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The activity of the artemisinic aldehyde Δ11(13) reductase promoter is important for artemisinin yield in different chemotypes of Artemisia annua L.

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An Erratum to this article was published on 22 May 2015

Abstract

The artemisinic aldehyde double bond reductase (DBR2) plays an important role in the biosynthesis of the antimalarial artemisinin in Artemisia annua. Artemisinic aldehyde is reduced into dihydroartemisinic aldehyde by DBR2. Artemisinic aldehyde can also be oxidized by amorpha-4,11-diene 12-hydroxylase and/or aldehyde dehydrogenase 1 to artemisinic acid, a precursor of arteannuin B. In order to better understand the effects of DBR2 expression on the flow of artemisinic aldehyde into either artemisinin or arteannuin B, we determined the content of dihydroartemisinic aldehyde, artemisinin, artemisinic acid and arteannuin B content of A. annua varieties sorted into two chemotypes. The high artemisinin producers (HAPs), which includes the ‘2/39’, ‘Chongqing’ and ‘Anamed’ varieties, produce more artemisinin than arteannuin B; the low artemisinin producers (LAPs), which include the ‘Meise’, ‘Iran#8’, ‘Iran#14’, ‘Iran#24’ and ‘Iran#47’ varieties, produce more arteannuin B than artemisinin. Quantitative PCR showed that the relative expression of DBR2 was significantly higher in the HAP varieties. We cloned and sequenced the promoter of the DBR2 gene from varieties of both the LAP and the HAP groups. There were deletions/insertions in the region just upstream of the ATG start codon in the LAP varities, which might be the reason for the different promoter activities of the HAP and LAP varieties. The relevance of promoter variation, DBR2 expression levels and artemisinin biosynthesis capabilities are discussed and a selection method for HAP varieties with a DNA marker is suggested. Furthermore, putative cis-acting regulatory elements differ between the HAP and LAP varieties.

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Abbreviations

AA:

Artemisinic acid

AAld:

Artemisinic aldehyde

AB:

Arteannuin B

ABA:

Abscisic acid

ADH1:

Alcohol dehydrogenase 1

ADS:

Amorpha-4,11-diene synthase

bHLH:

Basic/helix-loop-helix

ALDH1:

Aldehyde dehydrogenase 1

AP2:

APETALA2

ART:

Artemisinin

CaMV:

Cauliflower mosaic virus

CPR:

Cytochrome P450 reductase

CYP71AV1:

Amorpha-4,11-diene 12-hydroxylase

DBR2:

Artemisinic aldehyde Δ11(13) reductase

ERF:

Ethylene response factor

DHAA:

Dihydroartemisinic acid

DHAAld:

Dihydroartemisinic aldehyde

FAR:

β-Farnesene

FDS:

Farnesyl diphosphate synthase

GA:

Gibberellinic acid

GSP:

Gene specific primer

GST:

Glandular secretory trichome

HAP:

High artemisinin producer

HMGR:

3-Hydroxy-3-methyl-glutaryl-CoA reductase

IDI:

Isopentenyldiphosphate isomerase

JA:

Jasmonate

LAP:

Low artemisinin producer

MeJA:

Methyl jasmonate

MYB:

MYB transcription factor

OPR:

12-Oxophytodienoate reductase

SA:

Salicylic acid

TSS:

Transcription start site

WRKY:

WRKY transcription factor

References

  • Alam P, Abdin MZ (2011) Over-expression of HMG-CoA reductase and amorpha-4,11-diene synthase genes in Artemisia annua L. and its influence on artemisinin. Plant Cell Rep 30:1919–1928

    Article  CAS  PubMed  Google Scholar 

  • Baldi A, Dixit VK (2008) Yield enhancement strategies for artemisinin production by suspension cultures of Artemisia annua. Biores Technol 99:4609–4614

    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 Reg 63:45–54

    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

    Article  CAS  PubMed  Google Scholar 

  • Boter M, Ruiz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brown GD (2010) The biosynthesis of artemisinin (Qinghaosu) and the phytochemistry of Artemisia annua L. (Qinghao). Molecules 15:7603–7698

    Article  CAS  PubMed  Google Scholar 

  • Brown GD, Sy L-K (2004) In vivo transformations of dihydroartemisinic acid in Artemisia annua plants. Tetrahedron 60:1139–1159

    Article  CAS  Google Scholar 

  • Brown GD, Sy L-K (2006) In vivo transformations of artemisinic acid in Artemisia annua plants. Tetrahedron 60:1139–1159

    Article  Google Scholar 

  • Caretto S, Quarta A, Durante M, Nisi R, De Paolis A, Blando F, Mita G (2011) Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures. Plant Biol 13:51–58

