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Artemisia annua L. (Asteraceae) trichome‐specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin

Keat H. Teoh

Plant Biotechnology Institute, 110 Gymnasium Place, Saskatoon, Sask., Canada S7N OW9

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Devin R. Polichuk

Plant Biotechnology Institute, 110 Gymnasium Place, Saskatoon, Sask., Canada S7N OW9

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Darwin W. Reed

Plant Biotechnology Institute, 110 Gymnasium Place, Saskatoon, Sask., Canada S7N OW9

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Goska Nowak

Plant Biotechnology Institute, 110 Gymnasium Place, Saskatoon, Sask., Canada S7N OW9

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Patrick S. Covello

Corresponding Author

E-mail address:Patrick.Covello@nrc-cnrc.gc.ca

Plant Biotechnology Institute, 110 Gymnasium Place, Saskatoon, Sask., Canada S7N OW9

Corresponding author. Fax: +1 306 975 4839.
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First published: 30 January 2006
Cited by: 191

Abstract

Artemisinin, a sesquiterpene lactone endoperoxide derived from the plant Artemisia annua, forms the basis of the most important treatments of malaria in use today. In an effort to elucidate the biosynthesis of artemisinin, an expressed sequence tag approach to identifying the relevant biosynthetic genes was undertaken using isolated glandular trichomes as a source of mRNA. A cDNA clone encoding a cytochrome P450 designated CYP71AV1 was characterized by expression in Saccharomyces cerevisiae and shown to catalyze the oxidation of the proposed biosynthetic intermediates amorpha‐4,11‐diene, artemisinic alcohol and artemisinic aldehyde. The identification of the CYP71AV1 gene should allow for the engineering of semi‐synthetic production of artemisinin in appropriate plant or microbial hosts.

