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Research Articles

Gene Expression of Agronomically Important Secondary Metabolites in cv. ‘USDA Cascade’ Hop (Humulus lupulus L.) Cones during Critical Developmental Stages

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 356-369 | Received 11 Mar 2021, Accepted 23 Aug 2021, Published online: 26 Oct 2021

Literature cited

  • Neve, R. A. Hops; Chapman and Hall: London, 1991.
  • Binder, S.; Knill, T.; Schuster, J. Branched-Chain Amino Acid Metabolism in Higher Plants. Physiol. Plant. 2007, 129, 68–78. DOI: 10.1111/j.1399-3054.2006.00800.x.
  • Clark, S. M.; Vaitheeswaran, V.; Ambrose, S. J.; Purves, R. W.; Page, J. E. Transcriptome Analysis of Bitter Acid Biosynthesis and Precursor Pathways in Hop (Humulus lupulus). BMC Plant Biol. 2013, 13, 12. DOI: 10.1186/1471-2229-13-12.
  • Xu, H.; Zhang, F.; Liu, B.; Huhman, D. V.; Sumner, L. W.; Dixon, R. A.; Wang, G. Characterization of the Formation of Branched Short-Chain Fatty Acid:CoAs for Bitter Acid Biosynthesis in Hop Glandular Trichomes. Mol. Plant. 2013, 6, 1301–1317. DOI: 10.1093/mp/sst004.
  • Novák, P.; Krofta, K.; Matoušek, J. Chalcone Synthase Homologues from Humulus lupulus: Some Enzymatic Properties and Expression. Biologia Plant. 2006, 50, 48–54. DOI: 10.1007/s10535-005-0073-y.
  • Okada, Y.; Ito, K. Cloning and Analysis of Valerophenone Synthase Gene Expressed Specifically in Lupulin Gland of Hop (Humulus lupulus L.). Biosci. Biotechnol. Biochem. 2001, 65, 150–155. DOI: 10.1271/bbb.65.150.
  • Okada, Y.; Sano, Y.; Kaneko, T.; Abe, I.; Noguchi, H.; Ito, K. Enzymatic Reactions by Five Chalcone Synthase Homologs from Hop (Humulus lupulus L.). Biosci. Biotechnol. Biochem. 2004, 68, 1142–1145. DOI: 10.1271/bbb.68.1142.
  • Goese, M.; Kammhuber, K.; Bacher, A.; Zenk, M. H.; Eisenreich, W. Biosynthesis of Bitter Acids in hops. A (13)C-NMR and (2)H-NMR study on the building blocks of humulone. Eur. J. Biochem. 1999, 263, 447–454. DOI: 10.1046/j.1432-1327.1999.00518.x.
  • Wang, G.; Tian, L.; Aziz, N.; Broun, P.; Dai, X.; He, J.; King, A.; Zhao, P. X.; Dixon, R. A. Terpene Biosynthesis in Glandular Trichomes of Hop. Plant Physiol. 2008, 148, 1254–1266. DOI: 10.1104/pp.108.125187.
  • Nagel, J.; Culley, L. K.; Lu, Y.; Liu, E.; Matthews, P. D.; Stevens, J. F.; Page, J. E. EST Analysis of Hop Glandular Trichomes Identifies an O-Methyltransferase that Catalyzes the Biosynthesis of Xanthohumol. Plant Cell. 2008, 20, 186–200. DOI: 10.1105/tpc.107.055178.
  • Tsurumaru, Y.; Sasaki, K.; Miyawaki, T.; Momma, T.; Umemoto, N.; Yazaki, K. An Aromatic Prenyltransferase-like Gene HlPT-1 Preferentially Expressed in Lupulin Glands of Hop. Plant Biotechnol. 2010, 27, 199–204. DOI: 10.5511/plantbiotechnology.27.199.
  • 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. Commun. 2012, 417, 393–398. DOI: 10.1016/j.bbrc.2011.11.125.
