Developmental regulation of lupulin gland-associated genes in aromatic and bitter hops (Humulus lupulus L.)

. 2021 Nov 13 ; 21 (1) : 534. [epub] 20211113

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34773975
Odkazy

PubMed 34773975
PubMed Central PMC8590222
DOI 10.1186/s12870-021-03292-z
PII: 10.1186/s12870-021-03292-z
Knihovny.cz E-zdroje

BACKGROUND: Hop (Humulus lupulus L.) bitter acids are valuable metabolites for the brewing industry. They are biosynthesized and accumulate in glandular trichomes of the female inflorescence (hop cone). The content of alpha bitter acids, such as humulones, in hop cones can differentiate aromatic from bitter hop cultivars. These contents are subject to genetic and environmental control but significantly correlate with the number and size of glandular trichomes (lupulin glands). RESULTS: We evaluated the expression levels of 37 genes involved in bitter acid biosynthesis and morphological and developmental differentiation of glandular trichomes to identify key regulatory factors involved in bitter acid content differences. For bitter acid biosynthesis genes, upregulation of humulone synthase genes, which are important for the biosynthesis of alpha bitter acids in lupulin glands, could explain the higher accumulation of alpha bitter acids in bitter hops. Several transcription factors, including HlETC1, HlMYB61 and HlMYB5 from the MYB family, as well as HlGLABRA2, HlCYCB2-4, HlZFP8 and HlYABBY1, were also more highly expressed in the bitter hop cultivars; therefore, these factors may be important for the higher density of lupulin glands also seen in the bitter hop cultivars. CONCLUSIONS: Gene expression analyses enabled us to investigate the differences between aromatic and bitter hops. This study confirmed that the bitter acid content in glandular trichomes (lupulin glands) is dependent on the last step of alpha bitter acid biosynthesis and glandular trichome density.

Zobrazit více v PubMed

Mishra AK, Kocábek T, Nath VS, Awasthi PA, Shreshta A, Killi UK, Jakše J, Patzak J, Krofta K, Matoušek J. Dissection of dynamic transcriptome landscape of leaf, bract, and lupulin gland in hop (Humulus lupulus L.) Int J Mol Sci. 2020;21:233. doi: 10.3390/ijms21010233. PubMed DOI PMC

Patzak J, Krofta K, Henychová A, Nesvadba V. Number and size of lupulin glands, glandular trichomes of hop (Humulus lupulus L.), play a key role in contents of bitter acids and polyphenols in hop cone. Int J Food Sci Technol. 2015;50:1864–1872. doi: 10.1111/ijfs.12825. DOI

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;17:1600411. doi: 10.1002/pmic.201600411. PubMed DOI

Clark SM, Vaitheeswaran V, Ambrose SJ, Purves RW, Page JE. 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. PubMed DOI PMC

Xu H, Zhang F, Liu B, Huhman DV, Sumner LW, Dixon RA, 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. PubMed DOI

Okada Y, Ito K. Cloning and analysis of valerophenone synthase gene expressed specifically in lupulin gland of hop (Humulus lupulus L.) Biosci Biotech Biochem. 2001;65:150–155. doi: 10.1271/bbb.65.150. PubMed DOI

Okada K. The biosynthesis of isoprenoids and the mechanisms regulating it in plants. Biosci Biotechnol Biochem. 2011;75:1219–1225. doi: 10.1271/bbb.110228. PubMed DOI

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. DOI

Tsurumaru Y, Sasaki K, Miyawaki T, Uto Y, Momma T, Umemoto N, 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. doi: 10.1016/j.bbrc.2011.11.125. PubMed DOI

Li H, Ban Z, Qin H, Ma L, King AJ, 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. PubMed DOI PMC