Number of times cited: 191

  • , Expression of artemisinin biosynthesis and trichome formation genes in five Artemisia species, Industrial Crops and Products, 112, (130), (2018).
  • , Plant secretory structures: more than just reaction bags, Current Opinion in Biotechnology, 49, (73), (2018).
  • , Harnessing Plant Trichome Biochemistry for the Production of Useful Compounds, Molecular Pharming, (353-382), (2018).
  • , Overexpression of a type‐I isopentenyl pyrophosphate isomerase of Artemisia annua in the cytosol leads to high arteannuin B production and artemisinin increase, The Plant Journal, 91, 3, (466-479), (2017).
  • , Identification of a drimenol synthase and drimenol oxidase from Persicaria hydropiper, involved in the biosynthesis of insect deterrent drimanes, The Plant Journal, 90, 6, (1052-1063), (2017).
  • , AaMYB1 and its orthologue AtMYB61 affect terpene metabolism and trichome development in Artemisia annua and Arabidopsis thaliana, The Plant Journal, 90, 3, (520-534), (2017).
  • , , Angewandte Chemie, 129, 15, (4411-4415), (2017).
  • , An Efficient Chemoenzymatic Synthesis of Dihydroartemisinic Aldehyde, Angewandte Chemie International Edition, 56, 15, (4347-4350), (2017).
  • , Molecular cloning and characterization of the promoter of aldehyde dehydrogenase gene from Artemisia annua, Biotechnology and Applied Biochemistry, 64, 6, (902-910), (2017).
  • , Progress in terpene synthesis strategies through engineering of Saccharomyces cerevisiae , Critical Reviews in Biotechnology, 10.1080/07388551.2017.1299679, 37, 8, (974-989), (2017).
  • , Effects of different doses of cadmium on secondary metabolites and gene expression in Artemisia annua L., Frontiers of Medicine, 11, 1, (137), (2017).
  • , Promotion of artemisinin content in Artemisia annua by overexpression of multiple artemisinin biosynthetic pathway genes, Plant Cell, Tissue and Organ Culture (PCTOC), 129, 2, (251), (2017).
  • , Multienzyme Biosynthesis of Dihydroartemisinic Acid, Molecules, 22, 9, (1422), (2017).
  • , Amalgamation of Synthetic Biology and Chemistry for High-Throughput Nonconventional Synthesis of the Antimalarial Drug Artemisinin, Organic Process Research & Development, 10.1021/acs.oprd.6b00414, 21, 4, (551-558), (2017).
  • , Artemisinin the Nobel Molecule, , 10.1016/B978-0-444-63931-8.00005-9, (193-229), (2017).
  • , A Review of Biotechnological Artemisinin Production in Plants, Frontiers in Plant Science, 8, (2017).
  • , The molecular basis of glandular trichome development and secondary metabolism in plants, Plant Gene, 12, (1), (2017).
  • , Metabolic Engineering of Artemisia annua L., From Artemisia Annua L. to Artemisinins, 10.1016/B978-0-12-811655-5.00008-8, (163-208), (2017).
  • , Glandular trichome-specific expression of alcohol dehydrogenase 1 (ADH1) using a promoter-GUS fusion in Artemisia annua L., Plant Cell, Tissue and Organ Culture (PCTOC), 130, 1, (61), (2017).
  • , GLANDULAR TRICHOME‐SPECIFIC WRKY 1 promotes artemisinin biosynthesis in Artemisia annua, New Phytologist, 214, 1, (304-316), (2016).
  • , One‐Pot, Two‐Step Hydroxylation of the Macrocyclic Diterpenoid β‐Cembrenediol Catalyzed by P450 BM3 Mutants, ChemCatChem, 8, 24, (3755-3761), (2016).
  • , T‐shaped trichome‐specific expression of monoterpene synthase ADH2 using promoter–β‐GUS fusion in transgenic Artemisia annua L., Biotechnology and Applied Biochemistry, 63, 6, (834-840), (2015).
  • , The jasmonate‐responsive AaMYC2 transcription factor positively regulates artemisinin biosynthesis in Artemisia annua, New Phytologist, 210, 4, (1269-1281), (2016).
  • , Improvement of betulinic acid biosynthesis in yeast employing multiple strategies, BMC Biotechnology, 16, 1, (2016).
  • , Overexpression ofAaWRKY1Leads to an Enhanced Content of Artemisinin inArtemisia annua, BioMed Research International, 2016, (1), (2016).
  • , Branch Pathway Blocking inArtemisia annuais a Useful Method for Obtaining High Yield Artemisinin, Plant and Cell Physiology, 57, 3, (588), (2016).
  • , Overexpression of a Novel NAC Domain-Containing Transcription Factor Gene ( AaNAC1 ) Enhances the Content of Artemisinin and Increases Tolerance to Drought and Botrytis cinerea in Artemisia annua , Plant and Cell Physiology, 10.1093/pcp/pcw118, 57, 9, (1961-1971), (2016).
  • , Sesquiterpene lactone engineering in microbial and plant platforms: parthenolide and artemisinin as case studies, Applied Microbiology and Biotechnology, 100, 3, (1041), (2016).
