Skip to main content

Advertisement

SpringerLink
Log in

Overexpression of the gibberellin 20-oxidase gene from Torenia fournieri resulted in modified trichome formation and terpenoid metabolities of Artemisia annua L.

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

An Erratum to this article was published on 18 July 2017

This article has been updated

Abstract

Gibberellins (GAs) are diterpenoid hormones, control various physiological developments in plants. The role of gibberellins on morphology and secondary metabolite production was examined in Artemisia annua, a medicinal plant that has been acknowledged as a source of artemisinin, an antimalarial compound. Subsequently, the GA20ox gene from Torenia fournieri (TfGA20ox2) was transferred to A. annua by Agrobacterium-mediated transformation. Compared with wild type plants, all nine transgenic plants showed significantly higher plant heights and artemisinin contents. The highest artemisinin content and yield in TfGA20ox2-overexpressing plants was around two-fold higher than wild type. Moreover, transgenic plants had higher numbers of branches (52.4%) and greater branch lengths (60–203%), but smaller leaf size (77.6%). Interestingly, relative to wild type the number and size of glandular trichomes in transgenic leaves was about 30 and 35% higher, respectively. From GC–MS analysis, the proportion of diterpenes in transgenic plant extracts was 1.5-fold lower than those noticed in wild type, while the proportion of sesquiterpenes was increased about 1.6 times when compared to wild type. However, the content proportion of monoterpenes showed a slightly increase, whereas the level of triterpenes showed no variation. In addition, two monoterpenes (eucalyptol and borneol), four sesquiterpenes (α-caryophyllene, β-guaiene, δ-cadinene and β-cubebene) and one triterpenes (isomultiflorenone) were detected only in transgenic extract, whereas d-α-tocopherol, a diterpenoid compound was found only in wild type but not transgenic plant. These results suggested that gibberellins play a significant role in regards to morphology, trichome formation and terpenoid metabolite production in A. annua.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

  • 18 July 2017

    An erratum to this article has been published.

References

  • Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics Int 11(7):36–42

    Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Moinuddin (2011) Optimizing nitrogen levels combined with gibberellic acid for enhanced yield, photosynthetic attributes, enzyme activities, and artemisinin content of Artemisia annua. Front Agric China 5:51–59. doi:10.1007/s11703-011-1065-7

    Article  Google Scholar 

  • Agharkar M, Lomba P, Altpeter F, Zhang H, Kenworthy K, Lange T (2007) Stable expression of AtGA2ox1 in a low-input turfgrass (Paspalum notatum flugge) reduces bioactive gibberellin levels and improves turf quality under field conditions. Plant Biotechnol J 5:791–801. doi:10.1111/j.1467-7652.2007.00284.x

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344. doi:10.1104/pp.109.139352

    Article  PubMed  PubMed Central  Google Scholar 

  • Arsenault PR, Vail D, Wobbe KK, Erickson K, Weathers PJ (2010) Reproductive development modulates gene expression and metabolite levels with possible feedback inhibition of artemisinin in Artemisia annua L. Plant Physiol 154:958–968. doi:10.1104/pp.110.162552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldi A, Dixit VK (2008) Enhanced artemisinin production by cell cultures of Artemisia annua. Curr Trends Biotechnol Pharmacol 2:341–348

    CAS  Google Scholar 

  • Banyai W, Kirdmanee C, Mii M, Supaibulwatana K (2010) Overexpression of farnesyl pyrophosphate synthase (FPS) gene affected artemisinin content and growth of Artemisia annua L. Plant Cell Tissue Organ Cult 103:255–265. doi:10.1007/s11240-010-9775-8

    Article  CAS  Google Scholar 

  • Banyai W, Mii M, Supaibulwatana K (2011) Enhancement of artemisinin content and biomass in Artemisia annua by exogenous GA3 treatment. Plant Growth Regul 63:45–54. doi:10.1007/s10725-010-9510-9

    Article  CAS  Google Scholar 

  • Bertea CM, Freije JR, van der Woude H, Verstappen FW, Perk L, Marquez V, De Kraker JW, Posthumus MA, Jansen BJ, de Groot A, Franssen MC, Bouwmeester HJ (2005) Identification of intermediates and enzymes involved in the early steps of artemisinin biosynthesis in Artemisia annua. Planta Med 71:40–47. doi:10.1055/s-2005-837749

