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CYP94A1, a plant cytochrome P450-catalyzing fatty acid ω-hydroxylase, is selectively induced by chemical stress in Vicia sativa seedlings

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Abstract

CYP94A1 is a cytochrome P450 (P450) catalyzing fatty acid (FA) ω-hydroxylation in Vicia sativa seedlings. To study the physiological role of this FA monooxygenase, we report here on its regulation at the transcriptional level (Northern blot). Transcripts of CYP94A1, as those of two other P450-dependent FA hydroxylases (CYP94A2 and CYP94A3) from V. sativa, are barely detectable during the early development of the seedlings. CYP94A1 transcripts, in contrast to those of the two other isoforms, are rapidly (less than 20 min) and strongly (more than 100 times) enhanced after treatment by clofibrate, an hypolipidemic drug in animals and an antiauxin (p-chlorophenoxyisobutyric acid) in plants, by auxins (2,4-dichlorophenoxyacetic acid and indole-3-acetic acid), by an inactive auxin analog (2,3-dichlorophenoxyacetic acid), and also by salicylic acid. All these compounds activate CYP94A1 transcription only at high concentrations (50–500 μM range). In parallel, these high levels of clofibrate and auxins modify seedling growth and development. Therefore, the expression of CYP94A1 under these conditions and the concomitant morphological and cytological modifications would suggest the implication of this P450 in a process of plant defense against chemical injury.

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Abbreviations

2,3-D:

2,3-Dichlorophenoxyacetic acid

2,4-D:

2,4-Dichlorophenoxyacetic acid

FA:

Fatty acid

GST:

Glutathione-S-transferase

IAA:

Indole-3-acetic acid

P450:

Cytochrome P450

PCIB:

p-Chlorophenoxyisobutyric acid

PMSF:

Phenylmethane sulfonylfluoride

References

  • Benveniste I, Tijet N, Adas F, Philipps G, Salaün J-P, Durst F (1998) CYP86A1 from Arabidopsis thaliana encodes a cytochrome P450-dependent fatty acid ω-hydroxylase. Biochem Biophys Res Commun 243:688–693

    Article  CAS  PubMed  Google Scholar 

  • Berger J, Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409–435

    Article  CAS  PubMed  Google Scholar 

  • Capdevila JH, Harris RC, Falck JR (2002) Microsomal cytochrome P450 and eicosanoid metabolism. Cell Mol Life Sci 59:780–789

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Singh KB (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J 19:667–677

    Article  CAS  PubMed  Google Scholar 

  • Cowart LA, Wei S, Hsu M-H, Johnson EF, Krishna MU, Falck JR, Capdevila JH (2002) The CYP4A isoforms hydroxylate epoxyeicosatrienoic acids to form high affinity peroxisome proliferator-activated receptor ligands. J Biol Chem 277:35105–35112

    Article  CAS  PubMed  Google Scholar 

  • Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J 23:431–440

    Article  CAS  PubMed  Google Scholar 

  • Ellis JG, Tokuhisa JG, Llewellyn DJ, Bouchez D, Singh K, Dennis ES, Peacock WJ (1993) Does the ocs-element occur as a functional component of the promoters of plant genes? Plant J 4:433–443

    Article  CAS  PubMed  Google Scholar 

  • Gibson GG (1989) Comparative aspects of the mammalian cytochrome P450 IV gene family. Xenobiotica 19:1123–1148

    CAS  PubMed  Google Scholar 

  • Goodall GJ, Wiebauer K, Filipowicz W (1990) Analysis of pre-mRNA processing in transfected plant protoplasts. Methods Enzymol 881:148–161

    Google Scholar 

  • Harper JF, Binder BM, Sussman MR (1993) Calcium and lipid regulation of an Arabidopsis protein kinase expressed in Escherichia coli. Biochemistry 32:3282–3290

    Article  CAS  PubMed  Google Scholar 

  • Helvig C, Dishman E, Capdevila JH (1998) Molecular, enzymatic, and regulatory characterization of rat kidney cytochromes P450 4A2 and 4A3. Biochemistry 37:12546–12558

