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Cytochrome P450 Genes from the Sacred Lotus Genome

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Abstract

Cytochrome P450 monooxygenases (P450s) in the sacred lotus (Nelumbo nucifera) genome have been identified and named according to systematic P450 nomenclatures. Comparisons of these sequences with those in the papaya and grape CYPomes have indicated that gene blooms exist in the CYP89, CYP94, CYP96 and CYP714 families and that less dramatic expansions exist in the CYP71 and CYP72 families. Expansions in the CYP94 and CYP96 families may be associated with generation of the extremely hydrophobic leaf surfaces associated with the “lotus effect” in this water-adapted species, since these families are known to hydroxylate fatty acids and alkanes in the wax biosynthetic pathways of other plant species. Evolution of the CYP719 and CYP80 families may be associated with production of a number of benzylisoquinoline and aporphine alkaloids. Structures for anonaine and roemerine, two of the most abundant aporphine alkaloids in lotus leaves and seeds, contain methylenedioxy bridges that are known to be generated by members of the CYP719 family. With only one CYP719A22 gene existing in the lotus genome, it is likely that it is involved in making aporphine alkaloids. The fact that CYP719 has not previously been seen in angiosperm phylogeny below the order of Ranunculales suggests that its presence in lotus (in the Proteales) presents an evolutionary terminus prior to its loss in more recent eudicot species. With several CYP80 family genes existing in the lotus genome, there are multiple candidates for those involved in conducting benzylisoquinoline alkaloid synthesis.

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References

  • Angiosperm Phylogeny Group (2009) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121. doi:10.1111/j.1095-8339.2009.00996.x

    Article  Google Scholar 

  • Apuya NR, Park JH, Zhang L, Ahyow M, Davidow P, Van Fleet J, Rarang JC, Hippley M, Johnson TW, Yoo HD, Trieu A, Krueger S, Wu CY, Lu YP, Flavell RB, Bobzin SC (2008) Enhancement of alkaloid production in opium and California poppy by transactivation using heterologous regulatory factors. Plant Biotechnol J 6:160–175

    Article  PubMed  CAS  Google Scholar 

  • Bak S, Beisson F, Bishop G, Hamberger B, Hofer R, Paquette S, Werck-Reichhart D (2011) Cytochromes P450. Arabidopsis Book 9:e0144

    Article  PubMed  Google Scholar 

  • 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 omega-hydroxylase. Biochem Biophys Res Commun 243:688–693

    Article  PubMed  CAS  Google Scholar 

  • CoGepedia Sequenced plant genomes http://genomevolution.org/wiki/index.php/Sequenced_plant_genomes#Columbine

  • Cole TCH, Hilger HH (2010) Flowering plant systematics. www2.biologie.fu-berlin.de/sysbot/poster/poster1.pdf

  • Collu G, Unver N, Peltenburg-Looman AMG, van der Heijden R, Verpoorte R, Memelink J (2001) Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett 508:215–220

    Article  PubMed  CAS  Google Scholar 

  • Diaz Chavez ML, Rolf M, Gesell A, Kutchan TM (2011) Characterization of two methylenedioxy bridge-forming cytochrome P450-dependent enzymes of alkaloid formation in the Mexican prickly poppy Argemone mexicana. Arch Biochem Biophys 507:186–193

    Article  PubMed  CAS  Google Scholar 

  • Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Møller BL, 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  PubMed  CAS  Google Scholar 

  • Ensikat HJ, Ditsche-Kuru P, Neinhuis C, Barthlott W, Beilstein J (2011) Superhydrophobicity in perfection: the outstanding properties of the lotus leaf. Nanotechnol 2:152–161

    CAS  Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L, Jetter R (2007) The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol 145:653–667

    Article  PubMed  CAS  Google Scholar 

  • Heitz T, Widemann E, Lugan R, Miesch L, Ullman P, Desaubry L, Holder E, Grausem B, Kandel S, Miesch M, Werck-Reichhart PF (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  PubMed  CAS  Google Scholar 

  • Ikezawa N, Iwasa K, Sato F (2007) Molecular cloning and characterization of methylenedioxy bridge-forming enzymes involved in stylopine biosynthesis in Eschscholzia californica. FEBS J 274:1019–1035