    Article  CAS  PubMed  Google Scholar 

  • Bhakuni RS, Jain DC, Sharma RP, Kumar S (2001) Secondary metabolites of Artemisia annua and their biological activity. Curr Sci 80:35–48

    CAS  Google Scholar 

  • Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800. doi:10.1105/tpc.10.5.791

    Article  PubMed  PubMed Central  Google Scholar 

  • Bose SK, Yadav RK, Mishra S, Sangwan RS, Singh AK, Mishra B, Srivastava AK, Sangwan NS (2013) Effect of gibberellic acid and calliterpenone on plant growth attributes, trichomes, essential oil biosynthesis and pathway gene expression in differential manner in Mentha arvensis L. Plant Physiol Biochem 66:150–158. doi:10.1016/j.plaphy.2013.02.011

    Article  CAS  PubMed  Google Scholar 

  • Brisibe EA, Umoren UE, Brisibe F, Magalhäes PM, Ferreira JFS, Luthria D, Wu X, Prior RL (2009) Nutritional characterisation and antioxidant capacity of different tissues of Artemisia annua L. Food Chem 115:1240–1246. doi:10.1016/j.foodchem.2009.01.033

    Article  CAS  Google Scholar 

  • Carrera E, Jackson SD, Prat S (1999) Feedback control and diurnal regulation of gibberellin 20-oxidase transcript levels in potato. Plant Physiol 119:765–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan KL, Teo CKH, Jinadasa S, Yuen KH (1995) Selection of high artemisinin yielding Artemisia annua. Planta Med 61:285–287

    Article  CAS  PubMed  Google Scholar 

  • Chien JC, Sussex IM (1996) Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol 111:1321–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis IS, Ward DA, Thomas SG, Phillips AL, Davey MR, Power JB, Lowe KC, Croker SJ, Lewis MJ, Magness SL, Hedden P (2000) Induction of dwarfism in transgenic Solanum dulcamara by over-expression of a gibberellin 20-oxidase cDNA from pumpkin. Plant J 23:329–338. doi:10.1046/j.1365-313x.2000.00784.x

    Article  CAS  PubMed  Google Scholar 

  • Czesnick H, Lenhard M (2015) Size control in plants—lessons from leaves and flowers. Cold Spring Harb Perspect Biol 7:a019190. doi:10.1101/cshperspect.a019190

    Article  PubMed  Google Scholar 

  • de Varies PJ, Bich NN, Van Thien H, Hung LN, Ann TK, Kaqer PA, Heisterkamp SH (2000) Combinations of artemisinin and quinine for uncomplicated Falciparum malaria: efficacy and pharmacodynamics. Antimicrob Agents Chemother 44:1302–1308. doi:10.1128/AAC.44.5.1302-1308.2000

    Article  Google Scholar 

  • de Magalhães PM, Dupont I, Hendrickx A, Joly A, Raas T, Dessy S, Sergent T, Schneider YJ (2012) Anti-inflammatory effect and modulation of cytochrome P450 activities by Artemisia annua tea infusions in human intestinal Caco-2 cells. Food Chem 134:864–871. doi:10.1016/j.foodchem.2012.02.195

    Article  Google Scholar 

  • Efferth T, Romero MR, Wolf DG, Stamminger T, Marin JJG, Marschall M (2008) The antiviral activities of artemisinin and artesunate. Clin Infect Dis 47:804–811. doi:10.1086/591195

    Article  CAS  PubMed  Google Scholar 

  • Efferth T, Herrmann F, Tahrani A, Wink M (2011) Cytotoxic activity of secondary metabolites derived from Artemisia annua L. towards cancer cells in comparison to its designated active constituent artemisinin. Phytomedicine 18:959–969. doi:10.1016/j.phymed.2011.06.008

    Article  CAS  PubMed  Google Scholar 

  • Ennajdaoui H, Vachon G, Giacalone C, Besse I, Sallaud C, Herzog M, Tissier A (2010) Trichome specific expression of the tobacco (Nicotiana sylvestris) cembratrien-ol synthase genes is controlled by both activating and repressing cis-regions. Plant Mol Biol 73(6):673–685. doi:10.1007/s11103-010-9648-x

    Article  CAS  PubMed  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788. doi:10.1038/77355