    Article  CAS  PubMed  Google Scholar 

  • Covello PS (2008) Making artemisinin. Phytochemistry 69:2881–2885

    Article  CAS  PubMed  Google Scholar 

  • Covello PS, Teoh KH, Polichuk DR, Reed DW, Nowak G (2007) Functional genomics and the biosynthesis of artemisinin. Phytochemistry 68:1864–1871

    Article  CAS  PubMed  Google Scholar 

  • Duke MV, Paul RN, Elsohly HN, Sturtz G, Duke SO (1994) Localization of artemisinin and artemisitene in foliar tissues of glanded and glandless biotypes of Artemisia annua L. Int J Plant Sci 155:365–372

    Article  Google Scholar 

  • Guom X-X, Yang X-Q, Yang R-Y, Zeng Q-P (2010) Salicylic acid and methyl jasmonate but not Rose Bengal enhance artemisinin production through invoking burst of endogenous singlet oxygen. Plant Sci 178:390–397

    Article  Google Scholar 

  • Han J, Wang H, Lundgren A, Brodelius PE (2014) Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants. Phytochemistry 102:89–96

    Article  CAS  PubMed  Google Scholar 

  • Ji J Xiao, Shen Y, Ma D, Li Z, Pu G, Li X, Huang L, Liu B, Ye H, Wang H (2014) Cloning and characterization of AabHLH1, a bHLH transcription factor that positively regulates artemisinin biosynthesis in Artemisia annua. Plant Cell Physiol 55:1592–1604

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Lu X, Qiu B, Zhang F, Shen Q, Lv Z, Fu X, Yan T, Gao E, Zhu M, Chen L, Zhang L, Wang G, Sun X, Tang K (2014) Molecular cloning and characterization of a trichome-specific promoter of artemisinic aldehyde Δ11(13) reductase (DBR2) in Artemisia annua. Plant Mol Biol Rep 32:82–91

    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 biosynthetic pathway. Biologia 64:319–323

    Article  CAS  Google Scholar 

  • Kim J, Kim HY (2006) Molecular characterization of a bHLH transcription factor involved in Arabidopsis abscisic acid-mediated response. Biochim Biophys Acta 1759:191–194

    Article  CAS  PubMed  Google Scholar 

  • Lei C, Ma D, Pu G, Qiu X, Du Z, Wang H, Li G, Ye H, Liu B (2011) Foliar application of chitosan activates artemisinin biosynthesis in Artemisia annua L. Ind Crops Prod 33:176–182

    Article  CAS  Google Scholar 

  • Lescot M, Déhais P, Moreau Y, De Moor B, Rouzé P, Rombauts S (2002) PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Ma D, Pu G, Lei C, Ma L, Wang H, Guo Y, Chen J, Du Z, Wang H, Li G, Ye H, Liu B (2009a) Isolation and characterization of AaWRKY1, an Artemisia annua transcription factor that regulates the amorpha-4,11-diene synthase gene, a key gene of artemisinin biosynthesis. Plant Cell Physiol 50:2146–2161

    Article  CAS  PubMed  Google Scholar 

  • Ma C, Wang H, Lu X, Wang H, Xu G, Liu B (2009b) Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry. Metabolomics 5:497–506

    Article  CAS  Google Scholar 

  • Maes L, van Nieuwerburgh FCW, Zhang Y, Reed DW, Pollier J, Vande Casteele SRF, Inzé D, Covello PS, Deforce DLD, 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

    Article  CAS  PubMed  Google Scholar 

  • McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7:1015–1026

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miyamoto K, Shimizu T, Lin FQ, Sainsbury F, Thuenemann E, Lomonossoff G, Nojiri H, Yamane H, Okada K (2012) Identification of an E-box motif responsible for the expression of jasmonic acid-induced chitinase gene OsChia4a in rice. J Plant Physiol 169:621–627

    Article  CAS  PubMed  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T et al (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  CAS  PubMed  Google Scholar 

  • Olofsson L, Engström A, Lundgren A, Brodelius EP (2011) Relative epression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol 11:45

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Olofsson L, Lundgren A, Brodelius PE (2012) Trichome isolation with and without fixation using laser microdissection and pressure catapulting followed by RNA amplification: expression of genes of terpene metabolism in apical and sub-apical trichome cells of Artemisia annua L. Plant Sci 183:9–13

    Article  CAS  PubMed  Google Scholar 

  • Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D, Leavell MD, Tai A, Main D, Eng D, Polichuk DR, Teoh KH, Reed DW, Treynor T, Lenihan J, Jiang H, Fleck M, Bajad S, Dang G, Dengrove D, Diola D, Ellens KW, Fickes S, Galazzo J, Gaucher SP, Geistlinger T, Henry R, Hepp M, Horning T, Iqbal T, Jiang H, Kizer L, Lieu B, Melis D, Moss N, Regentin R, Secrest S, Tsuruta H, Vazquez R, Westblade LF, Xu L, Yu M, Zhang Y, Zhao L, Lievense J, Covello PS, Keasling JD, Reiling KK, Renninger NS, Newman JD (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496:528–532