  • Li, H.; Ban, Z.; Qin, H.; Ma, L.; King, A. J.; Wang, G. A Heteromeric Membrane-Bound Prenyltransferase Complex from Hop Catalyzes Three Sequential Aromatic Prenylations in the Bitter Acid Pathway. Plant Physiol. 2015, 167, 650–659. DOI: 10.1104/pp.114.253682.
  • Fung, S.; Zuurbier, K. W. M.; Paniego, N. B.; Scheffer, J. J. C.; Verpoorte, R. Conversation of Deoxyhumulone into the Hop Alpha-Acid Humulone. Phytochemistry 1997, 44, 1047–1053. DOI: 10.1016/S0031-9422(96)00671-1.
  • Champagne, A.; Boutry, M. A Comprehensive Proteome Map of Glandular Trichomes of Hop (Humulus lupulus L.) Female Cones: Identification of Biosynthetic Pathways of the Major Terpenoid-Related Compounds and Possible Transport Proteins. Proteomics 2017, 17, 1–10. DOI: 10.1002/pmic.201600411.
  • Kocábek, T.; Mishra, A. K.; Matoušek, J.; Patzak, J.; Lomnická, A.; Khare, M.; Krofta, K. The R2R3 Transcription Factor HlMYB8 and Its Role in Flavonoid Biosynthesis in Hop (Humulus lupulus L.). Plant Sci. 2018, 269, 32–46. DOI: 10.1016/j.plantsci.2018.01.004.
  • De Keukeleire, J.; Ooms, G.; Heyerick, A.; Roldan-Ruiz, I.; Van Bockstaele, E.; De Keukeleire, D. Formation and Accumulation of Alpha-Acids, Beta-Acids, Desmethylxanthohumol, and Xanthohumol during Flowering of Hops (Humulus lupulus L.). J. Agric. Food Chem. 2003, 51, 4436–4441. DOI: 10.1021/jf034263z.
  • Ban, Z.; Qin, H.; Mitchell, A. J.; Liu, B.; Zhang, F.; Weng, J. K.; Dixon, R. A.; Wang, G. Noncatalytic Chalcone Isomerase-Fold Proteins in Humulus lupulus Are Auxiliary Components in Prenylated Flavonoid Biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 2018, 115, E5223–E5232. DOI: 10.1073/pnas.1802223115.
  • 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. DOI: 10.1186/1471-2229-12-27.
  • Matoušek, J.; Kocábek, T.; Patzak, J.; Bříza, J.; Siglová, K.; Mishra, A. K.; Duraisamy, G. S.; Týcová, A.; Ono, E.; Krofta, K. 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. 2016, 92, 263–277. DOI: 10.1007/s11103-016-0510-7.
  • Matoušek, J.; Vrba, L.; Novák, P.; Patzak, J.; De Keukeleire, J.; Škopek, J.; Heyerick, A.; Roldán-Ruiz, I.; De Keukeleire, D. 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. DOI: 10.1021/jf050175y.
  • Matoušek, J.; Kocábek, T.; Patzak, J.; Škopek, J.; Maloukh, L.; Heyerick, A.; Fussy, Z.; Roldán-Ruiz, I.; Keukeleire, D. D. 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. DOI: 10.1021/jf071153+.
  • Aberl, A.; Coelhan, M. Determination of Volatile Compounds in Different Hop Varieties by Headspace-Trap GC/MS-in Comparison with Conventional Hop Essential Oil Analysis. J. Agric. Food Chem. 2012, 60, 2785–2792. DOI: 10.1021/jf205002p.
  • Takoi, K. Flavor Hops Varieties and Various Flavor Compounds Contributing to Their “Varietal Aromas”: A Review. Tech. Q. Master Brew. Assoc. Am. 2019, 56, 113–123.
  • Steenackers, B.; De Cooman, L.; De Vos, D. Chemical Transformations of Characteristic Hop Secondary Metabolites in Relation to Beer Properties and the Brewing Process: A Review. Food Chem. 2015, 172, 742–756. DOI: 10.1016/j.foodchem.2014.09.139.