  • , Cloning and Characterization of a Flavonoid 3′-Hydroxylase Gene from Tea Plant (Camellia sinensis), International Journal of Molecular Sciences, 17, 12, (261), (2016).
  • , Localization of sesquiterpene lactone biosynthesis in cells of capitate glandular trichomes of Helianthus annuus (Asteraceae), Protoplasma, 253, 2, (447), (2016).
  • , Artemisinin biosynthesis in Artemisia annua and metabolic engineering: questions, challenges, and perspectives, Phytochemistry Reviews, 15, 6, (1093), (2016).
  • , Elucidation of the biosynthesis of carnosic acid and its reconstitution in yeast, Nature Communications, 7, (12942), (2016).
  • , Plant cytochrome P450s: nomenclature and involvement in natural product biosynthesis, Protoplasma, 10.1007/s00709-015-0884-4, 253, 5, (1197-1209), (2015).
  • , Advances in Molecular Regulation of Artemisinin Biosynthesis, Botanical Research, 05, 03, (113), (2016).
  • , Artemisia annua glandular secretory trichomes: the biofactory of antimalarial agent artemisinin, Science Bulletin, 61, 1, (26), (2016).
  • , Cellular engineering of Artemisia annua and Artemisia dubia with the rol ABC genes for enhanced production of potent anti-malarial drug artemisinin, Malaria Journal, 15, 1, (2016).
  • , Transcriptional regulation of artemisinin biosynthesis in Artemisia annua L., Science Bulletin, 61, 1, (18), (2016).
  • , Root regulation of artemisinin production in Artemisia annua: trichome and metabolite evidence, Planta, 244, 5, (999), (2016).
  • , Recent advances in biosynthesis of bioactive compounds in traditional Chinese medicinal plants, Science Bulletin, 61, 1, (3), (2016).
  • , Molecular Farming in Artemisia annua, a Promising Approach to Improve Anti-malarial Drug Production, Frontiers in Plant Science, 7, (2016).
  • , Characterization of a trichome-specific promoter of the aldehyde dehydrogenase 1 (ALDH1) gene in Artemisia annua, Plant Cell, Tissue and Organ Culture (PCTOC), 126, 3, (469), (2016).
  • , Sesquiterpene Lactones: More Than Protective Plant Compounds With High Toxicity, Critical Reviews in Plant Sciences, 35, 1, (18), (2016).
  • , Transient production of artemisinin in Nicotiana benthamiana is boosted by a specific lipid transfer protein from A. annua, Metabolic Engineering, 38, (159), (2016).
  • , Artemisinin-based antimalarial research: application of biotechnology to the production of artemisinin, its mode of action, and the mechanism of resistance of Plasmodium parasites, Journal of Natural Medicines, 10.1007/s11418-016-1008-y, 70, 3, (318-334), (2016).
  • , Functional Analysis of Amorpha-4,11-Diene Synthase (ADS) Homologs from Non-Artemisinin-ProducingArtemisiaSpecies: The Discovery of Novel Koidzumiol and (+)-α-Bisabolol Synthases, Plant and Cell Physiology, 57, 8, (1678), (2016).
  • , Artemisia annuamutant impaired in artemisinin synthesis demonstrates importance of nonenzymatic conversion in terpenoid metabolism, Proceedings of the National Academy of Sciences, 113, 52, (15150), (2016).
  • , Metabolic engineering and synthetic biology of plant secondary metabolism, Plant Specialized Metabolism, 10.1201/9781315370453-14, (315-360), (2016).
  • , Overexpression of artemisinic aldehyde Δ11 (13) reductase gene–enhanced artemisinin and its relative metabolite biosynthesis in transgenic rtemisia annua L., Biotechnology and Applied Biochemistry, 62, 1, (17-23), (2014).
  • , Biosynthesis of the Diterpenoid Lycosantalonol via Nerylneryl Diphosphate in Solanum lycopersicum, PLOS ONE, 10, 3, (e0119302), (2015).
  • , Genetic Transformation of Artemisia carvifolia Buch with rol Genes Enhances Artemisinin Accumulation, PLOS ONE, 10, 10, (e0140266), (2015).
  • , A Basic Leucine Zipper Transcription Factor, AabZIP1, Connects Abscisic Acid Signaling with Artemisinin Biosynthesis in Artemisia annua, Molecular Plant, 8, 1, (163), (2015).
  • , Comparative profiling and dynamics of artemisinin related metabolites using efficient protocol and expression of biosynthetic pathway genes during developmental span of two elite varieties of Artemisia annua L, Journal of Plant Biochemistry and Biotechnology, 24, 2, (167), (2015).
  • , Genetic engineering of artemisinin biosynthesis: prospects to improve its production, Acta Physiologiae Plantarum, 10.1007/s11738-015-1771-5, 37, 2, (2015).