    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 28:1127–1135

    Article  CAS  PubMed  Google Scholar 

  • Putalun W, Luealon W, De-Eknamkul W, Tanaka H, Shoyama Y (2007) Improvement of artemisinin production by chitosan in hairy root cultures of Artemisia annua L. Biotechnol Lett 29:1143–1146

    Article  CAS  PubMed  Google Scholar 

  • RBM/UNITAID/WHO (2011) Artemisinin Conference, Hanoi, Viet Nam, November 2–3, 2011. http://www.mmv.org/sites/default/files/uploads/docs/events/2011/2011_Artemisinin_Conference_Report.pdf

  • Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134:1718–1732

    Article  CAS  PubMed Central  PubMed  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 

  • Sarvestani R, Peyghambary SA, Abbasi A (2014) Isolation and characterization of DBR2 gene promoter from Iranian Artemisia annua. J Agr Sci Tech 16:191–202

    CAS  Google Scholar 

  • Shen QX, Ho THD (1995) Functional dissection of an abscisic-acid (ABA)-inducible gene reveals 2 independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen QX, Zhang PN, Ho THD (1996) Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8:1107–1119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sipahimalani AT, Fulzele DP, Heble MR (1991) Rapid method for the detection and determination of artemisinin by gas chromatography. J Chromatogr A 538:452–455

    Article  CAS  Google Scholar 

  • Solano R, Nieto C, Avila J, Cañas L, Diaz I, Paz-Ares J (1995) Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB. Ph3) from Petunia hybrid. EMBO J 14:1773–1784

    CAS  PubMed Central  PubMed  Google Scholar 

  • Teoh KH, Polichuk DR, Reed DW, Nowak G, Covello PS (2006) Specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett 580:1411–1416

    Article  CAS  PubMed  Google Scholar 

  • Teoh KH, Polichuk DR, Reed DW, Covello PS (2009) Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annua. Botany 87:635–642

    Article  CAS  Google Scholar 

  • Ting H-M, Wang B, Ryden A-M, Woittiez L, van Herpen T, Verstappen FWA, Ruyter-Spira C, Jules Beekwilder J, Bouwmeester HJ, van der Krol A (2013) The metabolite chemotype of Nicotiana benthamiana transiently expressing artemisinin biosynthetic pathway genes is a function of CYP71AV1 type and relative gene dosage. New Phytol 199:352–366

    Article  CAS  PubMed  Google Scholar 

  • Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wallaart TE, Bouwmeester HJ, Hille J, Poppinga L, Maijers NC (2000) Amorpha-4,11-diene synthase: cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin. Planta 212:460–465

    Article  Google Scholar 

  • Wang H, Olofsson L, Lundgren A, Brodelius PE (2011) Trichome-specific expression of amorpha-4,11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L., as reported by a promoter-GUS fusion. Am J Plant Sci 2:619–628

    Article  CAS  Google Scholar 

  • Wang H, Han J, Kanagarajan S, Lundgren A, Brodelius PE (2013) Trichome-specific expression of the amorpha-4,11-diene 12-hydroxylase (cyp71av1) gene, encoding a key enzyme of artemisinin biosynthesis in Artemisia annua, as reported by a promoter-GUS fusion. Plant Mol Biol 81:119–138

    Article  CAS  PubMed  Google Scholar 

  • White NJ (1997) Assessment of the pharmacodynamic properties of antimalarial drugs in vivo. Antimicrob Agents Chemother 47:1413–1422

    Google Scholar 

  • Woerdenbag HJ, Pras N, Bos R, Visser JF, Hendriks H, Malingré TM (1991) Analysis of artemisinin and related sesquiterpenoids from Artemisia annua L. by combined gas chromatography/mass spectrometry. Phytochem Anal 2:215–219

    Article  CAS  Google Scholar 

  • World Health Organization (2014) World Malaria Report 2014 http://www.who.int/malaria/publications/world_malaria_report_2014/en/

  • Wu W, Yuan M, Zhang Q, Zhu YM, Yong L et al (2011) Chemotype-dependent metabolic response to methyl jasmonate elicitation in Artemisia annua. Planta Med 77:1048–1053

    Article  CAS  PubMed  Google Scholar 

  • Xu Y-H, Wang J-W, Wang S, Wang J-Y, Chen X-Y (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-γ-cadinene synthase-A. Plant Physiol 135:507–515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang TB, Poovaiah BW (2001) A calmodulin-binding/CGCG box DNA- binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yuan Y, Liu W, Zhang Q, Xiang L, Liu X, Chen M, Lin Z, Wang Q, Liao Z (2014) Overexpression of artemisinic aldehyde Δ11(13) reductase gene-enhanced artemisinin and its relative metabolite biosynthesis in transgenic Artemisia annua L. Biotechnol Appl Biochem. doi:10.1002/bab.1234