    Article  CAS  PubMed  Google Scholar 

  • Farag MA, Huhman DV, Lei Z, Sumner LW (2007) Metabolic profiling and systematic identification of flavonoids and isoflavonoids in roots and cell suspension cultures of Medicago truncatula using HPLC–UV–ESI–MS and GC–MS. Phytochemistry 68:342–354. doi:10.1016/j.phytochem.2006.10.023

    Article  CAS  PubMed  Google Scholar 

  • Ferreira JFS, Simon JE, Janick J (1995) Developmental studies of Artemisia annua: flowering and artemisinin production under greenhouse and field conditions. Planta Med 61:167–170. doi:10.1055/s-2006-958040

    Article  CAS  PubMed  Google Scholar 

  • Ferreira JFS, Zheljazkov VD, Gonzalez JM (2013) Artemisinin concentration and antioxidant capacity of Artemisia annua distillation byproduct. Ind Crops Prod 41:294–298. doi:10.1016/j.indcrop.2012.05.005

    Article  CAS  Google Scholar 

  • Gomes M, Ribeiro I, Warsame M, Karunajeewa H, Petzold M (2008) Rectal artemisinins for malaria: a review of efficacy and safety from individual patient data in clinical studies. BMC Infect Dis 8:39. doi:10.1186/1471-2334-8-39

    Article  PubMed  PubMed Central  Google Scholar 

  • Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac PG, Khan AM, Larson TR, Li Y, Pawson T, Penfield T, Rae AM, Rathbone DA, Reid S, Ross J, Smallwood MF, Segura V, Townsend T, Vyas D, Winzer T, Bowles D (2010) The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 327:328–331. doi:10.1126/science.1182612

    Article  CAS  PubMed  Google Scholar 

  • Guo XX, Yang XQ, Yang RY, Zeng QP (2010) Salicylic acid and methyl jasmonate but not Rose Bengal enhance artemisinin production through involving burst of endogenous singlet oxygen. Plant Sci 178:390–397. doi:10.1016/j.plantsci.2010.01.014

    Article  CAS  Google Scholar 

  • Hamama L, Naouar A, Gala R, Voisine L, Pierre S, Jeauffre J, Cesbron D, Leplat F, Foucher F, Dorion N, Hibrand-Saint Oyant L (2012) Overexpression of RoDELLA impacts the height, branching, and flowering behaviour of Pelargonium× domesticum transgenic plants. Plant Cell Rep 31:2015–2029. doi:10.1007/s00299-012-1313-1

    Article  CAS  PubMed  Google Scholar 

  • Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530. doi:10.1016/S1360-1385(00)01790-8

    Article  CAS  PubMed  Google Scholar 

  • Inthima P, Otani M, Hirano T, Hayashi Y, Abe T, Nakano M, Supaibulwatana K (2014) Mutagenic effects of heavy-ion beam irradiation on in vitro nodal segments of Artemisia annua L. Plant Cell Tissue Organ Cult 119: 131–139. doi:10.1007/s11240-014-0519-z

    Article  CAS  Google Scholar 

  • Jacobs WP, Case DB (1965) Auxin transport, gibberellin, and apical dominance. Science 148:1729–1731. doi:10.1126/science.148.3678.1729

    Article  CAS  PubMed  Google Scholar 

  • Jaleel CA, Gopi R, Manivannan P, Sankar B, Kishorekumar A, Panneerselvam R (2007) Antioxidant potentials and ajmalicine accumulation in Catharanthus roseus after treatment with giberellic acid. Colloids Surf B 60(2): 195–200. doi:10.1016/j.colsurfb.2007.06.009

    Article  CAS  Google Scholar 

  • Jiang B, Miao H, Chen S, Zhang S, Chen F, Fang W (2010) The Lateral suppressor-like gene, DgLsL, alternated the axillary branching in transgenic Chrysantemum (Chrysantemum× morifolium) by modulating IAA and GA content. Plant Mol Biol Rep 28:144–151. doi:10.1007/s11105-009-0130-3

    Article  CAS  Google Scholar 

  • Jing F, Zhang L, Li M, Tang Y, Wang Y, Wang Y, Wang Q, Pan Q, Wang G, Tang K (2009) Abscisic acid (ABA) treatment increases artemisinin content in Artemisia annua by enhancing the expression of genes in artemisinin biosynthesis pathway. Biologia 64:319–323. doi:10.2478/s11756-009-0040-8