  • , The activity of the artemisinic aldehyde Δ11(13) reductase promoter is important for artemisinin yield in different chemotypes of Artemisia annua L., Plant Molecular Biology, 88, 4-5, (325), (2015).
  • , Enhanced artemisinin yield by expression of rol genes in Artemisia annua, Malaria Journal, 14, 1, (2015).
  • , The Application of Synthetic Biology to Elucidation of Plant Mono-, Sesqui-, and Diterpenoid Metabolism, Molecular Plant, 8, 1, (6), (2015).
  • , Expression of artemisinin biosynthesis genes in eight Artemisia species at three developmental stages, Industrial Crops and Products, 76, (836), (2015).
  • , TRICHOME AND ARTEMISININ REGULATOR 1 Is Required for Trichome Development and Artemisinin Biosynthesis in Artemisia annua, Molecular Plant, 8, 9, (1396), (2015).
  • , Understanding of real alternative redox partner of Streptomyces peucetius DoxA: Prediction and validation using in silico and in vitro analyses, Archives of Biochemistry and Biophysics, 585, (64), (2015).
  • , Plant Omics: Isolation, Identification, and Expression Analysis of Cytochrome P450 Gene Sequences fromColeus forskohlii, OMICS: A Journal of Integrative Biology, 19, 12, (782), (2015).
  • , Promoters ofAaGL2andAaMIXTA-Like1genes ofArtemisia annuadirect reporter gene expression in glandular and non-glandular trichomes, Plant Signaling & Behavior, 10, 12, (e1087629), (2015).
  • , A Genome-Wide Scenario of Terpene Pathways in Self-pollinated Artemisia annua, Molecular Plant, 8, 11, (1580), (2015).
  • , Proteomic analysis of Artemisia annua – towards elucidating the biosynthetic pathways of the antimalarial pro-drug artemisinin, BMC Plant Biology, 15, 1, (2015).
  • , Cytochrome P450-enzymes involved in the biosynthesis of mono- and sesquiterpenes, Phytochemistry Reviews, 10.1007/s11101-013-9280-x, 14, 1, (7-24), (2013).
  • , Research progress relating to the role of cytochrome P450 in the biosynthesis of terpenoids in medicinal plants, Applied Microbiology and Biotechnology, 98, 6, (2371), (2014).
  • , Molecular Cloning and Characterization of a Trichome-Specific Promoter of Artemisinic Aldehyde Δ11(13) Reductase (DBR2) in Artemisia annua, Plant Molecular Biology Reporter, 32, 1, (82), (2014).
  • , Inducing Effect of Dihydroartemisinic Acid in the Biosynthesis of Artemisinins with Cultured Cells ofArtemisia annuaby Enhancing the Expression of Genes, The Scientific World Journal, 2014, (1), (2014).
  • , Valencene oxidase CYP706M1 from Alaska cedar (Callitropsis nootkatensis), FEBS Letters, 588, 6, (1001), (2014).
  • , 7-Deoxyloganetic acid synthase catalyzes a key 3 step oxidation to form 7-deoxyloganetic acid in Catharanthus roseus iridoid biosynthesis, Phytochemistry, 101, (23), (2014).
  • , Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L., Plant Physiology and Biochemistry, 74, (70), (2014).
  • , Functional analysis of orthologous artemisinic aldehyde Δ11(13)-reductase reveals potential artemisinin-producing activity in non-artemisinin-producing Artemisia absinthium, Plant Biotechnology, 31, 5, (483), (2014).
  • , Brassica villosa, a system for studying non-glandular trichomes and genes in the Brassicas, Plant Molecular Biology, 85, 4-5, (519), (2014).
  • , Cytochrome P450-mediated metabolic engineering: current progress and future challenges, Current Opinion in Plant Biology, 10.1016/j.pbi.2014.03.004, 19, (27-34), (2014).
  • , Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants, Phytochemistry, 102, (89), (2014).
  • , Transgenic approach to increase artemisinin content in Artemisia annua L., Plant Cell Reports, 33, 4, (605), (2014).
  • , Cloning and Characterization of AabHLH1, a bHLH Transcription Factor that Positively Regulates Artemisinin Biosynthesis in Artemisia annua, Plant and Cell Physiology, 55, 9, (1592), (2014).
  • , Modulation of artemisinin biosynthesis by elicitors, inhibitor, and precursor in hairy root cultures of Artemisia annua L. , Journal of Plant Interactions, 10.1080/17429145.2014.949885, 9, 1, (811-824), (2014).
  • , Studies on the expression of linalool synthase using a promoter-β-glucuronidase fusion in transgenic Artemisia annua, Journal of Plant Physiology, 171, 2, (85), (2014).
  • , Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes—current status and future opportunities, Plant Biotechnology Journal, 11, 2, (169-196), (2012).
  • , Terpenoid biosynthesis in trichomes—current status and future opportunities, Plant Biotechnology Journal, 11, 1, (2-22), (2012).
