösinger E, (1996) Induction of resistance in barley against Erysiphe gramini f. sp. hordei by free cutin monomers. Physiol Mol Plant Pathol 49, 103-120.
42. Schweizer P, Felix G, Buchala A, Müller C, &, Métraux JP, (1996) Perception of free cutin monomers by plant cells. Plant J 10, 331-341.
43. 2 elicitors. Plant Physiol 117, 1373-1380.
44. Pinot F, Benveniste II, Sala n JP, &, Durst F, (1998) Methyl jasmonate induces lauric acid omega-hydroxylase activity and accumulation of CYP94A1 transcripts but does not affect epoxide hydrolase activities in Vicia sativa seedlings. Plant Physiol 118, 1481-1486.
45. Palma J, Garrido M, Rodríguez-García M, &, del Río L, (1991) Peroxisome proliferation and oxidative stress mediated by activated oxygen species in plant peroxisomes. Arch Biochem Biophys 287, 68-74.
46. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, et al. (2005) Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310, 1180-1183.
47. Issemann I, &, Green S, (1990) Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature 347, 645-650.
48. Duan H, &, Schuler M, (2005) Differential expression and evolution of the Arabidopsis CYP86A subfamily. Plant Physiol 137, 1067-1081.
49. Lait C, Alborn H, Teal P, &, 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.
50. Hou C, &, Forman R, (2000) Growth inhibition of plant pathogenic fungi by hydroxy fatty acids. J Ind Microbiol Biotech 24, 275-276.
51. Stumpe M, &, Feussner I, (2006) Formation of oxylipins by CYP74 enzymes. Phytochem Rev 5, 347-357.
52. Gerhardt B, (1992) Fatty acid degradation in plants. Prog Lipid Res 31, 417-446.
53. Koiwai A, &, Matsuzaki T, (1988) Hydroxy and normal fatty acid distribution in stigmas of Nicotiana and other plants. Phytochemistry 27, 2827-2830.
54. 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.
55. Larkin J, (1994) Isolation of a cytochrome P450 homologue preferentially expressed in developing inflorescences of Zea mays. Plant Mol Biol 25, 343-353.
56. 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.
57. Nelson D, (2006) Plant cytochrome P450s from moss to poplar. Phytochem Rev 5, 193-204.
58. Rensing S, Lang D, Zimmer A, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P, Lindquist E, Kamisugi Y, et al. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69.
59. Wanders R, Komen J, &, Kemp S, (2010) Fatty acid omega-oxidation as a rescue pathway for fatty acid oxidation desorders in humans. FEBS J 278, 182-194.
60. Inge N, Van Bogaert I, Groeneboer S, Saerens K, &, Soetaert W, (2010) The role of cytochrome P450 monooxygenases in microbial fatty acid metabolism. FEBS J 278, 206-221.