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The “putative” role of transcription factors from HlWRKY family in the regulation of the final steps of prenylflavonid and bitter acids biosynthesis in hop (Humulus lupulus L.)

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Abstract

Lupulin glands localized in female hop (Humulus lupulus L.) cones are valuable source of bitter acids, essential oils and polyphenols. These compounds are used in brewing industry and are important for biomedical applications. In this study we describe the potential effect of transcription factors from WRKY family in the activation of the final steps of lupulin biosynthesis. In particular, lupulin gland-specific transcription factor HlWRKY1 that shows significant similarity to AtWRKY75, has ability to activate the set of promoters driving key genes of xanthohumol and bitter acids biosynthesis such as chalcone synthase H1, valerophenone synthase, prenyltransferase 1, 1L and 2 and O-methyltransferase-1. When combined with co-factor HlWDR1 and silencing suppressor p19, HlWRKY1 is able to enhance transient expression of gus gene driven by Omt1 and Chs_H1 promoters to significant level as compared to 35S promoter of CaMV in Nicotiana. benthamiana. Transformation of hop with dual Agrobacterium vector bearing HlWRKY1/HlWDR1 led to ectopic overexpression of these transgenes and further activation of lupulin-specific genes expression in hop leaves. It was further showed that (1) HlWRKY1 is endowed with promoter autoactivation; (2) It is regulated by post-transcriptional gene silencing (PTGS) mechanism; (3) It is stimulated by kinase co-expression. Since HlWRKY1 promotes expression of lupulin-specific HlMyb3 gene therefore it can constitute a significant component in hop lupulin regulation network. Putative involvement of HlWRKY1 in the regulation of lupulin biosynthesis may suggest the original physiological function of lupulin components in hop as flower and seed protective compounds.

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References

  • Agarwal P, Reddy MP, Chikara J (2011) WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep 38:3883–3896

    Article  CAS  PubMed  Google Scholar 

  • Albert NW, Davies KM, Schwinn KE (2014) Gene regulation networks generate diverse pigmentation patterns in plants. Plant Signal Behav 9:e29526

    Article  PubMed Central  Google Scholar 

  • Aravin A, Tuschl T (2005) Identification and characterization of small RNAs involved in RNA silencing. FEBS Lett 579:5830–5840

    Article  CAS  PubMed  Google Scholar 

  • Bai ML, Yang GS, Chen WT, Mao ZC, Kang HX, Chen GH, Yang YH, Xie BY (2012) Genome-wide identification of Dicer-like, argonaute and RNA-dependent RNA polymerase gene families and their expression analyses in response to viral infection and abiotic stresses in Solanum lycopersicum. Gene 501:52–62

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya S, Virani S, Zavro M, Haas GJ (2003) Inhibition of Streptococcus mutans and other oral Streptococci by hop (Humulus lupulus L.) constituents. Econ Bot 57:118–125

    Article  Google Scholar 

  • Blanco CA, Rojas A, Nimubona D (2007) Effects of acidity and molecular size on bacteriostatic properties of beer hop derivates. Trends Food Sci Tech 18:144–149

    Article  CAS  Google Scholar 

  • Bolca S, Wyns C, Possemiers S, Depypere H, De Keukeleire D, Bracke M, Verstraete W, Heyerick A (2009) Cosupplementation of isoflavones, prenylflavonoids, and lignans alters human exposure to phytoestrogen-derived 17 beta-estradiol equivalents. J Nutrit 139:2293–2300

    CAS  PubMed  Google Scholar 

  • Ceremuga TE, Johnson LA, Adams-Henderson JM, McCall S, Johnson D (2013) Investigation of the anxiolytic effects of xanthohumol, a component of humulus lupulus (Hops), in the male Sprague–Dawley rat. AANA J 81:193–198

    PubMed  Google Scholar 

  • Cheng Y, Zhou Y, Yang Y, Chi Y-J, Zhou J, Chen J-Y, Wang F, Fan B, Shi K, Zhou Y-H, Yu J-Q, Chen Z (2012) Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiol 159:810–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, Yu J-Q, Chen Z (2013) Protein–Protein interactions in the regulation of WRKY transcription factors. Mol Plant 6:287–300

    Article  CAS  PubMed  Google Scholar 

  • Choi C, Park Y, Kwon S, Yun C, Ahn I, Park S, Hwang D-J (2014) Identification of AtWRKY75 as a transcriptional regulator in the defense response to Pcc through the screening of Arabidopsis activation-tagged lines. Plant Biotech Rep 8:183–192