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. PubMed DOI PMC

Mishra AK, Duraisamy GS, Khare M, Kocábek T, Jakse J, Bříza J, Patzak J, Sano T, Matoušek J. Genome-wide transcriptome profiling of transgenic hop (Humulus lupulus L.) constitutively overexpressing HlWRKY1 and HlWDR1 transcription factors. BMC Genom. 2018;19:739. doi: 10.1186/s12864-018-5125-8. PubMed DOI PMC

Matoušek J, Kocábek T, Patzak J, Bříza J, Siglová K, Mishra AK, Duraisamy GS, 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. PubMed DOI

Kocábek T, Mishra AK, 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. PubMed DOI

Barth-Haas Group . In: Barth-Haas Hops Companion: A brewer's guide to hop varieties and hop products. 3. Kostelecky T, editor. Yakima: John I. Haas Incorporated; 2016. p. 183.

Sabo J, Kisgeci J, Ikic I. Content of active components in dependence on the number of lupulin glands in the hop cones. Rostlinna Vyroba. 2001;47:201–204.

Srecec S, Zechner-Krpan V, Marag S, Spoljaric I, Kvaternjak I, Mrsic G. Morphogenesis, volume and number of hop (Humulus lupulus L.) glandular trichomes, and their influence on alpha-acid accumulation in fresh bracts of hop cones. Acta Botanica Croatica. 2011;70:1–8. doi: 10.2478/v10184-010-0017-2. DOI

Huchelmann A, Boutry M, Hachez C. Plant glandular Trichomes: natural cell factories of high biotechnological interest. Plant Physiol. 2017;175:6–22. doi: 10.1104/pp.17.00727. PubMed DOI PMC

Schuurink R, Tissier A. Glandular trichomes: micro-organs with model status? New Phytol. 2020;225:2251–2266. doi: 10.1111/nph.16283. PubMed DOI

Hauser MT. Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci. 2014;5:320. doi: 10.3389/fpls.2014.00320. PubMed DOI PMC

Yang C, Li H, Zhang J, Wang T, Ye Z. Fine-mapping of the woolly gene controlling multicellular trichome formation and embryonic development in tomato. Theor Appl Genet. 2011;123:625–633. doi: 10.1007/s00122-011-1612-x. PubMed DOI

Gao S, Gao Y, Xiong C, Yu G, Chang J, Yang Q, Yang C, Ye Z. The tomato B-type cyclin gene, SlCycB2, plays key roles in reproductive organ development, trichome initiation, terpenoids biosynthesis and Prodenia litura defense. Plant Sci. 2017;262:103–114. doi: 10.1016/j.plantsci.2017.05.006. PubMed DOI

Chang J, Yu T, Yang Q, Li C, Xiong C, Gao S, Xie Q, Zheng F, Li H, Tian Z, Yang C, Ye Z. Hair, encoding a single C2H2 zinc-finger protein, regulates multicellular trichome formation in tomato. Plant J. 2018;96:90–102. doi: 10.1111/tpj.14018. PubMed DOI

Xu J, van Herwijnen ZO, Dräger DB, Sui C, Haring MA, Schuurink RC. SlMYC1 regulates type VI glandular Trichome formation and terpene biosynthesis in tomato glandular cells. Plant Cell. 2018;30:2988–3005. doi: 10.1105/tpc.18.00571. PubMed DOI PMC

Yang C, Gao Y, Gao S, Yu G, Xiong C, Chang J, Li H, Ye Z. Transcriptome profile analysis of cell proliferation molecular processes during multicellular trichome formation induced by tomato Wov gene in tobacco. BMC Genomics. 2015;16:e868. doi: 10.1186/s12864-015-2099-7. PubMed DOI PMC

Liu Y, Liu D, Khan AR, Liu B, Wu M, Huang L, Wu J, Song G, Ni H, Ying H, Yu H, Gan Y. NbGIS regulates glandular trichome initiation through GA signaling in tobacco. Plant Mol Biol. 2018;98:153–167. doi: 10.1007/s11103-018-0772-3. PubMed DOI