    Google Scholar 

  • Zare Mehrjerdi M, Bihamta M-R, Omidi M, Naghavi M-R, Soltanloo H, Ranjbar M (2013) Effects of exogenous methyl jasmonate and 2-isopentenyladenine on artemisinin production and gene expression in Artemisia annua. Turk J Bot 37:499–505

    Article  CAS  Google Scholar 

  • Zhang YS, Ye HC, Liu BY, Wangand 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

    CAS  Google Scholar 

  • Zhang Y, Teoh KH, Reed DW, Maes L, Goossens A, Olson DJH, Ross ARS, Covello PS (2008) The molecular cloning of artemisinic aldehyde Δ11(13) reductase and its role in glandular trichome-dependent biosynthesis of artemisinin in Artemisia annua. J Biol Chem 283:21501–21508

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Jing F, Li F, Li M, Wang Y, Wang G, Sun X, Tang K (2009) Development of transgenic Artemisia annua (Chinese wormwood) plants with an enhanced content of artemisinin, an effective anti-malarial drug, by hairpin-RNA-mediated gene silencing. Biotechnol Appl Biochem 52:199–207

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Professor Kexuan Tang of Shanghai Jiao Tong University for technical advice and assistance. We also thank Tehran University and Ghent University for providing A. annua seeds. This work was supported by the Faculty of Life and Health Sciences, Linnaeus University.

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Author notes

  1. Rashidi Sajad Monafared

    Present address: Department of Plant Breeding and Biotechnology, Faculty of Agriculture, Tarbiat Modares University, 14115-336, Tehran, Iran

  2. Hongzhen Wang

    Present address: Zhejiang Agriculture and Forestry University, Linan, 311300, Zhejiang, People’s Republic of China

Authors and Affiliations

  1. Department of Chemistry and Biomedical Sciences, Linnaeus University, Kalmar, Sweden

    Ke Yang, Rashidi Sajad Monafared, Hongzhen Wang, Anneli Lundgren & Peter E. Brodelius

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Correspondence to Peter E. Brodelius.

Electronic supplementary material

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11103_2015_284_MOESM1_ESM.pdf

Figure 1S. GC–MS analysis of artemisinin and arteannuin B and their biosynthetic precursors. A: Artemisinin standard showing the thermal breakdown into 3 products; B: Separation of precursors of artemisinin and arteannuin B biosynthesis; C: Separation of artemisinin and arteannuin B (PDF 241 kb)

Figure 2S. Alignment of the nucleotide sequences of the DBR2 and OPR3 cDNA (PDF 15 kb)

11103_2015_284_MOESM3_ESM.pdf

Figure 3S. Nucleotide sequence of the DBR2 gene from the ‘Anamed’ variety of Artemisia annua. UPPERCASE: exons; lowercase: introns (PDF 37 kb)

Figure 4S. Alignment of DBR2 and OPR3 promoters (PDF 24 kb)

11103_2015_284_MOESM5_ESM.pdf

Figure 5S. Alignment of the nucleotide sequences of the 3′-end of the DBR2 promoters amplified by PCR (variable region) (cf. Figure 7). Putative cis-acting regulatory elements are shown in different colours. → indicates that the putative cis-acting element is located to the leading strand; ← indicates that the putative cis-acting element is located to the lagging strand; ↔ indicates that the putative cis-acting element is located to both strands (PDF 76 kb)

11103_2015_284_MOESM6_ESM.pdf

Figure 6S. Alignment of cloned fragment and cDNA and EST sequences from the NBCI GenBank as indicated. The sequences carry the 3′-end of promoters and the 5′-end of the open reading frames. The ATG start codon is marked with *** (PDF 30 kb)

11103_2015_284_MOESM7_ESM.pdf

Figure 7S. Alignment of the conserved nucleotide sequences of the DBR2 promoters amplified by PCR (cf. Figure 5). Putative cis-acting regulatory elements are shown in different colours. → indicates that the putative cis-acting element is located to the leading strand; ← indicates that the putative cis-acting element is located to the lagging strand; ↔ indicates that the putative cis-acting element is located to both strands (PDF 81 kb)

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Supplementary material 9 (DOC 162 kb)

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Yang, K., Monafared, R.S., Wang, H. et al. The activity of the artemisinic aldehyde Δ11(13) reductase promoter is important for artemisinin yield in different chemotypes of Artemisia annua L.. Plant Mol Biol 88, 325–340 (2015). https://doi.org/10.1007/s11103-015-0284-3

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