    Article  CAS  Google Scholar 

  • Karaket N, Wiyakrutta S, Lacaille-Dubois MA, Supaibulwatana K (2014) T-DNA insertion alters the terpenoid content composition and bioactivity of transgenic Artemisia annua. Nat Prod Commun 9:363–366

    CAS  PubMed  Google Scholar 

  • Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y, Yamaguchi S (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J Biol Chem 277:45188–45194

    Article  CAS  PubMed  Google Scholar 

  • Kende H, Zeevaart JAD (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210. doi:10.1105/tpc.9.7.1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange BM (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6866–6871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Tian X, Zhang Y, Wang C, Jiang H (2013) The discovery of Artemisia annua L. in the Shengjindian cemetery, Xinjiang, China and its implications for early uses of traditional Chinese herbal medicine qinghao. J Ethnopharmacol 146:278–286. doi:10.1016/j.jep.2012.12.044

    Article  PubMed  Google Scholar 

  • Lommen WJM, Schenk E, Bouwmeester HJ, Verstappen FWA (2006) Trichome dynamics and artemisinin accumulation during development and senescence of Artemisia annua leaves. Planta Med 72:336–345. doi:10.1055/s-2005-91620

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Zhang L, Zhang F, Jiang W, Shen Q, Zhang L, Lv Z, Wang G, Tang K (2013) AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea. New Phytol 198:1191–1202. doi:10.1111/nph.12207

    Article  CAS  PubMed  Google Scholar 

  • Lubbe A, Seibert I, Klimkait T, van der Kooy R (2012) Ethnopharmacology in overdrive: The remarkable anti-HIV activity of Artemisia annua. J Ethnopharmacol 141:854–859. doi:10.1016/j.jep.2012.03.024

    Article  PubMed  Google Scholar 

  • Maes L, Van Nieuwerburgh F, Zhang Y, Reed D, Pollier J, Vande Casteele S, Inze D, Covello P, Deforce DL, Goossens A (2011) Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol 189:176–189. doi:10.1111/j.1469-8137.2010.03466.x

    Article  CAS  PubMed  Google Scholar 

  • Mansouri H, Asrar Z, Amarowicz R (2011) The respose of terpenoids to exogenous gibberellic acid in Cannabis sativa at vegetative stage. Acta Physiol Plant 33:1085–1091. doi:10.1007/s11738-010-0636-1

    Article  CAS  Google Scholar 

  • Merke P, Bengtsson M, Bouwmeester HJ, Maarten A, Posthumus MA, Brodelius P (2000) Molecular cloning, expression, and characterization of amorpha-4,11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L. Arch Biochem Biophys 381:173–180. doi:10.1006/abbi.2000.1962

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-essays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x

    Article  CAS  Google Scholar 

  • Mutasa-Göttgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989. doi:10.1093/jxb/erp040

    Article  PubMed  Google Scholar 

  • Nair P, Misra A, Singh A, Shukla AK, Gupta MM, Gupta AK, Gupta V, Khanuja SP, Shasany AK (2013) Differentially expressed genes during contrasting growth stages of Artemisia annua for artemisinin content. PLoS ONE 8(4):e60375. doi:10.1371/journal.pone.0060375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelissen H, Rymen B, Jikumaru Y, Demuynck K, Van Lijsebettens M, Kamiya Y, Inze´ D, Beemster GT (2012) A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr Biol 22:1183–1187. doi:10.1016/j.cub.2012.04.065

    Article  CAS  PubMed  Google Scholar 

  • Niki T, Nishijima T, Nakayama M, Hisamatsu T, Oyama-Okubo N, Yamazaki H, Hedden P, Lange T, Mander LN, Koshioka M (2001) Production of dwarf lettuce by overexpressing a pumpkin gibberellin 20-oxidase gene. Plant Physiol 126:965–972. doi:10.1104/pp.126.3.965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oikawa T, Koshioka M, Kojima K, Yoshida H, Kawata M (2004) A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice. Plant Mol Biol 55:687–700. doi:10.1007/s11103-004-1692-y