    Article  Google Scholar 

  • Chytilová E, Macas J, Galbraith DW (1999) Green fluorescent protein targeted to the nucleus, a transgenic phenotype useful for studies in plant biology. Ann Bot 83:645–654

    Article  Google Scholar 

  • Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA binding selectivity of WRKY transcription factors lend structural clues into WRKY domain function. Plant Mol Biol 68:81–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark SM, Vaitheeswaran V, Ambrose SJ, Purves RW, Page JE (2013) Transcriptome analysis of bitter acid biosynthesis and precursor pathways in hop (Humulus lupulus). BMC Plant Biol 13:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, de los Santos B, Romero F, Pliego-Alfaro F, Muñoz-Blanco J, Caballero JL (2009) Evidence for a positive regulatory role of strawberry (Fragaria x ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. J Exp Bot 60:3043–3065

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Feller A, Machemer K, Braun LE, Grotewold E (2011) Evolutionary and comparative analysis of Myb and bHLH plant transcription factors. Plant J 66:94–116

    Article  CAS  PubMed  Google Scholar 

  • Füssy Z, Patzak J, Stehlík J, Matoušek J (2013) Imbalance in expression of hop (Humulus lupulus) chalcone synthase H1 and its regulators during hop stunt viroid pathogenesis. J Plant Physiol 170:688–695

    Article  PubMed  Google Scholar 

  • Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell 22:481–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatica-Arias A, Farag MA, Stanke M, Matoušek J, Wessjohann L, Weber G (2012) Flavonoid production in transgenic hop (Humulus lupulus L.) altered by PAP1/MYB75 from Arabidopsis thaliana L. Plant Cell Rep 31:111–119

    Article  CAS  PubMed  Google Scholar 

  • Gatica-Arias A, Stanke M, Häntzschel KR, Matoušek J, Weber G (2013) Over-expression of the transcription factor HlMYB3 in transgenic hop (Humulus lupulus L. cv. Tettnanger) modulates the expression of genes involved in the biosynthesis of flavonoids and phloroglucinols. Plant Cell Tiss Org 113:279–289

    Article  CAS  Google Scholar 

  • Gerhäuser C (2005) Beer constituents as potential cancer chemopreventive agents. Eur J Cancer 41:1941–1954

    Article  PubMed  Google Scholar 

  • German MA, Luo S, Schroth G, Meyers BC, Green PJ (2009) Construction of parallel analysis of RNA ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc 4:356–362

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549

    Article  CAS  Google Scholar 

  • Hajheidari M, Farrona S, Huettel B, Koncz Z, Koncz C (2012) CDKF,1 and CDKD protein kinases regulate phosphorylation of serine residues in the C-terminal domain of Arabidopsis RNA polymerase II. Plant Cell 24:1626–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holsters M, de Waele D, Depicker A, Messens E, van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163:181–187

    Article  CAS  PubMed  Google Scholar 

  • Horlemann C, Schwekendiek A, Höhnle M, Weber G (2003) Regeneration and Agrobacterium-mediated transformation of hop (Humulus lupulus L.) Plant Cell Rep 22:210–217

    Article  CAS  PubMed  Google Scholar 

  • Hough JS, Howard GA, Slater CA (1957) Bacteriostatic activities of hop resin materials. J I Brewing 63:331–333

    Article  Google Scholar 

  • Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297

    Article  PubMed  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  • Kato N, Dubouzet E, Kokabu Y, Yoshida S, Taniguchi Y, Dubouzet JG, Yazaki K, Sato F (2007) Identification of a WRKY protein as a transcriptional regulator of benzylisoquinoline alkaloid biosynthesis in coptis japonica. Plant Cell Physiol 48:8–18

    Article  CAS  PubMed  Google Scholar 

  • Kramer MF (2011) Stem-loop RT-qPCR for miRNAs. Curr Protoc Mol Biol 15 10

    PubMed  Google Scholar 

  • Langley RA, Kado CL (1972) Studies on Agrobacterium tumefaciens. Condition of mutagenesis by N-methyl-N′-nitro-N-nitrosoguanidine and relationship of Agrobacterium tumefaciens mutants to crown gall induction. Mutat Res 14:277–286

    Article  CAS  Google Scholar 

  • Larson AE, Yu RR, Lee OA, Price S, Haas GJ, Johnson EA (1996) Antimicrobial activity of hop extracts against Listeria monocytogenes in media and in food. Int J Food Microbiol 33:195–207

    Article  CAS  PubMed  Google Scholar 

  • Lei L, Li Y, Wang Q, Xu J, Chen Y, Yang H, Ren D (2014) Activation of MKK9-MPK3/MPK6 enhances phosphate acquisition in Arabidopsis thaliana. New Phytol 203:1146–1160