Yan T, Li L, Xie L, Chen M, Shen Q, Pan Q, Fu X, Shi P, Tang Y, Huang H, Huang Y, Huang Y, Tang K. A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua. New Phytol. 2018;218:567–578. doi: 10.1111/nph.15005. PubMed DOI

Li SF, Milliken ON, Pham H, Seyit R, Napoli R, Preston J, Koltunow AM, Parish RW. The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell. 2009;21:72–89. doi: 10.1105/tpc.108.063503. PubMed DOI PMC

Matías-Hernández L, Jiang W, Yang K, Tang K, Brodelius PE, Pelaz S. AaMYB1 and its orthologue AtMYB61 affect terpene metabolism and trichome development in Artemisia annua and Arabidopsis thaliana. Plant J. 2017;90:520–534. doi: 10.1111/tpj.13509. PubMed DOI

Saddic LA, Huvermann B, Bezhani S, Su Y, Winter CM, Kwon CS, Collum RP, Wagner D. The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expressionof CAULIFLOWER. Development. 2006;133:1673–1682. doi: 10.1242/dev.02331. PubMed DOI

Zhao J-L, Pan J-S, Guan Y, Nie J-T, Yang J-J, Qu M-L, He H-L, Cai R. Transcriptome analysis in Cucumis sativus identifies genes involved in multicellular trichome development. Genomics. 2015;105:296–303. doi: 10.1016/j.ygeno.2015.01.010. PubMed DOI

Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T. Characterization of the class IV homeodomain-leucine zipper gene family in Arabidopsis. Plant Physiol. 2006;141:1363–1375. doi: 10.1104/pp.106.077388. PubMed DOI PMC

Filyushin MA, Slugina MA, Shchennikova AV, Kochieva EZ. Identification and expression analysis of the YABBY1 Gene in wild tomato species. Russ J Genet. 2018;54:536–547. doi: 10.1134/S1022795418050022. DOI

Pesch M, Dartan B, Birkenbihl R, Somssich IE, Hülskamp M. Arabidopsis TTG2 regulates TRY expression through enhancement of activator complex-triggered activation. Plant Cell. 2014;26:4067–4083. doi: 10.1105/tpc.114.129379. PubMed DOI PMC

Peng Y, Thrimawithana AH, Cooney JM, Jensen JD, Espley RV, Allan AC. The proanthocyanin-related transcription factors MYBC1 and WRKY44 regulate branch points in the kiwifruit anthocyanin pathway. Sci Rep. 2020;10:14161. doi: 10.1038/s41598-020-70977-0. PubMed DOI PMC

Li SF, Allen PJ, Napoli RS, Browne RG, Pham H, Parish RW. MYB–bHLH–TTG1 regulates Arabidopsis seed coat biosynthesis pathways directly and indirectly via multiple tiers of transcription factors. Plant Cell Physiol. 2020;61:1005–1018. doi: 10.1093/pcp/pcaa027. PubMed DOI

Jörgens CI, Grünewald N, Hülskamp M, Uhrig JF. A role for ABIL3 in plant cell morphogenesis. Plant J. 2010;62:925–935. PubMed

Padgitt-Cobb LK, Kingan SB, Wells J, Elser J, Kronmiller B, Moore D, et al. A draft phased assembly of the diploid Cascade hop (Humulus lupulus) genome. Plant Genome. 2021:e20072. 10.1002/tpg2.20072. PubMed

Natsume S, Takagi H, Shiraishi A, Murata J, Toyonaga H, Patzak J, Takagi M, Yaegashi H, Uemura A, Mitsuoka C, Yoshida K, Krofta K, Satake H, Terauch R, Ono E. The draft genome of hop (Humulus lupulus), an essence for brewing. Plant Cell Physiol. 2015;56:428–441. doi: 10.1093/pcp/pcu169. PubMed DOI

Hill ST, Sudarsanam R, Henning J, Hendrix D. HopBase: a unified resource for Humulus genomics. Database. 2017, 2017:bax009. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...