Transcriptome analysis of bitter acid biosynthesis and precursor pathways in hop (Humulus lupulus)

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Clark, Shawn M ^a   Vaitheeswaran, Vinidhra ^a   Ambrose, Stephen J ^a   Purves, Randy W ^a   Page, Jonathan E ^a,b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HUMULUS; HUMULUS LUPULUS;

CYCLOHEXENE DERIVATIVE; HUMULON; TERPENE; VEGETABLE PROTEIN;

ARTICLE; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; HUMULUS; METABOLISM; METHODOLOGY; SIGNAL TRANSDUCTION;

CYCLOHEXENES; GENE EXPRESSION PROFILING; HUMULUS; PLANT PROTEINS; SIGNAL TRANSDUCTION; TERPENES;

MLCS; MLOWN;

EID: 84872685434     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-12     Document Type: Article

References (56)

1. Cleemput MV, Heyerick A, Libert C, Swerts K, Philippé J, Keukeleire DD, Haegeman G, Bosscher KD. Hop bitter acids efficiently block inflammation independent of GRα, PPARβ, or PPARγ. Mol Nutr Food Res 2009, 53:1143-1155. 10.1002/mnfr.200800493, 19655312.
2. Verzele M, Steenbeke G, Verhagen LC, Strating J. Preparative liquid chromatography of hop and beer bitter acids. J Chromatogr A 1989, 484:361-368.
3. Stevens JF, Page JE. Xanthohumol and related prenylflavonoids from hops and beer: to your good health!. Phytochemistry 2004, 65:1317-1330. 10.1016/j.phytochem.2004.04.025, 15231405.
4. Kavalier AR, Litt A, Ma C, Pitra NJ, Coles MC, Kennelly EJ, Matthews PD. Phytochemical and morphological characterization of hop (Humulus lupulus L.) cones over five developmental stages using high performance liquid chromatography coupled to time-of-flight mass spectrometry, ultrahigh performance liquid chromatography photodiode. J Agric Food Chem 2011, 59:4783-4793. 10.1021/jf1049084, 21456557.
5. Nagel J, Culley L, Lu Y, Liu E, Matthews PD, Stevens JF, Page JE. EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell 2008, 20:186-200. 10.1105/tpc.107.055178, 2254931, 18223037.
6. Schilmiller AL, Last RL, Pichersky E. Harnessing plant trichome biochemistry for the production of useful compounds. Plant J 2008, 54:702-711. 10.1111/j.1365-313X.2008.03432.x, 18476873.
7. Tissier A. Glandular trichomes: what comes after expressed sequence tags?. Plant J 2012, 70:51-68. 10.1111/j.1365-313X.2012.04913.x, 22449043.
8. Wang G, Tian L, Aziz N, Broun P, Dai X, He J, King A, Zhao PX, Dixon RA. Terpene biosynthesis in glandular trichomes of hop. Plant Physiol 2008, 148:1254-1266. 10.1104/pp.108.125187, 2577278, 18775972.
9. Stout J, Boubakir Z, Ambrose S, Purves R, Page J. The hexanoyl-CoA precursor for cannabinoid biosynthesis is formed by an acyl-activating enzyme in trichomes of Cannabis sativa. Plant J 2012, 71:353-365.
10. Gagne SJ, Stout JM, Liu E, Boubakir Z, Clark SM, Page JE. A cannabinoid pathway cyclase enzyme reveals a new catalytic route to plant polyketides. Proc Natl Acad Sci USA 2012, 109:12811-12816. 10.1073/pnas.1200330109, 3411943, 22802619.
11. Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA, Harper A, Aziz N, Li Y, Larson TR, Giovannoni J, Dixon RA, Broun P. Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiol 2008, 148:1830-1846. 10.1104/pp.108.129510, 2593661, 18931142.
12. Walters DS, Steffens JC. Branched-chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters. Plant Physiol 1990, 93:1544-1551. 10.1104/pp.93.4.1544, 1062709, 16667654.
13. Binder S, Knill T, Schuster J. Branched-chain amino acid metabolism in higher plants. Physiol Plant 2007, 129:68-78.
14. Diebold R, Schuster J, Däschner K, Binder S. The branched-chain amino acid transaminase gene family in Arabidopsis encodes plastid and mitochondrial proteins. Plant Physiol 2002, 129:540-550. 10.1104/pp.001602, 161671, 12068099.