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Peng J, Wen X, Guo H (2012) Gene network analysis and functional studies of senescence-associated genes reveal novel regulators of Arabidopsis leaf senescence. J Integr Plant Biol 54:526–539

    Article  CAS  PubMed  Google Scholar 

  • Li H, Ban Z, Qin H, Ma L, King AJ, Wang G (2015) A heteromeric membrane-bound prenyltransferase complex from hop catalyzes three sequential aromatic prenylations in the bitter acid pathway. Plant Physiol 167:650–659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maliga P, Klessig DF, Cashmore AR, Gruissem W, Varner JE (1995) Methods in plant molecular biology: a laboratory course manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Maloukh L, Matoušek J, Van-Bockstaele E, Roldán-Ruiz I (2009) Housekeeping gene selection for real time-PCR normalization in female hop (Humulus lupulus L) tissues. J Plant Biochem Biotechnol 18:53–58

    Article  CAS  Google Scholar 

  • Matoušek J, Vrba L, Novák P, Patzak J, De Keukeleire J, Škopek J, Heyerick A, Roldán-Ruiz I, De Keukeleire D (2005) 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 53:4793–4798

    Article  PubMed  Google Scholar 

  • Matoušek J, Vrba L, Škopek J, Orctová L, Pešina K, Heyerick A, Baulcombe D, De Keukeleire D (2006) Sequence analysis of a “true” chalcone synthase (chs_H1) oligofamily from hop (Humulus lupulus L.) and PAP1 activation of chs_H1 in heterologous systems. J Agric Food Chem 54:7606–7615

    Article  PubMed  Google Scholar 

  • Matoušek J, Kocábek T, Patzak J, Škopek J, Maloukh L, Heyerick A, Füssy Z, Roldán-Ruiz I, De Keukeleire D (2007) HlMyb3, a putative regulatory factor in hop (Humulus lupulus L.), shows diverse biological effects in heterologous transgenotes. J Agric Food Chem 55:7767–7776

    Article  PubMed  Google Scholar 

  • Matoušek J, Kocábek T, Patzak J, Stehlík J, Füssy Z, Krofta K, Heyerick A, Roldán-Ruiz I, Maloukh L, De Keukeleire D (2010) Cloning and molecular analysis of HlbZip1 and HlbZip2 transcription factors putatively involved in the regulation of the lupulin metabolome in hops (Humulus lupulus L.) J Agric Food Chem 58:902–912

    Article  PubMed  Google Scholar 

  • Matoušek J, Kocábek T, Patzak J, Füssy Z, Procházková J, Heyerick A (2012) 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 12:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Matoušek J, Piernikarczyk RJ, Týcová A, Duraisamy GS, Kocábek T, Steger G (2015) Expression of SANT/HTH Myb mRNA, a plant morphogenesis-regulating transcription factor, changes due to viroid infection. J Plant Physiol 183:85–94

    Article  PubMed  Google Scholar 

  • Mizobuchi S, Sato Y (1985) Antifungal Activities of hop bitter resins and related compounds. Agric Biol Chem 49:399–403

    CAS  Google Scholar 

  • Murashige TF, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nagel J, Culley LK, Lu Y, Liu E, Matthews PD, Stevens JF, Page JE (2008) EST analysis of hop glandular trichomes identifies an O-Methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell 20:186–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Natsume S, Takagi H, Shiraishi A, Murata J, Toyonaga H, Patzak J, Takagi M, Yaegashi H, Uemura A, Mitsuoka Ch, Yoshida K, Krofta K, Satake H, Terauchi R, Ono E (2015) The draft genome of hop (Humulus lupulus), an essence for brewing. Plant Cell Physiol 56:428–441

    Article  CAS  PubMed  Google Scholar 

  • Novák P, Krofta K, Matoušek J (2006) Chalcone synthase homologues from Humulus lupulus: some enzymatic properties and expression. Biol Plant 50:48–54

    Article  Google Scholar 

  • Okada Y, Ito K (2001) Cloning and analysis of valerophenone synthase gene expressed specifically in lupulin gland of hop (Humulus lupulus L.) Biosci Biotech Bioch 65:150–155

    Article  CAS  Google Scholar 

  • Oliveira MM, Pais MS (1990) Glandular trichomes of Humulus lupulus var. Brewer’s Gold (hops): ultrastructural aspects of peltate trichomes. J Submicrosc Cytol Pathol 22:241–248