  • , a, a trichome‐specific AP2/ERF transcription factor of rtemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to otrytis cinerea, New Phytologist, 198, 4, (1191-1202), (2013).
  • , The metabolite chemotype of icotiana benthamiana transiently expressing artemisinin biosynthetic pathway genes is a function of 711 type and relative gene dosage, New Phytologist, 199, 2, (352-366), (2013).
  • , Plant P450s as versatile drivers for evolution of species-specific chemical diversity, Philosophical Transactions of the Royal Society B: Biological Sciences, 10.1098/rstb.2012.0426, 368, 1612, (20120426-20120426), (2013).
  • , Expression and Localization of Amorpha-4,11-diene Synthase in Artemisia annua L., Plant Molecular Biology Reporter, 31, 1, (32), (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 Molecular Biology, 81, 1-2, (119), (2013).
  • , Metabolic engineering and in vitro biosynthesis of phytochemicals and non-natural analogues, Plant Science, 10.1016/j.plantsci.2013.05.005, 210, (10-24), (2013).
  • , Promotion of artemisinin biosynthesis in transgenic Artemisia annua by overexpressing ADS, CYP71AV1 and CPR genes, Industrial Crops and Products, 49, (380), (2013).
  • , Arsenic, chromium and NaCl induced artemisinin biosynthesis in Artemisia annua L.: A valuable antimalarial plant, Ecotoxicology and Environmental Safety, 98, (59), (2013).
  • , Studies on the Expression of Sesquiterpene Synthases Using Promoter-β-Glucuronidase Fusions in Transgenic Artemisia annua L, PLoS ONE, 8, 11, (e80643), (2013).
  • , Rational engineering of plasticity residues of sesquiterpene synthases fromArtemisia annua: product specificity and catalytic efficiency, Biochemical Journal, 451, 3, (417), (2013).
  • , The stacked over-expression of FPS, CYP71AV1 and CPR genes leads to the increase of artemisinin level in Artemisia annua L., Plant Biotechnology Reports, 7, 3, (287), (2013).
  • , Artemisinic acid: A promising molecule potentially suitable for the semi-synthesis of artemisinin, RSC Advances, 10.1039/c3ra40525g, 3, 21, (7622), (2013).
  • , Differentially Expressed Genes during Contrasting Growth Stages of Artemisia annua for Artemisinin Content, PLoS ONE, 8, 4, (e60375), (2013).
  • , Efficient Somatic Embryogenesis and Organogenesis of Self-Pollination <i>Artemisia annua</i> Progeny and Artemisinin Formation in Regenerated Plants, American Journal of Plant Sciences, 04, 11, (2206), (2013).
  • , The effect of roots and media constituents on trichomes and artemisinin production in Artemisia annua L., Plant Cell Reports, 32, 2, (207), (2013).
  • , Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua, BMC Plant Biology, 13, 1, (220), (2013).
  • , High-level semi-synthetic production of the potent antimalarial artemisinin, Nature, 496, 7446, (528), (2013).
  • , The Roles of a Flavone-6-Hydroxylase and 7-O-Demethylation in the Flavone Biosynthetic Network of Sweet Basil, Journal of Biological Chemistry, 288, 3, (1795), (2013).
  • , Methylerythritol Phosphate Pathway of Isoprenoid Biosynthesis, Annual Review of Biochemistry, 10.1146/annurev-biochem-052010-100934, 82, 1, (497-530), (2013).
  • , Metabolic engineering of plants for artemisinin synthesis, Biotechnology and Genetic Engineering Reviews, 29, 2, (135), (2013).
  • , Isolation and Characterization of CPRgene Promoter from Artemisia annua by Thermal Asymmetric Interlaced Polymerase Chain Reaction (TAIL-PCR), American Journal of Biochemistry and Molecular Biology, 3, 4, (379), (2013).
  • , Comparative functional analysis of CYP71AV1 natural variants reveals an important residue for the successive oxidation of amorpha‐4,11‐diene, FEBS Letters, 587, 3, (278-284), (2012).
  • , An Overview of Heterologous Organisms Used to Produce Artemisinin and Its Precursors, CHINESE BULLETIN OF BOTANY, 47, 6, (571), (2013).
  • , Glandular trichomes: what comes after expressed sequence tags?, The Plant Journal, 70, 1, (51-68), (2012).
  • , Pyran Formation by an Atypical CYP‐Mediated Four‐Electron Oxygenation–Cyclization Cascade in an Engineered Aureothin Pathway, ChemBioChem, 13, 15, (2196-2199), (2012).
  • , Metabolic engineering for the production of clinically important molecules: Omega‐3 fatty acids, artemisinin, and taxol, Biotechnology Journal, 7, 1, (20-33), (2011).
  • , Bioactive Plant Isoprenoids, Studies in Natural Products Chemistry Volume 37, 10.1016/B978-0-444-59514-0.00005-5, (135-171), (2012).
