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Fatty acid ω-hydroxylases from Solanum tuberosum

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Potato StCYP86A33 complements the Arabidopsis AtCYP86A1 mutant, horst - 1.

Abstract

Suberin is a cell-wall polymer that comprises both phenolic and aliphatic components found in specialized plant cells. Aliphatic suberin is characterized by bi-functional fatty acids, typically ω-hydroxy fatty acids and α,ω-dioic acids, which are linked via glycerol to form a three-dimensional polymer network. In potato (Solanum tuberosum L.), over 65 % of aliphatics are either ω-hydroxy fatty acids or α,ω-dioic acids. Since the biosynthesis of α,ω-dioic acids proceeds sequentially through ω-hydroxy fatty acids, the formation of ω-hydroxy fatty acids represents a significant metabolic commitment during suberin deposition. Four different plant cytochrome P450 subfamilies catalyze ω-hydroxylation, namely, 86A, 86B, 94A, and 704B; though to date, only a few members have been functionally characterized. In potato, CYP86A33 has been identified and implicated in suberin biosynthesis through reverse genetics (RNAi); however, attempts to express the CYP86A33 protein and characterize its catalytic function have been unsuccessful. Herein, we describe eight fatty acid ω-hydroxylase genes (three CYP86As, one CYP86B, three CYP94As, and a CYP704B) from potato and demonstrate their tissue expression. We also complement the Arabidopsis cyp86A1 mutant horst-1 using StCYP86A33 under the control of the Arabidopsis AtCYP86A1 promoter. Furthermore, we provide preliminary analysis of the StCYP86A33 promoter using a hairy root transformation system to monitor pStCYP86A33::GUS expression constructs. These data confirm the functional role of StCYP86A33 as a fatty acid ω-hydroxylase, and demonstrate the utility of hairy roots in the study of root-specific genes.

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References

  • Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Benveniste I, Bronner R, Wang Y, Compagnon V, Michler P, Schreiber L, Salaün JP, Durst F, Pinot F (2005) CYP94A1, a plant cytochrome P450-catalyzing fatty acid omega-hydroxylase, is selectively induced by chemical stress in Vicia sativa seedlings. Planta 221:881–890

    Article  CAS  PubMed  Google Scholar 

  • Bernards MA (2002) Demystifying suberin. Can J Bot 80:227–240

    Article  CAS  Google Scholar 

  • Bernards MA, Lopez ML, Jajicek J, Lewis NG (1995) Hydroxycinnamic acid polymers constitute the polyaromatic domain of suberin. J Biol Chem 270:7382–7386

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Campagnon 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

    Article  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean BB, Kolattukudy PE (1976) Synthesis of suberin during wound healing in jade leaves, tomato fruit and bean pods. Plant Physiol 58:411–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Moller LB, Preuss D (2009) CYP704B1 is a long-chain fatty acid ω-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151:574–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durst F, Nelson DR (1995) Diversity and evolution of plant P450 and P450-Reductases. Drug Metab Drug Interact 12:189–206

    CAS  Google Scholar 

  • Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New York

    Google Scholar 

  • Graça J (2015) Suberin: the biopolyester at the frontier of plants. Front Chem. doi:10.3389/fchem.2015.00062

    PubMed  PubMed Central  Google Scholar 

  • Graça J, Pereira H (2000a) Methanolysis of bark suberins: analysis of glycerol and acid monomers. Phytochem Anal 11:45–51

    Article  Google Scholar 

  • Graça J, Pereira H (2000b) Diglycerol alkendioates in suberin: building units of a poly(acylglycerol) polyester. Biomacromolecules 1:519–522

    Article  CAS  PubMed  Google Scholar 

  • Graça J, Pereira H (2000c) Suberin structure in potato periderm: glycerol, long-chain monomers, and glyceryl and feruloyl dimers. J Agric Food Chem 48:5476–5483

    Article  CAS  PubMed  Google Scholar 

  • Graça J, Santos S (2007) Suberin: a biopolyester of plants’ skin. Macromole Biosci 7:128–135

    Article  CAS  Google Scholar 

  • Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57:155–171

    Article  CAS  PubMed  Google Scholar 

  • Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Desaubry L, Grausem B, Kandel S, Miesch M, Werck-Reichhart D, Pinot F (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone jasmonyl-isoleucine for catabolic turnover. J Biol Chem 287:6296–6306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant Cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holloway PJ (1983) Some variations in the composition of suberin from the cork layers of higher plants. Phytochemistry 22:495–502

    Article  CAS  Google Scholar 

  • Kitaoka N, Matsubara T, Sato M, Takahashi K, Wakuta S, Kawaide H, Matsui H, Nabeta K, Matsuura H (2011) Arabidopsis CYP94B3 encodes jasmonyl-l-isoleucine 12-hydroxylase, a key enzyme in the oxidative catabolism of jasmonate. Plant Cell Physiol 52:1757–1765