    Article  PubMed  CAS  Google Scholar 

  • Ikezawa N, Iwasa K, Sato F (2008) Molecular cloning and characterization of CYP80G2, a cytochrome P450 that catalyzes an intramolecular C-C phenol coupling of (S)-reticuline in magnoflorine biosynthesis, from cultured Coptis japonica cells. J Biol Chem 283:8810–8821

    Article  PubMed  CAS  Google Scholar 

  • Ikezawa N, Iwasa K, Sato F (2009) CYP719A subfamily of cytochrome P450 oxygenases and isoquinoline alkaloid biosynthesis in Eschscholzia californica. Plant Cell Rep 28:123–133

    Article  PubMed  CAS  Google Scholar 

  • Itoh A, Saitoh T, Tani K, Uchigaki M, Sugimoto Y, Yamada J, Nakajima H, Ohshiro H, Sun S, Tanahashi T (2011) Bisbenzylisoquinoline alkaloids from Nelumbo nucifera. Chem Pharm Bull (Tokyo) 59:947–951

    Article  CAS  Google Scholar 

  • Jaillon O et al (2007) French-Italian public consortium for grapevine genome characterization. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y et al (2012) A genome triplication associated with early diversification of the core eudicots. Genome Biol 13(1):R3

    Article  PubMed  Google Scholar 

  • Kandel S, Sauveplane V, Olry A, Diss L, Benveniste I, Pinot F (2006) Cytochrome P450-dependent fatty acid hydroxylases in plants. Phytochem Rev 5:359–372

    Article  CAS  Google Scholar 

  • Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc Natl Acad Sci USA 108:9298–9303

    Article  PubMed  CAS  Google Scholar 

  • Kraus PF, Kutchan TM (1995) Molecular cloning and heterologous expression of a cDNA encoding berbamunine synthase, a C–O phenol-coupling cytochrome P450 from the higher plant Berberis stolonifera. Proc Natl Acad Sci USA 92:2071–2075

    Article  PubMed  CAS  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 

  • Li R, Reed DW, Liu E, Nowak J, Pelcher LE, Page JE, Covello PS (2006) Functional genomic analysis of alkaloid biosynthesis in Hyoscyamus niger reveals a cytochrome P450 involved in littorine rearrangement. Chem Biol 13:513–520

    Article  PubMed  CAS  Google Scholar 

  • Luo X, Chen B, Liu J, Yao S (2005) Simultaneous analysis of n-nornuciferine, o- nornuciferine, nuciferine, and roemerine in leaves of Nelumbo nucifera Gaertner by high-performance liquid chromatography-photodiode array detection-electrospray mass spectrometry. Anal Chim Acta 538:129–133

    Article  CAS  Google Scholar 

  • Magome H, Nomura T, Hanada A, Takeda-Kamiya N, Ohnishi T, Shinma Y, Katsumata T, Kawaide H, Kamiya Y, Yamaguchi S (2013) CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proc Natl Acad Sci USA 110:1947–1952

    Article  PubMed  CAS  Google Scholar 

  • Ming R et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996

    Article  PubMed  CAS  Google Scholar 

  • Ming R et al (2013) The genome of the long-living Sacred lotus (Nelumbo nucifera, Gaertner). Genome Biology in press

  • Mizutani M, Ohta D (2010) Diversification of P450 genes during land plant evolution. Ann Rev Plant Biol 61:291–315

    Article  CAS  Google Scholar 

  • Mukherjee PK, Mukherjee D, Maji AK, Rai S, Heinrich M (2009) The sacred lotus (Nelumbo nucifera)-phytochemical and therapeutic profile. J Pharm Pharmacol 61:407–422

    PubMed  CAS  Google Scholar 

  • Nelson DR (2006) Plant cytochrome P450s from moss to poplar. Phytochem Rev 5:193–204. doi:10.1007/s11101-006-9015-3