  • , Molecular characterization of the pentacyclic triterpenoid biosynthetic pathway in Catharanthus roseus, Planta, 236, 5, (1571), (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 Science, 183, (9), (2012).
  • , Biosynthesis of the Respiratory Toxin Bongkrekic Acid in the Pathogenic Bacterium Burkholderia gladioli, Chemistry & Biology, 10.1016/j.chembiol.2012.07.022, 19, 9, (1164-1174), (2012).
  • , The Jasmonate-Responsive AP2/ERF Transcription Factors AaERF1 and AaERF2 Positively Regulate Artemisinin Biosynthesis in Artemisia annua L., Molecular Plant, 5, 2, (353), (2012).
  • , Overexpression of the cytochrome P450 monooxygenase (cyp71av1) and cytochrome P450 reductase (cpr) genes increased artemisinin content in Artemisia annua (Asteraceae), Genetics and Molecular Research, 11, 3, (3298), (2012).
  • , Characterization of cytochrome P450 monooxygenases isolated from trichome enriched fraction of Artemisia annua L. leaf, Gene, 510, 2, (193), (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 Molecular Biology Reporter, 30, 4, (838), (2012).
  • , Enhanced artemisinin production from engineered yeast precursors upon biotransformation, Biocatalysis and Biotransformation, 30, 2, (190), (2012).
  • , Biochemical characterization and identification of a cinnamyl alcohol dehydrogenase from Artemisia annua, Plant Science, 193-194, (85), (2012).
  • , Tuning P450 Enzymes as Oxidation Catalysts, ACS Catalysis, 10.1021/cs300001x, 2, 4, (647-666), (2012).
  • , The production of artemisinin precursors in tobacco, Plant Biotechnology Journal, 9, 4, (445-454), (2010).
  • , Gel‐based and gel‐free proteomic analysis of Nicotiana tabacum trichomes identifies proteins involved in secondary metabolism and in the (a)biotic stress response, PROTEOMICS, 11, 3, (440-454), (2011).
  • , Enhancement of artemisinin content in tetraploid Artemisia annua plants by modulating the expression of genes in artemisinin biosynthetic pathway, Biotechnology and Applied Biochemistry, 58, 1, (50-57), (2011).
  • , Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants, New Phytologist, 189, 1, (176-189), (2010).
  • , Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures, Plant Biology, 13, 1, (51-58), (2010).
  • , β-Cyclodextrins enhance artemisinin production in Artemisia annua suspension cell cultures, Applied Microbiology and Biotechnology, 90, 6, (1905), (2011).
  • , Artemisinin production in Artemisia annua: studies in planta and results of a novel delivery method for treating malaria and other neglected diseases, Phytochemistry Reviews, 10, 2, (173), (2011).
  • , Cloning and characterization of trichome-specific promoter of cpr71av1 gene involved in artemisinin biosynthesis in Artemisia annua L., Molecular Biology, 45, 5, (751), (2011).
  • , Singlet oxygen as a signaling transducer for modulating artemisinin biosynthetic genes in Artemisia annua, Biologia Plantarum, 55, 4, (669), (2011).
  • , Trichomes + roots + ROS = artemisinin: regulating artemisinin biosynthesis in Artemisia annua L., In Vitro Cellular & Developmental Biology - Plant, 47, 3, (329), (2011).
  • , Zingiber zerumbet CYP71BA1 catalyzes the conversion of α-humulene to 8-hydroxy-α-humulene in zerumbone biosynthesis, Cellular and Molecular Life Sciences, 68, 6, (1033), (2011).
  • , Increases in leaf artemisinin concentration in Artemisia annua in response to the application of phosphorus and boron, Industrial Crops and Products, 34, 3, (1465), (2011).
  • , Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.), Phytochemistry, 72, 14-15, (1739), (2011).
  • , Trichome-Specific Expression of Amorpha-4,11-Diene Synthase, a Key Enzyme of Artemisinin Biosynthesis in <i>Artemisia annua</i> L., as Reported by a Promoter-GUS Fusion, American Journal of Plant Sciences, 02, 04, (619), (2011).
  • , Foliar application of chitosan activates artemisinin biosynthesis in Artemisia annua L., Industrial Crops and Products, 33, 1, (176), (2011).
  • , A chicory cytochrome P450 mono-oxygenase CYP71AV8 for the oxidation of (+)-valencene, FEBS Letters, 585, 1, (178), (2011).
  • , Structural Fine-Tuning of a Multifunctional Cytochrome P450 Monooxygenase, Journal of the American Chemical Society, 10.1021/ja110146z, 133, 7, (2292-2302), (2011).
  • , Computational Identification of Sweet Wormwood (Artemisia annua) microRNA and Their mRNA Targets, Genomics, Proteomics & Bioinformatics, 9, 6, (200), (2011).
  • , Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L, BMC Plant Biology, 11, 1, (45), (2011).
  • , Characterization of development and artemisinin biosynthesis in self-pollinated Artemisia annua plants, Planta, 234, 4, (685), (2011).
  • , Effect of wounding on gene expression involved in artemisinin biosynthesis and artemisinin production in Artemisia annua, Russian Journal of Plant Physiology, 57, 6, (882), (2010).
  • , Sesquiterpenes, Comprehensive Natural Products II, 10.1016/B978-008045382-8.00005-8, (609-641), (2010).
  • , Overexpression of farnesyl pyrophosphate synthase (FPS) gene affected artemisinin content and growth of Artemisia annua L., Plant Cell, Tissue and Organ Culture (PCTOC), 103, 2, (255), (2010).
  • , Salicylic acid and methyl jasmonate but not Rose Bengal enhance artemisinin production through invoking burst of endogenous singlet oxygen, Plant Science, 178, 4, (390), (2010).
  • , Artemisinin biosynthesis in growing plants of Artemisia annua. A 13CO2 study, Phytochemistry, 71, 2-3, (179), (2010).
  • , Nicotiana benthamiana as a Production Platform for Artemisinin Precursors, PLoS ONE, 5, 12, (e14222), (2010).
  • , Post-modification Enzymes Involved in the Biosynthesis of Plant Terpenoids, Acta Botanica Yunnanica, 31, 5, (461), (2010).
  • , DMSO triggers the generation of ROS leading to an increase in artemisinin and dihydroartemisinic acid in Artemisia annua shoot cultures, Plant Cell Reports, 29, 2, (143), (2010).
  • , Production of Pharmaceuticals by Plant Tissue Cultures, Comprehensive Natural Products II, 10.1016/B978-008045382-8.00065-4, (615-628), (2010).
  • , A glandular trichome-specific monoterpene alcohol dehydrogenase from Artemisia annua, Phytochemistry, 71, 11-12, (1264), (2010).
  • , Plant Secondary Metabolism Engineering: Methods, Strategies, Advances, and Omics, Comprehensive Natural Products II, 10.1016/B978-008045382-8.00068-X, (629-668), (2010).
  • , Biochemical Conservation and Evolution of Germacrene A Oxidase in Asteraceae, Journal of Biological Chemistry, 285, 22, (16588), (2010).
  • , The Genetic Map of Artemisia annua L. Identifies Loci Affecting Yield of the Antimalarial Drug Artemisinin, Science, 327, 5963, (328), (2010).
  • , A genomics resource for investigating regulation of essential oil production in Lavandula angustifolia, Planta, 231, 4, (835), (2010).
  • , The improvement of amorpha‐4,11‐diene production by a yeast‐conform variant, Journal of Applied Microbiology, 106, 3, (941-951), (2009).
  • , Medicinal Plants, Compendium of Transgenic Crop Plants, (141-156), (2009).
  • , Salicylic acid activates artemisinin biosynthesis in Artemisia annua L., Plant Cell Reports, 28, 7, (1127), (2009).
  • , Synergistic re-channeling of mevalonate pathway for enhanced artemisinin production in transgenic Artemisia annua, Plant Science, 177, 1, (57), (2009).
  • , Terpenoid metabolic profiling analysis of transgenic Artemisia annua L. by comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry, Metabolomics, 5, 4, (497), (2009).
  • , 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 and Cell Physiology, 50, 12, (2146), (2009).
  • , Essential oil production: relationship with abundance of glandular trichomes in aerial surface of plants, Acta Physiologiae Plantarum, 31, 1, (13), (2009).
  • , Localization of enzymes of artemisinin biosynthesis to the apical cells of glandular secretory trichomes of Artemisia annua L., Phytochemistry, 70, 9, (1123), (2009).
  • , Guaianolides in apiaceae: perspectives on pharmacology and biosynthesis, Phytochemistry Reviews, 8, 3, (581), (2009).
  • , Increased Accumulation of Artemisinin and Anthocyanins in Artemisia annua Expressing the Arabidopsis Blue Light Receptor CRY1, Plant Molecular Biology Reporter, 27, 3, (334), (2009).
  • , Quantification of Three Key Enzymes Involved in Artemisinin Biogenesis in Artemisia annua by Polyclonal Antisera-Based ELISA, Plant Molecular Biology Reporter, 27, 1, (50), (2009).
  • , Molecular cloning and characterization of Dbr1, a 2-alkenal reductase from Artemisia annuaThe nucleotide sequence reported in this article has been deposited in the GenBank database under accession No. FJ750460.This paper is one of a selection of papers published in a Special Issue from the National Research Council of Canada – Plant Biotechnology Institute., Botany, 87, 6, (643), (2009).