15. Maloney GS, Kochevenko A, Tieman D, Tohge T, Krieger U, Zamir D, Taylor MG, Fernie AR, Klee HJ. Characterization of the branched-chain amino acid aminotransferase enzyme family in tomato. Plant Physiol 2010, 153:925-936. 10.1104/pp.110.154922, 2899903, 20435740.
16. Kochevenko A, Klee HJ, Fernie AR, Araújo WL. Molecular identification of a further branched-chain aminotransferase 7 (BCAT7) in tomato plants. J Plant Physiol 2012, 169:437-443. 10.1016/j.jplph.2011.12.002, 22226341.
17. Mooney BP, Miernyk JA, Randall DD. The complex fate of α-ketoacids. Ann Rev Plant Biol 2002, 53:357-375.
18. Lutziger I, Oliver DJ. Characterization of two cDNAs encoding mitochondrial lipoamide dehydrogenase from Arabidopsis. Plant Physiol 2001, 127:615-623. 10.1104/pp.010321, 125096, 11598235.
19. Goese M, Kammhuber K, Bacher A, Zenk MH, Eisenreich W. Biosynthesis of bitter acids in hops. A 13C-NMR and 2H-NMR study on the building blocks of humulone. Eur J Biochem 1999, 263:447-454. 10.1046/j.1432-1327.1999.00518.x, 10406953.
20. Paniego NB, Zuurbier KW, Fung SY, Van Der Heijden R, Scheffer JJ, Verpoorte R. Phlorisovalerophenone synthase, a novel polyketide synthase from hop (Humulus lupulus L.) cones. Eur J Biochem 1999, 262:612-616. 10.1046/j.1432-1327.1999.00444.x, 10336650.
21. Tsurumaru Y, Sasaki K, Miyawaki T, Uto Y, Momma T, Umemoto N, Momose M, Yazaki K. HlPT-1, a membrane-bound prenyltransferase responsible for the biosynthesis of bitter acids in hops. Biochem Biophys Res Comm 2012, 417:393-398. 10.1016/j.bbrc.2011.11.125, 22166201.
22. Zuurbier KWM, Paniego NB, Scheffer JJC, Verpoorte R. Conversion of deoxyhumulone into the hop α-acid humulone. Phytochemistry 1997, 44:1047-1053.
23. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652. 10.1038/nbt.1883, 21572440.
24. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659. 10.1093/bioinformatics/btl158, 16731699.
25. Nikolau BJ, Ohlrogge JB, Wurtele ES. Plant biotin-containing carboxylases. Arch Biochem Biophys 2003, 414:211-222. 10.1016/S0003-9861(03)00156-5, 12781773.
26. Fatland BL, Ke J, Anderson MD, Mentzen WI, Cui LW, Allred CC, Johnston JL, Nikolau BJ, Wurtele ES. Molecular characterization of a heteromeric ATP-citrate lyase that generates cytosolic acetyl-coenzyme A in Arabidopsis. Plant Physiol 2002, 130:740-756. 10.1104/pp.008110, 166603, 12376641.
27. Martinez-Carrion M, Hubert E, Iriarte A, Mattingly JZS. Mechanism of aminotransferase action. Transaminase 1985, 307-317. Wiley, MD New York, Christen P.
28. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016. 10.1006/jmbi.2000.3903, 10891285.
29. Nelson BK, Cai X, Nebenführ A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 2007, 51:1126-1136. 10.1111/j.1365-313X.2007.03212.x, 17666025.
30. Wang G, Dixon RA. Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc Natl Acad Sci USA 2009, 106:9914-9919. 10.1073/pnas.0904069106, 2701037, 19482937.
31. Schilmiller AL, Miner DP, Larson M, McDowell E, Gang DR, Wilkerson C, Last RL. Studies of a biochemical factory: tomato trichome deep expressed sequence tag sequencing and proteomics. Plant Physiol 2010, 153:1212-1223. 10.1104/pp.110.157214, 2899918, 20431087.
32. Bleeker P, Spyropoulou E. RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Mol Biol 2011, 77:323-336. 10.1007/s11103-011-9813-x, 3193516, 21818683.
33. Aziz N, Paiva NL, May GD, Dixon RA. Transcriptome analysis of alfalfa glandular trichomes. Planta 2005, 221:28-38. 10.1007/s00425-004-1424-1, 15578217.
34. Zonneveld BJM, Leitch IJ, Bennett MD. First nuclear DNA amounts in more than 300 angiosperms. Ann Bot 2005, 96:229-244. 10.1093/aob/mci170, 15905300.