    Article  CAS  PubMed  Google Scholar 

  • Olofsson L, Engstrom A, Lundgren A, Brodelius PE (2011) Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol 11:45. doi:10.1186/1471-2229-11-45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsson ME, Olofsson LM, Lindahl AL, Lundgren A, Brodelius M, Brodelius PE (2009) Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular trichomes of Artemisia annua L. Phytochemistry 70:1123–1128. doi:10.1016/j.phytochem.2009.07.009

    Article  CAS  PubMed  Google Scholar 

  • Otani M, Meguro S, Gondaira H, Hayashi M, Saito M, Han DS, Mori S, Li T, Niki T, Nishijima T, Koshioka M, Nakano M (2014) Overexpression of the gibberellin 20-oxidase or gibberellin 3-oxidase gene from Torenia fournieri affecting plant morphology in transgenic Tricyrtis sp. Acta Hortic (ISHS) 1025:23–30. http://www.actahort.org/books/1025/1025_2.htm

  • Pansuksan K, Sangthong R, Nakamura I, Mii M, Supaibulwatana K (2014) Tetraploid induction of Mitracarpus hirtus L. by colchicine and its characterization including antibacterial activity. Plant Cell Tissue Organ Cult 117(3):381–391. doi:10.1007/s11240-014-0447-y

    Article  CAS  Google Scholar 

  • Perazza D, Vachon G, Herzog M (1998) Gibberellins promote trichome formation by up regulating GLABROUS1 in Arabidopsis. Plant Physiol 117:375–383. doi:10.1104/pp.117.2.375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polichuk DR, Zhang Y, Reed DW, Schmidt JF, Covello PS (2010) A glandular trichome-specific monoterpene alcohol dehydrogenase from Artemisia annua. Phytochemistry 71:1264–1269. doi:10.1016/j.phytochem.2010.04.026

    Article  CAS  PubMed  Google Scholar 

  • Pu GB, Ma DM, Chen JL, Ma LQ, Wang H, Li GF, Ye HC, Liu BY (2009) Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 7:1127–1135. doi:10.1007/s00299-009-0713-3

    Article  Google Scholar 

  • Ram M, Khan MA, Jha P, Khan S, Kiran U, Ahmad MM, Javed S, Abdin MZ (2010) HMG-CoA reductase limits artemisinin biosynthesis and accumulation in Artemisia annua L. plants. Acta Physiol Plant 32:859–866. doi:10.1007/s11738-010-0470-5

    Article  CAS  Google Scholar 

  • Romero MR, Efferth T, Serrano MA, Macias RI, Briz O, Marin JJ (2005) Effect of artemisinin/artesunate as inhibitors of hepatitis B virus production in an “in vitro” replicative system. Antivir Res 68:75–83. doi:10.1016/j.antiviral.2005.07.005

    Article  CAS  PubMed  Google Scholar 

  • Ross JJ, MacKenzie-Hose AK, Davies P, Lester DR, Twitchin B, Reid JB (1999) Further evidence for feedback regulation of gibberellin biosynthesis in pea. Physiol Plant 105:532–538. doi:10.1034/j.1399-3054.1999.105319.x

    Article  CAS  Google Scholar 

  • Ross JJ, O’Neill DP, Smith JJ, Huub L, Kerckhoffs J, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis. Plant J 21:547–552. doi:10.1046/j.1365-313x.2000.00702.x

    Article  CAS  PubMed  Google Scholar 

  • Ruddat M, Pharis RP (1966) Participation of gibberellin in the control of apical dominance in soybean and redwood. Planta 71:222–228. doi:10.1007/BF00384884

    Article  CAS  PubMed  Google Scholar 

  • Schmiderer C, Grausgruber-Gröger S, Grassi P, Steinborn R, Novak J (2010) Influence of gibberellin and daminozide on the expression of terpene synthases in common sage (Salvia officinalis). J Plant Physiol 167:779–786. doi:10.1016/j.jplph.2009.12.009

    Article  CAS  PubMed  Google Scholar 

  • Scott TK, Case DB, Jacobs WP (1967) Auxin-gibberellin interaction in apical dominance. Plant Physiol 42:1329–1333. doi:10.1104/pp.42.10.1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverstone AL, Mak PY, Martinez EC, Sun TP (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146:1087–1099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh NP, Ferreira JFS, Park JS, Lai HC (2011) Cytotoxicity of ethanolic extracts of Artemisia annua to Molt-4 human leukemia cells. Planta Med 77:1788–1793. doi:10.1055/s-0030-1271157