    Google Scholar 

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patzak J, Krofta K, Henychová A, Nesvadba V (2015) Number and size of lupulin glands, glandular trichomes of hop (Humulus lupulus L.), play key-role in contents of bitter acids and polyphenols in hop cone. Int J Food Sci Technol 50:1864–1872

    Article  CAS  Google Scholar 

  • Pesch M, Dartan B, Birkenbihl R, Somssich IE, Hülskamp M (2014) Arabidopsis TTG2 regulates TRY expression through enhancement of activator complex-triggered activation. Plant Cell 26:4067–4083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Ramsay NA, Glover BJ (2005) MYB–bHLH–WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10:63–70

    Article  CAS  PubMed  Google Scholar 

  • Rishmawi L, Pesch M, Juengst C, Schauss AC, Schrader A, Hülskamp M (2014) Non-cell-autonomous regulation of root hair patterning genes by WRKY75 in Arabidopsis thaliana. Plant Physiol 165:186–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy AT, Leggett G, Koutoulis A (2001) Development of a shoot multiplication system for hop (Humulus lupulus L.). In vitro cell. Dev Biol 37:79–83

    CAS  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Schluttenhofer C, Yuan L (2015) Regulation of specialized metabolism by WRKY transcription factors. Plant Physiol 167:295–306

    Article  CAS  PubMed  Google Scholar 

  • Schmalreck AF, Teuber M (1975) Structural features determining the antibiotic potencies of natural and synthetic hop bitter resins, their precursors and derivatives. Can J Microbiol 21:205–212

    Article  CAS  PubMed  Google Scholar 

  • Schumacher J, Meyer N, Riesner D, Weidemann HL (1986) Diagnostic procedure for detection of viroids and viruses with circular RNAs by “return”-gel electrophoresis. J Phytopath 115:332–343

    Article  Google Scholar 

  • Singh KB (1998) Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiol 118:1111–1120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevens JF, Page JE (2004) Xanthohumol and related prenylflavonoids from hops and beer: to your good health!. Phytochemistry 65:1317–1330

    Article  CAS  PubMed  Google Scholar 

  • Stirnimann CU, Petsalaki E, Russell RB, Müfler CW (2010) WD40 proteins propel cellular network. Trends Bioch Sci 35:565–574

    Article  CAS  Google Scholar 

  • Strizhov N, Keller M, Mathur J, Koncz-Kálmán Z, Bosch D, Prudovsky E, Schell J, Sneh B, Koncz C, Zilberstein A (1996) A synthetic cryIC gene, encoding a Bacillus thuringiensis delta-endotoxin, confers Spodoptera resistance in alfalfa and tobacco. Proc Natl Acad Sci USA 93:15012–15017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama R, Oda H, Kurosaki F (2006) Two distinct phases of glandular trichome development in hop (Humulus lupulus L.). Plant Biotech 23:493–496

    Article  CAS  Google Scholar 

  • Suttipanta S, Pattanaik S, Kulshrestha M, Patra B, Singh SK, Yuan L (2011) The Transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol 157:2081–2093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tai TH, Tanksley SD (1990) A rapid and inexpensive method for isolation of total DNA from dehydrated plant tissue. Plant Mol Biol Rep 8:297–303

    Article  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 CM, Jones DA, English JJ, Carroll BJ, Bennetzen JL, Harrison K, Burbidge A, Bishop GJ, Jones JDG (1994) Analysis of the chromosomal distribution of transposon-carrying T-DNAs in tomato using the inverse polymerase chain reaction. Mol Gen Genet 242:573–585

    Article  CAS  PubMed  Google Scholar 

  • Tohge T, Nishiyama Y, Hirai M, Yano M, Nakajima J, Awazuhara M, Inoue E, Takahashi H, Goodenowe D, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42:218–235

    Article  CAS  PubMed  Google Scholar 

  • Töpfer R, Matzeit V, Gronenborn B, Schell J, Steinbiss HH (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucl Acids Res 15:5890

    Article  PubMed  PubMed Central  Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157

    Article  CAS  Google Scholar 

  • Tsurumaru Y, Sasaki K, Miyawaki T, Momma T, Umemoto N, Yazaki K (2010) An aromatic prenyltransferase-like gene HlPT-1 preferentially expressed in lupulin glands of hop. Plant Biotech 27:199–204

    Article  CAS  Google Scholar 

  • Tsurumaru Y, Sasaki K, Miyawaki T, Uto Y, Momma T, Umemoto N, Momose M, Yazaki K (2012) HlPT-1, a membrane-bound prenyltransferase responsible for the biosynthesis of bitter acids in hops. Biochem Biophys Res Commun 417:393–398