35. Matoušek J, Kocábek T, Patzak J, Füssy Z, Procházková J, Heyerick A. Combinatorial analysis of lupulin gland transcription factors from R2R3Myb, bHLH and WDR families indicates a complex regulation of chs_H1 genes essential for prenylflavonoid biosynthesis in hop (Humulus lupulus L.). BMC Plant Biol 2012, 12:27. 10.1186/1471-2229-12-27, 3340318, 22340661.
36. Matousek J, Vrba L, Novák P, Patzak J, Keukeleire JD, Skopek J, Heyerick A, Roldán-Ruiz I, Keukeleire DD. Cloning and molecular analysis of the regulatory factor HlMyb1 in hop (Humulus lupulus L.) and the potential of hop to produce bioactive prenylated flavonoids. J Agric Food Chem 2005, 53:4793-4798. 10.1021/jf050175y, 15941318.
37. Matousek J, Kocábek T, Patzak J, Skopek J, Maloukh L, Heyerick A, Fussy Z, Roldán-Ruiz I, Keukeleire DD. HlMyb3, a putative regulatory factor in hop (Humulus lupulus L.), shows diverse biological effects in heterologous transgenotes. J Agric Food Chem 2007, 55:7767-7776. 10.1021/jf071153+, 17708645.
38. Marks MD, Tian L, Wenger JP, Omburo SN, Soto-Fuentes W, He J, Gang DR, Weiblen GD, Dixon RA. Identification of candidate genes affecting Δ9-tetrahydrocannabinol biosynthesis in Cannabis sativa. J Exp Bot 2009, 60:3715-3726. 10.1093/jxb/erp210, 2736886, 19581347.
39. Knill T, Schuster J, Reichelt M, Gershenzon J, Binder S. Arabidopsis branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol 2008, 146:1028-1039. 10.1104/pp.107.111609, 2259058, 18162591.
40. Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES. Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biol 2008, 8:76. 10.1186/1471-2229-8-76, 2483283, 18616834.
41. Meisel L, Fonseca B, González S, Baeza-Yates R, Cambiazo V, Campos R, Gonźalez M, Orellana A, Retamales J, Silva H. A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol Res 2005, 38:83-88.
42. Shao Z, Zhao H, Zhao H. DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways. Nucleic Acids Res 2009, 37:e16. 10.1093/nar/gkn724, 2632897, 19074487.
43. Baggerly KA, Deng L, Morris JS, Aldaz CM. Differential expression in SAGE: accounting for normal between-library variation. Bioinformatics 2003, 19:1477-1483. 10.1093/bioinformatics/btg173, 12912827.
44. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008, 36:3420-3435. 10.1093/nar/gkn176, 2425479, 18445632.
45. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
46. Cohen SA, Michaud DP. Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via high-performance liquid chromatography. Anal Biochem 1993, 211:279-287. 10.1006/abio.1993.1270, 8317704.
47. Perera MADN, Choi S-Y, Wurtele ES, Nikolau BJ. Quantitative analysis of short-chain acyl-coenzymeAs in plant tissues by LC-MS-MS electrospray ionization method. J Chromatogr B Analyt Technol Biomed Life Sci 2009, 877:482-488. 10.1016/j.jchromb.2008.12.053, 19157998.
48. Claros MG, Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 1996, 241:779-786. 10.1111/j.1432-1033.1996.00779.x, 8944766.
49. Emanuelsson O, Nielsen H, von Heijne G. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 1999, 8:978-841. 10.1110/ps.8.5.978, 2144330, 10338008.
50. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
51. Prohl C, Kispal G, Lill R. Branched-chain-amino-acid transaminases of yeast Saccharomyces cerevisiae. Methods Enzymol 2000, 324:365-375.
52. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 2006, 45:616-629. 10.1111/j.1365-313X.2005.02617.x, 16441352.
53. Sparkes IA, Runions J, Kearns A, Hawes C. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 2006, 1:2019-2025. 10.1038/nprot.2006.286, 17487191.
54. van Bakel H, Stout JM, Cote AG, Tallon C, Sharpe AG, Hughes TR, Page JE. The draft genome and transcriptome of Cannabis sativa. Genome Biol 2011, 12:R102. 10.1186/gb-2011-12-10-r102, 3359589, 22014239.
55. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404, 17846036.
56. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.