    Article  CAS  PubMed  Google Scholar 

  • Kolattukudy PE (1980) Biopolyester membranes of plants: cutin and suberin. Science 208:990–1000

    Article  CAS  PubMed  Google Scholar 

  • Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonyl-l-isoleucine. PNAS 108:9298–9303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar GNM, Lulai EC, Suttle JC, Knowles NR (2010) Age-induced loss of wound-healing ability in potato tubers is partly regulated by ABA. Planta 232:1433–1445

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Lescot M, Dhais P, Thijs G, Marchal K, MoreauY Van, de Peer Y, Rouz P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lulai EC, Suttle JC, Pederson SM (2008) Regulatory involvement of abscisic acid in potato tuber wound-healing. J Exp Bot 59:1175–1186

    Article  CAS  PubMed  Google Scholar 

  • Makhzoum AB, Sharma P, Bernards MA, Trémouillaux-Guiller J (2011) Hairy roots: an ideal platform for transgenic plant production and other promising applications. In: Gang DR (ed) Recent advances in phytochemistry, vol 42. Springer, London, pp 95–142

    Google Scholar 

  • Meyer CJ, Peterson CA, Bernards MA (2011a) A comparison of suberin monomers from the multiseriate exodermis of Iris germanica during maturation under differing growth conditions. Planta 233:773–786

    Article  CAS  PubMed  Google Scholar 

  • Meyer CJ, Peterson CA, Bernards MA (2011b) Spatial and temporal deposition of suberin during maturation of the onion root exodermis. Botany 89:119–131

    Article  CAS  Google Scholar 

  • Ranathunge K, Schreiber L (2011) Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. J Exp Bot 62:1961–1974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    Article  PubMed  PubMed Central  Google Scholar 

  • Sprenger-Haussels M, Weisshaar B (2000) Transactivation properties of parsley proline-rich bZIP transcription factors. Plant J 22:1–8

    Article  CAS  PubMed  Google Scholar 

  • Stålberg K, Ellerstöm M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199:515–519

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas R, Fang X, Ranathunge K, Peterson CA, Bernards MA (2007) Soybean root suberin: anatomical distribution, chemical composition and relationship to partial resistance to Phytophthora sojae. Plant Physiol 144:299–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tocquin P, Corbesier L, Havelange A, Pieltain A, Kurtem E, Bernier G, Perilleux C (2003) A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol 3:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis MYB homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urban P, Mignotte C, Kazmaier M, Delorme F, Pompon D (1997) Cloning, Yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. J Biol Chem 272:19176–19186

    Article  CAS  PubMed  Google Scholar 

  • Vieweg MF, Frühling M, Quandt HJ, Heim U, Bäumlein H, Pühler A, Küster H, Andreas MP (2004) The promoter of the Vicia faba L. leghemoglobin gene vflb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and nonlegume plants. Mol Plant-Microbe Interact 17:62–69

    Article  CAS  PubMed  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 omega-hydroxylation in development. PNAS 14:9694–9699

    Article  Google Scholar 

  • Widemann E, Grausem B, Renault H, Pineau E, Heinrich C, Lugan R, Ullmann P, Miesch L, Aubert Y, Miesch M, Heitz T, Pinot F (2015) Sequential oxidation of jasmonyl–phenylalanine and jasmonyl-isoleucine by multiple cytochrome P450 of the CYP94 family through newly defined aldehyde intermediates. Phytochemistry 117:388–399

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Pan S, Cheng S et al (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–197

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a Natural Sciences and Engineering Research Council Discovery Grant to MAB.

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Authors and Affiliations

  1. Department of Biology and the Biotron, The University of Western Ontario, London, ON, N6A 5B7, Canada

    Anica Bjelica, Meghan L. Haggitt, Kathlyn N. Woolfson, Daniel P. N. Lee, Abdullah B. Makhzoum & Mark A. Bernards

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  1. Anica Bjelica
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  2. Meghan L. Haggitt
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  3. Kathlyn N. Woolfson
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  4. Daniel P. N. Lee
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  5. Abdullah B. Makhzoum
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  6. Mark A. Bernards
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Correspondence to Mark A. Bernards.

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Communicated by M. Petersen.

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Bjelica, A., Haggitt, M.L., Woolfson, K.N. et al. Fatty acid ω-hydroxylases from Solanum tuberosum . Plant Cell Rep 35, 2435–2448 (2016). https://doi.org/10.1007/s00299-016-2045-4

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  • DOI: https://doi.org/10.1007/s00299-016-2045-4

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