    Article  CAS  Google Scholar 

  • Nelson DR (2009) The cytochrome P450 homepage. Human Genomics 4:59–65

    PubMed  CAS  Google Scholar 

  • Nelson DR, Werck-Reichhart D (2011) A P450 centric view of plant evolution. Plant J 66:194–211

    Article  PubMed  CAS  Google Scholar 

  • Nelson DR, Ming R, Alam M, Schuler MA (2008) Comparison of cytochrome P450 genes from six plant genomes. Tropical Plant Biology 1:216–235

    Article  CAS  Google Scholar 

  • Nishimura K, Horii S, Tanahashi T, Sugimoto Y, Yamada J (2013) Synthesis and pharmacological activity of alkaloids from embryo of lotus, Nelumbo nucifera. Chem Pharm Bull (Tokyo) 61:59–68

    Article  CAS  Google Scholar 

  • Pinot F, Beisson F (2011) Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles. FEBS J 278:195–205

    Article  PubMed  CAS  Google Scholar 

  • Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. doi:10.1038/nature10158

    Article  Google Scholar 

  • Schuler MA, Duan H, Bilgin M, Ali S (2006) Arabidopsis P450s through the looking glass: a window on plant biochemistry. Phytochem Rev 5:205–237

    Article  CAS  Google Scholar 

  • Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404

    Article  PubMed  CAS  Google Scholar 

  • Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18:1944–1954

    Article  PubMed  CAS  Google Scholar 

  • Tijet N, Helvig C, Pinot F, LeBouquin R, Lesot A, Durst F, Salaun JP, 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

    PubMed  CAS  Google Scholar 

  • Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, Ruelens P, Maere S, Van de Peer Y, Geuten K (2012) Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Mol Biol Evol 29:3793–3806

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Liu Y, Cai Y, Zhang F, Xia G, Xiang F (2010) Cloning and functional analysis of geraniol 10-hydroxylase, a cytochrome P450 from Swertia mussotii Franch. Biosci Biotechnol Biochem 74:1583–1590

    Article  PubMed  CAS  Google Scholar 

  • Waterman MR, Lepesheva GI (2005) Sterol 14 alpha-demethylase, an abundant and essential mixed function oxidase. Biochem Biophys Res Commun 338:418–422

    Article  PubMed  CAS  Google Scholar 

  • You M, Wickramaratne DB, Silva GL, Chai H, Chagwedera TE, Farnsworth NR, Cordell GA, Kinghorn AD, Pezzuto JM (1995) (−)-Roemerine, an aporphine alkaloid from Annona senegalensis that reverses the multidrug-resistance phenotype with cultured cells. J Nat Prod 58:598–604

    Article  PubMed  CAS  Google Scholar 

  • Zelenski SG (1977) Alkaloids of Nelumbo lutea (Wild.) pers. (Nymphaeaceae). J Pharm Sci 66:1627–1628

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Zhang B, Yan D, Dong W, Yang W, Li Q, Zeng L, Wang J, Wang L, Hicks LM, He Z (2011) Two Arabidopsis cytochrome P450 monooxygenases, CYP714A1 and CYP714A2, function redundantly in plant development through gibberellin deactivation. Plant J 67:342–353. doi:10.1111/j.1365-313X.2011.04596.x

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) Elongated uppermost internode encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work supported in part by The National Science Foundation grant IOS-1242275 to DRN.

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Correspondence to David R. Nelson or Mary A. Schuler.

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Communicated by Paul Moore

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Supplemental Table S1

Data for Fig. 5. (PDF 60 kb)

Supplemental Table S2

Number of occurrences of P450 transcripts in six different lotus tissues (at > 50 RPKM). (PDF 35.4 kb)

Supplemental Table S3

Expression data for 240 transcripts sorted by tissue (XLSX 274 kb)

Supplemental Figure S1

A tree of the papaya and lotus CYP72 sequences without other CYP72 clan members. Notice that CYP72A234 clusters where it should next to CYP72A226 and CYP72A227. (PDF 2 kb)

(DOCX 322 kb)

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Nelson, D.R., Schuler, M.A. Cytochrome P450 Genes from the Sacred Lotus Genome. Tropical Plant Biol. 6, 138–151 (2013). https://doi.org/10.1007/s12042-013-9119-z

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