  • Bocquet, L.; Sahpaz, S.; Hilbert, J. L.; Rambaud, C.; Rivière, C. Humulus lupulus L., a Very Popular Beer Ingredient and Medicinal Plant: Overview of Its Phytochemistry, Its Bioactivity, and Its Biotechnology. Phytochem. Rev. 2018, 17, 1047–1090. DOI: 10.1007/s11101-018-9584-y.
  • Okada, Y.; Sugimoto, M.; Ito, K. Molecular Cloning and Expression of Farnesyl Pyrophosphate Synthase Gene Responsible for Essential Oil Biosynthesis in Hop (Humulus lupulus). J. Plant Physiol. 2001, 158, 1183–1188. DOI: 10.1078/S0176-1617(04)70145-5.
  • Pichersky, E.; Lewinsohn, E.; Croteau, R. Purification and Characterization of S-Linalool Synthase, an Enzyme Involved in the Production of Floral Scent in Clarkia breweri. Arch. Biochem. Biophys. 1995, 316, 803–807. DOI: 10.1006/abbi.1995.1107.
  • Tominaga, T.; Des Gachons, C. P.; Dubourdieu, D. A New Type of Flavor Precursors in Vitis vinifera L. cv. Sauvignon Blanc: S-Cysteine Conjugates. J. Agric. Food Chem. 1998, 46, 5215–5219. DOI: 10.1021/jf980481u.
  • Gros, J.; Tran, T. T. H.; Collin, S. Enzymatic Release of Odourant Polyfunctional Thiols from Cysteine Conjugates in Hop. J. Inst. Brew. 2013, 119, 221–227. DOI: 10.1002/jib.80.
  • Kishimoto, T.; Morimoto, M.; Kobayashi, M.; Yako, N.; Wanikawa, A. Behaviors of 3-Mercaptohexan-1-ol and 3-Mercaptohexyl Acetate during Brewing Processes. J. Am. Soc. Brew. Chem. 2008, 66, 192–196. DOI: 10.1094/ASBCJ-2008-0702-01.
  • Darriet, P.; Tominaga, T.; Lavigne, V.; Boidron, J.-N.; Dubourdieu, D. Identification of a Powerful Aromatic Component of Vitis vinifera L. var. Sauvignon Wines: 4-Mercapto-4-Methylpentan-2-One. Flavour Fragr. J. 1995, 10, 385–392. DOI: 10.1002/ffj.2730100610.
  • Roland, A.; Viel, C.; Reillon, F.; Delpech, S.; Boivin, P.; Schneider, R.; Dagan, L. First Identification and Quantification of Glutathionylated and Cysteinylated Precursors of 3-Mercaptohexan-1-ol and 4-Methyl-4-Mercaptopentan-2-One in Hops (Humulus lupulus). Flavour Fragr. J. 2016, 31, 455–463. DOI: 10.1002/ffj.3337.
  • Kishimoto, T.; Kobayashi, M.; Yako, N.; Iida, A.; Wanikawa, A. Comparison of 4-Mercapto-4-Methylpentan-2-One Contents in Hop Cultivars from Different Growing Regions. J. Agric. Food Chem. 2008, 56, 1051–1057. DOI: 10.1021/jf072173e.
  • Lin, J.; Massonnet, M.; Cantu, D. The Genetic Basis of Grape and Wine Aroma. Hortic. Res. 2019, 6–81. DOI: 10.1038/s41438-019-0163-1
  • Kobayashi, H.; Takase, H.; Suzuki, Y.; Tanzawa, F.; Takata, R.; Fujita, K.; Kohno, M.; Mochizuki, M.; Suzuki, S.; Konno, T. Environmental Stress Enhances Biosynthesis of Flavor Precursors, S-3-(Hexan-1-ol)-Glutathione and S-3-(Hexan-1-ol)-L-Cysteine, in Grapevine through Glutathione S-Transferase Activation. J. Exp. Bot. 2011, 62, 1325–1336. DOI: 10.1093/jxb/erq376.
  • Thibon, C.; Cluzet, S.; Mérillon, J. M.; Darriet, P.; Dubourdieu, D. 3-Sulfanylhexanol Precursor Biogenesis in Grapevine Cells: The Stimulating Effect of Botrytis cinerea. J. Agric. Food Chem. 2011, 59, 1344–1351. DOI: 10.1021/jf103915y.