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison Y (1977) The pollen-stigma interaction: pollen tube penetration in crocus. Ann Bot 41:913–922

    Google Scholar 

  • Holloway PJ (1982) The chemical constitution of plant cutins. In: Cutler DF, Alvin KL, Price CE (eds) The plant cuticle, linnean society symposium, vol 10. Academic, London, pp 45–88

  • Kirsch C, Takamiya-Wik M, Reinhold S, Hahlbrock K, Somssich IE (1997) Rapid, transient, and highly localized induction of plastidial omega-3 fatty acid desaturase mRNA at fungal infection sites in Petroselinum crispum. Proc Natl Acad Sci USA 94:2079–2084

    Article  CAS  PubMed  Google Scholar 

  • Kolattukudy PE (1980) Cutin, suberin, and waxes. In: Stumpf PK (ed) Biochemistry of plants, a comprehensive treatise. Lipids: structure and function, vol 4. Academic, New York, pp 571–646

  • Le Bouquin R, Pinot F, Benveniste I, Salaün J-P, Durst F (1999) Cloning and functional characterization of CYP94A2, a medium chain fatty acid hydroxylase from Vicia sativa. Biochem Biophys Res Commun 261:156–162

    Article  CAS  PubMed  Google Scholar 

  • Le Bouquin R, Skrabs M, Kahn R, Benveniste I, Salaün J-P, 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 ω-alcohol and to the corresponding diacid. Eur J Biochem 268:3083–3090

    Article  CAS  PubMed  Google Scholar 

  • Okita RT, Okita JR (2001) Cytochrome P450 4A fatty acid omega hydroxylases. Curr Drug Metab 2:265–281

    Article  CAS  PubMed  Google Scholar 

  • Paul RU, Holk A, Scherer GFE (1998) Fatty acids and lysophospholipids as potential second messengers in auxin action. Rapid activation of phospholipase A2 activity by auxin in suspension-cultured parsley and soybean cells. Plant J 16:601–611

    CAS  Google Scholar 

  • Pinot F, Benveniste I, Salaün J-P, Durst F (1998) Methyljasmonate induces lauric acid ω-hydroxylase activity and accumulation of CYP94A1 transcripts but does not affect epoxide hydrolase activities in Vicia sativa seedlings. Plant Physiol 118:1481–1486

    Article  CAS  PubMed  Google Scholar 

  • Pinot F, Benveniste I, Salaün J-P, Loreau O, Noël J-P, 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

    Article  CAS  PubMed  Google Scholar 

  • Pinot F, Skrabs M, Compagnon V, Salaün J-P, Benveniste I, Schreiber L, Durst F (2000) ω-Hydroxylation of epoxy- and hydroxy-fatty acids by CYP94A1: possible involvement in plant defence. Biochem Soc Trans 28:867–870

    CAS  PubMed  Google Scholar 

  • Scheller U, Zimmer T, Kärgel E, Schunck W-H (1996) Characterization of the n-alkane and fatty acid hydroxylating cytochrome P450 forms 52A3 and 52A4. Arch Biochem Biophys 328:245–254

    CAS  PubMed  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 337:1267–1280

    Article  Google Scholar 

  • Schweizer P, Felix G, Buchala A, Müller C, Métraux JP (1996a) Perception of free cutin monomers by plant cells. Plant J 10:331–341

    Article  CAS  Google Scholar 

  • Schweizer P, Jeanguenat A, Whitacre D, Métraux JP, Mösinger E (1996b) Induction of resistance in barley against Erysiphe gramini f. sp. Hordei by free cutin monomers. Physiol Mol Plant Pathol 49:569–589

    Article  Google Scholar 

  • Shah J, Klessig DF (1999) Salicylic acid: signal perception and transduction. In: Hooykaas PJJ, Hall MA, Libbenga KR (eds) New comprehensive biochemistry. Biochemistry and molecular biology of plant hormones, vol 33. Elsevier, Amsterdam, pp 513–541