  • , Functional genomics for plant natural product biosynthesis, Natural Product Reports, 26, 11, (1466), (2009).
  • , Molecular cloning of an aldehyde dehydrogenase implicated in artemisinin biosynthesis in Artemisia annuaThis paper is one of a selection of papers published in a Special Issue from the National Research Council of Canada – Plant Biotechnology Institute., Botany, 87, 6, (635), (2009).
  • , Terpenoid biomaterials, The Plant Journal, 54, 4, (656-669), (2008).
  • , Harnessing plant trichome biochemistry for the production of useful compounds, The Plant Journal, 54, 4, (702-711), (2008).
  • , Transcriptome analysis approaches for the isolation of trichome-specific genes from the medicinal plant Cistus creticus subsp. creticus, Plant Molecular Biology, 68, 6, (633), (2008).
  • , Bioconversion of Mono- and Sesquiterpenoids by Recombinant Human Cytochrome P450 Monooxygenases, Pharmaceutical Biology, 46, 10-11, (710), (2008).
  • , Development of an Adonis aestivalis expressed sequence tag population as a resource for genes of the carotenoid pathway, Genome, 51, 11, (888), (2008).
  • , Heme-iron oxygenases: powerful industrial biocatalysts?, Current Opinion in Chemical Biology, 10.1016/j.cbpa.2008.01.029, 12, 2, (177-186), (2008).
  • , The Molecular Cloning of Artemisinic Aldehyde Δ11(13) Reductase and Its Role in Glandular Trichome-dependent Biosynthesis of Artemisinin inArtemisia annua, Journal of Biological Chemistry, 283, 31, (21501), (2008).
  • , Cloning of artemisinin biosynthetic cDNAs and novel ESTs and quantification of low temperature-induced gene overexpression, Science in China Series C: Life Sciences, 51, 3, (232), (2008).
  • , Transcriptome analysis of different cell types from glandular trichomes of Artemisia annua, Journal of Biotechnology, 136, (S233), (2008).
  • , Structural and mechanistic analysis of trichodiene synthase using site-directed mutagenesis: Probing the catalytic function of tyrosine-295 and the asparagine-225/serine-229/glutamate-233–Mg2+B motif, Archives of Biochemistry and Biophysics, 469, 2, (184), (2008).
  • , Metabolic engineering of microorganisms for isoprenoid production, Natural Product Reports, 10.1039/b802939c, 25, 4, (656), (2008).
  • , Production of artemisinin by genetically-modified microbes, Biotechnology Letters, 30, 4, (581), (2008).
  • , Biological Production of Artemisinin for Malaria Therapy, Medicinal Plant Biotechnology, (529-542), (2008).
  • , Licorice  -amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin, Proceedings of the National Academy of Sciences, 105, 37, (14204), (2008).
  • , Natural sesquiterpenoids, Natural Product Reports, 10.1039/b706427f, 24, 6, (1350), (2007).
  • , Understandin gIsoprenoid Biochemistry, Teaching Innovations in Lipid Science, 10.1201/9781420012804.ch8, (123-134), (2010).
  • , In vivo transformations of artemisinic acid in Artemisia annua plants, Tetrahedron, 63, 38, (9548), (2007).
  • , Implementation of functional genomics for gene discovery in alkaloid producing plants, Phytochemistry Reviews, 6, 1, (35), (2007).
  • , Artemisinin: current state and perspectives for biotechnological production of an antimalarial drug, Applied Microbiology and Biotechnology, 10.1007/s00253-006-0452-0, 72, 1, (11-20), (2006).
  • , Production of isoprenoid pharmaceuticals by engineered microbes, Nature Chemical Biology, 10.1038/nchembio836, 2, 12, (674-681), (2006).
  • , Artemisinin: The biosynthetic pathway and its regulation in Artemisia annua, a terpenoid-rich species, In Vitro Cellular & Developmental Biology - Plant, 10.1079/IVP2006782, 42, 4, (309-317), (2006).
  • , Heterologous expression and strategies for encapsulation of membrane-localized plant P450s, Phytochemistry Reviews, 5, 2-3, (507), (2006).
  • , Combinatorial biosynthesis of medicinal plant secondary metabolites, Biomolecular Engineering, 10.1016/j.bioeng.2006.08.001, 23, 6, (265-279), (2006).
  • , Transcriptome Analysis of Medicinal Plant with Next‐Generation Sequencing Technologies, Encyclopedia of Analytical Chemistry, (1-12), (2014).
  • , Plant Metabolic Engineering Strategies for the Production of Pharmaceutical Terpenoids, Frontiers in Plant Science, 10.3389/fpls.2016.01647, 7, (2016).
  • , High-Level Production of Amorpha-4,11-Diene, a Precursor of the Antimalarial Agent Artemisinin, in Escherichia coli, PLoS ONE, 10.1371/journal.pone.0004489, 4, 2, (e4489), (2009).