    Article  CAS  PubMed  Google Scholar 

  • Smith TC, Weathers PJ, Cheetham RD (1997) Effects of gibberellic acid on hairy root cultures of Artemisia annua: growth and artemisinin production. In Vitro Cell Dev Biol 33: 75–79. doi:10.1007/s11627-997-0044-4

    Article  CAS  Google Scholar 

  • Soetaert SS, Van Neste CM, Vandewoestyne ML, Head SR, Goossens A, Van Nieuwerburgh FC Deforce DL (2013) Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua. BMC Plant Biol 13:220

    Article  PubMed  PubMed Central  Google Scholar 

  • Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048. doi:10.1073/pnas.132266399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subbaraj A, Funnell K, Woolley D (2010) Dormancy and flowering are regulated by the reciprocal interaction between cytokinin and gibberellin in Zantedeschia. J Plant Growth Regul 29(4):487–499. doi:10.1007/s00344-010-9160-1

    Article  CAS  Google Scholar 

  • Sultana S, Hu H, Gao L, Mao J, Luo J, Jongsma MA, Wang C (2015) Molecular cloning and characterization of the trichome specific chrysanthemyl diphosphate/chrysanthemol synthase promoter from Tanacetum cinerariifolium. Sci Hortic 185:193–199. doi:10.1016/j.scienta.2015.01.032

    Article  CAS  Google Scholar 

  • Tan H, Xiao L, Gao S, Li Q, Chen J, Xiao Y, Ji Q, Chen R, Chen W, Zhang L (2015) Trichome and artemisinin regulator 1 is required for trichome development and artemisinin biosynthesis in Artemisia annua. Mol Plant 8(9):1396–1411. doi:10.1016/j.molp.2015.04.002

    Article  CAS  PubMed  Google Scholar 

  • Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675. doi:10.1105/tpc.105.035766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thimann KV, Skoog F (1933) Studies on the growth hormone of plants: III. The inhibiting action of the growth hormone on bud development. Proc Natl Acad Sci USA 19:714–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas SG, Sun TP (2004) Update on gibberellin signaling. A tale of the tall and the short. Plant Physiol 135:668–676. doi:10.1104/pp.104.040279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Towler MJ, Weathers PJ (2007) Evidence of artemisinin production from IPP stemming from both the mevalonate and the nonmevalonate pathways. Plant Cell Rep 26:2129–2136. doi:10.1007/s00299-007-0420-x

    Article  CAS  PubMed  Google Scholar 

  • Tu YY (2011) The discovery of artemisinin (qinghaosu) and gifts from Chinese medicine. Nat med 17:1217–1220. doi:10.1038/nm.2471

    Article  CAS  PubMed  Google Scholar 

  • Vidal AM, Gisbert C, Talón M, Primo-Millo E, López-Díaz I, García-Martínez JL (2001) The ectopic overexpression of a citrus gibberellin 20-oxidase alters the gibberellin content and induces an elongated phenotype in tobacco. Physiol Plant 112:251–260. doi:10.1034/j.1399-3054.2001.1120214.x

    Article  CAS  PubMed  Google Scholar 

  • Wang E, Gan S, Wagner GJ (2002) Isolation and characterization of the CYP71D16 trichome-specific promoter from Nicotiana tabacum L. J Exp Bot 53(376):1891–1897. doi:10.1093/jxb/erf054

    Article  CAS  PubMed  Google Scholar 

  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408. doi:10.1104/pp.100.1.403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu GS, Lu JJ, Guo JJ, Huang MQ, Gan L, Chen XP, Wang YT (2013) Synergistic anti-cancer activity of the combination of dihydroartemisinin and doxorubicin in breast cancer cells. Pharmacol Rep 65:453–459. doi:10.1016/S1734-1140(13)71021-1

    Article  CAS  PubMed  Google Scholar 

  • Xiao YH, Li DM, Yin MH, Li XB, Zhang M, Wang YJ, Dong J, Zhao J, Luo M, Luo XY, Hou L, Hu L, Pei Y (2010) Gibberellin 20-oxidase promotes initiation and elongation of cotton fibers by regulating gibberellin synthesis. J Plant Physiol 167:829–837. doi:10.1016/j.jplph.2010.01.003