  • Simpson AECM (1997) The cytochrome P450 4 (CYP4) family. Gen Pharmacol 28:351–359

    CAS  PubMed  Google Scholar 

  • Tijet N, Helvig C, Pinot F, Le Bouquin R, Lesot A, Durst F, Salaün J-P, 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

    CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle T (1994) The ocs element in the soybean GH2/4 promoter is activated by both active and inactive auxin and salicylic acid analogues. Plant Mol Biol 26:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Ohmiya A, Hagen G, Guilfoyle T (1995) The soybean GH2/4 gene that encodes a glutathione S-transferase has a promoter that is activated by a wide range of chemical agents. Plant Physiol 108:919–927

    Article  CAS  PubMed  Google Scholar 

  • Van der Hoeven PCJ, Siderius M, Korthout HAAJ, Drabkin AV, De Boer SH (1996) Calcium and free fatty acid-modulated protein kinase as putative effector of the fusicoccin 14–3-3 receptor. Plant Physiol 111:857–865

    Article  CAS  PubMed  Google Scholar 

  • Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum, L.) Anal Biochem 223:7–12

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Chin C-K, Gianfagna T (2000) Relationship between cutin monomers and tomato resistance to powdery mildew infection. Physiol Mol Plant Pathol 57:55–61

    Article  CAS  Google Scholar 

  • 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 ω-hydroxylation in development. Proc Natl Acad Sci USA 98:9694–9699

    Article  CAS  PubMed  Google Scholar 

  • Yi H, Park D, Lee Y (1996) In vivo evidence for the involvement of phospholipase A and protein kinase in the signal transduction pathway for auxin-induced corn coleoptile elongation. Plant Physiol 96:359–368

    Article  CAS  Google Scholar 

  • Zeier J, Goll A, Yokoyama M, Karahara I, Schreiber L (1999) Structure and chemical composition of endodermal and rhizodermal/hypodermal walls of several species. Plant Cell Environ 22:271–279

    Article  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge Ms. Marie-France Poulet for skilful technical assistance and Dr. Dawn Little for critical reading of the manuscript. We thank gratefully Dr. Bernard Grausem for effective computer assistance. We thank also Dr. Christiane Garaud (CNRS-IBMP-Strasbourg) for offering the opportunity for transmission electron microscopic investigations. We are indebted to Professor Félix Mauch (University of Fribourg, Switzerland) for the generous gift of an Arabidopsis GST6 cDNA clone. Financial support by the Centre National de la Recherche Scientifique is gratefully acknowledged.

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Author notes

  1. Yong Wang

    Present address: Institut d’Ecologie-Biologie et Physiologie Végétales, Université de Lausanne, CH, 1015, Lausanne, Switzerland

  2. Lukas Schreiber

    Present address: Botanisches Institut und Botanischer Garten, Kirschallee 1, 53115, Bonn, Germany

  3. Jean-Pierre Salaün

    Present address: Biochimie et Biologie Moléculaire-Faculté de Médecine-CS, 93837-29238, Brest Cedex3, France

Authors and Affiliations

  1. CNRS - Institut de Biologie Molèculaire des Plantes - UPR2357 - Département ≪Réponses métaboliques à l’environnement biotique≫, Université Louis-Pasteur, 28 Rue Goethe, 67083, Strasbourg Cedex, France

    Irène Benveniste, Roberte Bronner, Yong Wang, Vincent Compagnon, Pierre Michler, Lukas Schreiber, Jean-Pierre Salaün, Francis Durst & Franck Pinot

  2. IBMP-Institut de Botanique, 28 Rue Goethe, 67083, Strasbourg Cedex, France

    Irène Benveniste

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  1. Irène Benveniste
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  2. Roberte Bronner
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Correspondence to Irène Benveniste.

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Benveniste, I., Bronner, R., Wang, Y. et al. CYP94A1, a plant cytochrome P450-catalyzing fatty acid ω-hydroxylase, is selectively induced by chemical stress in Vicia sativa seedlings. Planta 221, 881–890 (2005). https://doi.org/10.1007/s00425-005-1503-y

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