    Article  CAS  PubMed  Google Scholar 

  • Turck F, Zhou A, Somssich IE (2004) Stimulus-dependent, promoter specific binding of transcription factor WRKY1 to Its native promoter and the defense-related gene PcPR1-1 in Parsley. Plant Cell 16:2573–2585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Cleemput M, Cattoor K, De Bosscher K, Haegeman G, De Keukeleire D, Heyerick A (2009) Hop (Humulus lupulus)-derived bitter acids as multipotent bioactive compounds. J Nat Prod 72:1220–1230

    Article  PubMed  Google Scholar 

  • Verweij W, Spelt CE, Bliek M, de Vries M, Wit N, Faraco M, Koes R, Quattrocchio FM (2016) Functionally similar WRKY proteins regulate vacuolar acidification in petunia and hair development in Arabidopsis. Plant Cell 28:786–803

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220

    Article  CAS  PubMed  Google Scholar 

  • Vrba L, Matoušek J (2005) Expression of modified 7SL RNA gene in transgenic Solanum tuberosum plants. Biol Plant 49:371–380

    Article  CAS  Google Scholar 

  • Wang G, Tian L, Aziz N, Broun P, Dai X, He J, King A, Zhao PX, Dixon RA (2008) Terpene biosynthesis in glandular trichomes of hop. Plant Physiol 148:1254–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276

    Article  CAS  PubMed  Google Scholar 

  • Zanoli P, Zavatti M (2008) Pharmacognostic and pharmacological profile of Humulus lupulus L. J Ethnopharmacol 116:383–396

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Z, Wang H, Wang Y, Guan S, Wan F, Tang J, Zhang R, Xie L, Lu Y (2015) Characterization of the cis elements in the proximal promoter regions of the anthocyanin pathway genes reveals a common regulatory logic that governs pathway regulation. J Exp Bot 66:3775–3789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to thank Helena Matoušková, Olga Horáková, Lidmila Orctová and Jana Jehlíková from Biology Centre of the CAS v.v.i., Institute of Plant Molecular Biology (IPMB) for excellent technical assistance. The authors would like to acknowledge prof. Csaba Koncz from the Max Planck Institute for Plant Breeding, Cologne (Germany) for valuable discussions and for providing the vector plasmid for Agrobacterium transformation. This work was supported by the Czech Science Foundation GACR 13-03037S, by the cooperative project FP7-REGPOT-2012-2013-1 MODBIOLIN No. 316304, GAJU 143/2013/P and by institutional support RVO:60077344.

Author contributions

JM conceived and coordinated the project, isolated and cloned the genes into Agrobacterium vectors, performed degradome analysis, TK was responsible for transient expression experiments, JP screened ESTs, JB did the hop transformation and particle bombardment assays, participated on the promoters cloning, KS did the EMSA and RT-qPCR of transgenic hop, AKM performed bioinformatics analyses, GSD participated on the gene cloning, AT did the RT-qPCR of tissue specificity expression analysis, EO provided the genomic sequences of hop, KK did the HPLC analysis of lupulin metabolites. JM wrote the manuscript, TK and AKM edited the manuscript. All authors have read and approved the final manuscript.

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Authors and Affiliations

  1. Biology Centre of the Czech Academy of Sciences v.v.i, Institute of Plant Molecular Biology, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Jaroslav Matoušek, Tomáš Kocábek, Jindřich Bříza, Kristýna Siglová, Ajay Kumar Mishra, Ganesh Selvaraj Duraisamy & Anna Týcová

  2. Hop Research Institute, Co. Ltd., Kadaňská 2525, 438 46, Žatec, Czech Republic

    Josef Patzak & Karel Krofta

  3. Faculty of Science, University of South Bohemia in České Budějovice, Branišovská 1760, 370 05, České Budějovice, Czech Republic

    Kristýna Siglová & Anna Týcová

  4. Research Institute, Suntory Global Innovation Center (SIC) Ltd., 1-1-1 Wakayamadai, Shimamoto, Mishima, Osaka, 618-8503, Japan

    Eiichiro Ono

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  1. Jaroslav Matoušek
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Correspondence to Jaroslav Matoušek.

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Matoušek, J., Kocábek, T., Patzak, J. et al. The “putative” role of transcription factors from HlWRKY family in the regulation of the final steps of prenylflavonid and bitter acids biosynthesis in hop (Humulus lupulus L.). Plant Mol Biol 92, 263–277 (2016). https://doi.org/10.1007/s11103-016-0510-7

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