    Article  CAS  PubMed  Google Scholar 

  • Xu YL, Li L, Gage DA, Zeevaart JA (1999) Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis. Plant Cell 11:927–935. doi:10.1105/tpc.11.5.927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav RK, Sangwan RS, Sabir F, Srivastava AK, Sangwan NS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol Biochem 74:70–83. doi:10.1016/j.plaphy.2013.10.023

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. doi:10.1146/annurev.arplant.59.032607.092804

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Pan S, Fan G, Dong L, Ren J, Zhu Y (2015) Evaluation of volatile profile of Sichuan dongcai, a traditional salted vegetable, by SPME–GC–MS and E-nose. LWT—Food Sci Technol 64: 528–535. doi:10.1016/j.lwt.2015.06.063

    CAS  Google Scholar 

  • Yu ZX, Li JX, Yang CQ, Hu WL, Wang LJ, Chen XY (2012) The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol Plant 5:353–365. doi:10.1093/mp/ssr087

    Article  CAS  PubMed  Google Scholar 

  • Zhang YS, Ye HC, Liu BY, Wang H, Li GF (2005) Exogenous GA3 and flowering induce the conversion of artemisinic acid to artemisinin in Artemisia annua plants. Russ J Plant Physiol 52:58–62. doi:10.1007/s11183-005-0009-6

    Article  CAS  Google Scholar 

  • Zhang L, Lu X, Shen Q, Chen Y, Wang T, Zhang F, Wu S, Jiang W, Liu P, Zhang L, Wang Y, Tang K (2012) Identification of putative Artemisia annua ABCG transporter unigenes related to artemisinin yield following expression analysis in different plant tissues and in response to methyl jasmonate and abscisic acid treatments. Plant Mol Biol Report 4:838–847. doi:10.1007/s11105-011-0400-8

    Article  Google Scholar 

  • Zhou Z, Sun L, Zhao Y, An L, Yan A, Meng X, Gan Y (2013) Zinc finger protein 6 (ZFP6) regulates trichome initiation by integrating gibberellin and cytokinin signaling in Arabidopsis thaliana. New Phytol 198:699–708. doi:10.1111/nph.12211

    Article  CAS  PubMed  Google Scholar 

  • Zwenger S, Basu C (2008) Plant terpenoids: applications and potentials. Biotechnol Mol Biol Rev 3:1–7

    Google Scholar 

Download references

Acknowledgements

This work got financially supported by the Faculty of Science, Mahidol University (MU), Kingdom of Thailand. We also acknowledge the partial financial assistance from the Graduate School of Science and Technology, Niigata University (NU), Japan that supported through the Global Circus Project for PhD Double Degree Program between NU and MU. The authors would like to express thankfulness to the Office of the Higher Education Commission, Thailand to providing scholarship of the “Strategic Scholarships for Frontier Research Network program for the Joint Ph.D. Program Thai Doctoral degree” for P. Inthima. The Manuscript was kindly proofed by Dr. Christopher B. Smith, Faculty of Science, Mahidol University, Thailand.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Faculty of Science, Mahidol University, 272 Rama VI Road, Ratchathewi District, Bangkok, 10400, Thailand

    Phithak Inthima & Kanyaratt Supaibulwatana

  2. Faculty of Agriculture, Niigata University, 2-8050 Ikarashi, Niigata, 950-2181, Japan

    Phithak Inthima, Masaru Nakano & Masahiro Otani

  3. National Institute of Floricultural Science, 2-1 Fujimoto, Tsukuba, 305-8519, Japan

    Tomoya Niki & Takaaki Nishijima

  4. College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, 252-0880, Japan

    Masaji Koshioka

Authors
  1. Phithak Inthima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masaru Nakano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masahiro Otani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomoya Niki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takaaki Nishijima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Masaji Koshioka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kanyaratt Supaibulwatana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kanyaratt Supaibulwatana.

Additional information

An erratum to this article is available at https://doi.org/10.1007/s11240-017-1269-5.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Inthima, P., Nakano, M., Otani, M. et al. Overexpression of the gibberellin 20-oxidase gene from Torenia fournieri resulted in modified trichome formation and terpenoid metabolities of Artemisia annua L.. Plant Cell Tiss Organ Cult 129, 223–236 (2017). https://doi.org/10.1007/s11240-017-1171-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-017-1171-1

Keywords

Search

Navigation