  • Martin, M. Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads. EMBnet. J. 2011, 17, 10–12. DOI: 10.14806/ej.17.1.200.
  • Padgitt-Cobb, L. K.; Kingan, S. B.; Wells, J.; Elser, J.; Kronmiller, B.; Moore, D.; Concepcion, G.; Peluso, P.; Rank, D.; Jaiswal, P.; et al. A Draft Phased Assembly of the Diploid Cascade Hop (Humulus lupulus) Genome. Plant Genome. 2021, 14, e20072. DOI: 10.1002/tpg2.20072.
  • Dobin, A.; Davis, C. A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T. R. STAR: Ultrafast Universal RNA-Seq Aligner. Bioinformatics 2013, 29, 15–21. DOI: 10.1093/bioinformatics/bts635.
  • Pertea, M.; Pertea, G. M.; Antonescu, C. M.; Chang, T. C.; Mendell, J. T.; Salzberg, S. L. StringTie Enables Improved Reconstruction of a Transcriptome from RNA-Seq Reads. Nat. Biotechnol. 2015, 33, 290–295. DOI: 10.1038/nbt.3122.
  • Trapnell, C.; Roberts, A.; Goff, L.; Pertea, G.; Kim, D.; Kelley, D. R.; Pimentel, H.; Salzberg, S. L.; Rinn, J. L.; Pachter, L. Differential Gene and Transcript Expression Analysis of RNA-Seq Experiments with TopHat and Cufflinks. Nat. Protoc. 2012, 7, 562–578. DOI: 10.1038/nprot.2012.016.
  • Love, M. I.; Huber, W.; Anders, S. Moderated Estimation of Fold Change and Dispersion for RNA-Seq Data with DESeq2. Genome Biol. 2014, 15, 550–521. DOI: 10.1186/s13059-014-0550-8.
  • Schwacke, R.; Ponce-Soto, G. Y.; Krause, K.; Bolger, A. M.; Arsova, B.; Hallab, A.; Gruden, K.; Stitt, M.; Bolger, M. E.; Usadel, B. MapMan4: A Refined Protein Classification and Annotation Framework Applicable to Multi-Omics Data Analysis. Mol. Plant. 2019, 12, 879–892. DOI: 10.1016/j.molp.2019.01.003.
  • Luhua, S.; Hegie, A.; Suzuki, N.; Shulaev, E.; Luo, X.; Cenariu, D.; Ma, V.; Kao, S.; Lim, J.; Gunay, M. B.; et al. Linking Genes of Unknown Function with Abiotic Stress Responses by High-Throughput Phenotype Screening. Physiol. Plant. 2013, 148, 322–333., DOI: 10.1111/ppl.12013.
  • Zhang, X.; Gou, M.; Liu, C. J. Arabidopsis Kelch Repeat F-Box Proteins Regulate Phenylpropanoid Biosynthesis via Controlling the Turnover of Phenylalanine Ammonia-Lyase. Plant Cell. 2013, 25, 4994–5010. DOI: 10.1105/tpc.113.119644.
  • Castro, C. B.; Whittock, L. D.; Whittock, S. P.; Leggett, G.; Koutoulis, A. DNA Sequence and Expression Variation of Hop (Humulus lupulus) Valerophenone Synthase (VPS), a Key Gene in Bitter Acid Biosynthesis. Ann. Bot. 2008, 102, 265–273. DOI: 10.1093/aob/mcn089.
  • Gullner, G.; Komives, T.; Király, L.; Schröder, P. Glutathione S-Transferase Enzymes in Plant-Pathogen Interactions. Front. Plant Sci. 2018, 9, 1836. DOI: 10.3389/fpls.2018.01836.
  • Eriksen, R. L.; Padgitt-Cobb, L. K.; Townsend, M. S.; Henning, J. A. Gene Expression for Secondary Metabolite Biosynthesis in Hop (Humulus lupulus L.) Leaf Lupulin Glands Exposed to Heat and Low-Water Stress. Sci. Rep. 2021, 11, 1–18.